[{"sourceid":"4968113","sourcedb":"","project":"","target":"","text":"Structural diversity in a human antibody germline library ABSTRACT To support antibody therapeutic development, the crystal structures of a set of 16 germline variants composed of 4 different kappa light chains paired with 4 different heavy chains have been determined. All four heavy chains of the antigen-binding fragments (Fabs) have the same complementarity-determining region (CDR) H3 that was reported in an earlier Fab structure. The structure analyses include comparisons of the overall structures, canonical structures of the CDRs and the VH:VL packing interactions. The CDR conformations for the most part are tightly clustered, especially for the ones with shorter lengths. The longer CDRs with tandem glycines or serines have more conformational diversity than the others. CDR H3, despite having the same amino acid sequence, exhibits the largest conformational diversity. About half of the structures have CDR H3 conformations similar to that of the parent; the others diverge significantly. One conclusion is that the CDR H3 conformations are influenced by both their amino acid sequence and their structural environment determined by the heavy and light chain pairing. The stem regions of 14 of the variant pairs are in the ‘kinked’ conformation, and only 2 are in the extended conformation. The packing of the VH and VL domains is consistent with our knowledge of antibody structure, and the tilt angles between these domains cover a range of 11 degrees. Two of 16 structures showed particularly large variations in the tilt angles when compared with the other pairings. The structures and their analyses provide a rich foundation for future antibody modeling and engineering efforts. Introduction At present, therapeutic antibodies are the largest class of biotherapeutic proteins that are in clinical trials. The use of monoclonal antibodies as therapeutics began in the early 1980s, and their composition has transitioned from murine antibodies to generally less immunogenic humanized and human antibodies. The technologies currently used to obtain human antibodies include transgenic mice containing human antibody repertoires, cloning directly from human B cells, and in vitro selection from antibody libraries using various display technologies. Once a candidate antibody is identified, protein engineering is usually required to produce a molecule with the right biophysical and functional properties. All engineering efforts are guided by our understanding of the atomic structures of antibodies. In such efforts, the crystal structure of the specific antibody may not be available, but modeling can be used to guide the engineering efforts. Today's antibody modeling approaches, which normally focus on the variable region, are being developed by the application of structural principles and insights that are evolving as our knowledge of antibody structures continues to expand. Our current structural knowledge of antibodies is based on a multitude of studies that used many techniques to gain insight into the functional and structural properties of this class of macromolecule. Five different antibody isotypes occur, IgG, IgD, IgE, IgA and IgM, and each isotype has a unique role in the adaptive immune system. IgG, IgD and IgE isotypes are composed of 2 heavy chains (HCs) and 2 light chains (LCs) linked through disulfide bonds, while IgA and IgM are double and quintuple versions of antibodies, respectively. Isotypes IgG, IgD and IgA each have 4 domains, one variable (V) and 3 constant (C) domains, while IgE and IgM each have the same 4 domains along with an additional C domain. These multimeric forms are linked with an additional J chain. The LCs that associate with the HCs are divided into 2 functionally indistinguishable classes, κ and λ. Both κ and λ polypeptide chains are composed of a single V domain and a single C domain. The heavy and light chains are composed of structural domains that have ∼110 amino acid residues. These domains have a common folding pattern often referred to as the “immunoglobulin fold,” formed by the packing together of 2 anti-parallel β-sheets. All immunoglobulin chains have an N-terminal V domain followed by 1 to 4 C domains, depending upon the chain type. In antibodies, the heavy and light chain V domains pack together forming the antigen combining site. This site, which interacts with the antigen (or target), is the focus of current antibody modeling efforts. This interaction site is composed of 6 complementarity-determining regions (CDRs) that were identified in early antibody amino acid sequence analyses to be hypervariable in nature, and thus are responsible for the sequence and structural diversity of our antibody repertoire. The sequence diversity of the CDR regions presents a substantial challenge to antibody modeling. However, an initial structural analysis of the combining sites of the small set of structures of immunoglobulin fragments available in the 1980s found that 5 of the 6 hypervariable loops or CDRs had canonical structures (a limited set of main-chain conformations). A CDR canonical structure is defined by its length and conserved residues located in the hypervariable loop and framework residues (V-region residues that are not part of the CDRs). Furthermore, studies of antibody sequences revealed that the total number of canonical structures are limited for each CDR, indicating possibly that antigen recognition may be affected by structural restrictions at the antigen-binding site. Later studies found that the CDR loop length is the primary determining factor of antigen-binding site topography because it is the primary factor for determining a canonical structure. Additional efforts have led to our current understanding that the LC CDRs L1, L2, and L3 have preferred sets of canonical structures based on length and amino acid sequence composition. This was also found to be the case for the H1 and H2 CDRs. Classification schemes for the canonical structures of these 5 CDRs have emerged and evolved as the number of depositions in the Protein Data Bank of Fab fragments of antibodies grow. Recently, a comprehensive CDR classification scheme was reported identifying 72 clusters of conformations observed in antibody structures. The knowledge and predictability of these CDR canonical structures have greatly advanced antibody modeling efforts. In contrast to CDRs L1, L2, L3, H1 and H2, no canonical structures have been observed for CDR H3, which is the most variable in length and amino acid sequence. Some clustering of conformations was observed for the shortest lengths; however, for the longer loops, only the portions nearest the framework (torso, stem or anchor region) were found to have defined conformations. In the torso region, 2 primary groups could be identified, which led to sequence-based rules that can predict with some degree of reliability the conformation of the stem region. The “kinked” or “bulged” conformation is the most prevalent, but an “extended” or “non-bulged” conformation is also, but less frequently, observed. The cataloging and development of the rules for predicting the conformation of the anchor region of CDR H3 continue to be refined, producing new insight into the CDR H3 conformations and new tools for antibody engineering. Current antibody modeling approaches take advantage of the most recent advances in homology modeling, the evolving understanding of the CDR canonical structures, the emerging rules for CDR H3 modeling and the growing body of antibody structural data available from the PDB. Recent antibody modeling assessments show continued improvement in the quality of the models being generated by a variety of modeling methods. Although antibody modeling is improving, the latest assessment revealed a number of challenges that need to be overcome to provide accurate 3-dimensional models of antibody V regions, including accuracies in the modeling of CDR H3. The need for improvement in this area was also highlighted in a recent study reporting an approach and results that may influence future antibody modeling efforts. One important finding of the antibody modeling assessments was that errors in the structural templates that are used as the basis for homology models can propagate into the final models, producing inaccuracies that may negatively influence the predictive nature of the V region model. To support antibody engineering and therapeutic development efforts, a phage library was designed and constructed based on a limited number of scaffolds built with frequently used human germ-line IGV and IGJ gene segments that encode antigen combining sites suitable for recognition of peptides and proteins. This Fab library is composed of 3 HC germlines, IGHV1-69 (H1-69), IGHV3-23 (H3-23) and IGHV5-51(H5-51), and 4 LC germlines (all κ), IGKV1-39 (L1-39), IGKV3-11 (L3-11), IGKV3-20 (L3-20) and IGKV4-1 (L4-1). Selection of these genes was based on the high frequency of their use and their cognate canonical structures that were found binding to peptides and proteins, as well as their ability to be expressed in bacteria and displayed on filamentous phage. The implementation of the library involves the diversification of the human germline genes to mimic that found in natural human libraries. The crystal structure determinations and structural analyses of all germline Fabs in the library described above along with the structures of a fourth HC germline, IGHV3-53 (H3-53), paired with the 4 LCs of the library have been carried out to support antibody therapeutic development. All 16 HCs of the Fabs have the same CDR H3 that was reported in an earlier Fab structure. This is the first systematic study of the same VH and VL structures in the context of different pairings. The structure analyses include comparisons of the overall structures, canonical structures of the L1, L2, L3, H1 and H2 CDRs, the structures of all CDR H3s, and the VH:VL packing interactions. The structures and their analyses provide a foundation for future antibody engineering and structure determination efforts. Results Crystal structures Crystal data, X-ray data, and refinement statistics. Fab\tH1-69:L1-39\tH1-69:L3-11\tH1-69:L3-20\tH1-69:L4-1\t \tPDB identifier\t5I15\t5I16\t5I17\t5I18\t \tCrystal Data\t \t \t \t \t \tCrystallization Solution\t \t \t \t \t \t Buffer, pH\t0.1 M MES- pH 6.5\t0.1 M MES pH 6.5\t0.1 M MES, pH 6.5\t0.1 M HEPES, pH 7.5\t \t Precipitant1\t5 M Na Formate\t25% PEG 3350\t2.0 M Amm Sulfate\t10% PEG 8000\t \t Additive1\t \t0.2 M Na Formate\t5% MPD\t8% EG\t \t Space Group\tP3121\tC2\tP422\tP4212\t \t Molecules/AU\t1\t2\t2\t1\t \t Unit Cell\t \t \t \t \t \t a(Å)\t129.2\t212.0\t152.5\t120.0\t \t b(Å)\t129.2\t55.1\t152.5\t120.0\t \t c(Å)\t91.8\t80.3\t123.4\t64.2\t \t β(°)\t90.0\t97.8\t90.0\t90.0\t \t γ(°)\t120.0\t90.0\t90.0\t90.0\t \t Vm (Å3/Da)\t4.67\t2.44\t3.77\t2.39\t \t Solvent Content (%)\t74\t50\t67\t48\t \tX-Ray Data2\t \t \t \t \t \t Resolution (Å)\t30-2.6 (2.7-2.6)\t30.0-1.9 (1.95-1.9)\t30.0-3.3 (3.4-3.3)\t30-1.9 (2.0-1.9)\t \t Measured Reflections\t136,745 (8,650)\t241,145 (16,580)\t237,504 (15,007)\t801,080 (19,309)\t \t Unique Reflections\t27,349 (1,730)\t71,932 (5,198)\t22,379 (1,590)\t35,965 (2,194)\t \t Completeness (%)\t99.3 (98.7)\t99.0 (97.3)\t99.5 (96.8)\t98.5 (82.8)\t \t Redundancy\t5.0 (5.0)\t3.4 (3.2)\t10.6 (9.4)\t22.3 (8.8)\t \t Rmerge\t0.048 (0.522)\t0.044 (0.245)\t0.086 (0.536)\t0.093 (0.231)\t \t \u003c I/σ \u003e\t21.2 (3.9)\t17.8 (4.7)\t25.5 (4.5)\t29.2 (8.1)\t \t B-factor (Å2)\t60.5\t33.2\t61.0\t19.6\t \tRefinement\t \t \t \t \t \t Resolution (Å)\t15-2.6\t15-1.9\t15-3.3\t15-1.9\t \t Number of Reflections\t26,238\t70,346\t21,197\t34,850\t \t Number of All Atoms\t3,224\t6,975\t6,398\t3,695\t \t Number of Waters\t2\t472\t0\t399\t \t R-factor (%)\t20.5\t19.2\t20.2\t16.7\t \t R-free (%)\t24.1\t22.2\t24.7\t21.3\t \tRMSD\t \t \t \t \t \t Bond Lengths (Å)\t0.006\t0.005\t0.005\t0.008\t \t Bond Angles (°)\t1.2\t1.1\t1.0\t1.1\t \t Mean B-factor (Å2)\t65.3\t34.4\t80.1\t20.0\t \tRamachandran Plot (%)\t \t \t \t \t \t Outliers\t0.0\t0.0\t0.9\t0.0\t \t Favored\t92.3\t96.9\t93.1\t96.9\t \t Abbreviations: Amm, ammonium;EG, ethylene glycol; PEG, polyethylene glycol. Values for high-resolution shell are in parentheses. (Continued) Crystal data, X-ray data, and refinement statistics. Fab\tH3-23:L1-39\tH3-23:L3-11\tH3-23:L3-20\tH3-23:L4-1\t \t PDB identifier\t5I19\t5I1A\t5I1C\t5I1D\t \tCrystal Data\t \t \t \t \t \tCrystallization Solution\t \t \t \t \t \t Buffer, pH\tNo Buffer\t0.1 M Na Acetate, pH 4.5\t0.1 M MES, pH 6.5\t0.1 M HEPES, pH 7.5\t \t Precipitant1\t20% PEG 3350\t2.0 M Amm Sulfate\t16% PEG 3350\t2.0 M Amm Sulfate\t \t Additive1\t0.2 M Li Citrate\t5% PEG 400\t0.2 M Amm Acetate\t2% PEG 400\t \t Space Group\tP41212\tP212121\tP6222\tP212121\t \t Molecules/AU\t1\t2\t1\t2\t \tUnit Cell\t \t \t \t \t \t a(Å)\t96.6\t60.9\t121.5\t62.7\t \t b(Å)\t96.6\t110.6\t121.5\t111.0\t \t c(Å)\t105.4\t158.9\t160.4\t160.0\t \t β(°)\t90\t90\t90\t90\t \t Vm (Å3/Da)\t2.60\t2.82\t3.60\t2.90\t \t Solvent Content (%)\t53\t56\t66\t57\t \tX-Ray Data2\t \t \t \t \t \t Resolution (Å)\t30-2.8 (2.9-2.8)\t30-2.0 (2.1-2.0)\t30-2.25 (2.3-2.25)\t30-2.0 (2.1-2.0)\t \t Measured Reflections\t177,681 (12,072)\t351,312 (8,634)\t887,349 (59,919)\t873,523 (49,118)\t \t Unique Reflections\t12,678 (899)\t58,989 (2,870)\t32,572 (2,300)\t75,540 (5,343)\t \t Completeness (%)\t99.5 (97.4)\t80.9 (54.2)\t96.9 (94.8)\t99.7 (96.9)\t \t Redundancy\t14.0 (13.4)\t6.0 (3.0)\t27.2 (26.1)\t11.6 (9.2)\t \t Rmerge\t0.091 (0.594)\t0.066 (0.204)\t0.086 (0.478)\t0.094 (0.488)\t \t \u003c I/σ \u003e\t31.2 (5.1)\t20.4 (4.6)\t37.0 (10.4)\t21.6 (5.0)\t \t B-factor (Å2)\t42.8\t27.1\t33.7\t29.4\t \tRefinement\t \t \t \t \t \t Resolution (Å)\t15-2.8\t15-2.0\t15-2.25\t15-2.0\t \t Number of Reflections\t11,972\t57,599\t31,411\t74,238\t \t Number of All Atoms\t3,234\t6,948\t3,472\t7,210\t \t Number of Waters\t0\t416\t222\t635\t \t R-factor (%)\t23.9\t20.5\t22.0\t21.6\t \t R-free (%)\t31.5\t25.5\t26.6\t25.1\t \tRMSD\t \t \t \t \t \t Bond Lengths (Å)\t0.009\t0.010\t0.005\t0.008\t \t Bond Angles (°)\t1.3\t1.3\t1.0\t1.1\t \t Mean B-factor (Å2)\t48.4\t36.7\t47.7\t46.4\t \tRamachandran Plot (%)\t \t \t \t \t \t Outliers\t0.0\t0.0\t0.0\t0.0\t \t Favored\t92.3\t96.8\t97.5\t97.6\t \t Abbreviations: Amm, ammonium; PEG, polyethylene glycol. Values for high-resolution shell are in parentheses. (Continued) Crystal data, X-ray data, and refinement statistics. Fab\tH3-53:L1-39\tH3-53:L3-11\tH3-53:L3-20\tH3-53:L4-1\t \tPDB indentifier\t5I1E\t5I1G\t5I1H\t5I1I\t \tCrystal Data\t \t \t \t \t \tCrystallization Solution\t \t \t \t \t \t Buffer, pH\tNo buffer\t0.1 M Na Acetate pH 4.5\t0.1 M Na Acetate pH 4.5\t0.1M MES, pH 6.5\t \t Precipitant1\t16% PEG 3350\t25% PEG 3350\t19% PEG 4000\t17% PEG 3350\t \t Additive1\t0.2 M Amm Sulfate 5% Dioxane\t0.2 M Li2SO4\t0.2 M Amm Sulfate\t0.2 M Na Formate, 5% MPD\t \t Space Group\tP6522\tP6522\tP6522\tP31\t \t Molecules/AU\t1\t1\t1\t1\t \tUnit Cell\t \t \t \t \t \t a(Å)\t89.4\t88.1\t89.4\t68.1\t \t b(Å)\t89.4\t88.1\t89.4\t68.1\t \t c(Å)\t212.4\t219.6\t211.7\t95.6\t \t β(°)\t90\t90\t90\t90\t \t γ(°)\t120\t120\t120\t120\t \t Vm (Å3/Da)\t2.57\t2.64\t2.57\t2.64\t \t Solvent Content (%)\t52\t53\t52\t53\t \tX-Ray Data2\t \t \t \t \t \t Resolution (Å)\t30-2.7 (2.8-2.7)\t30-2.3 (2.4-2.3)\t30-2.2 (2.3-2.0)\t30-2.5 (2.6-2.5)\t \t Measured Reflections\t297,367 (19,369)\t333,739 (8,008)\t381,125 (1,591)\t137,992 (9,883)\t \t Unique Reflections\t14,402 (1,003)\t21,683 (1,135)\t24,323 (964)\t16,727 (1,227)\t \t Completeness (%)\t99.6 (96.8)\t93.8 (68.4)\t95.3 (52.0)\t98.6 (98.1)\t \t Redundancy\t20.6 (19.3)\t15.4 (7.1)\t15.7 (1.7)\t8.2 (8.1)\t \t Rmerge\t0.095 (0.451)\t0.057 (0.324)\t0.062 (0.406)\t0.047 (0.445)\t \t \u003c I/σ \u003e\t38.3 (8.1)\t36.7 (5.5)\t36.2 (1.6)\t31.6 (5.6)\t \t B-factor (Å2)\t33.2\t37.3\t33.7\t54.8\t \tRefinement\t \t \t \t \t \t Resolution (Å)\t15-2.7\t15-2.3\t15-2.2\t15-2.5\t \t Number of Reflections\t13,583\t20,255\t24,962\t15,811\t \t Number of All Atoms\t3,335\t3,271\t3,298\t3,239\t \t Number of Waters\t88\t70\t71\t21\t \t R-factor (%)\t19.1\t29.8\t22.8\t25.0\t \t R-free (%)\t26.4\t38.3\t26.6\t33.7\t \tRMSD\t \t \t \t \t \t Bond Lengths (Å)\t0.008\t0.005\t0.005\t0.006\t \t Bond Angles (°)\t1.2\t1.0\t1.0\t1.1\t \t Mean B-factor (Å2)\t49.1\t46.3\t51.7\t88.9\t \tRamachandran Plot (%)\t \t \t \t \t \t Outliers\t0.2\t0.2\t0.2\t1.2\t \t Favored\t96.7\t97.1\t96.5\t90.9\t \t Abbreviations: Amm, ammonium; PEG, polyethylene glycol. Values for high-resolution shell are in parentheses. (Continued) Crystal data, X-ray data, and refinement statistics. Fab\tH5-51:L1-39\tH5-51:L3-11\tH5-51:L3-20\tH5-51:L4-1\t \t PDB identifier\t4KMT\t5I1J\t5I1K\t5I1L\t \tCrystal Data\t \t \t \t \t \tCrystallization Solution\t \t \t \t \t \t Buffer, pH\t0.1 M CHES, pH 9.5\t0.1 M Tris, pH 8.5\t0.1 M CHES, pH 9.5\t0.1 M Tris, pH 8.5\t \t Precipitant1\t1.8 M Amm Sulfate\t25% PEG 3350\t1.0 M Amm Sulfate\t24% PEG 3350\t \t Additive1\t5% dioxane\t0.2 M MgCl2\t \t0.2 M Amm Sulfate\t \t Space Group\tP212121\tP212121\tP212121\tP21\t \t Molecules/AU\t1\t1\t1\t2\t \tUnit Cell\t \t \t \t \t \t a(Å)\t63.7\t64.1\t63.8\t106.0\t \t b(Å)\t73.8\t73.8\t74.1\t38.0\t \t c(Å)\t103.1\t103.0\t103.0\t112.3\t \t β(°)\t90\t90\t90\t100.4\t \t Vm (Å3/Da)\t2.53\t2.56\t2.54\t2.28\t \t Solvent Content (%)\t51\t52\t51\t46\t \tX-Ray Data2\t \t \t \t \t \t Resolution (Å)\t30-2.1 (2.2-2.1)\t30-2.5 (2.6-2.5)\t30-1.65 (1.7-1.65)\t30-1.95 (2.0-1.95)\t \t Measured Reflections\t131,839 (6,655)\t120,521 (7,988)\t246,750 (4,142)\t320,324 (12,119)\t \t Unique Reflections\t27,026 (1,885)\t17,286 (1,236)\t53,058 (2,141)\t61,554 (3,243)\t \t Completeness (%)\t93.6 (89.8)\t99.7 (97.3)\t89.8 (49.8)\t94.4 (67.1)\t \t Redundancy\t4.9 (3.5)\t7.0 (6.5)\t4.7 (1.9)\t5.2 (3.7)\t \t Rmerge\t0.079 (0.278)\t0.080 (0.281)\t0.034 (0.131)\t0.060 (0.395)\t \t \u003c I/σ \u003e\t16.8 (5.7)\t21.1(6.9)\t27.5 (5.8)\t19.7 (3.1)\t \t B-factor (Å2)\t26.0\t27.0\t21.6\t31.4\t \tRefinement\t \t \t \t \t \t Resolution (Å)\t15-2.1\t15-2.5\t15-1.65\t15-1.95\t \t Number of Reflections\t25,857\t16,328\t51,882\t60,181\t \t Number of All Atoms\t3,676\t3,454\t3,814\t7,175\t \t Number of Waters\t302\t196\t527\t445\t \t R-factor (%)\t17.1\t17.7\t17.2\t19.4\t \t R-free (%)\t22.0\t25.8\t19.7\t25.8\t \tRMSD\t \t \t \t \t \t Bond Lengths (Å)\t0.006\t0.009\t0.005\t0.009\t \t Bond Angles (°)\t1.0\t1.3\t1.3\t1.3\t \t Mean B-factor (Å2)\t25.2\t38.2\t20.0\t19.5\t \tRamachandran Plot (%)\t \t \t \t \t \t Outliers\t0.0\t0.0\t0.0\t0.0\t \t Favored\t98.4\t97.9\t98.1\t98.0\t \t Abbreviations: Amm, ammonium; PEG, polyethylene glycol. Values for high-resolution shell are in parentheses. The crystal structures of a germline library composed of 16 Fabs generated by combining 4 HCs (H1-69, H3-23, H3-53 and H5-51) and 4 LCs (L1-39, L3-11, L3-20 and L4-1) have been determined. The Fab heavy and light chain sequences for the variants numbered according to Chothia are shown in Fig. S1. The four different HCs all have the same CDR H3 sequence, ARYDGIYGELDF. Crystallization of the 16 Fabs was previously reported. Three sets of the crystals were isomorphous with nearly identical unit cells (Table 1). These include (1) H3-23:L3-11 and H3-23:L4-1 in P212121, (2) H3-53:L1-39, H3-53:L3-11 and H3-53:L3-20 in P6522, and (3) H5-51:L1-39, H5-51:L3-11 and H5-51:L3-20 in P212121. Crystallization conditions for the 3 groups are also similar, but not identical (Table 1). Variations occur in the pH (buffer) and the additives, and, in group 3, PEG 3350 is the precipitant for one variants while ammonium sulfate is the precipitant for the other two. The similarity in the crystal forms is attributed in part to cross-seeding using the microseed matrix screening for groups 2 and 3. The crystal structures of the 16 Fabs have been determined at resolutions ranging from 3.3 Å to 1.65 Å (Table 1). The number of Fab molecules in the crystallographic asymmetric unit varies from 1 (for 12 Fabs) to 2 (for 4 Fabs). Overall the structures are fairly complete, and, as can be expected, the models for the higher resolution structures are more complete than those for the lower resolution structures (Table S1). Invariably, the HCs have more disorder than the LCs. For the LC, the disorder is observed at 2 of the C-terminal residues with few exceptions. Apart from the C-terminus, only a few surface residues in LC are disordered. The HCs feature the largest number of disordered residues, with the lower resolution structures having the most. The C-terminal residues including the 6xHis tags are disordered in all 16 structures. In addition to these, 2 primary disordered stretches of residues are observed in a number of structures (Table S1). One involves the loop connecting the first 2 β-strands of the constant domain (in all Fabs except H3-23:L1-39, H3-23:L3-11 and H3-53:L1-39). The other is located in CDR H3 (in H5-51:L3-11, H5-51:L3-20 and in one of 2 copies of H3-23:L4-1). CDR H1 and CDR H2 also show some degree of disorder, but to a lesser extent. CDR canonical structures Several CDR definitions have evolved over decades of antibody research. Depending on the focus of the study, the CDR boundaries differ slightly between various definitions. In this work, we use the CDR definition of North et al., which is similar to that of Martin with the following exceptions: 1) CDRs H1 and H3 begin immediately after the Cys; and 2) CDR L2 includes an additional residue at the N-terminal side, typically Tyr. CDR H1 The superposition of CDR H1 backbones for all HC:LC pairs with heavy chains: (A) H1-69, (B) H3-23, (C) H3-53 and (D) H5-51. Canonical structures. Pairs\tPDB\tCDR H1\tCDR H2\tCDR H3\t \tH1-69\t \tKASGGTFSSYAIS\tGIIPIFGTAN\tARYDGIYGELDF\t \tH1-69:L1-39\t5I15\tH1-13-4\tH2-10-1\tH3-12-1\t \tH1-69:L3-11\t5I16\tH1-13-1/H1-13-1\tH2-10-1/H2-10-1\tH3-12-1/H3-12-1\t \tH1-69:L3-20\t5I17\tH1-13-3/H1-13-6\tH2-10-1/NA\tH3-12-1/H3-12-1\t \tH1-69:L4-1\t5I18\tH1-13-10\tH2-10-1\tH3-12-1\t \tH3-23\t \tAASGFTFSSYAMS\tAISGSGGSTY\tAKYDGIYDGIYGELDF\t \tH3-23:L1-39\t5I19\tH1-13-1\tH2-10-2\tH3-12-1\t \tH3-23:L3-11\t5I1A\tH1-13-1/H1-13-1\tH2-10-2/H2-10-2\tH3-12-1/H3-12-1\t \tH3-23:L3-20\t5I1C\tH1-13-1\tH2-10-2\tH3-12-1\t \tH3-23:L4-1\t5I1D\tH1-13-1/H1-13-1\tH2-10-2/H2-10-2\tH3-12-1/NA\t \tH3-53\t \tAASGFTVSSNYMS\tVIYSGGSTY\tARYDGIYGELDF\t \tH3-53:L1-39\t5I1E\tH1-13-1\tH2-9-3\tH3-12-1\t \tH3-53:L3-11\t5I1G\tH1-13-1\tH2-9-3\tH3-12-1\t \tH3-53:L3-20\t5I1H\tH1-13-1\tH2-9-3\tH3-12-1\t \tH3-53:L4-1\t5I1I\tH1-13-1\tH2-9-3\tNA\t \tH5-51\t \tKGSGYSFTSYWIG\tIIYPGDSDTR\tARYDGIYGELDF\t \tH5-51:L1-39\t4KMT\tH1-13-1\tH2-10-1\tH3-12-1\t \tH5-51:L3-11\t5I1J\tH1-13-1\tH2-10-1\tNA\t \tH5-51:L3-20\t5I1K\tH1-13-1\tH2-10-1\tNA\t \tH5-51:L4-1\t5I1L\tH1-13-1/H1-13-1\tH2-10-1/H2-10-1\tH3-12-1/H3-12-1\t \t \t \tCDR L1\tCDR L2\tCDR L3\t \tL1-39\t \tRASQSISSYLN\tYAASSLQS\tQQSYSTPLT\t \tH1-69:L1-39\t5I15\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tH3-23:L1-39\t5I19\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tH3-53:L1-39\t5I1E\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tH5-51:L1-39\t4KMT\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tL3-11\t \tRASQSVSSYLA\tYDASNRAT\tQQRSNWPLT\t \tH1-69:L3-11\t5I16\tL1-11-1/L1-11-1\tL2-8-1/L2-8-1\tL3-9-cis7-1/L3-9-cis7-1\t \tH3-23:L3-11\t5I1A\tL1-11-1/L1-11-1\tL2-8-1/L2-8-1\tL3-9-cis7-1/L3-9-cis7-1\t \tH3-53:L3-11\t5I1G\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tH5-51:L3-11\t5I1J\tL1-11-1\tL2-8-1\tL3-9-cis7-1\t \tL3-20\t \tRASQSVSSSYLA\tYGASSRAT\tQQYGSSPLT\t \tH1-69:L3-20\t5I17\tL1-12-2/L1-12-1\tL2-8-1/L2-8-1\tL3-9-cis7-1/L3-9-cis7-1\t \tH3-23:L3-20\t5I1C\tL1-12-2\tL2-8-1\tL3-9-cis7-1\t \tH3-53:L3-20\t5I1H\tL1-12-1\tL2-8-1\tL3-9-cis7-1\t \tH5-51:L3-20\t5I1K\tL1-12-1\tL2-8-1\tL3-9-cis7-1\t \tL4-1\t \tKSSQSVLYSSNNKNYLA\tYWASTRES\tQQYYSTPLT\t \tH1-69:L4-1\t5I18\tL1-17-1\tL2-8-1\tL3-9-cis7-1\t \tH3-23:L4-1\t5I1D\tL1-17-1/L1-17-1\tL2-8-1/L2-8-1\tL3-9-cis7-1/L3-9-cis7-1\t \tH3-53:L4-1\t5I1I\tL1-17-1\tL2-8-1\tL3-9-cis7-1\t \tH5-51:L4-1\t5I1L\tL1-17-1/L1-17-1\tL2-8-1/L2-8-1\tL3-9-cis7-1/L3-9-cis7-1\t \t CDRs are defined using the Dunbrack convention [12]. Assignments for 2 copies of the Fab in the asymmetric unit are given for 5 structures. No assignment (NA) for CDRs with missing residues. The four HCs feature CDR H1 of the same length, and their sequences are highly similar (Table 2). The CDR H1 backbone conformations for all variants for each of the HCs are shown in Fig. 1. Three of the HCs, H3-23, H3-53 and H5-51, have the same canonical structure, H1-13-1, and the backbone conformations are tightly clustered for each set of Fab structures as reflected in the rmsd values (Fig. 1B-D). Some deviation is observed for H3-53, mostly due to H3-53:L4-1, which exhibits a significant degree of disorder in CDR H1. The electron density for the backbone is weak and discontinuous, and completely missing for several side chains.    The CDR H1 structures with H1-69 shown in Fig. 1A are quite variable, both for the structures with different LCs and for the copies of the same Fab in the asymmetric unit, H1-69:L3-11 and H1-69:L3-20. In total, 6 independent Fab structures produce 5 different canonical structures, namely H1-13-1, H1-13-3, H1-13-4, H1-13-6 and H1-13-10. A major difference of H1-69 from the other germlines in the experimental data set is the presence of Gly instead of Phe or Tyr at position 27 (residue 5 of 13 in CDR H1). Glycine introduces the possibility of a higher degree of conformational flexibility that undoubtedly translates to the differences observed, and contributes to the elevated thermal parameters for the atoms in the amino acid residues in this region. CDR H2 The superposition of CDR H2 backbones for all HC:LC pairs with heavy chains: (A) H1-69, (B) H3-23, (C) H3-53 and (D) H5-51. The canonical structures of CDR H2 have fairly consistent conformations (Table 2, Fig. 2). Each of the 4 HCs adopts only one canonical structure regardless of the pairing LC. Germlines H1-69 and H5-51 have the same canonical structure assignment H2-10-1, H3-23 has H2-10-2, and H3-53 has H2-9-3. The conformations for all of these CDR H2s are tightly clustered (Fig. 2). In one case, in the second Fab of H1-69:L3-20, CDR H2 is partially disordered (Δ55-60).   Although three of the germlines have CDR H2 of the same length, 10 residues, they adopt 2 distinctively different conformations depending mostly on the residue at position 71 from the so-called CDR H4. Arg71 in H3-23 fills the space between CDRs H2 and H4, and defines the conformation of the tip of CDR H2 so that residue 54 points away from the antigen binding site. Germlines H1-69 and H5-51 are unique in the human repertoire in having an Ala at position 71 that leaves enough space for H-Pro52a to pack deeper against CDR H4 so that the following residues 53 and 54 point toward the putative antigen. Conformations of CDR H2 in H1-69 and H5-51, both of which have canonical structure H2-10-1, show little deviation within each set of 4 structures. However, there is a significant shift of the CDR as a rigid body when the 2 sets are superimposed. Most likely this is the result of interaction of CDR H2 with CDR H1, namely with the residue at position 33 (residue 11 of 13 in CDR H1). Germline H1-69 has Ala at position 33 whereas in H5-51 position 33 is occupied by a bulky Trp, which stacks against H-Tyr52 and drives CDR H2 away from the center. CDR L1 The superposition of CDR L1 backbones for all HC:LC pairs with light chains: (A) L1-39, (B) L3-11, (C) L3-20 and (D) L4-1. The four LC CDRs L1 feature 3 different lengths (11, 12 and 17 residues) having a total of 4 different canonical structure assignments. Of these LCs, L1-39 and L3-11 have the same canonical structure, L1-11-1, and superimpose very well (Fig. 3A, B). For the remaining 2, L3-20 has 2 different assignments, L1-12-1 and L1-12-2, while L4-1 has a single assignment, L1-17-1.   L4-1 has the longest CDR L1, composed of 17 amino acid residues (Fig. 3D). Despite this, the conformations are tightly clustered (rmsd is 0.20 Å). The backbone conformations of the stem regions superimpose well. Some changes in conformation occur between residues 30a and 30f (residues 8 and 13 of 17 in CDR L1). This is the tip of the loop region, which appears to have similar conformations that fan out the structures because of the slight differences in torsion angles in the backbone near Tyr30a and Lys30f. L3-20 is the most variable in CDR L1 among the 4 germlines as indicated by an rmsd of 0.54 Å (Fig. 3C). Two structures, H3-53:L3-20 and H5-51:L3-20 are assigned to canonical structure L1-12-1 with virtually identical backbone conformations. The third structure, H3-23:L3-20, has CDR L1 as L1-12-2, which deviates from L1-12-1 at residues 29-32, i.e., at the site of insertion with respect to the 11-residue CDR. The fourth member of the set, H1-69:L3-20, was crystallized with 2 Fabs in the asymmetric unit. The conformation of CDR L1 in these 2 Fabs is slightly different, and both conformations fall somewhere between L1-12-1 and L1-12-2. This reflects the lack of accuracy in the structure due to low resolution of the X-ray data (3.3 Å). CDR L2 The superposition of CDR L2 backbones for all HC:LC pairs with light chains: (A) L1-39, (B) L3-11, (C) L3-20 and (D) L4-1. All four LCs have CDR L2 of the same length and canonical structure, L2-8-1 (Table 2). The CDR L2 conformations for each of the LCs paired with the 4 HCs are clustered more tightly than any of the other CDRs (rmsd values are in the range 0.09-0.16 Å), and all 4 sets have virtually the same conformation despite the sequence diversity of the loop. No significant conformation outliers are observed (Fig. 4).   CDR L3 The superposition of CDR L3 backbones for all HC:LC pairs with light chains: (A) L1-39, (B) L3-11, (C) L3-20 and (D) L4-1. As with CDR L2, all 4 LCs have CDR L3 of the same length and canonical structure, L3-9-cis7-1 (Table 2). The conformations of CDR L3 for L1-39, L3-11, and particularly for L320, are not as tightly clustered as those of L4-1 (Fig. 5). The slight conformational variability occurs in the region of amino acid residues 90-92, which is in contact with CDR H3.   CDR H3 conformational diversity As mentioned earlier, all 16 Fabs have the same CDR H3, for which the amino acid sequence is derived from the anti-CCL2 antibody CNTO 888. The loop and the 2 β-strands of the CDR H3 in this ‘parent’ structure are stabilized by H-bonds between the carbonyl oxygen and peptide nitrogen atoms in the 2 strands. An interesting feature of these CDR H3 structures is the presence of a water molecule that interacts with the peptide nitrogens and carbonyl oxygens near the bridging loop connecting the 2 β-strands. This water is present in both the bound (4DN4) and unbound (4DN3) forms of CNTO 888. The stem region of CDR H3 in the parental Fab is in a ‘kinked’ conformation, in which the indole nitrogen of Trp103 forms a hydrogen bond with the carbonyl oxygen of Leu100b. The carboxyl group of Asp101 forms a salt bridge with Arg94. These interactions are illustrated in Fig. S2. Ribbon representations of (A) the superposition of all CDR H3s of the structures with complete backbone traces. (B) The CDR H3s rotated 90° about the y axis of the page. The structure of each CDR H3 is represented with a different color. Despite having the same amino acid sequence in all variants, CDR H3 has the highest degree of structural diversity and disorder of all of the CDRs in the experimental set. Three of the 21 Fab structures (including multiple copies in the asymmetric unit), H5-51:L3-11, H551:L3-20 and H3-23:L4-1 (one of the 2 Fabs), have missing (disordered) residues at the apex of the CDR loop. Another four of the Fabs, H3-23:L1-39, H3-53:L1-39, H3-53:L3-11 and H3-53:L4-1 have missing side-chain atoms. The variations in CDR H3 conformation are illustrated in Fig. 6 for the 18 Fab structures that have ordered backbone atoms.   A comparison of representatives of the “kinked” and “extended” structures. (A) The “kinked” CDR H3 of H1-69:L3-11 with purple carbon atoms and yellow dashed lines connecting the H-bond pairs for Leu100b O and Trp103 NE1, Arg94 NE and Asp101 OD1, and Arg94 NH2 and Asp101 OD2. (B) The “extended” CDR H3 of H1-69:L3-20 with green carbon atoms and yellow dashed lines connecting the H-bond pairs for Asp101 OD1 and OD2 and Trp103 NE1. In 10 of the 18 Fab structures, H1-69:L1-39, H1-69:L3-11 (2 Fabs), H1-69:L4-1, H3-23:L3-11 (2 Fabs), H3-23:L3-20, H3-53:L3-11, H3-53:L3-20 and H5-51:L1-39, the CDRs have similar conformations to that found in 4DN3. The bases of these structures have the ‘kinked’ conformation with the H-bond between Trp103 and Leu100b. A representative CDR H3 structure for H1-69:L1-39 illustrating this is shown in Fig. 7A. The largest backbone conformational deviation for the set is at Tyr99, where the C=O is rotated by 90° relative to that observed in 4DN3. Also, it is worth noting that only one of these structures, H1-69:L4-1, has the conserved water molecule in CDR H3 observed in the 4DN3 and 4DN4 structures. In fact, it is the only Fab in the set that has a water molecule present at this site. The CDR H3 for this structure is shown in Fig. S3.   The remaining 8 Fabs can be grouped into 5 different conformational classes. Three of the Fabs, H3-23:L1-39, H3-23:L4-1 and H3-53:L1-39, have distinctive conformations. The stem regions in these 3 cases are in the ‘kinked’ conformation consistent with that observed for 4DN3. The five remaining Fabs, H5-51:L4-1 (2 copies), H1-69:L3-20 (2 copies) and H3-53:L4-1, have 3 different CDR H3 conformations (Fig. S4). The stem regions of CDR H3 for the H5-51:L4-1 Fabs are in the ‘kinked’ conformation while, surprisingly, those of the H1-69:L3-20 pair and H3-53:L4-1 are in the ‘extended’ conformation (Fig. 7B). VH:VL domain packing The VH and VL domains have a β-sandwich structure (also often referred as a Greek key motif) and each is composed of a 4-stranded and a 5-stranded antiparallel β-sheets. The two domains pack together such that the 5-stranded β-sheets, which have hydrophobic surfaces, interact with each other bringing the CDRs from both the VH and VL domains into close proximity. The domain packing of the variants was assessed by computing the domain interface interactions, the VH:VL tilt angles, the buried surface area and surface complementarity. The results of these analyses are shown in Tables 3, 4 and S2. VH:VL interface amino acid residue interactions The conserved VH:VL interactions as viewed along the VH/VL axis. The VH residues are in blue, the VL residues are in orange. The VH:VL interface is pseudosymmetric, and involves 2 stretches of the polypeptide chain from each domain, namely CDR3 and the framework region between CDRs 1 and 2. These stretches form antiparallel β-hairpins within the internal 5-stranded β-sheet. There are a few principal inter-domain interactions that are conserved not only in the experimental set of 16 Fabs, but in all human antibodies. They include: 1) a bidentate hydrogen bond between L-Gln38 and H-Gln39; 2) H-Leu45 in a hydrophobic pocket between L-Phe98, L-Tyr87 and L-Pro44; 3) L-Pro44 stacked against H-Trp103; and 4) L-Ala43 opposite the face of H-Tyr91 (Fig. 8). With the exception of L-Ala43, all other residues are conserved in human germlines. Position 43 may be alternatively occupied by Ser, Val or Pro (as in L4-1), but the hydrophobic interaction with H-Tyr91 is preserved. These core interactions provide enough stability to the VH:VL dimer so that additional VH-VL contacts can tolerate amino acid sequence variations in CDRs H3 and L3 that form part of the VH:VL interface.   In total, about 20 residues are involved in the VH:VL interactions on each side (Fig. S5). Half of them are in the framework regions and those residues (except residue 61 in HC, which is actually in CDR2 in Kabat's definition) are conserved in the set of 16 Fabs. The side chain conformations of these conserved residues are also highly similar. One notable exception is H-Trp47, which exhibits 2 conformations of the indole ring. In most of the structures, it has the χ2 angle of ∼80°, while the ring is flipped over (χ2 = −100°) in H5-51:L3:11 and H5-51:L3-20. Interestingly, these are the only 2 structures with residues missing in CDR H3 because of disorder, although both structures are determined at high resolution and the rest of the structure is well defined. Apparently, residues flanking CDR H3 in the 2 VH:VL pairings are inconsistent with any stable conformation of CDR H3, which translates into a less restricted conformational space for some of them, including H-Trp47. VH:VL tilt angles The relative orientation of VH and VL has been measured in a number of different ways. Presented here are the results of 2 different approaches for determining the orientation of one domain relative to the other. The first approach uses ABangles, the results of which are shown in Table S2. The four LCs all are classified as Type A because they have a proline at position 44, and the results for each orientation parameter are within the range of values of this type reported by Dunbar and co-workers. In fact, the parameter values for the set of 16 Fabs are in the middle of the distribution observed for 351 non-redundant antibody structures determined at 3.0 Å resolution or better. The only exception is HC1, which is shifted toward smaller angles with the mean value of 70.8° as compared to the distribution centered at 72° for the entire PDB. This probably reflects the invariance of CDR H3 in the current set as opposed to the CDR H3 diversity in the PDB. The second approach used for comparing tilt angles involved computing the difference in the tilt angles between all pairs of structures. For structures with 2 copies of the Fab in the asymmetric unit, only one structure was used. The differences between independent Fabs in the same structure are 4.9° for H1-69:L3-20, 1.6° for H1-69:L3-11, 1.4° for H3-23:L4-1, 3.3° for H3-23:L3-11, and 2.5° for H5-51:L4-1. With the exception of H1-69:L3-20, the angles are within the range of 2-3° as are observed in the identical structures in the PDB. In H1-69:L3-20, one of the Fabs is substantially disordered so that part of CDR H2 (the outer β-strand, residues 55-60) is completely missing. This kind of disorder may compromise the integrity of the VH domain and its interaction with the VL. Indeed, this Fab has the largest twist angle HC2 within the experimental set that exceeds the mean value by 2.5 standard deviations (Table S2). An illustration of the difference in tilt angle for 2 pairs of variants by the superposition of the VH domains of (A) H1-69:L3-20 on that of H5-51:L1-39 (the VL domain is off by a rigid-body roatation of 10.5°) and (B) H1-69:L4-1 on that of H5-51:L1-39 (the VL domain is off by a rigid-body roatation of 1.6°). Differences in VH:VL tilt angles.  \tH1-69:L1-39\tH1-69:L3-11\tH1-69:L3-20\tH1-69:L4-1\tH3-23:L1-39\tH3-23:L3-11\tH3-23:L3-20\tH3-23:L4-1\tH3-53:L1-39\tH3-53:L3-11\tH3-53:L3-20\tH3-53:L4-1\tH5-51:L1-39\tH5-51:L3-11\tH5-51:L3-20\tH5-51:L4-1\t \tH1-69:L1-39\t0\t2.1\t8.9\t1.1\t4.2\t3.0\t9.5\t1.5\t3.3\t3.6\t3.1\t1.6\t1.8\t2.9\t2.4\t5.2\t \tH1-69:L3-11\t \t0\t7.3\t2.9\t2.5\t2.0\t8.4\t1.3\t2.6\t2.9\t3.2\t1.8\t3.9\t4.6\t4.4\t5.0\t \tH1-69:L3-20\t \t \t0\t9.2\t5.0\t8.7\t7.4\t7.6\t8.9\t8.6\t9.4\t7.9\t10.5\t10.1\t11.0\t9.7\t \tH1-69:L4-1\t \t \t \t0\t4.6\t3.9\t10.1\t1.8\t4.4\t4.7\t4.1\t2.3\t1.6\t2.5\t2.3\t6.2\t \tH3-23:L1-39\t \t \t \t \t0\t4.0\t8.0\t2.8\t4.8\t4.8\t5.4\t3.6\t6.0\t6.2\t6.6\t6.6\t \tH3-23:L3-11\t \t \t \t \t \t0\t9.3\t3.0\t2.1\t2.9\t3.3\t3.3\t4.6\t5.8\t5.0\t5.2\t \tH3-23:L3-20\t \t \t \t \t \t \t0\t8.9\t7.9\t7.0\t7.6\t7.9\t10.5\t9.7\t10.7\t6.2\t \tH3-23:L4-1\t \t \t \t \t \t \t \t0\t3.6\t3.8\t3.7\t1.5\t3.2\t3.7\t3.8\t5.6\t \tH3-53:L1-39\t \t \t \t \t \t \t \t \t0\t1.0\t1.6\t2.9\t4.6\t5.3\t4.8\t3.1\t \tH3-53:L3-11\t \t \t \t \t \t \t \t \t \t0\t1.3\t2.9\t4.8\t5.2\t5.0\t2.3\t \tH3-53:L3-20\t \t \t \t \t \t \t \t \t \t \t0\t2.5\t3.8\t4.2\t3.9\t2.2\t \tH3-53:L4-1\t \t \t \t \t \t \t \t \t \t \t \t0\t2.9\t3.0\t3.3\t4.2\t \tH5-51:L1-39\t \t \t \t \t \t \t \t \t \t \t \t \t0\t1.9\t0.6\t5.8\t \tH5-51:L3-11\t \t \t \t \t \t \t \t \t \t \t \t \t \t0\t1.9\t5.7\t \tH5-51:L3-20\t \t \t \t \t \t \t \t \t \t \t \t \t \t \t0\t5.8\t \tH5-51:L4-1\t \t \t \t \t \t \t \t \t \t \t \t \t \t \t \t0\t \t The differences in the tilt angle are shown for all pairs of V regions in Table 3. They range from 0.6° to 11.0°. The smallest differences in the tilt angle are between the Fabs in isomorphous crystal forms. The largest deviations in the tilt angle, up to 11.0°, are found for 2 structures, H1-69:L3-20 and H3-23:L3-20, that stand out from the other Fabs. One of the 2 structures, H1-69:L3-20, has its CDR H3 in the ‘extended’ conformation; the other structure has it in the ‘kinked’ conformation. Two examples illustrating large (10.5°) and small (1.6°) differences in the tilt angles are shown in Fig. 9.    VH:VL buried surface area and complementarity VH:VL surface areas and surface complementarity. Chain Pairs\tPDB\tContact surfaceVH (Å2)\tContact surfaceVL (Å2)\tInterface(Å2)\tSurface complementarity\t \tH1-69:L1-39\t5I15\t727\t771\t749\t0.743\t \tH1-69:L3-11\t5I16\t802\t870\t836\t0.762\t \tH1-69:L3-20\t5I17\t713\t736\t725\t0.723\t \tH1-69:L4-1\t5I18\t729\t736\t733\t0.734\t \tH3-23:L1-39\t5I19\t795\t817\t806\t0.722\t \tH3-23:L3-11\t5I1A\t822\t834\t828\t0.725\t \tH3-23:L3-20\t5I1C\t670\t698\t684\t0.676\t \tH3-23:L4-1\t5I1D\t743\t770\t757\t0.708\t \tH3-53:L1-39\t5I1E\t698\t719\t709\t0.712\t \tH3-53:L3-11\t5I1G\t747\t758\t753\t0.690\t \tH3-53:L3-20\t5I1H\t743\t735\t739\t0.687\t \tH3-53:L4-1\t5I1I\t689\t693\t691\t0.711\t \tH5-51:L1-39\t4KMT\t761\t808\t785\t0.728\t \tH5-51:L3-11\t5I1J\t648\t714\t681\t0.717\t \tH5-51:L3-20\t5I1K\t622\t643\t633\t0.740\t \tH5-51:L4-1\t5I1L\t790\t792\t791\t0.704\t \t Some side chain atoms in CDR H3 are missing. Residues in CDR H3 are missing: YGE in H5-51:L3-11, GIY in H5-51:L3-20. The results of the PISA contact surface calculation and surface complementarity calculation are shown in Table 4. The interface areas are calculated as the average of the VH and VL contact surfaces. Six of the 16 structures have CDR H3 side chains or complete residues missing, and therefore their interfaces are much smaller than in the other 10 structures with complete CDRs (the results are provided for all Fabs for completeness). Among the complete structures, the interface areas range from 684 to 836 Å2. Interestingly, the 2 structures that have the largest tilt angle differences with the other variants, H3-23:L3-20 and H1-69:L3-20, have the smallest VH:VL interfaces, 684 and 725 Å2, respectively. H3-23:L3-20 is also unique in that it has the lowest value (0.676) of surface complementarity.   Stability of germline pairings Melting temperatures for the 16 Fabs.  \tL3-20\tL4-1\tL3-11\tL1-39\tHC average\t \tH1-69\t73.6\t74.8\t75.6\t80.3\t76.1\t \tH3-23\t74.8\t75.2\t4.8\t81.5\t76.6\t \tH3-53\t68.4\t68.0\t71.5\t73.9\t70.5\t \tH5-51\t68.4\t68.4\t71.9\t77.0\t71.4\t \tLC average\t71.3\t71.6\t73.5\t78.2\t \t \t Colors: blue (Tm \u003c 70°C), green (70°C \u003c Tm \u003c 73°C), yellow (73°C \u003c Tm \u003c 78°C), orange (Tm \u003e 78°C). Melting temperatures (Tm) were measured for all Fabs using differential scanning calorimetry (Table 5). It appears that for each given LC, the Fabs with germlines H1-69 and H3-23 are substantially more stable than those with germlines H3-53 and H5-51. In addition, L1-39 provides a much higher degree of stabilization than the other 3 LC germlines when combined with any of the HCs. As a result, the Tm for pairs H1-69:L1-39 and H3-23:L1-39 is 12-13° higher than for pairs H3-53:L3-20, H3-53:L4-1, H5-51:L3-20 and H5-51:L4-1.   These findings correlate well with the degree of conformational disorder observed in the crystal structures. Parts of CDR H3 main chain are completely disordered, and were not modeled in Fabs H5-51:L3-20 and H5-51:L3-11 that have the lowest Tms in the set. No electron density is observed for a number of side chains in CDRs H3 and L3 in all Fabs with germline H3-53, which indicates loose packing of the variable domains. All those molecules are relatively unstable, as is reflected in their low Tms. Discussion This is the first report of a systematic structural investigation of a phage germline library. The 16 Fab structures offer a unique look at all pairings of 4 different HCs (H1-69, H3-23, H3-53, and H5-51) and 4 different LCs (L1-39, L3-11, L3-20 and L4-1), all with the same CDR H3. The structural data set taken as a whole provides insight into how the backbone conformations of the CDRs of a specific heavy or light chain vary when it is paired with 4 different light or heavy chains, respectively. A large variability in the CDR conformations for the sets of HCs and LCs is observed. In some cases the CDR conformations for all members of a set are virtually identical, for others subtle changes occur in a few members of a set, and in some cases larger deviations are observed within a set. The five variants that crystallized with 2 copies of the Fab in the asymmetric unit serve somewhat as controls for the influence of crystal packing on the conformations of the CDRs. In four of the 5 structures the CDR conformations are consistent. In only one case, that of H1-69:L3-20 (the lowest resolution structure), do we see differences in the conformations of the 2 copies of CDRs H1 and L1. This variability is likely a result of 2 factors, crystal packing interactions and internal instability of the variable domain. For the CDRs with canonical structures, the largest changes in conformation occur for CDR H1 of H1-69 and H3-53. The other 2 HCs, H3-23 and H5-51, have canonical structures that are remarkably well conserved (Fig. 1). Of the 4 HCs, H1-69 has the greatest number of canonical structure assignments (Table 2). H1-69 is unique in having a pair of glycine residues at positions 26 and 27, which provide more conformational freedom in CDR H1. Besides IGHV1-69, only the germlines of the VH4 family possess double glycines in CDR H1, and it will be interesting to see if they are also conformationally unstable. Having all 16 VH:VL pairs with the same CDR H3 provides some insights into why molecular modeling efforts of CDR H3 have proven so difficult. As mentioned in the Results section, this data set is composed of 21 Fabs, since 5 of the 16 variants have 2 Fab copies in the asymmetric unit. For the 18 Fabs with complete backbone atoms for CDR H3, 10 have conformations similar to that of the parent, while the others have significantly different conformations (Fig. 6). Thus, it is likely that the CDR H3 conformation is dependent upon 2 dominating factors: 1) amino acid sequence; and 2) VH and VL context. More than half of the variants retain the conformation of the parent despite having differences in the VH:VL pairing. This subset includes 2 structures with 2 copies of the Fab in the asymmetric unit, all of which are nearly identical in conformation. This provides an internal control showing a consistency in the conformations. The remaining 8 structures exhibit “non-parental” conformations, indicating that the VH and VL context can also be a dominating factor influencing CDR H3. Importantly, there are 5 distinctive conformations in this subset. This subset also has 2 structures with 2 Fab copies in the asymmetric unit. Each pair has nearly identical conformations providing an internal check on the consistency of the conformations. Interestingly, as described earlier, these 2 pairs differ in the stem regions with the H1-69:L3-20 pair in the ‘extended’ conformation and H5-51:L4-1 pair in the ‘kinked’ conformation. The conformations are different from each other, as well as from the parent. The CDR H3 conformational analysis shows that, for each set of variants of one HC paired with the 4 different LCs, both “parental” and “non-parental” conformations are observed. The same variability is observed for the sets of variants composed of one LC paired with each of the 4 HCs. Thus, no patterns of conformational preference for a particular HC or LC emerge to shed any direct light on what drives the conformational differences. This finding supports the hypothesis of Weitzner et al. that the H3 conformation is controlled both by its sequence and its environment. In looking at a possible correlation between the tilt angle and the conformation of CDR H3, no clear trends are observed. Two variants, H1-69:L3-20 and H3-23:L3-20, have the largest differences in the tilt angles compared to other variants as seen in Table 3. The absolute VH:VL orientation parameters for the 2 Fabs (Table S2) show significant deviation in HL, LC1 and HC2 values (2-3 standard deviations from the mean). One of the variants, H3-23:L3-20, has the CDR H3 conformation similar to the parent, but the other, H1-69:L3-20, is different. As noted in the Results section, the 2 variants, H1-69:L3-20 and H3-23:L3-20, are outliers in terms of the tilt angle; at the same time, both have the smallest VH:VL interface. These smaller interfaces may perhaps translate to a significant deviation in how VH is oriented relative to VL than the other variants. These deviations from the other variants can also be seen to some extent in VH:VL orientation parameters in Table S2, as well as in the smaller number of residues involved in the VH:VL interfaces of these 2 variants (Fig. S5). These differences undoubtedly influence the conformation of the CDRs, in particular CDR H1 (Fig. 1A) and CDR L1 (Fig. 3C), especially with the tandem glycines and multiple serines present, respectively. Pairing of different germlines yields antibodies with various degrees of stability. As indicated by the melting temperatures, germlines H1-69 and H3-23 for HC and germline L1-39 for LC produce more stable Fabs compared to the other germlines in the experimental set. Structural determinants of the differential stability are not always easy to decipher. One possible explanation of the clear preference of LC germline L1-39 is that CDR L3 has smaller residues at positions 91 and 94, allowing for more room to accommodate CDR H3. Other germlines have bulky residues, Tyr, Arg and Trp, at these positions, whereas L1-39 has Ser and Thr. Various combinations of germline sequences for VL and VH impose certain constraints on CDR H3, which has to adapt to the environment. A more compact CDR L3 may be beneficial in this situation. At the other end of the stability range is LC germline L3-20, which yields antibodies with the lowest Tms. While pairings with H3-53 and H5-51 may be safely called a mismatch, those with H1-69 and H3-23 have Tms about 5-6° higher. Curiously, the 2 Fabs, H1-69:L3-20 and H3-23:L3-20, deviate markedly in their tilt angles from the rest of the panel. It is possible that by adopting extreme tilt angles the structure modulates CDR H3 and its environment, which apparently cannot be achieved solely by conformational rearrangement of the CDR. Note that most of the VH:VL interface residues are invariant; therefore, significant change of the tilt angle must come with a penalty in free energy. Yet, for the 2 antibodies, the total gain in stability merits the domain repacking. Overall, the stability of the Fab, as measured by Tm, is a result of the mutual adjustment of the HC and LC variable domains and adjustment of CDR H3 to the VH:VL cleft. The final conformation represents an energetic minimum; however, in most cases it is very shallow, so that a single mutation can cause a dramatic rearrangement of the structure. In summary, the analysis of this structural library of germline variants composed of all pairs of 4 HCs and 4LCs, all with the same CDR H3, offers some unique insights into antibody structure and how pairing and sequence may influence, or not, the canonical structures of the L1, L2, L3, H1 and H2 CDRs. Comparison of the CDR H3s reveals a large set of variants with conformations similar to the parent, while a second set has significant conformational variability, indicating that both the sequence and the structural context define the CDR H3 conformation. Quite unexpectedly, 2 of the variants, H1-69:L3-20 and H3-53:L4-1, have the ‘extended’ stem region differing from the other 14 that have a ‘kinked’ stem region. Why this is the case is unclear at present. These data reveal the difficulty of modeling CDR H3 accurately, as shown again in Antibody Modeling Assessment II. Furthermore, antibody CDRs, H3 in particular, may go through conformational changes upon binding their targets, making structural prediction for docking purposes an even more difficult task. Fortunately, for most applications of antibody modeling, such as engineering affinity and biophysical properties, an accurate CDR H3 structure is not always necessary. For those applications where accurate CDR structures are essential, such as docking, the results in this work demonstrate the importance of experimental structures. With the recent advances in expression and crystallization methods, Fab structures can be obtained rapidly. The set of 16 germline Fab structures offers a unique dataset to facilitate software development for antibody modeling. The results essentially support the underlying idea of canonical structures, indicating that most CDRs with germline sequences tend to adopt predefined conformations. From this point of view, a novel approach to design combinatorial antibody libraries would be to cover the range of CDR conformations that may not necessarily coincide with the germline usage in the human repertoire. This would insure more structural diversity, leading to a more diverse panel of antibodies that would bind to a broad spectrum of targets. Materials and methods Fab production, purification and crystallization The production, purification and crystallization of the Fabs reported in this article were described previously. Briefly, the 16 Fabs were produced by combining 4 different HC and 4 different LC germline constructs. The human HC germlines were IGHV1-69 (H1-69), IGHV3-23 (H3-23), IGHV3-53 (H3-53) and IGHV5-51 (H5-51) in the IMGT nomenclature. The human LC germlines were IGKV1-39 (L1-39), IGKV3-11 (L3-11), IGKV3-20 (L3-20) and IGKV4-1 (L4-1) corresponding to O12, L6, A27 and B3 in the V-BASE nomenclature. CDR H3 of the anti-CCL2 antibody CNTO 888 with the amino acid sequence ARYDGIYGELDF  was used in all Fab constructs. The J region genes were IGHJ1 for the HC and IGKJ1 for the LC for all Fabs. Human IgG1 and κ constant regions were used in all Fab constructs. A 6xHis tag was added to the C-terminus of the HC to facilitate purification. The Fabs were expressed in HEK 293E cells and purified by affinity and size-exclusion chromatography. For crystallization, the Fabs were dialyzed into 20 mM Tris buffer, pH 7.4, with 50 mM NaCl and concentrated to 12-18 mg/mL. Automated crystallization screening was carried out using the vapor diffusion method at 20°C with an Oryx4 (Douglas Instruments) or a Mosquito (TTP Labtech) crystallization robot in a sitting drop format using Corning 3550 plates. Initial screening was carried out with an in-house 192-well screen optimized for Fab crystallization and the Hampton 96-well Crystal Screen HT (Hampton Research). For the majority of the Fabs, the crystallization protocol employed microseed matrix screening using self-seeding or cross-seeding approaches. A summary of the final crystallization conditions for each of the Fabs is presented in Table 1. X-ray data collection For 13 of the Fab crystals, X-ray data collection was carried out at Janssen Research and Development, LLC using a Rigaku MicroMax™-007HF microfocus X-ray generator equipped with a Saturn 944 CCD detector and an X-stream™ 2000 cryocooling system (Rigaku), and for the remaining 3, X-ray data collection was carried out at the Advanced Photon Source (APS) synchrotron at Argonne National Laboratory using the IMCA 17-ID beamline with a Pilatus 6M detector. For X-ray data collection, the Fab crystals were soaked for a few seconds in a cryo-protectant solution containing the corresponding mother liquor supplemented with 17-25% glycerol (Table S1). The crystals for which data were collected in-house were flash cooled in the stream of nitrogen at 100 K. Crystals sent to the APS were flash cooled in liquid nitrogen prior to shipping them to the synchrotron. Diffraction data for all variants were processed with the program XDS. X-ray data statistics are given in Table 1. Structure determination A summary of the methods used in the structure solution and refinement of the 16 Fabs is presented in Table S1. Twelve of the structures were solved by molecular replacement with Phaser using different combinations of search models for the VH, VL and constant domains. Four of the structures, H3-53:L1-39, H3-53:L3-11, H5-51:L1-39 and H5-51:L3-11, were solved by direct replacement followed by rigid body refinement with REFMAC. All structures were refined using REFMAC. Model adjustments were carried out using the program Coot. The refinement statistics are given in Table 1. Other crystallographic calculations were performed with the CCP4 suite of programs. The structural figures were prepared using the PyMOL Molecular Graphics System, Version 1.0 (Schrödinger, LLC). Structural analysis The canonical structure assignments (Table 2) were made using PyIgClassify, an online canonical structure classification tool (http://dunbrack2.fccc.edu/pyigclassify/) that uses the rules set forth by Dunbrack and coworkers. The conformational variability within the CDRs was assessed by calculating the root-mean-square deviation (rmsd) from the average structure that was generated after superposition of all structures of the set using the main-chain atoms of the CDR in question. The rmsd was calculated for all main-chain atoms (N, CA, C, O) of the CDR. The contact surface areas of the VH and VL domains at the VH:VL inteface were computed with the CCP4 program PISA. The surface complementarity of the VH and VL domains was computed using the CCP4 program SC. VH:VL tilt angles The orientation of the VH domain with respect to the VL domain was assessed using 2 different approaches. The first approach calculates the 6 VH:VL orientation parameters that describe the VH:VL relationship according to Dunbar and co-workers using a script downloaded from the website (http://opig.stats.ox.ac.uk/webapps/abangle). The six parameters include 5 angles, HL, H1, H2, L1 and L2, and a distance, dc. These parameters are derived by first defining 2 planes, one for each domain, based on core residues in the domains. The distance between the planes, dc, is determined along a vector between the planes that is used to establish a consistent coordinate system. The torsion angle between the domains, HL, is much like the VH:VL packing angle defined by Abhinandan and Martin. The tilt of one domain relative to the other is defined by the HC1 and LC1 angles, and the twist of one domain relative to the other is defined by the HC2 and LC2 angles. The second approach calculates the difference in the tilt angle between pairs of Fvs, which reflects the relative orientation between the VH and VL domains. The difference with respect to the reference structure is calculated by sequential root-mean-square superposition of the VL and VH domains using β-sheet core Cα positions (Chothia numbering scheme): 3–13, 18–25, 33–38, 43–49, 61–67, 70–76, 85–90, 97–103 for VL; 3–7, 18–24, 34–40, 44–51, 56–59, 67–72, 77–82a, 87–94, 102–110 for VH. The κ angle in the spherical polar angular system (ω, ϕ, κ) of the latter transformation is the difference in the tilt angle. Differential scanning calorimetry DSC experiments were performed on a VP-capillary DSC system (MicroCal Inc., Northampton, MA) in which temperature differences between the reference and sample cell are continuously measured and calibrated to power units. Samples were heated from 10°C to 95°C at a heating rate of 60°C/hour. The pre-scan time was 15 minutes and the filtering period was 10 seconds. The concentration used in the DSC experiments was about 0.4 mg/mL in phosphate-buffered saline. Analysis of the resulting thermograms was performed using MicroCal Origin 7 software. Melting temperature of proteins was determined by deconvolution of the DSC scans using non-2 state model in the MicroCal Origin 7 software. Scans were deconvoluted using a non-2 state model with either 1-step transition or 2-step transition depending on the number of resolved peaks observed in a scan. Accession numbers Atomic coordinates and structure factors have been deposited in the Protein Data Bank with accession numbers 4KMT, 5I15, 5I16, 5I17, 5I18, 5I19, 5I1A, 5I1C, 5I1D, 5I1E, 5I1G, 5I1H, 5I1I, 5I1J, 5I1K and 5I1L. Supplementary Material Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed. 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Structures and models De novo selection of high-affinity antibodies from synthetic fab libraries displayed on phage as pIX fusion proteins Analysis of heavy and light chain pairings indicates that receptor editing shapes the human antibody repertoire Structural basis for high selectivity of anti-CCL2 neutralizing antibody CNTO 888 Protein crystallization with microseed matrix screening: application to human germline antibody Fabs Framework residue-71 is a major determinant of the position and conformation of the 2nd hypervariable region in the VH domains of immunoglobulins Modeling the anti-CEA antibody combining site by homology and conformational search Major antigen-induced domain rearrangements in an antibody Energy-based analysis and prediction of the orientation between light- and heavy-chain antibody variable domains Analysis and prediction of VH/VL packing in antibodies ABangle: characterising the VH-VL orientation in antibodies Inference of macromolecular assemblies from crystalline state Shape complementarity at protein/protein interfaces Structural evidence for induced fit as a mechanism for antibody-antigen recognition Nomenclature of the human immunoglobulin genes  Two routes for production and purification of Fab fragments in biopharmaceutical discovery research: papain digestion of mAb and transient expression in mammalian cells An automated microseed matrix-screening method for protein crystallization Promoting crystallization of antibody-antigen complexes via microseed matrix screening XDS Phaser crystallographic software REFMAC5 for the refinement of macromolecular crystal structures Features and development of Coot Overview of the CCP4 suite and current 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