Structural comparison of different antibodies interacting with parvovirus capsids

Journal of Virology

Volumn 83, Issue 11, 2009, Pages 5556-5566

  Hafenstein, Susan ^a   Bowman, Valorie D ^a   Sun, Tao ^a   Nelson, Christian D S ^b,c   Palermo, Laura M ^b,d   Chipman, Paul R ^a   Battisti, Anthony J ^a   Parrish, Colin R ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b Cornell University ^*  (United States)

^c BROWN UNIVERSITY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIBODY; EPITOPE; IMMUNOGLOBULIN F(AB) FRAGMENT; NEUTRALIZING ANTIBODY; ANTIGEN; MONOCLONAL ANTIBODY;

AMINO ACID SEQUENCE; ANTIBODY STRUCTURE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; FELINE PANLEUKOPENIA VIRUS; MOUSE; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARVOVIRUS; PRIORITY JOURNAL; RAT; VIRUS CAPSID; VIRUS MORPHOLOGY; ANTIBODY SPECIFICITY; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; IMMUNOLOGY; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CANINE PARVOVIRUS; FELINE PARVOVIRUS; MIRIDAE; PARVOVIRUS;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ANTIGENS; CAPSID; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; IMMUNOGLOBULIN FAB FRAGMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PARVOVIRUS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 66149137648     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02532-08     Document Type: Article

References (64)

1. Abdelmagid, O. Y., L. Larson, L. Payne, A. Tubbs, T. Wasmoen, and R. Schultz. 2004. Evaluation of the efficacy and duration of immunity of a canine combination vaccine against virulent parvovirus, infectious canine hepatitis virus, and distemper virus experimental challenges. Vet. Ther. 5:173-186.
2. Agbandje, M., R. McKenna, M. G. Rossmann, M. L. Strassheim, and C. R. Parrish. 1993. Structure determination of feline panleukopenia virus empty particles. Proteins 16:155-171. (Pubitemid 23153102)
3. Alzari, P. M., M. B. Lascombe, and R. J. Poljak. 1988. Three-dimensional structure of antibodies. Annu. Rev. Immunol. 6:555-580. (Pubitemid 19141596)
4. Baker, T. S., N. H. Olson, and S. D. Fuller. 1999. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63:862-922.
5. 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. (Pubitemid 30055786)
6. Benson, S. D., J. K. Bamford, D. H. Bamford, and R. M. Burnett. 2004. Does common architecture reveal a viral lineage spanning all three domains of life? Mol. Cell 16:673-685. (Pubitemid 39586527)
7. Bowman, V. D., E. S. Chase, A. W. E. Franz, P. R. Chipman, X. Zhang, K. L. Perry, T. S. Baker, and T. J. Smith. 2002. An antibody to the putative aphid recognition site on cucumber mosaic virus recognizes pentons but not hexons. J. Virol. 76:12250-12258. (Pubitemid 35304322)
8. Brioen, P., D. Dekegel, and A. Boeye. 1983. Neutralization of poliovirus by antibody-mediated polymerization. Virology 127:463-468.
9. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54:905-921. (Pubitemid 28443603)
10. Casal, J. I., J. P. Langeveld, E. Cortes, W. W. Schaaper, E. van Dijk, C. Vela, S. Kamstrup, and R. H. Meloen. 1995. Peptide vaccine against canine parvovirus: identification of two neutralization subsites in the N terminus of VP2 and optimization of the amino acid sequence. J. Virol. 69:7274-7277.
11. Chang, S. F., J. Y. Sgro, and C. R. Parrish. 1992. Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties. J. Virol. 66:6858-6867.
12. Che, Z., N. H. Olson, D. Leippe, W. M. Lee, A. G. Mosser, R. R. Rueckert, T. S. Baker, and T. J. Smith. 1998. Antibody-mediated neutralization of human rhinovirus 14 explored by means of cryoelectron microscopy and X-ray crystallography of virus-Fab complexes. J. Virol. 72:4610-4622. (Pubitemid 28215635)
13. Chothia, C. 1975. Structural invariants in protein folding. Nature 254:304-308.
14. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50:760-763.
15. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60:2126-2132. (Pubitemid 41742764)
16. Fry, E. E., S. M. Lea, T. Jackson, J. W. I. Newman, F. M. Ellard, W. E. Blakemore, R. Abu-Ghazaleh, A. Samuel, A. M. Q. King, and D. I. Stuart. 1999. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18:543-554. (Pubitemid 29057239)
17. Govindasamy, L., K. Hueffer, C. R. Parrish, and M. Agbandje-McKenna. 2003. Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants. J. Virol. 77:12211-12221. (Pubitemid 37339874)
18. Hafenstein, S., V. D. Bowman, P. R. Chipman, C. M. Bator Kelly, F. Lin, M. E. Medof, and M. G. Rossmann. 2007. Interaction of decay-accelerating factor with coxsackievirus B3. J. Virol. 81:12927-12935. (Pubitemid 350156930)
19. Hafenstein, S., L. M. Palermo, V. A. Kostyuchenko, C. Xiao, M. C. Morais, C. D. Nelson, V. D. Bowman, A. J. Battisti, P. R. Chipman, C. R. Parrish, and M. G. Rossmann. 2007. Asymmetric binding of transferrin receptor to parvovirus capsids. Proc. Natl. Acad. Sci. USA 104:6585-6589. (Pubitemid 47175544)
20. Hangartner, L., R. M. Zinkernagel, and H. Hengartner. 2006. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6:231-243. (Pubitemid 43290992)
21. Hewat, E. A., and D. Blaas. 1996. Structure of a neutralizing antibody bound bivalently to human rhinovirus 2. EMBO J. 15:1515-1523. (Pubitemid 26112373)
22. Hewat, E. A., T. C. Marlovits, and D. Blaas. 1998. Structure of a neutralizing antibody bound monovalently to human rhinovirus 2. J. Virol. 72:4396-4402. (Pubitemid 28188746)
23. Hewat, E. A., N. Verdaguer, I. Fita, W. Blakemore, S. Brookes, A. King, J. Newman, E. Domingo, M. G. Mateu, and D. I. Stuart. 1997. Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: positioning of a highly mobile antigenic loop. EMBO J. 16:1492-1500. (Pubitemid 27151944)
24. Hoelzer, K., L. A. Shackelton, C. R. Parrish, and E. C. Holmes. 2008. Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J. Gen. Virol. 89:2280-2289.
25. Hueffer, K., L. Govindasamy, M. Agbandje-McKenna, and C. R. Parrish. 2003. Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses. J. Virol. 77:10099-10105. (Pubitemid 37122091)
26. Hueffer, K., J. S. Parker, W. S. Weichert, R. E. Geisel, J. Y. Sgro, and C. R. Parrish. 2003. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J. Virol. 77:1718-1726. (Pubitemid 36109983)
27. Katpally, U., C. E. Wobus, K. Dryden, H. W. Virgin IV, and T. J. Smith. 2008. Structure of antibody-neutralized murine norovirus and unexpected differences from virus-like particles. J. Virol. 82:2079-2088.
28. Langeveld, J. P., J. I. Casal, E. Cortes, G. van de Wetering, R. S. Boshuizen, W. M. Schaaper, K. Dalsgaard, and R. H. Meloen. 1994. Effective induction of neutralizing antibodies with the amino terminus of VP2 of canine parvovirus as a synthetic peptide. Vaccine 12:1473-1480. (Pubitemid 24347936)
29. Langeveld, J. P., J. I. Casal, C. Vela, K. Dalsgaard, S. H. Smale, W. C. Puijk, and R. H. Meloen. 1993. B-cell epitopes of canine parvovirus: distribution on the primary structure and exposure on the viral surface. J. Virol. 67:765-772. (Pubitemid 23032054)
30. Lee, B., and F. M. Richards. 1971. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:379-400.
31. Liang, X. 2008. CXCR4, inhibitors and mechanisms of action. Chem. Biol. Drug Des. 72:97-110.
32. Llamas-Saiz, A. L., M. Agbandje-McKenna, J. S. Parker, A. T. Wahid, C. R. Parrish, and M. G. Rossmann. 1996. Structural analysis of a mutation in canine parvovirus which controls antigenicity and host range. Virology 225:65-71. (Pubitemid 26390053)
33. Lok, S. M., V. Kostyuchenko, G. E. Nybakken, H. A. Holdaway, A. J. Battisti, S. Sukupolvi-Petty, D. Sedlak, D. H. Fremont, P. R. Chipman, J. T. Roehrig, M. S. Diamond, R. J. Kuhn, and M. G. Rossmann. 2008. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 15:312-317.
34. Nandhagopal, N., A. A. Simpson, J. R. Gurnon, X. Yan, T. S. Baker, M. V. Graves, J. L. Van Etten, and M. G. Rossmann. 2002. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl. Acad. Sci. USA 99:14758-14763.
35. Nelson, C. D., L. M. Palermo, S. L. Hafenstein, and C. R. Parrish. 2007. Different mechanisms of antibody-mediated neutralization of parvoviruses revealed using the Fab fragments of monoclonal antibodies. Virology 361:283-293. (Pubitemid 46574854)
36. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326. (Pubitemid 27085611)
37. Palermo, L. M., S. L. Hafenstein, and C. R. Parrish. 2006. Purified feline and canine transferrin receptors reveal complex interactions with the capsids of canine and feline parvoviruses that correspond to their host ranges. J. Virol. 80:8482-8492. (Pubitemid 44384860)
38. Parker, J. S. L., and C. R. Parrish. 1997. Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid. J. Virol. 71:9214-9222. (Pubitemid 27492363)
39. Parrish, C. R. 1991. Mapping specific functions in the capsid structure of canine parvovirus and feline panleukopenia virus using infectious plasmid clones. Virology 183:195-205.
40. Parrish, C. R., and L. E. Carmichael. 1983. Antigenic structure and variation of canine parvovirus type-2, feline panleukopenia virus, and mink enteritis virus. Virology 129:401-414.
41. Parrish, C. R., L. E. Carmichael, and D. F. Antczak. 1982. Antigenic relationships between canine parvovirus type 2, feline panleukopenia virus and mink enteritis virus using conventional antisera and monoclonal antibodies. Arch. Virol. 72:267-278.
42. Pollock, R. V., and L. E. Carmichael. 1982. Maternally derived immunity to canine parvovirus infection: transfer, decline, and interference with vaccination. J. Am. Vet. Med. Assoc. 180:37-42.
43. Rao, S. T., and M. G. Rossmann. 1973. Comparison of super-secondary structures in proteins. J. Mol. Biol. 76:241-256.
44. Rimmelzwaan, G. F., J. Carlson, F. G. C. M. UytdeHaag, and A. D. M. E. Osterhaus. 1990. A synthetic peptide derived from the amino acid sequence of canine parvovirus structural proteins which defines a B cell epitope and elicits antiviral antibody in BALB c mice. J. Gen. Virol. 71:2741-2745. (Pubitemid 20370521)
45. Rossmann, M. G. 2000. Fitting atomic models into electron-microscopy maps. Acta Crystallogr. D 56:1341-1349.
46. Rossmann, M. G., and P. Argos. 1975. A comparison of the heme binding pocket in globins and cytochrome b5. J. Biol. Chem. 250:7525-7532.
47. Rossmann, M. G., and P. Argos. 1976. Exploring structural homology of proteins. J. Mol. Biol. 105:75-95.
48. Rossmann, M. G., E. Arnold, J. W. Erickson, E. A. Frankenberger, J. P. Griffith, H. J. Hecht, J. E. Johnson, G. Kamer, M. Luo, A. G. Mosser, et al. 1985. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145-153. (Pubitemid 16243130)
49. Rossmann, M. G., R. Bernal, and S. V. Pletnev. 2001. Combining electron microscopic with X-ray crystallographic structures. J. Struct. Biol. 136:190-200. (Pubitemid 33733556)
50. Rossmann, M. G., Y. He, and R. J. Kuhn. 2002. Picornavirus-receptor interactions. Trends Microbiol. 10:324-331. (Pubitemid 34756532)
51. Rossmann, M. G., and J. E. Johnson. 1989. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58:533-573. (Pubitemid 19172980)
52. Rossmann, M. G., and A. C. Palmenberg. 1988. Conservation of the putative receptor attachment site in picornaviruses. Virology 164:373-382. (Pubitemid 18157161)
53. Smith, T. J., N. H. Olson, R. H. Cheng, E. S. Chase, and T. S. Baker. 1993. Structure of a human rhinovirus-bivalently bound antibody complex: implications for viral neutralization and antibody flexibility. Proc. Natl. Acad. Sci. USA 90:7015-7018. (Pubitemid 23222379)
54. Strassheim, M. L., A. Gruenberg, P. Veijalainen, J. Y. Sgro, and C. R. Parrish. 1994. Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid. Virology 198:175-184. (Pubitemid 124018773)
55. Taniguchi, K., Y. Morita, T. Urasawa, and S. Urasawa. 1987. Cross-reactive neutralization epitopes on VP3 of human rotavirus: analysis with monoclonal antibodies and antigenic variants. J. Virol. 61:1726-1730. (Pubitemid 17069776)
56. Thouvenin, E., S. Laurent, M. F. Madelaine, D. Rasschaert, J. F. Vautherot, and E. A. Hewat. 1997. Bivalent binding of a neutralising antibody to a calicivirus involves the torsional flexibility of the antibody hinge. J. Mol. Biol. 270:238-246. (Pubitemid 27296684)
57. Truyen, U., A. Gruenberg, S. F. Chang, B. Obermaier, P. Veijalainen, and C. R. Parrish. 1995. Evolution of the feline-subgroup parvoviruses and the control of canine host range in vivo. J. Virol. 69:4702-4710.
58. Tsao, J., M. S. Chapman, M. Agbandje, W. Keller, K. Smith, H. Wu, M. Luo, T. J. Smith, M. G. Rossmann, R. W. Compans, and C. R. Parrish. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464. 59. Vagin, A., and A. Teplyakov. 1997. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30:1022-1025. (Pubitemid 121000431)
59. Whitelegg, N. R., and A. R. Rees. 2000. WAM: an improved algorithm for modelling antibodies on the WEB. Protein Eng. 13:819-824. (Pubitemid 32233940)
60. Wikoff, W. R., G. Wang, C. R. Parrish, R. H. Cheng, M. L. Strassheim, T. S. Baker, and M. G. Rossmann. 1994. The structure of a neutralized virus: canine parvovirus complexed with neutralizing antibody fragment. Structure 2:595-607. (Pubitemid 124001303)
61. Wilson, I. A., and R. L. Stanfield. 1994. Antibody-antigen interactions: new structures and new conformational changes. Curr. Opin. Struct. Biol. 4:857-867.
62. Xiao, C., and M. G. Rossmann. 2007. Interpretation of electron density with stereographic roadmap projections. J. Struct. Biol. 158:182-187. (Pubitemid 46719989)
63. Yuan, W., and C. R. Parrish. 2000. Comparison of two single-chain antibodies that neutralize canine parvovirus: analysis of an antibody-combining site and mechanisms of neutralization. Virology 269:471-480. (Pubitemid 30210919)
64. Zhang, Y., J. Corver, P. R. Chipman, W. Zhang, S. V. Pletnev, D. Sedlak, T. S. Baker, J. H. Strauss, R. J. Kuhn, and M. G. Rossmann. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613. (Pubitemid 36712358)