Source: http://www.asmscience.org/content/book/10.1128/9781555816698.ch06
Timestamp: 2019-04-18 23:14:55+00:00

Document:
This chapter begins with a discussion of some of the obstacles that have hampered progress in studying cell entry pathways for picornaviruses and other non-enveloped viruses. The chapter reviews what is known about the early steps leading to internalization of the viruses into intracellular vesicles, focusing on examples (for key members of the family) that point out the diversity in the cell entry pathways used as well as the common themes. It finishes with an exploration (admittedly poliovirus centered) of what we know about the machinery that facilitates translocation of the genome across the membrane once the virus has been internalized. The virion- to-135S (or A particle) transition has not been observed in the aphthoviruses (foot-and-mouth disease viruses [FMDVs] and equine rhinitis virus) or cardioviruses (encephalomyocarditis virus, mengovirus). Although clathrin-mediated endocytosis may serve as the predominant entry pathway for some picornaviruses (including FMDV, minor group rhinoviruses, and probably major group rhinoviruses), it is clear that other picornaviruses use a variety of other endocytic pathways. In a recent study it was shown that the coxsackievirus B3 first binds to DAF (CD55) on the apical surfaces of the cells. This study clearly demonstrates the importance of virus-induced signaling in cell entry. Advances in detectors and optics that should become available in the future will improve the resolution achievable in both cryo-electron microscopy (cryo-EM) and cryo-electron tomography (cryo-ET) approaches, making it possible to approach near-atomic resolution from cryo-EM studies of intermediates in vitro and unprecedented resolution for structures determined in situ.
Structure of the virus-receptor-liposome complex as determined by cryo-EM (left) and cryo-ET (right). Both reconstructions are at approximately 30-Å resolution. The reconstructions are consistent with earlier models that suggested that the initial complex of the virus with the receptor on the cell surface would involve five copies of the receptor and bring a particle five-fold axis close to the membrane. The membrane in the reconstructions appears as an isolated patch due to masking and to variability in the membrane structure (both of which result from variabilities in size and deformations of the liposome) outside the immediate footprint of the five bound receptors. The reconstructions clearly show the densities for the three-domain receptor, including bulges that correspond to glycosylation sites in the second domain of the receptor. Both reconstructions also show a prominent crown-shaped bump in the membrane immediately below, where the virus five-fold axis makes its closest approach to the membrane. The appearance of this feature is consistent with an outward deformation of the outer leaflet of the membrane.
Structures of 80S particles. (A) Cryo-EM of preparations of 80S particles, showing that the preparations are heterogeneous with variable levels of density (presumably RNA) inside the particles. (B) A small percentage of these particles (5 to 10%) have density (again, presumably RNA) both inside and outside the particle. The density outside the particle is highly branched, suggesting that the RNA has refolded after exiting the particle, and in many cases, the externalized densities from neighboring particles intermingle. The particles can be classified into two clusters (80Se and 80Sl) based on the capsid structure. Cryo-EM reconstructions of the 80Se particles (C, D, and E) and 80Sl particles (F, G, and H) show the whole particle (C and F), a close-up of the outer surface (D and G), and the inner surface (E and H), including the prominent ridge crossing the two-fold axis that appears to “staple together” two neighboring pentamers.
The structure of 80S particles caught in the act of releasing their RNA. The figure shows a cryo-ET reconstruction of a single virus particle. The density for the capsid (dark grey) is the average of over 20 icosahedrally averaged subtomograms. The density for the RNA comes from a single unaveraged tomogram. Cryo-ET reconstructions of other particles are similar, differing only in the appearance of the RNA, which is unique to each reconstruction. The reconstructions clearly show that the RNA is released from the base of the canyon near a quasi-three-fold axis (see Color Plate 8). This site corresponds to sites of noticeable thinning of the shell in the icosahedral cryo-EM reconstructions of the 80Se and 80Sl particles.
1. Arita, M.,, S. Koike,, J. Aoki,, H. Horie, and, A. Nomoto. 1998. Interaction of poliovirus with its purified receptor and conformational alteration in the virion. J. Virol. 72: 3578– 3586.
2. Arnold, E.,, M. Luo,, G. Vriend,, M. G. Rossmann,, A. C. Palmenberg,, G. D. Parks,, M. J. H. Nicklin, and, E. Wimmer. 1987. Implications of the picornavirus capsid structure for polyprotein processing. Proc. Natl. Acad. Sci. USA 84: 21– 25.
3. Basavappa, R.,, R. Syed,, O. Flore,, J. P. Icenogle,, D. J. Filman, and, J. M. Hogle. 1994. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 Å resolution. Protein Sci. 3: 1651– 1669.
4. Belnap, D. M.,, D. J. Filman,, B. L. Trus,, N. Cheng,, F. P. Booy,, J. F. Conway,, S. Curry,, C. N. Hiremath,, S. K. Tsang,, A. C. Steven, and, J. M. Hogle. 2000. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74: 1342– 1354.
5. Belnap, D. M.,, W. D. Grochulski,, N. H. Olson, and, T. S. Baker. 1993. Use of radial density plots to calibrate image magnification for frozen-hydrated specimens. Ultramicroscopy 48: 347– 358.
6. Belnap, D. M.,, B. M. McDermott, Jr.,, D. J. Filman,, N. Cheng,, B. L. Trus,, H. J. Zuccola,, V. R. Racaniello,, J. M. Hogle, and, A. C. Steven. 2000. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl. Acad. Sci. USA 97: 73– 78.
7. Berka, U.,, A. Khan,, D. Blaas, and, R. Fuchs. 2009. Human rhinovirus type 2 uncoating at the plasma membrane is not affected by a pH gradient but is affected by the membrane potential. J. Virol. 83: 3778– 3787.
8. Berryman, S.,, S. Clark,, P. Monaghan, and, T. Jackson. 2005. Early events in integrin αvβ6-mediated cell entry of foot-and-mouth disease virus. J. Virol. 79: 8519– 8534.
9. Bostina, M.,, D. Bubeck,, C. Schwartz,, D. Nicastro,, D. J. Filman, and, J. M. Hogle. 2007. Single particle cryoelectron tomography characterization of the structure and structural variability of poliovirus-receptor-membrane complex at 30 Å resolution. J. Struct. Biol. 160: 200– 210.
10. Bothner, B.,, X. F. Dong,, L. Bibbs,, J. E. Johnson, and, G. Siuzdak. 1998. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 273: 673– 676.
11. Brabec, M.,, G. Baravalle,, D. Blaas, and, R. Fuchs. 2003. Conformational changes, plasma membrane penetration, and infection by human rhinovirus type 2: role of receptors and low pH. J. Virol. 77: 5370– 5377.
12. Brandenburg, B.,, L. Y. Lee,, M. Lakadamyali,, M. J. Rust,, X. Zhuang, and, J. M. Hogle. 2007. Imaging poliovirus entry in live cells. PLoS Biol. 5: e183.
13. Bubeck, D.,, D. J. Filman,, N. Cheng,, A. C. Steven,, J. M. Hogle, and, D. M. Belnap. 2005. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79: 7745– 7755.
14. Bubeck, D.,, D. J. Filman, and, J. M. Hogle. 2005. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct. Mol. Biol. 12: 615– 618.
15. Chen, Z.,, C. Stauffacher,, Y. Li,, T. Schmidt,, W. Bomu,, G. Kamer,, M. Shanks,, G. Lomonossoff, and, J. E. Johnson. 1989. Protein-RNA interactions in an icosahedral virus at 3.0 Å resolution. Science 245: 154– 159.
16. Chow, M.,, J. F. E. Newman,, D. Filman,, J. M. Hogle,, D. J. Rowlands, and, F. Brown. 1987. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327: 482– 486.
17. Coyne, C. B., and, J. M. Bergelson. 2005. CAR: a virus receptor within the tight junction. Adv. Drug Deliv. Rev. 57: 869– 882.
18. Coyne, C. B., and, J. M. Bergelson. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124: 119– 131.
19. Coyne, C. B.,, K. S. Kim, and, J. M. Bergelson. 2007. Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J. 26: 4016– 4028.
20. Crowell, R. L.,, B. J. Landau, and, L. Philipson. 1971. The early interaction of coxsackievirus B3 with HeLa cells. Proc. Soc. Exp. Biol. Med. 137: 1082– 1088.
21. Crowell, R. L., and, L. Philipson. 1971. Specific alterations of coxsackievirus B3 eluted from HeLa cells. J. Virol. 8: 509– 515.
22. Curry, S.,, M. Chow, and, J. M. Hogle. 1996. The poliovirus 135S particle is infectious. J. Virol. 70: 7125– 7131.
23. Danthi, P.,, M. Tosteson,, Q. H. Li, and, M. Chow. 2003. Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus. J. Virol. 77: 5266– 5274.
24. Davis, M. P.,, G. Bottley,, L. P. Beales,, R. A. Killington,, D. J. Rowlands, and, T. J. Tuthill. 2008. Recombinant VP4 of human rhinovirus induces permeability in model membranes. J. Virol. 82: 4169– 4174.
25. De Sena, J., and, B. Mandel. 1976. Studies on the in vitro un-coating of poliovirus. I. Characterization of the modifying factor and the modifying reaction. Virology 70: 470– 483.
26. De Sena, J., and, B. Mandel. 1977. Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle. Virology 78: 554– 566.
27. DeTulleo, L., and, T. Kirchhausen. 1998. The clathrin endocytic pathway in viral infection. EMBO J. 17: 4585– 4593.
28. Doedens, J.,, L. A. Maynell,, M. W. Klymkowsky, and, K. Kirkegaard. 1994. Secretory pathway function, but not cytoskeletal integrity, is required in poliovirus infection. Arch. Virol. Suppl. 9: 159– 172.
29. Dubra, M. S.,, J. L. La Torre,, E. A. Scodeller,, C. D. Denoya, and, C. Vasquez. 1982. Cores in foot-and-mouth disease virus. Virology 116: 349– 353.
30. Fenwick, M. L., and, P. D. Cooper. 1962. Early interactions between poliovirus and ERK cells. Some observations on the nature and significance of the rejected particles. Virology 18: 212– 223.
31. Filman, D. J.,, R. Syed,, M. Chow,, A. J. Macadam,, P. D. Minor, and, J. M. Hogle. 1989. Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 8: 1567– 1579.
32. Fricks, C. E., and, J. M. Hogle. 1990. Cell-induced conformational change of poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64: 1934– 1945.
33. Golden, J., and, S. C. Harrison. 1982. Proteolytic dissection of turnip crinkle virus subunit in solution. Biochemistry 21: 3862– 3866.
34. Gomez Yafal, A.,, G. Kaplan,, V. R. Racaniello, and, J. M. Hogle. 1993. Characterization of poliovirus conformational alteration mediated by soluble cell receptors. Virology 197: 501–505.
35. Guttman, N., and, D. Baltimore. 1977. Morphogenesis of poliovirus. IV. Existence of particles sedimenting at 150S and having the properties of provirion. J. Virol. 23: 363– 367.
36. Harber, J. J.,, J. Bradley,, C. W. Anderson, and, E. Wimmer. 1991. Catalysis of poliovirus VP0 maturation cleavage is not mediated by serine 10 of VP2. J. Virol. 65: 326– 334.
37. He, Y.,, V. D. Bowman,, S. Mueller,, C. M. Bator,, J. Bella,, X. Peng,, T. S. Baker,, E. Wimmer,, R. J. Kuhn, and, M. G. Rossmann. 2000. Interaction of the poliovirus receptor with poliovirus. Proc. Natl. Acad. Sci. USA 97: 79– 84.
38. He, Y.,, S. Mueller,, P. R. Chipman,, C. M. Bator,, X. Peng,, V. D. Bowman,, S. Mukhopadhyay,, E. Wimmer,, R. J. Kuhn, and, M. G. Rossmann. 2003. Complexes of poliovirus serotypes with their common cellular receptor, CD155. J. Virol. 77: 4827– 4835.
39. Hewat, E. A., and, D. Blaas. 2004. Cryoelectron microscopy analysis of the structural changes associated with human rhinovirus type 14 uncoating. J. Virol. 78: 2935– 2942.
40. Hewat, E. A.,, E. Neumann, and, D. Blaas. 2002. The concerted conformational changes during human rhinovirus 2 uncoating. Mol. Cell 10: 317– 326.
41. Hindiyeh, M.,, Q. H. Li,, R. Basavappa,, J. M. Hogle, and, M. Chow. 1999. Poliovirus mutants at histidine 195 of VP2 do not cleave VP0 into VP2 and VP4. J. Virol. 73: 9072– 9079.
42. Hogle, J. M. 2002. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56: 677– 702.
43. Hogle, J. M.,, M. Chow, and, D. J. Filman. 1985. Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229: 1358– 1365.
44. Huang, Y.,, J. M. Hogle, and, M. Chow. 2000. Is the 135S poliovirus particle an intermediate during cell entry? J. Virol. 74: 8757– 8761.
45. Jacobson, M. F., and, D. Baltimore. 1968. Morphogenesis of poliovirus. I. Association of the viral RNA with coat protein. J. Mol. Biol. 33: 369– 378.
46. Johns, H. L.,, S. Berryman,, P. Monaghan,, G. J. Belsham, and, T. Jackson. 2009. A dominant-negative mutant of rab5 inhibits infection of cells by foot-and-mouth disease virus: implications for virus entry. J. Virol. 83: 6247– 6256.
47. Joklik, W. K., and, J. E. Darnell. 1961. The adsorption and early fate of purified poliovirus in HeLA cells. Virology 13: 439– 447.
48. Kaplan, G.,, M. S. Freistadt, and, V. R. Racaniello. 1990. Neutralization of poliovirus by cell receptors expressed in insect cells. J. Virol. 64: 4697– 4702.
49. Karjalainen, M.,, E. Kakkonen,, P. Upla,, H. Paloranta,, P. Kankaanpaa,, P. Liberali,, G. H. Renkema,, T. Hyypia,, J. Heino, and, V. Marjomaki. 2008. A Raft-derived, Pak1-regulated entry participates inα 2β 1 integrin-dependent sorting to caveosomes. Mol. Biol. Cell 19: 2857– 2869.
50. Lee, W.-M.,, S. S. Monroe, and, R. R. Rueckert. 1993. Role of maturation cleavage in infectivity of picornaviruses: activation of an infectosome. J. Virol. 67: 2110– 2122.
51. Lewis, J. K.,, B. Bothner,, T. J. Smith, and, G. Siuzdak. 1998. Antiviral agent blocks breathing of the common cold virus. Proc. Natl. Acad. Sci. USA 95: 6774– 6778.
52. Li, Q.,, A. G. Yafal,, Y. M.-H. Lee,, J. Hogle, and, M. Chow. 1994. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J. Virol. 68: 3965– 3970.
53. Lonberg-Holm, K.,, L. B. Gosser, and, J. C. Kauer. 1975. Early alteration of poliovirus in infected cells and its specific inhibition. J. Gen. Virol. 27: 329– 345.
54. Lonberg-Holm, K.,, L. B. Gosser, and, E. J. Shimshick. 1976. Interaction of liposomes with subviral particles of poliovirus type 2 and rhinovirus type 2. J. Virol. 19: 746– 749.
55. Lonberg-Holm, K., and, B. D. Korant. 1972. Early interaction of rhinovirus with host cells. J. Virol. 9: 29– 40.
56. Lucic, V.,, A. H. Kossel,, T. Yang,, T. Bonhoeffer,, W. Baumeister, and, A. Sartori. 2007. Multiscale imaging of neurons grown in culture: from light microscopy to cryo-electron tomography. J. Struct. Biol. 160: 146– 156.
57. Mak, T. W.,, D. J. O’Callaghan, and, J. S. Colter. 1970. Studies of the early events of the replicative cycle of three variants of Mengo encephalomyelitis virus in mouse fibroblast cells. Virology 42: 1087– 1096.
58. Mak, T. W.,, D. J. O’Callaghan, and, J. S. Colter. 1970. Studies of the pH inactivation of three variants of Mengo encephalomyelitis virus. Virology 40: 565– 571.
59. Marongiu, M. E.,, A. Pani,, M. V. Corrias,, M. Sau, and, P. La Colla. 1981. Poliovirus morphogenesis. I. Identification of 80S dissociable particles and evidence for the artifactual production of procapsids. J. Virol. 39: 341– 347.
60. Marsh, M., and, A. Helenius. 2006. Virus entry: open sesame. Cell 124: 729– 740.
61. McDermott, B. M.,, A. H. Rux,, R. J. Eisenberg,, G. H. Cohen, and, V. R. Racaniello. 2000. Two distinct binding affinities of poliovirus for its cellular receptor. J. Biol. Chem. 275: 23089– 23096.
62. Mercer, J., and, A. Helenius. 2009. Virus entry by macropinocytosis. Nat. Cell Biol. 11: 510– 520.
63. O’Donnell, V.,, M. LaRocco,, H. Duque, and, B. Baxt. 2005. Analysis of foot-and-mouth disease virus internalization events in cultured cells. J. Virol. 79: 8506– 8518.
64. O’Donnell, V.,, J. M. Pacheco,, D. Gregg, and, B. Baxt. 2009. Analysis of foot-and-mouth disease virus integrin receptor expression in tissues from naïve and infected cattle. J. Comp. Pathol. 141: 98– 112.
65. Patel, K. P.,, C. B. Coyne, and, J. M. Bergelson. 2009. Dynamin- and lipid raft-dependent entry of decay-accelerating factor (DAF)-binding and non-DAF-binding coxsackieviruses into nonpolarized cells. J. Virol. 83: 11064– 11077.
66. Pelkmans, L., and, A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15: 414– 22.
67. Pérez, L., and, L. Carrasco. 1993. Entry of poliovirus into cells does not require a low-pH step. J. Virol. 67: 4543– 4548.
68. Pietiainen, V.,, V. Marjomaki,, P. Upla,, L. Pelkmans,, A. Helenius, and, T. Hyypia. 2004. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol. Biol. Cell 15: 4911– 4925.
69. Prchla, E.,, C. Plank,, E. Wagner,, D. Blaas, and, R. Fuchs. 1995. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131: 111– 123.
70. Robinson, I. K., and, S. C. Harrison. 1982. Structure of the expanded state of tomato bushy stunt virus. Nature 297: 563–568.
71. Roivainen, M.,, L. Piirainen,, T. Rysä,, A. Närvänen, and, T. Hovi. 1993. An immunodominant N-terminal region of VP1 protein of poliovirion that is buried in crystal structure can be exposed in solution. Virology 195: 762– 765.
72. Rowlands, D. J.,, D. V. Sangar, and, F. Brown. 1975. A comparative chemical and serological study of the full and empty particles of foot-and mouth disease virus. J. Gen. Virol. 26: 227– 238.
73. Sartori, A.,, R. Gatz,, F. Beck,, A. Rigort,, W. Baumeister, and, J. M. Plitzko. 2007. Correlative microscopy: bridging the gap between fluorescence light microscopy and cryo-electron tomography. J. Struct. Biol. 160: 135– 145.
74. Schober, D.,, P. Kronenberger,, E. Prchla,, D. Blaas, and, R. Fuchs. 1998. Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J. Virol. 72: 1354– 1364.
75. Schwartz, C. L.,, V. I. Sarbash,, F. I. Ataullakhnov,, J. R. Mc-Intosh, and, D. Nicastro. 2007. Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. J. Microsc. 227: 98– 109.
76. Selinka, H.-C.,, A. Zibert, and, E. Wimmer. 1991. Poliovirus can enter and infect mammalian cells by way of an intercellular adhesion molecule 1 pathway. Proc. Natl. Acad. Sci. USA 88: 3598– 3602.
77. Smith, A. E., and, A. Helenius. 2004. How viruses enter animal cells. Science 304: 237– 242.
78. Speir, J. A.,, S. Munshi,, G. Wang,, T. S. Baker, and, J. E. Johnson. 1995. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3: 63– 78.
79. Tosteson, M. T., and, M. Chow. 1997. Characterization of the ion channels formed by poliovirus in planar lipid membranes. J. Virol. 71: 507– 511.
80. Tosteson, M. T.,, H. Wang,, A. Naumov, and, M. Chow. 2004. Poliovirus binding to its receptor in lipid bilayers results in particle-specific, temperature-sensitive channels. J. Gen. Virol. 85: 1581– 1589.
81. Tsang, S. K.,, B. M. McDermott,, V. R. Racaniello, and, J. M. Hogle. 2001. A kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J. Virol. 75: 4984– 4989.
82. Tuthill, T. J.,, D. Bubeck,, D. J. Rowlands, and, J. M. Hogle. 2006. Characterization of early steps in the poliovirus infection process: receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. J. Virol. 80: 172– 180.
83. Tuthill, T. J.,, K. Harlos,, T. S. Walter,, N. J. Knowles,, E. Groppelli,, D. J. Rowlands,, D. I. Stuart, and, E. E. Fry. 2009. Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism? PLoS Pathog. 5: e1000 620.
84. Vaughan, J. C.,, B. Brandenburg,, J. M. Hogle, and, X. Zhuang. 2009. Rapid actin-dependent viral motility in live cells. Biophys. J. 97: 1647– 1656.
85. Xing, L.,, K. Tjarnlund,, B. Lindqvist,, G. G. Kaplan,, D. Feigelstock,, R. H. Cheng, and, J. M. Casasnovas. 2000. Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J. 19: 1207– 1216.
86. Zhang, P.,, S. Mueller,, M. C. Morais,, C. M. Bator,, V. D. Bowman,, S. Hafenstein,, E. Wimmer, and, M. G. Rossmann. 2008. Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proc. Natl. Acad. Sci. USA 105: 18284– 18289.

References: V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V.