# PROFESSIONAL RESUME

# Edward A. Berry

ADDRESS Ernest Orlando Lawrence Berkeley National Laboratory

Physical Biosciences Division, MailStop 64-R121

1 Cyclotron Road

Berkeley, CA 94720-8118

TITLE Staff Scientist

TELEPHONE +1-510-486-4335

EMAIL EABerry@LBL.gov

HTTP: http://sb20.lbl.gov/cytbc1

**A. EDUCATION/TRAINING**

[INSTITUTION AND LOCATION DEGREE YEAR(s) FIELD OF STUDY]{.underline}

College of Charleston, S.C. B.S. 1974 Biology

Cornell University Ph.D. 1981 Biochemistry

Dartmouth Medical School Postdoctoral 1981-1984 Biochemistry

Univ. of Illinois (Urbana-Champaign) Postdoctoral 1984-1987 Biophysics

**B. POSITIONS AND HONORS.**

#### Positions and Employment

1987 -- present Staff Scientist II, Lawrence Berkeley Laboratory,
University of California at Berkeley.

**[Honors]{.underline}**

2007 (-2009) Selected Mentor, Pew Latin Postdoctoral Fellow Julio Lenin
Domínguez-Ramírez

Feb. 2006 Co-chair, platform session on electron transport, Biophysical
Society Annual meeting,\
Salt Lake City, Utah, USA, Feb 18-24 2006.

2006-2009 Elected Council member, Biophysical Society Bioenergetics
subcommittee

April 2006 Outside thesis committee member, Univ. of Illinois/U-C, Cesar
Luna-Chavez

Dec 2005 Invited speaker at Bioenergetics Symposium, Bari Italy 17-22
December 2005

June 2005 Invited speaker at Gordon Research Conference on cellular
bioenergetics

Mar 10 2005 NIH Study Section Member, Special Emphasis Panel/Scientific
Review Groups 2005/05 ZRG1 BCMB-B (02/03) (M)

July 16 2004 NIH Study Section Member, Special Emphasis Panel/Initial
Review Group 2004/10 ZRG1 BPC-B (02) (M),

Feb. 2004 Organizer and co-chair of Biophysical Society Bioenergetics
Subgroup Symposium \"Structural Biology Of Photosynthesis\" February
14-18, 2004 Baltimore, Maryland, USA

August 2003 Invited speaker at Nobel Symposium 126 \"Membrane Proteins:
Structure, Functions, And Assembly\" August 22-24, Friiberghs Herrgård,
Sweden

Nov-Dec 2002 Recipient of Fellowship from French Ministry of Youth,
Education, and Research for investigations at the Institut de Biologie
Physico-Chimique, Paris France

June 2001 Thesis examiner, Uppsala University, for Momi Iwata\'s thesis
defense

Sept 9-14 2000 Organizer and Chairperson of European Bioenergetics
Congress Symposium \"Cytochrome bc complexes\" Brighton, UK.

Feb. 12, 2000 Organizer and co-chair of Biophysical Society
Bioenergetics Subgroup Symposium \"Three-dimensional structure
determination: Cytochrome bc1 and b6f complexes\" New Orleans,
Louisiana, USA

June 17-28, 1998 Instructor at EMBO Practical course \"Current Methods
in Membrane Protein Research\", EMBL, Heidelberg

**\
C. Selected peer-reviewed publications (in chronological order).**

1\. Berry, E.A. and Hinkle, P.C. (1983) Measurement of the
Electrochemical Proton Gradient in Submito-chondrial Particles. **J.
Biol. Chem., 258**, 1474-1486.

2\. Berry, E.A. and Trumpower, B.L. (1985) Pathways of Electrons and
Protons Through the Cytochrome bc1 complex of the Mitochondrial
Respiratory Chain. In \"**Coenzyme Q**\" (G. Lenaz, Ed.), Wiley & Sons,
365-389.

3\. Berry, E.A. and Trumpower, B.L. (1985) Isolation of Ubiquinol
Oxidase from *Paracoccus denitrificans* and Resolution into Cytochrome
bc1 and Cytochrome c-aa3 Complexes. **J. Biol. Chem. 260**, 2458-2467.

4\. Berry, E.A. and Trumpower, B.L. (1987) Simultaneous Determination of
Hemes a, b, and c from Pyridine Hemochrome Spectra. **Anal. Biochem.
161**, 1-15

5\. Crofts, A., Robinson, H., Andrews, K., van Doren, S., and Berry, E.
(1988) Catalytic Sites for Reduction and Oxidation of Quinones. In
**Cytochrome Systems**, (Papa,S. et al. eds.) Plenum Press, N.Y. pp.
617-624.

6\. Huang, L.-s. and Berry, E.A.(1990) Purification and Characterization
of the Proton Translocating Plasma Membrane ATPase of Red Beet Storage
Tissue. **Biochim. Biophys. Acta 1039**, 241-252.

7\. Berry, E.A, Huang, L.-s. and DeRose, V. (1991) Ubiquinol-Cytochrome
c Oxidoreductase of Higher Plants. Isolation and Characterization of the
bc1 Complex from Potato Tuber Mitochondria. **J. Biol. Chem. 266**,
9064-9077.

8\. Berry, E.A. , Huang, L.-S., Earnest, T.N. and Jap, B.K.(1992) X-ray
Diffraction by Crystals of Beef Heart Ubiquinol:Cytochrome c
Oxidoreductase. **J. Mol. Biol. 224**, 1161-1166

9\. Garcia-Horsman, J.A., Berry, E., Shapleigh, J.P., Alben, J.O., and
Gennis, R.B. (1994) A Novel Cytochrome c Oxidase from Rhodobacter
sphaeroides that Lacks CuA. **Biochemistry 33,** 3113-3119.

10\. Berry E.A.; Shulmeister VM; Huang LS; Kim SH. (1995) A new crystal
form of bovine heart ubiquinol:cytochrome c oxidoreductase -
determination of space group and unit-cell parameters. **Acta
Crystallographica D:** **51**, 235-239.

11\. Zhang, Z., Huang, L.-S., Shulmeister, V.M., Chi, Y.I., Kim, K.K.,
Hung, L.-W., Crofts, A.R., Berry, E.A., and Kim, S.-H. (1998) Electron
transfer by domain movement in cytochrome bc1. **Nature 392**, 677-684.

12\. Crofts AR, Berry EA**. (**1998**)** Structure and function of the
cytochrome bc~1~ complex of mitochondria and photosynthetic bacteria.
**Curr. Opin. Struct. Biol. 8,** 501-509

13\. Crofts AR, Hong S, Ugulava N, Barquera B, Gennis R, Guergova-Kuras
M, Berry EA (1999) Pathways for proton release during ubihydroquinone
oxidation by the bc(1) complex. **Proc Natl Acad Sci U S A 96**,
10021-10026

14\. Berry E.A , Zhang Z.,, Huang L.S, and Kim S.H.(1999) Structures of
Quinone binding sites in bc complexes: Functional implications
**Biochem. Soc. Transactions 27**, 565-572.

15\. Berry E.A,, Huang L.S, Zhang Z., and Kim S.H.(1999) The Structure
of the Avian Mitochondrial Cytochrome bc~1~ Complex. **J. Bioen.
Biomemb. 31**, 177-190.

16\. Crofts AR, Hong S, Zhang Z and Berry EA (1999) Physicochemical
aspects of the movement of the Rieske iron sulfur protein during quinol
oxidation by the *bc*~1~ complex from mitochondria and photosynthetic
bacteria. **Biochemistry 38**; 15827-15839.

17\. Horvath A, Berry EA, Maslov DA (2000) Translation of the edited
mRNA for cytochrome b in trypanosome mitochondria. **Science 287**,
1639-40

18\. McFadden DC, Tomavo S, Berry EA, Boothroyd JC (2000)
Characterization of cytochrome b from *Toxoplasma gondii* and Q(o)
domain mutations as a mechanism of atovaquone-resistance. **Mol Biochem
Parasitol 108**(1):1-12

19\. Chi Y-I, Huang L-S, Zhang Z, Fernández-Velasco JG and Berry EA
(2000) X-Ray Structure of a Truncated Form of Cytochrome *f* from
*Chlamydomonas reinhardtii.* **Biochemistry 39**:7689-701

20\. Edward A. Berry, E.A., Zhang, Z., Bellamy, H.D., and Huang, L.-S.
(2000) Crystallographic location of two Zn^2+^-binding sites in the
avian cytochrome bc~1~ complex. **Biochimica et Biophysica Acta**
**1459**, 440-448

21\. Berry EA, Guergova-Kuras M, Huang L.-S., Crofts AR (2000) Structure
And Function Of Cytochrome bc Complexes. **Annu Rev Biochem
69**:1005-1075

22\. Horvath A, Berry EA, Huang L.-S., Maslov D.A. (2000) Leishmania
tarentolae: A Parallel Isolation of Cytochrome bc(1) and Cytochrome c
Oxidase. **Exp Parasitol 96**(3):160-167

23\. Lee SY, Cho HS, Pelton JG, Yan D, Henderson RK, King DS, Huang L,
Kustu S, Berry EA, Wemmer DE. (2001) Crystal structure of an activated
response regulator bound to its target. **Nat Struct Biol 8**:52-56

24\. Meshnick S R, Berry E A, Nett J, Kazanjian P, Trumpower B.(2001)
The interaction of atovaquone with the *P. carinii* cytochrome
***bc~1~*** complex. **J Eukaryot Microbiol 2001;Suppl**:169S-171S .

25\. Cobessi D, Huang LS, Ban M, Pon NG, Daldal F, Berry EA. (2002) The
2.6 A resolution structure of Rhodobacter capsulatus bacterioferritin
with metal-free dinuclear site and heme iron in a crystallographic
\'special position\'. **Acta Crystallogr D Biol Crystallogr 58**(Pt
1):29-38

26\. Huang, L.-S., Cobessi, D., and Berry, E.A. (2003) Crystallization
of the Cytochrome bc1 complex. in \"**Methods and Results in Membrane
Protein Crystallization**\" (S. Iwata, Ed) pp. 203-226, IUL press, La
Jolla.

27\. Popot, J.-L., Berry, E.A., Charvolin, D., Creuzenet, C., Ebel, C,
Engelman, D.M., Flötenmeyer, M., Giusti, F., Gohon, Y., Hervé, P., Hong,
Q., Lakey. J.H., Leonard. K.,. Shuman, H.A., Timmins, P, Warschawski,
D.E., Zito, F., Zoonens,M., Pucci, B. and Tribet, C. (2003) Amphipols:
polymeric surfactants for membrane biology research. **Cell. Mol. Life
Sci. 60**, 1559-74

28\. Kolling, D.R.J., Samoilova, R.I., Holland, J. T., Berry, E.A.,
Dikanov, S.A. , and Crofts,A.R. (2003) Exploration of ligands to the
Qi-site semiquinone in the bc1 complex using high resolution EPR. **J.
Biol. Chem. 278**:39747-54

29\. Berry E.A. and Huang L.S. (2003) Observations concerning the quinol
oxidation site of the cytochrome bc1 complex. **FEBS Lett 555**: 13-20

30\. Bowman, M.K., Berry, E.A., Roberts,A.G., and Kramer, D.M. (2004)
Orientation of the g-Factor Axes of the Rieske Subunit in Cytochrome bc1
Complex **Biochemistry 43**:430-436.

31\. Berry E.A., Huang L.-S., Saechao L.K., Pon N.G., Valkova-Valchanova
M. and Daldal F. (2004) X-Ray Structure of Rhodobacter Capsulatus
Cytochrome bc1: Comparison with its Mitochondrial and Chloroplast
Counterparts. **Photosynthesis Research 81**: 251-275

32\. Huang, L.-S., Borders, T. M., Shen, J. T., Wang, C.-J., and Berry,
E. A. (2005) Crystallization of Mitochondrial Respiratory Complex II
from Chicken Heart: a Membrane Protein Complex Diffracting to 2.0 Å.
**Biological Cryst.** (Acta Cryst.) **D61**, 380-387.

33\. Huang, L.-S., Cobessi, D., Tung, E.Y., Berry, E.A.(2005) Binding Of
The Respiratory Chain Inhibitor Antimycin To The Mitochondrial *bc~1~*
Complex: A New Crystal Structure Reveals An Altered Intramolecular
Hydrogen-Bonding Pattern. **J. Mol. Biol. 351**, 573-97

34\. Huang, L.-S., Sun, G., Cobessi, D., Wang, A., Shen, J.T., Tung,
E.Y., Anderson,V.E., Berry, E.A. (2006) 3-Nitropropionic acid is a
suicide inhibitor of mitochondrial respiration that, upon oxidation by
Complex II, forms a covalent adduct with a catalytic-base arginine in
the active site of the enzyme. **J. Biol. Chem. 281**, 5965-5972.

35\. Huang,L.-S., Shen,J.T., Wang,A.C., Berry,E.A. (2006)
Crystallographic studies of the binding of ligands to the dicarboxylate
site of Complex II, and the identity of the ligand in the
\"oxalacetate-inhibited\" state. **Biophys. Biochim. Acta -
Bioenergetics** **1757** 1073--1083

36\. Devanathan S., Salamon Z., Tollin G., Fitch J. C., Meyer T. E.,
Berry E. A., and, and Cusanovich M. A. (2007) Plasmon Waveguide
Resonance Spectroscopic Evidence for Differential Binding of Oxidized
and Reduced Rhodobacter capsulatus Cytochrome c~2~ to the Cytochrome
bc~1~ Complex Mediated by the Conformation of the Rieske Iron-Sulfur
Protein. **Biochemistry**;46(24):7138-45.

37\. Giachini,L., Francia, F, Veronesi, G, Lee,D-W, Daldal, F., Huang,
L.-S., Berry, E.A., Cocco, T., Papa, S., Federico Boscherini
[׀׀]{dir="rtl"}, F., Venturoli, G. (2007) X-ray absorption studies of
Zn^2+^ binding sites in bacterial, avian and bovine cytochrome bc1
complexes. **Biophys. J.** (In Press; published on June 15, 2007 as
doi:10.1529/biophysj.107.110957)

38\. Berry, EA, Lee,D-W, Huang, L.-S., Daldal, F. (2007) Structural and
Mutational Studies of the Cytochrome bc~1~ Complexes in **The Purple
Photosynthetic Bacteria** (Hunter NC, Daldal F, Thurnauer MC, and Beatty
TJ, eds) (Invited paper).

**D. Structures solved and deposited with the PDB.**

Reso- Number

##### PDB ID Date lution of Reflns Rcryst Rfree 

1bcc 23-Mar-98 3.16 107167 0.27 0.31\
Cytochrome bc1 Complex From Chicken

2bcc 18-Sep-98 3.50 80760 0.284 0.317\
Stigmatellin-Bound Cytochrome bc~1~ Complex From Chicken

3bcc 23-Mar-98 3.70 71026 0.289 0.321\
Stigmatellin And Antimycin Bound Cytochrome bc1 Complex From Chicken

1cfm 18-Sep-98 2.00 46907 0.214 0.271\
Cytochrome f From Chlamydomonas Reinhardtii

1jgc 24-Jun-01 2.60 22526 0.225 0.242\
The 2.6 A Structure Resolution Of Rhodobacter Capsulatus
Bacterioferritin With Metal-Free Dinuclear Site And Heme Iron In A
Crystallographic Special Position

1pp9 16-Jun-03 2.10 305496 0.250 0.287\
Bovine Cytochrome bc1 Complex With Stigmatellin Bound

1ppj 16-Jun-03 2.10 285060 0.224 0.260\
Bovine Cytochrome bc1 Complex With Stigmatellin And Antimycin

1yq3 01-Feb-05 2.20 78719 0.175 0.223\
Avian Respiratory Complex II With Oxaloacetate And Ubiquinone

1yq4 01-Feb-05 2.33 68868 0.202 0.252\
Avian Respiratory Complex II With 3-Nitropropionate And Ubiquinone

1zrt 22-May-05 3.50 33265 0.300 0.358\
*Rhodobacter capsulatus* Cytochrome bc1 Complex With Stigmatellin Bound

2a06 16-Jun-05 2.10 276810 0.222 0.258\
Bovine Cytochrome bc1 Complex With Stigmatellin Bound

2fbw 10-Dec-05 2.10 162208 0.187 0.227\
Avian Respiratory Complex II With Carboxin Bound

2h88 06-Jun-06 1.74 291095 0.178 0.206\
Avian Mitochondrial Respiratory Complex II At 1.8 Angstrom Resolution

2h89 06-Jun-06 2.40 59635 0.226 0.279\
Avian Respiratory Complex II With Malonate Bound

**E. Recent publication highlights**

Berry E.A. and Huang L.S. (2003) Observations concerning the quinol
oxidation site of the cytochrome bc1 complex. **FEBS Lett 555**: 13-20

> **Abstract:** A direct hydrogen bond between ubiquinone/quinol bound
> at the QO site and a cluster-ligand histidine of the iron-sulfur
> protein (ISP) is described as a major determining factor explaining
> much experimental data on position of the ISP ectodomain, electron
> paramagnetic resonance (EPR) lineshape and midpoint potential of the
> iron-sulfur cluster, and the mechanism of the bifurcated electron
> transfer from ubiquinol to the high and low potential chains of the
> bc1 complex.

Berry E.A., Huang L.-S., Saechao L.K., Pon N.G., Valkova-Valchanova M.
and Daldal F. (2004) X-Ray Structure of Rhodobacter Capsulatus
Cytochrome bc1: Comparison with its Mitochondrial and Chloroplast
Counterparts. **Photosynthesis Research 81**: 251-275

> **Abstract:** Ubihydroquinone: cytochrome (cyt)c oxidoreductase, or
> cyt bc~1~, is a widespread, membrane integral enzyme that plays a
> crucial role during photosynthesis and respiration. It is one of the
> major contributors of the electrochemical proton gradient, which is
> subsequently used for ATP synthesis. The simplest form of the cyt
> bc~1~ is found in bacteria, and it contains only the three
> ubiquitously conserved catalytic subunits: the Fe-S protein, cyt b and
> cyt c~1~. Here we present a preliminary X-ray structure of Rhodobacter
> capsulatus cyt bc~1~ at 3.8 A and compare it to the available
> structures of its homologues from mitochondria and chloroplast. Using
> the bacterial enzyme structure, we highlight the structural
> similarities and differences that are found among the three catalytic
> subunits between the members of this family of enzymes. In addition,
> we discuss the locations of currently known critical mutations, and
> their implications in terms of the cyt bc~1~ catalysis.

Huang, L.-S., Borders, T. M., Shen, J. T., Wang, C.-J., and Berry, E. A.
(2005) Crystallization of Mitochondrial Respiratory Complex II from
Chicken Heart: a Membrane Protein Complex Diffracting to 2.0 Å.
**Biological Cryst. (Acta Cryst.) D61**, 380-387.

> **Abstract:** A procedure is presented for preparation of
> diffraction-quality crystals of a vertebrate mitochondrial respiratory
> complex II. The crystals have the potential to diffract to at least
> 2.0 A with optimization of post-crystal-growth treatment and
> cryoprotection. This should allow determination of the structure of
> this important and medically relevant membrane-protein complex at
> near-atomic resolution and provide great detail of the mode of binding
> of substrates and inhibitors at the two substrate-binding sites.

Huang, L.-S., Cobessi, D., Tung, E.Y., Berry, E.A. (2005) Binding Of The
Respiratory Chain Inhibitor Antimycin To The Mitochondrial bc1 Complex:
A New Crystal Structure Reveals An Altered Intramolecular
Hydrogen-Bonding Pattern. **J. Mol. Biol. 351**, 573-97

> **Abstract:** Antimycin A (antimycin), one of the first known and most
> potent inhibitors of the mitochondrial respiratory chain, binds to the
> quinone reduction site of the cytochrome bc1 complex.
> Structure--activity relationship studies have shown that the
> N-formylamino-salicyl-amide group is responsible for most of the
> binding specificity, and suggested that a low pKa for the phenolic OH
> group and an intramolecular H-bond between that OH and the carbonyl O
> of the salicylamide linkage are important. Two previous X-ray
> structures of antimycin bound to vertebrate bc1 complex gave
> conflicting results.
>
> A new structure reported here of the bovine mitochondrial bc1 complex
> at 2.28 A° resolution with antimycin bound, allows us for the first
> time to reliably describe the binding of antimycin and shows that the
> intramolecular hydrogen bond described in solution and in the
> small-molecule structure is replaced by one involving the NH rather
> than carbonyl O of the amide linkage, with rotation of the amide group
> relative to the aromatic ring. The phenolic OH and formylamino N form
> H-bonds with conserved Asp228 of cytochrome b, and the formylamino O
> H-bonds via a water molecule to Lys227. A strong density, the right
> size and shape for a diatomic molecule is found between the other side
> of the dilactone ring and the aA helix.

Huang, L.-S., Sun, G., Cobessi, D., Wang, A., Shen, J.T., Tung, E.Y.,
Anderson,V.E., Berry, E.A. (2006) 3-Nitropropionic acid is a suicide
inhibitor of mitochondrial respiration that, upon oxidation by Complex
II, forms a covalent adduct with a catalytic-base arginine in the active
site of the enzyme. **J. Biol. Chem. 281**, 5965-5972.

> **Abstract:** We report three new structures of mitochondrial
> respiratory Complex II (succinate ubiquinone
> oxidoreductase,E.C.1.3.5.1) at up to 2.1 Å resolution, with various
> inhibitors. The structures define the conformation of the bound
> inhibitors and suggest the residues involved in substrate binding and
> catalysis at the dicarboxylate site.
>
> In particular they support the role of Arg 297 as a general base
> catalyst accepting a proton in the dehydrogenation of succinate. The
> dicarboxylate ligand in oxaloacetate-containing crystals appears to be
> the same as that reported for Shewanella flavocytochrome c treated
> with fumarate. The plant and fungal toxin 3-nitropropionic acid, an
> irreversible inactivator of succinate dehydrogenase, forms a covalent
> adduct with the side chain of Arg 297 .The modification eliminates a
> trypsin cleavage site in the flavoprotein, and tandem mass
> spectroscopic analysis of the new fragment shows the mass of Arg 297
> to be increased by 83 Da and to have the potential of losing 44 Da,
> consistent with decarboxylation, during fragmentation.

**F. Research Programs**

# [Ongoing Research]{.underline} 

# DK44842 (Berry, Edward A.) 03/01/92-11/30/08

National Institute of Diabetes and Digestive and Kidney Diseases

3D Crystals of Cytochrome Reductase, A Membrane Protein

The goal of this project is to obtain structural information about the
cytochrome reductase complex from the analysis of 3-dimensional
crystals.

Role: P.I.; crystallography and structure determination.

**GM62563 (Berry, Edward A.) 05/01/00-08/31/07.**

National Institute of General Medical Sciences

3-D Crystal Structure: Vertebrate Mitochondrial Complex II

The goal: optimize crystallization of Complex II and from the crystals
solve the structure with a variety of ligands at the active sites.

Role: P.I.; crystallography and structure determination.

**Informal: Collaboration with Jean-Luc Popot\'s Membrane Protein
Group**

at the Institute of Biophysical Chemistry, Paris on developing amphipols
as stabilizing

agents for membrane proteins in solution.

**Pending: Marie Curie Initial Training Networks (ITN) \"Structural
Biology of Membrane Proteins\"**

PI: Alain Milon

Role: Visiting Scientist

**G. REFERENCES:**

1\. Sung-Hou Kim

Lawrence Berkeley National Laboratory

Physical Biosciences Division

One Cyclotron Road

Mail Stop: 3-220 Calvin Lab

Berkeley, California 94720-1460

USA

Phone: (510) 486-4333

Fax: (510) 486-5272

Email: SHKim@lbl.gov

2\. Antony R. Crofts

Department of Biochemistry

419 Roger Adams Lab, 600 S. Mathews Ave.

Urbana, IL 61801

or

Center for Biophysics and Computational Biology

156 Davenport Hall, 607 S. Mathews Ave.

Urbana, IL 61801

Phone: (217) 333-2043 Fax: (217) 244-6615

Email: a-crofts@life.uiuc.edu

3\. Bernard L. Trumpower

Professor of Biochemistry Dartmouth Medical School

Department of Biochemistry

7200 Vail Bldg., Room 413

Hanover NH 03755-3844

Phone: (603) 650-1621

Fax: (603) 650-1128

Email: Trumpower@Dartmouth.edu

4\. Fevzi Daldal

University of Pennsylvania

103B Carolyn Lynch Laboratory

Department of Biology

University of Pennsylvania

Philadelphia, PA 19104 USA

Phone: +1 215 898.4394

Email: fdaldal@sas.upenn.edu

5\. Peter C. Hinkle

207 Biotechnology Building

Cornell University

Ithaca, N.Y 14853

Phone: 607-255-5704

Email: pch5@cornell.edu