Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice

Journal of Virology

Volumn 79, Issue 17, 2005, Pages 10931-10943

  Kontou, Maria ^a,d   Govindasamy, Lakshmanan ^a   Nam, Hyun Joo ^a   Bryant, Nathan ^a   Llamas Saiz, Antonio L ^b,e   Foces Foces, Concepción ^b   Hernando, Eva ^c,f   Rubio, Mari Paz ^c,g   McKenna, Robert ^a   Almendral, José M ^c   Agbandje McKenna, Mavis ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d UNIVERSITY OF THESSALY   (Greece)

^e UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN;

ARTICLE; COMPARATIVE STUDY; CONFORMATION; CRYSTAL STRUCTURE; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; VIROGENESIS; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS EXPRESSION; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS PATHOGENESIS; VIRUS STRAIN; WILD TYPE;

CAPSID; CAPSID PROTEINS; MINUTE VIRUS OF MICE; MODELS, MOLECULAR; PROTEIN CONFORMATION; TROPISM; VIRULENCE;

MICE MINUTE VIRUS; MIRIDAE; PARVOVIRUS; TRIXIS;

EID: 23844475355     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.17.10931-10943.2005     Document Type: Article

References (69)

1. Agbandje, M., S. Kajigaya, R. McKenna, N. S. Young, and M. G. Rossmann. 1994. The structure of human parvovirus B19 at 8 Å resolution. Virology 203:106-115.
2. Agbandje, M., R. McKenna, M. G. Rossmann, M. L. Strassheim, and P. R. Parrish. 1993. Structure determination of feline panleukopenia virus empty particles. Proteins 16:155-171.
3. Agbandje-McKenna, M., A. L. Llamas-Saiz, F. Wang, P. Tattersall, and M. G. Rossmann. 1998. Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6:1369-1381.
4. Agbandje-McKenna, M., C. R. Parrish, and M. G. Rossmann. 1995. The structure of parvoviruses. Semin. Virol. 6:299-309.
5. Astell, C. R., E. M. Gardiner, and P. Tattersall. 1986. DNA sequence of the lymphotropic variant of minute virus of mice, MVM(i), and comparison with the DNA sequence of the fibrotropic prototype strain. J. Virol. 57:656-669.
6. Ball-Goodrich, L. J., and P. Tattersall. 1992. Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. J. Virol. 66:3415-3423.
7. Barbis, D. P., S.-F. Chang, and C. R. Parrish. 1992. Mutations adjacent to the dimple of the canine parvovirus capsid structure affect sialic acid binding. Virology 191:301-308.
8. Bergeron, J., B. Hébert, and P. Tijssen. 1996. Genome organization of the Kresse strain of porcine parvovirus: identification of allotropic determinant and comparison with those of NADL-2 and field isolates. J. Virol. 70:2508-2515.
9. Bloom, M. E., J. M. Fox, B. D. Berry, K. L. Oie, and J. B. Wolfinbarger. 1998. Construction of pathogenic molecular clones of Aleutian rnink disease parvovirus that replicate both in vivo and in vitro. Virology 251:288-296.
10. Bloom, M. E., H. Kanno, S. Mori, and J. B. Wolfinbarger. 1994. Aleutian mink disease parvovirus: puzzles and paradigms. Infect. Agents Dis. 3:279-301.
11. Brownstein, D. G., A. L. Smith, R. O. Jacoby, E. A. Johnson, G. Hansen, and P. Tattersall. 1991. Pathogenesis of infection with a virulent allotropic variant of minute virus of mice and regulation by host genotype. Lab. Investig. 65:357-363.
12. Brownstein, D. G., A. L. Smith, E. A. Johnson, D. J. Pintel, L. K. Naeger, and P. Tattersall. 1992. The pathogenesis of infection with minute virus of mice depends on expression of the small nonstructural protein NS2 and on the genotype of the allotropic determinants VP1 and VP2. J. Virol. 66:3118-3124.
13. Bruemmer, A., F. Scholari, M. Lopez-Ferber, J. F. Conway, and E. A. Hewat, 2005. Structure of an insect parvovirus (Junonia coenia Densovirus) determined by cryo-electron microscopy. J. Mol. Biol. 347:791-801.
14. Brunger, A. T. 1992. The free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355:472-474.
15. 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.
16. Carreira, A., M. Menéndez, J. Reguera, J. M. Almendral, and M. G. Mateu. 2004. In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279:6517-6525.
17. 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.
18. Chipman, P. R., M. Agbandje-McKenna, S. Kajigaya, K. E. Brown, N. S. Young, T. S. Baker, and M. G. Rossmann. 1996. Cryo-electron microscopy studies of empty capsids of human parvovirus B19 complexed with its cellular receptor. Proc. Natl. Acad. Sci. USA 93:7502-7506.
19. Cotmore, S. F., A. M. D'abramo, Jr., C. M. Ticknor, and P. Tattersall. 1999. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 254:169-181.
20. Cotmore, S. F., and P. Tattersall. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
21. DeLano, W. L. 2002. The PyMol molecular graphics systems. DeLano Scientific, San Carlos, CA.
22. Esnouf, R. 1999. BOBSCRIPT. Further additions to MOLSCRIPT version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D 55:938-940.
23. Farr, G. A., and P. Tattersall. 2004. A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 323:243-256.
24. Fox, J. M., M. A. McCrackin Stevenson, and M. E. Bloom. 1999. Replication of Aleutian mink disease parvovirus in vivo is influenced by residues in the VP2 protein. J. Virol. 73:8713-8719.
25. Gasteiger, E., A. Gattiker, C. Hoogland, I. Ivanyi, R. D. Appel, and A. Bairoch. 2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31:3784-3788.
26. 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.
27. Hernando, E., A. L. Llamas-Saiz, C. Foces-Foces, R. McKenna, I. Portman, M. Agbandje-McKenna, and J. M. Almendral. 2000. Biochemical and physical characterization of parvovirus minute virus of mice virus-like particles. Virology 267:299-309.
28. Horiuchi, M., H. Goto, N. Ishiguro, and M. Shinagawa. 1994. Mapping of determinants of the host range for canine cells in the genome of canine parvovirus using canine parvovirus/mink enteritis virus chimeric viruses. J. Gen. Virol. 75:1319-1328.
29. Horiuchi, M., N. Ishiguro, H. Goto, and M. Shinagawa. 1992. Characterization of the stage(s) in the virus replication cycle at which the host-cell specificity of the feline parvovirus subgroup is regulated in canine cells. Virology 189:600-608.
30. Hueffer, K., L. Govindasamy, M. Agbandje-McKenna, and C. R. Parrish. 2003. Combinations of two capsid regions control host range and specific transferrin receptor binding by canine parvovirus. J. Virol. 77:10099-10105.
31. 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.
32. Jones, T., J.-Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 97:110-119.
33. Kaufmann, B., A. A. Simpson, and M. G. Rossmann. 2004. The structure of human parvovirus B19. Proc. Natl. Acad. Sci. USA 101:11628-11633.
34. Kronenberg, S., J. A. Kleinschmidt, and B. Böttcher. 2001. Electron cryomicroscopy and image reconstruction of adeno-associated virus type 2 empty capsids. EMBO Rep. 2:997-1002.
35. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
36. Llamas-Saiz, A. L., M. Agbandje-McKenna, J. S. L. Parker, A. T. M. 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.
37. Llamas-Saii, A. L., M. Agbandje-McKenna, W. R. Wikoff, J. Bratton, P. Tattersall, and M. G. Rossmann. 1997. Structure determination of minute virus of mice. Acta Crystallogr. D 53:93-102.
38. Maxwell, I. H., A. L. Spitzer, F. Maxwell, and D. J. Pintel. 1995. The capsid determinant of fibrotropism for the MVMp strain of minute virus of mice functions via VP2 and not VP1. J. Virol. 69:5829-5832.
39. McKenna, R., N. H. Olson, P. R. Chipman, T. S. Baker, T. F. Booth, J. Christensen, B. Aasted, J. M. Fox, M. E. Bloom, J. B. Wolfinbarger, and M. Agbandje-McKenna. 1999. Three-dimensional structure of Aleutian mink disease parvovirus: implications for disease pathogenicity. J. Virol. 73:6882-6891.
40. Merritt, E. A., and D. J. Bacon. 1997. Raster3D-photorealistic molecular graphics. Methods Enzymol. 277:505-524.
41. Molitor, T. W., and H. S. Joo. 1990. Clinical and pathological features of porcine parvovirus-related disease and its diagnosis, p. 135-150. In P. Tijssen (ed.), Handbook of parvoviruses, vol. II. CRC Press, Boca Raton, Fla.
42. Nicholls, A., K. A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11:281-296.
43. Otwinowski, Z., and W. Minor. 1997. Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
44. Padron, E., V. D. Bowman, N. Kaludov, L. Govindasamy, H. Levy, P. Nick, R. McKenna, N. Muzyczka, J. A. Chiorini, T. S. Baker, and M. Agbandje-McKenna. 2005. The structure of adeno-associated virus 4. J. Virol. 79:5047-5058.
45. 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.
46. Parrish, C. R., C. F. Aquadro, and L. E. Carmichael. 1988. Canine host range and a specific epitope map along with variant sequences in the capsid protein gene of canine parvovirus and related feline, mink and raccoon parvoviruses. Virology 166:293-307.
47. Ramírez, J. C., A. Fiaren, and J. M. Almendral. 1996. Parvovirus minute virus of mice strain I multiplication and pathogenesis in the newborn mouse brain are restricted to proliferative areas and to migratory cerebral young neurons. J. Virol. 70:8109-8116.
48. Reddy, V. S., P. Natarajan, B. Okerberg, K. Li, K. V. Damodaran, R. T. Morton, C. L. Brooks III, and J. E. Johnson. 2001. Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses. J. Virol. 75:11943-11947.
49. Rossmann, M. G., and P. Argos. 1976. Exploring structural homology of proteins. J. Mol. Biol. 105:75-95.
50. Rossmann, M. G., R. McKenna, L. Tong, D. Xia, J. Dai, H. Wu, H. K. Choi, and R. E. Lynch. 1992. Molecular replacement real-space averaging. J. Appl. Crystallogr. 25:166-180.
51. Segovia, J. C., J. A. Bueren, and J. M. Almendral. 1995. Myeloid depression follows infection of susceptible newborn mice with the parvovirus minute virus of mice (strain i). J. Virol. 69:3229-3232.
52. Segovia, J. C., J. M. Gallego, J. A. Bueren, and J. M. Almendral. 1999. Severe leukopenia and dysregulated erythropoiesis in SCID mice persistently infected with the parvovirus minute virus of mice. J. Virol. 73:1774-1784.
53. Simpson, A. A., V. Chandrasekar, B. Hebert, G. M. Sullivan, M. G. Rossrnann, and C. R. Parrish. 2000. Host range and variability of calcium binding by surface loops in the capsids of canine and feline parvoviruses. J. Mol. Biol. 300:597-610.
54. Simpson, A. A., P. R. Chipman, T. S. Baker, P. Tijssen, and M. G. Rossmann. 1998. The structure of an insect parvovirus (Galleria mellonella densovirus) at 3.7 Å resolution. Structure 6:1355-1367.
55. Simpson, A. A., B. Hébert, G. M. Sullivan, C. R. Parrish, Z. Zádori, P. Tijssen, and M. G. Rossmann. 2002. The structure of the porcine parvovirus: comparison with related viruses. J. Mol. Biol. 315:1189-1198.
56. Spalhotz, B. A., and P. Tattersall. 1983. Interaction of minute virus of mice with differentiated cells: strain-dependent target cell specificity is mediated by intracellular factors. J. Virol. 46:937-939.
57. Strassheim, L. S., 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.
58. Tattersall, P., A. J. Shatkin, and P. Ward. 1977. Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111:375-394.
59. Tong, L., and M. G. Rossmann. 1997. Rotation function calculations with GLRF program. Methods Enzymol. 276:594-611.
60. Tresnan, D. B., L. Southard, W. Weichert, J.-Y. Sgro, and C. R. Parrish. 1995. Analysis of the cell and erythrocyte binding activities of the dimple and canyon regions of the canine parvovirus capsid. Virology 211:123-132.
61. Truyen, U., M. Agbandje, and C. R. Parrish. 1994. Characterization of the feline host range and a specific epitope of feline panleukopenia virus. Virology 200:494-503.
62. Truyen, U., J. F. Evermann, E. Vieler, and C. R. Parrish. 1996. Evolution of canine parvovirus involved loss and gain of feline host range. Virology 215:186-189.
63. Tsao, T., 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.
64. Walters, R., M. Agbandje-McKenna, V. D. Bowman, T. O. Moninger, N. H. Olson, M. Seiler, J. A. Chiorini, T. S. Baker, and J. Zabner. 2004. Structure of adeno-associated virus serotype 5. J. Virol. 78:3361-3371.
65. 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 15:595-607.
66. Willwand, K., and B. Hirt. 1993. The major capsid protein VP2 of minute virus of mice (MVM) can form particles which bind to the 3′-terminal hairpin of MVM replicative-form DNA and package single-stranded viral progeny DNA. J. Virol. 67:5660-5663.
67. Wu, H., W. Keller, and M. G. Rossmann. 1993. Determination and refinement of the canine parvovirus empty-capsid structure. Acta Crystallogr. D 49:572-579.
68. Xie, Q., W. Bu, S. Bhatia, J. Hare, T. Somasundaram, A. Azzi, and M. S. Chapman. 2002. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. USA 99:10405-10410.
69. Xie, Q., and M. S. Chapman. 1996. Canine parvovirus capsid structure, analyzed at 2.9 Å resolution. J. Mol. Biol. 264:497-520.