Linkage of reduced receptor affinity and superinfection to pathogenesis of TR1.3 murine leukemia virus

Journal of Virology

Volumn 80, Issue 9, 2006, Pages 4601-4609

  Murphy, Samuel L ^a   Chung Landers, Maeran ^a   Honczarenko, Marek ^b   Gaulton, Glen N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; GLYCOPROTEIN 70; TRYPTOPHAN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; BRAIN CAPILLARY; BRAIN HEMORRHAGE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEATH; ENDOTHELIUM CELL; FLOW CYTOMETRY; FRIEND LEUKEMIA VIRUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MURINE LEUKEMIA VIRUS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; RECEPTOR AFFINITY; SUPERINFECTION; SYNCYTIUM; VIRUS PARTICLE; VIRUS PATHOGENESIS;

ANIMALS; CATIONIC AMINO ACID TRANSPORTER 1; CELL LINE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; LEUKEMIA VIRUS, MURINE; MEMBRANE FUSION; MICE; RECEPTORS, VIRUS; SUPERINFECTION; VIRAL ENVELOPE PROTEINS; VIRION;

FRIEND MURINE LEUKEMIA VIRUS; MURINE LEUKEMIA VIRUS;

EID: 33646176035     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.9.4601-4609.2006     Document Type: Article

References (56)

1. Albritton, L. M., L. Tseng, D. Scadden, and J. M. Cunningham. 1989. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659-666.
2. Bae, Y., S. M. Kingsman, and A. J. Kingsman. 1997. Functional dissection of the Moloney murine leukemia virus envelope protein gp70. J. Virol. 71:2092-2099.
3. Battini, J. L., S. C. Kayman, A. Pinter, J. M. Heard, and O. Danos. 1994. Role of N-linked glycosylation in the activity of the Friend murine leukemia virus SU protein receptor-binding domain. Virology 202:496-499.
4. Berkowitz, R. D., and S. P. Goff. 1993. Point mutations in Moloney murine leukemia virus envelope protein: effects on infectivity, virion association, and superinfection resistance. Virology 196:748-757.
5. Bishayee, S., M. Strand, and J. T. August. 1978. Cellular membrane receptors for oncovirus envelope glycoprotein: properties of the binding reaction and influence of different reagents on the substrate and the receptors. Arch. Biochem. Biophys. 189:161-171.
6. Burns, J. C., T. Friedmann, W. Driever, M. Burrascano, and J. K. Yee. 1993. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc. Natl. Acad. Sci. USA 90:8033-8037.
7. Choppin, J., L. Schaffar-Deshayes, P. Debre, and J. P. Levy. 1981. Lymphoid cell surface receptor for Moloney leukemia virus envelope glycoprotein gp71. I. Binding characteristics. J. Immunol. 126:2347-2351.
8. Chung, M., K. Kizhatil, L. M. Albritton, and G. N. Gaulton. 1999. Induction of syncytia by neuropathogenic murine leukemia viruses depends on receptor density, host cell determinants, and the intrinsic fusion potential of envelope protein. J. Virol. 73:9377-9385.
9. Daniel, R., R. A. Katz, and A. M. Skalka. 1999. A role for DNA-PK in retroviral DNA integration. Science 284:644-647.
10. Davey, R, A., C. A. Hamson, J. J. Healey, and J. M. Cunningham. 1997. In vitro binding of purified murine ecotropic retrovirus envelope surface protein to its receptor, MCAT-1. J. Virol. 71:8096-8102.
11. Davey, R. A., Y. Zuo, and J. M. Cunningham. 1999. Identification of a receptor-binding pocket on the envelope protein of Friend murine leukemia virus. J. Virol. 73:3758-3763.
12. Etemad-Moghadam, B., Y. Sun, E. K. Nicholson, M. Fernandes, K. Liou, R. Gomila, J. Lee, and J. Sodroski. 2000. Envelope glycoprotein determinants of increased fusogenicity in a pathogenic simian-human immunodeficiency virus (SHIV-KB9) passaged in vivo. J. Virol. 74:4433-4440.
13. Pass, D., R. A. Davey, C. A. Hamson, P. S. Kim, J. M. Cunningham, and J. M. Berger. 1997. Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 angstrom resolution. Science 277:1662-1666.
14. Ganguly, K., V. S. Kalyanaraman, and M. G. Sarngadharan. 1983. Analysis of the interaction between Rauscher murine leukemia virus and murine cell membrane receptor by in vitro binding assay. Cancer Lett. 18:79-86.
15. Gorry, P. R., J. Taylor, G. H. Holm, A. Mehle, T. Morgan, M. Cayabyab, M. Farzan, H. Wang, J. E. Bell, K. Kunstman, J. P. Moore, S. M. Wolinsky, and D. Gabuzda. 2002. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J. Virol. 76:6277-6292.
16. Heard, J. M., and O. Danos. 1991. An amino-terminal fragment of the Friend murine leukemia virus envelope glycoprotein binds the ecotropic receptor. J. Virol. 65:4026-4032.
17. Hein, S., V. Prassolov, Y. Zhang, D. Ivanov, J. Lohler, S. R. Ross, and C. Stocking. 2003. Sodium-dependent myo-inositol transporter 1 is a cellular receptor for Mus cervicolor M813 murine leukemia virus. J. Virol. 77:5926-5932.
18. Hudson, T. J., D. M. Church, S. Greenaway, H. Nguyen, A. Cook, R. G. Steen, W. J. Van Etten, A. B. Castle, M. A. Strivens, P. Trickett, C. Heuston, C. Davison, A. Southwell, R. Hardisty, A. Varela-Carver, A. R. Haynes, P. Rodriguez-Tome, H. Doi, M. S. Ko, J. Pontius, L. Schriml, L. Wagner, D. Maglott, S. D. Brown, E. S. Lander, G. Schuler, and P. Denny. 2001. A radiation hybrid map of mouse genes. Nat. Genet. 29:201-205.
19. Kadan, M. J., S. Sturm, W. F. Anderson, and M. A. Eglitis. 1992. Detection of receptor-specific murine leukemia virus binding to cells by immunofluorescence analysis. J. Virol. 66:2281-2287.
20. Kalyanaraman, V. S., M. G. Sarngadharan, and R. C. Gallo. 1978. Characterization of Rauscher murine leukemia virus envelope glycoprotein receptor in membranes from murine fibroblasts. J. Virol. 28:686-696.
21. Karlsson, G. B., M. Halloran, D. Schenten, J. Lee, P. Racz, K. Tenner-Racz, J. Manola, R. Gelman, B. Etemad-Moghadam, E. Desjardins, R. Wyatt, N. P. Gerard, L. Marcon, D. Margolin, J. Fanton, M. K. Axthelm, N. L. Letvin, and J. Sodroski. 1998. The envelope glycoprotein ectodomains determine the efficiency of CD4+ T lymphocyte depletion in simian-human immuno-deficiency virus-infected macaques. J. Exp. Med. 188:1159-1171.
22. Kim, J. W., E. I. Closs, L. M. Albritton, and J. M. Cunningham. 1991. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature 352:725-728.
23. Kuhmann, S. E., E. J. Platt, S. L. Kozak, and D. Kabat. 2000. Cooperation of multiple CCR5 coreceptors is required for infections by human immuno-deficiency virus type 1. J. Virol. 74:7005-7015.
24. LaBranche, C. C., M. M. Sauter, B. S. Haggarty, P. J. Vance, J. Romano, T. K. Hart, P. J. Bugelski, and J. A. Hoxie. 1994. Biological, molecular, and structural analysis of a cytopatliic variant from a molecularly cloned simian immunodeficiency virus. J. Virol. 68:7665-7667.
25. LaBranche, C. C., M. M. Sauter, B. S. Haggarty, P. J. Vance, J. Romano, T. K. Hart, P. J. Bugelski, M. Marsh, and J. A. Hoxie. 1995. A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells. J. Virol. 69:5217-5227.
26. Landers, M. C., N. Dugger, M. Quadros, P. M. Hoffman, and G. N. Gaulton. 2004. Neuropathogenic murine leukemia virus TR1.3 induces selective syncytia formation of brain capillary endothelium. Virology 321:57-64.
27. Lavillette, D., B. Boson, S. J. Russell, and F. L. Cosset. 2001. Activation of membrane fusion by murine leukemia viruses is controlled in cis or in trans by interactions between the receptor-binding domain and a conserved disulfide loop of the carboxy terminus of the surface glycoprotein. J. Virol. 75:3685-3695.
28. Lavillette, D., M. Maurice, C. Roche, S. J. Russell, M. Sitbon, and F. L. Cosset. 1998. A praline-rich motif downstream of the receptor binding domain modulates conformation and fusogenicity of murine retroviral envelopes. J. Virol. 72:9955-9965.
29. Lavillette, D., A. Ruggieri, B. Boson, M. Maurice, and F. L. Cosset. 2002. Relationship between SU subdomains that regulate the receptor-mediated transition from the native (fusion-inhibited) to the fusion-active conformation of the murine leukemia virus glycoprotein. J. Virol. 76:9673-9685.
30. Lu, C. W., and M. J. Roth. 2003. Role of the mutation Q252R in activating membrane fusion in the murine leukemia virus surface envelope protein. J. Virol. 77:10841-10849.
31. Matano, T., T. Odawara, M. Ohshima, H. Yoshikura, and A. Iwamoto. 1993. trans-dominant interference with virus infection at two different stages by a mutant envelope protein of Friend murine leukemia virus. J. Virol. 67:2026-2033.
32. McCarthy, L. C., J. Terrett, M. E. Davis, C. J. Knights, A. L. Smith, R. Critcher, K. Schmitt, J. Hudson, N. K. Spurr, and P. N. Goodfellow. 1997. A first-generation whole genome-radiation hybrid map spanning the mouse genome. Genome Res. 7:1153-1161.
33. Panda, B. R., S. M. Kingsman, and A. J. Kingsman. 2000. Mutational analysis of the putative receptor-binding domain of Moloney murine leukemia virus glycoprotein gp70. Virology 273:90-100.
34. Park, B. H., E. Lavi, K. J. Blank, and G. N. Gaulton. 1993. Intracerebral hemorrhages and syncytium formation induced by endothelial cell infection with a murine leukemia virus. J. Virol. 67:6015-6024.
35. Park, B. H., E. Lavi, and G. N. Gaulton. 1994. Intracerebral hemorrhages and infarction induced by a murine leukemia virus is influenced by host determinants within endothelial cells. Virology 203:393-396.
36. Park, B. H., E. Lavi, A. Stieber, and G. N. Gaulton. 1994. Pathogenesis of cerebral infarction and hemorrhage induced by a murine leukemia virus. Lab. Investig. 70:78-85.
37. Park, B. H., B. Matuschke, E. Lavi, and G. N. Gaulton. 1994. A point mutation in the env gene of a murine leukemia virus induces syncytium formation and neurologic disease. J. Virol. 68:7516-7524.
38. Pasieka, T. J., L. Maresova, K. Shiraki, and C. Grose. 2004. Regulation of varicella-zoster virus-induced cell-to-cell fusion by the endocytosis-competent glycoproteins gH and gE. J. Virol. 78:2884-2896.
39. Ragheb, J. A., H. Yu, T. Hofmann, and W. F. Andersen. 1995. The amphotropic and ecotropic murine leukemia virus envelope TM subunits are equivalent mediators of direct membrane fusion: implications for the role of the ecotropic envelope and receptor in syncytium formation and viral entry. J. Virol. 69:7205-7215.
40. Rocancourt, D., C. Bonnerot, H. Jouin, M. Emerman, and J. F. Nicolas. 1990. Activation of a β-galactosidase recombinant provirus: application to titration of human immunodeficiency virus (HIV) and HIV-infected cells. J. Virol. 64:2660-2668.
41. Ross, S. R., J. J. Schofleld, C. J. Farr, and M. Bucan. 2002. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. USA 99:12386-12390.
42. Rowe, L. B., M. E. Barter, and J. T. Eppig. 2000. Cross-referencing radiation hybrid data to the recombination map: lessons from mouse chromosome 18. Genomics 69:27-36.
43. Rowe, W. P., W. E. Pugh, and J. W. Hartley. 1970. Plaque assay techniques for murine leukemia viruses. Virology 42:1136-1139.
44. Rubin, H. 1960. A virus in chick embryos which induces resistance in vitro to infection with Rous sarcoma virus. Proc. Natl. Acad. Sci. USA 46:1105-1119.
45. Sauter, M. M., A. Pelchen-Matthews, R. Bron, M. Marsh, C. C. LaBranche, P. J. Vance, J. Romano, B. S. Haggarty, T. K. Hart, W. M. Lee, and J. A. Hoxie. 1996. An internalization signal in the simian immunodeficiency virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface. J. Cell Biol. 132:795-811.
46. Siess, D. C., S. L. Kozak, and D. Kabat. 1996. Exceptional fusogenicity of Chinese hamster ovary cells with murine retroviruses suggests roles for cellular factor(s) and receptor clusters in the membrane fusion process. J. Virol. 70:3432-3439.
47. Sisk, W. P., J. D. Bradley, R. J. Leipold, A. M. Stoltzfus, M. Ponce de Leon, M. Hilf, C. Peng, G. H. Cohen, and R. J. Eisenberg. 1994. High-level expression and purification of secreted forms of herpes simplex virus type 1 glycoprotein gD synthesized by baculovirus-infected insect cells. J. Virol. 68:766-775.
48. Sitbon, M., B. Sola, L. Evans, J. Nishio, S. F. Hayes, K. Nathanson, C. F. Garon, and B. Chesebro. 1986. Hemolytic anemia and erythroleukemia, two distinct pathogenic effects of Friend MuLV: mapping of the effects to different regions of the viral genome. Cell 47:851-859.
49. Spitzer, D., K. E. Dittmar, M. Rohde, H. Hauser, and D. Wirth. 2003. Green fluorescent protein-tagged retroviral envelope protein for analysis of virus-cell interactions. J. Virol. 77:6070-6075.
50. Steck, F. T., and H. Rubin. 1966. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology 29:642-653.
51. Szurek, P. F., and B. R. Brooks. 2000. Synthesis of virus-specific high-mobility DNA after temperature upshift of SC-1 cells chronically infected with moloney murine leukemia virus mutant M. J. Virol. 74:7055-7063.
52. Van Etten, W. J., R. G. Steen, H. Nguyen, A. B. Castle, D. K. Slonim, B. Ge, C. Nusbaum, G. D. Schuler, E. S. Lander, and T. J. Hudson. 1999. Radiation hybrid map of the mouse genome. Nat. Genet. 22:384-387.
53. Wang, H., M. P. Kavanaugh, R. A. North, and D. Kabat. 1991. Cell-surface receptor for ecotropic murine retroviruses is a basic amino-acid transporter. Nature 352:729-731.
54. Watkins, B. A., R. Crowley, A. E. Davis, A. T. Louie, and M. S. Reitz, Jr. 1997. Syncytium formation induced by human immunodeficiency virus type 1 isolates correlates with affinity for CD4. J. Gen. Virol. 78:2513-2522.
55. Weiss, R., N. Teich, H. Varmus, and J. Coffin (ed.). 1984. RNA tumor viruses, vol. 1, p. 210-260. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
56. Yoshimura, F. K., T. Wang, and S. Nanua. 2001. Mink cell focus-forming murine leukemia virus killing of mink cells involves apoptosis and superinfection. J. Virol. 75:6007-6015.