Genetics of host resistance to retroviruses and cancer

Retroviruses and Insights into Cancer

Volumn , Issue , 2011, Pages 95-118

  Okeoma, Chioma M ^a   Ross, Susan R ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Innate immunity; Intrinsic immunity; Oncogene; Virus receptor; Virus resistance genes

Indexed keywords

EID: 84865100938     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-09581-3_4     Document Type: Chapter

References (161)

1. Abudu, A., Takaori-Kondo, A., Izumi, T., et al. 2006. Murine retrovirus escapes from murine APOBEC3 via two distinct novel mechanisms. Curr. Biol. 16:1565-1570.
2. Acha-Orbea, H, Shakhov, A. N., Scarpellino, L., et al. 1991. Clonal deletion of Vb14-bearing T cells in mice transgenic for mammary tumor virus. Nature 350:207-210.
3. Albritton, L. M., Tseng, L., Scadden, D., et al. 1989. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659-666.
4. Arnaud, F., Caporale, M., Varela, M., et al. 2007. A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog. 3:e170-e170
5. An, P., Bleiber, G., Duggal, P., et al. 2004. APOBEC3G genetic variants and their influence on the progression to AIDS. J. Virol. 78:11070-11076.
6. Bacon, L. D., Hunt, H. D., Cheng, H. H. 2000. A review of the development of chicken lines to resolve genes determining resistance to diseases. Poult. Sci. 79:1082-1093.
7. Baillie, G. J., van de Lagemaat, L. N., Baust, C., et al. 2004. Multiple groups of endogenous betaretroviruses in mice, rats and other mammals. J. Virol. 78:5784-5798.
8. Ball, J. K., Arthur L. O., Dekaban G. A. 1985. The involvement of type-B retrovirus in the induction of thymic lymphomas. Virology 140:159-172.
9. Barnard, R. J. O., Elleder, D., Young, J. A. T. 2006. Avian sarcoma and leukosis virus-receptor interactions: From classical genetics to novel insights into virus-cell membrane fusion. Virology 344:25-29.
10. Bates, P., Young, J. A. T., Varmus, H. E. 1993. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell 74:1043-1051.
11. Begovich, A. B., Vu, T. H., Jones, P. P. 1990. Characterization of the molecular defects in the mouse E beta f and E beta q genes. Implications for the origin of MHC polymorphism. J. Immunol. 144:1957-1964.
12. Bentvelzen, P., Brinkhof, J., Haaijman, J. J. 1978. Genetic control of endogenous murine mammary tumour viruses reinvestigated. Eur J Cancer 14:1137-1147.
13. Berkhout, B., Grigoriev, A., Bakker, M., et al. 2002. Codon and amino acid usage in retroviral genomes is consistent with virus-specific nucleotide pressure. AIDS Res. and Hum. Retroviruses 18:133-141.
14. Best, S., Le Tissier P., Towers G., et al. 1996. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382:826-829.
15. Beutler B. 2000. Tlr4: Central component of the sole mammalian LPS sensor. Curr. Opinion in Immunol. 12:20-26.
16. Beutner, U., McLellan B., Draus E., et al. 1996. Lack of MMTV superantigen presentation in MHC Class II-deficient mice. Cell Immunol. 168:141-147.
17. Bhadra, S., Lozano, M. M., Dudley, J. P. 2005. Conversion of mouse mammary tumor virus to a lymphomagenic virus. J. Virol. 79:12592-12596.
18. Bhadra, S., Lozano, M. M., Payne, S. M., et al. 2006. Endogenous MMTV proviruses induce susceptibility to both viral and bacterial pathogens. PLoS Pathog. 2:e128-e128.
19. Bieniasz, P. D. 2004. Intrinsic immunitye: A front-line defense against viral attack. Nat. Immunol. 5:1109-1115.
20. Bishop, K. N., Verma, M., Kim, E. Y., et al. 2008. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 4:e1000231.
21. Bittner, J. J. 1936. Some possible effects of nursing on the mammary gland tumor incidence in mice. Science 84:162.
22. Bramblett, D., Liu, J., Lozano, M., et al. 1997. Mouse mammary tumor virus: A virus that exploits the immune system. Leukemia. 11 Suppl. 3:183-186.
23. Brojatsch, J., Naughton, J., Rolls, M. M., et al. 1996. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845-855.
24. Browne, E. P., and Littman, D. R. 2008. Species specific restriction of Apobec3 mediated hypermutation. J. Virol. in Press.
25. Buggiano, V., Goldman, A., Nepomnaschy, I., et al. 1999. Characterization of two infectious mouse mammary tumor viruses: Superantigenicity and tumorigenicity. Scand J. Immunol. 49:269-277.
26. Burzyn, D., Rassa, J. C., Kim, D., et al. 2004. Toll-like receptor 4-dependent activation of dendritic cells by a retrovirus. J. Virol. 78:576-584.
27. Callahan, R., Sherr, C. J., Todaro, G. J. 1977. A new class of murine retroviruses: Immunological and biochemical comparison of novel isolates from Mus cervicolor and Mus caroli. Virology 80:401-416.
28. Case, L. K., Petell, L., Yurkovetskiy, L., et al. 2008. Replication of beta-and gammaretroviruses is restricted in I/LnJ mice via the same genetic mechanism. J. Virol.
29. Case, L. K., Purdy, A., Golovkina, T. V. 2005. Molecular and cellular basis of the retrovirus resistance in I/LnJ mice. J. Immunol. 175:7543-7549.
30. Chai, N., and Bates, P. 2006. Na+/H+ exchanger type 1 is a receptor for pathogenic subgroup J avian leukosis virus. Proc Natl Acad Sci U S A. 103:5531-5536.
31. Chesebro, B., and Wehrly, K. 1978. Rfv-1 and Rfv-2, two H-2-associated genes that influence recovery from Friend leukemia virus-induced splenomegaly. J. Immunol. 120:1081-1085.
32. Chesebro, B., and Wehrly, K. 1979. Identification of a non-H-2 gene (Rfv-3) influencing recovery from viremia and leukemia induced by Friend virus complex. Proc. Natl. Acad. Sci. U S A 76:425-429.
33. Chesters, P. M., Howes, K., Petherbridge, L., et al. 2002. The viral envelope is a major determinant for the induction of lymphoid and myeloid tumours by avian leukosis virus subgroups A and J, respectively. J. Gen. Virol. 83:2553-2561.
34. Chiu, Y. L., and Greene, W. C. 2006. APOBEC3 cytidine deaminases: distinct antiviral actions along the retroviral life cycle. J. Biol. Chem. 281:8309-8312.
35. Chiu, Y. L., Soros, V. B., Kreisberg, J. F., et al. 2005. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435:108-114.
36. Choi, Y., Kappler, J. W., Marrack, P. 1991. A super antigen encoded in the open reading frame of the 3' long terminal repeat of the mouse mammary tumor virus Nature 350:203-207.
37. Clausse, N., Smith, R., Calberg-Bacq, C. M., et al. 1993. Mouse mammary-tumor virus activates Fgf-3/Int-2 less frequently in tumors from virgin than from parous mice. Int. J. Cancer 55:157-163.
38. Courreges, M. C., Burzyn, D., Nepomnaschy, I., et al. 2007. Critical role of dendritic cells in mouse mammary tumor virus in vivo infection. J. Virol. 81:3769-3777.
39. Cullen, B. R. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80:1067-1076.
40. Dandekar, S., Rossito, P., Pickett, S., et al. 1987. Molecular characterization of the Akvr1 restriction gene: A defective endogenous retrovirus-borne gene identical to Fv4-r. J. Virol. 61:308-314.
41. Debre, P., Gisselbrecht, S., Pozo, F., et al. 1979. Genetic control of sensitivity to Moloney leukemia virus in mice. II. Mapping of three resistant genes within the H-2 complex. J. Immunol. 123:1806-1812.
42. Dembic, Z., Ayane, M., Klein, J., et al. 1985. Inbred and wild mice carry identical deletions in their E alpha MHC genes. EMBO J. 4:127-131.
43. DesGroseillers, L., and Jolicoeur, P. 1983. Physical mapping of the Fv-1 tropism host range determinant of BALB/c murine leukemia viruses. J. Virol. 46:685-696.
44. Dudley, J., and Risser, R. 1984. Amplification and novel locations of endogenous mouse mammary tumor virus genomes in mouse T-cell lymphomas. J. Virol. 49:92-101.
45. Dux, A. 1972. Genetic aspects in the genesis of mammary cancer. In RNA Viruses and Host Genome in Oncogenesis, eds. P. Emmelot, and P. Bentvelzen, pp. 301-308. Amsterdam: North-Holland Publ.
46. Dux, A., and Demant, P. 1987. MHC-controlled susceptibility to C3H-MTV-induced mouse mammary tumors is predominantly systemic rather than local. Int. J Cancer 40:372-377.
47. Dzuris, J. L., Golovkina, T. V., and Ross, S. R. 1997. Both T and B cells shed infectious MMTV. J. Virol. 71:6044-6048.
48. Dzuris, J. L., Zhu, W., Golovkina, T. V., et al. 1999. Lack of receptor interference by endogenous expression of the mouse mammary tumor virus envelope protein. Virology 263:418-426.
49. Elleder, D., Stepanets, V., Melder, D. C., et al. 2005. The receptor for the subgroup C avian sarcoma and leukosis viruses, Tvc, is related to mammalian butyrophilins, members of the immunoglobulin superfamily. J. Virol. 79:10408-10419.
50. Finke, D., and Acha-Orbea, H. 2001. Differential migration of in vivo primed B and T lymphocytes to lymphoid and non-lymphoid organs. Eur. J. Immunol. 31:2603-2611.
51. Finke, D., Luther, S. A., and Acha-Orbea, H. 2003. The role of neutralizing antibodies for mouse mammary tumor virus transmission and mammary cancer development. Proc. Natl. Acad. Sci. U S A. 100:199-204.
52. Goff, S. P. 2004a. Genetic control of retrovirus susceptibility in mammalian cells. Annu. Rev. Genet. 38:61-85.
53. Goff, S. P. 2004b. Retrovirus restriction factors. Mol. Cell 16:849-859.
54. Golovkina, T. V., Chervonsky, A., Dudley, J. P., et al. 1992. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell 69:637-645.
55. Golovkina, T. V., Dudley, J. P., and Ross, S. R. 1998. Superantigen activity is need for mouse mammary tumor virus spread within the mammary gland. J. Immunol. 161:2375-2382.
56. Golovkina, T. V., Prescott, J. A., and Ross, S. R. 1993. Mouse mammary tumor virus-induced tumorigenesis in sag transgenic mice: A laboratory model of natural selection. J. Virol. 67:7690-7694.
57. Harris, R. S., Bishop, K. N., Sheehy, A. M., et al. 2003. DNA deamination mediates innate immunity to retroviral infection. Cell 113:803-809.
58. Hasenkrug, K. J., and Chesebro, B. 1997. Immunity to retroviral infection: The Friend virus model. Proc. Natl. Acad. Sci. U S A. 94:7811-7816.
59. Hasenkrug, K. J., Valenzuela, A., Letts, V. A., et al. 1995. Chromosome mapping of Rfv3, a host resistance gene to Friend murine retrovirus. J. Virol. 69:2617-2620.
60. Held W., Waanders, G., Shakhov, A. N., et al. 1993. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell 74:529-540.
61. Held, W., Waanders, G. A., MacDonald, H. R., et al. 1994. MHC class II hierarchy of superantigen presentation predicts efficiency of infection with mouse mammary tumor virus. Int Immunol. 6:1403-1407.
62. Hoatlin, M. E., and Kabat, D. 1995. Host-range control of a retroviral disease: Friend erythroleukemia. Trends Microbiol. 3:51-57.
63. Holmes, R. K., Malim, M. H., and Bishop, K. N. 2007. APOBEC-mediated viral restriction: Not simply editing? TIBS. 32:118-128.
64. Hook, L. M., Agafonova, Y., Ross, S. R., et al. 2000. Genetics of mouse mammary tumor virusinduced mammary tumors: Linkage of tumor induction to the gag gene. J. Virol. 74:8876-8883.
65. Ignatowicz, L., Kappler, J., and Marrack, P. 1992. The effects of chronic infection with a superantigen-producing virus. J. Exp Med. 175:917-923.
66. Ikeda, H., Sato, H., and Odaka, T. 1981. Mapping of the Fv-4 mouse gene controlling resistance to murine leukemia viruses. Int. J. Cancer 28:237-240.
67. Ikeda, H., and Sugimura, H. 1989. Fv-4 resistance gene: A truncated endogenous murine leukemia virus with ecotropic interference properties. J. Virol. 63:5405-5412.
68. Jenkins, N. A., Copeland, N. G., Taylor, B. A., et al. 1982. Ecotropic murine leukemia virus DNA content of normal and lymphomatous tissues of BXH-2 recombinant inbred mice. J. Virol. 42:379-388.
69. Jolicoeur, P., and Baltimore, D. 1976. Effect of Fv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses. Proc. Natl. Acad. Sci. U S A. 73:2236-2240.
70. Jude, B. A., Pobezinskaya, Y., Bishop, J., et al. 2003. Subversion of the innate immune system by a retrovirus. Nat. Immunol. 4:573-578.
71. Jung, Y. T., and Kozak, C. A. 2000. A single amino acid change in the murine leukemia virus capsid gene responsible for the Fv1(nr) phenotype. J. Virol. 74:5385-5387.
72. Kanari, Y., Clerici, M., Abe, H., et al. 2005. Genotypes at chromosome 22q12-13 are associated with HIV-1-exposed but uninfected status in Italians. AIDS. 19:1015-1024.
73. Kozak, C. A., and Chakraborti, A. 1996. Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance. Virology 225:300-305.
74. Kozak, C., et al. 1987. A standardized nomenclature for endogenous mouse mammary tumor viruses. J. Virol. 61:1651-1654.
75. Lander, E. S., et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
76. LaRue, R. S., et al. 2009. Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83:494-497.
77. Liddament, M. T., Brown, W. L., Schumacher, A. J., et al. 2004. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14:1385-1391.
78. Lilly, F. 1966. The inheritance of susceptibility to the Gross leukemia virus in mice. Genetics 53:529-539.
79. Lilly, F. 1968. The effect of histocompatibility-2 type on response to friend leukemia virus in mice. J. Exp. Med. 127:465-473.
80. Limjoco, T. I., Dickie, P., Ikeda, H., et al. 1993. Transgenic Fv-4 mice resistant to Friend virus. J. Virol. 67:4163-4168.
81. Liu, R., Paxton, W. A., Choe, S., et al. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-378.
82. Liu, S. L., and Miller, A. D. 2007. Oncogenic transformation by the jaagsiekte sheep retrovirus envelope protein. Oncogene 26:789-801.
83. Lonai, P., and Haran-Ghera, N. 1977. Resistance genes to murine leukemia in the I immune response gene region of the H-2 complex. J. Exp. Med. 146:1164-1168.
84. Low, A., Okeoma, C. M., Lovsin, N., et al. 2009. Enhanced replication and pathogenesis of moloney murine leukemia virus in mice defective in the murine APOBEC3 gene. Virology 385:455-463.
85. Luther, S. A., Gulbranson-Judge, A., Acha-Orbea, H., et al. 1996. Viral superantigen drives extrafollicular and follicular B cell differentiation leading to virus-specific antibody production. J. Exp. Med. 185:551-562.
86. MacDearmid, C. C., Case L. K., Starling, C. L., et al. 2006. Gradual elimination of retroviruses in YBR/Ei mice. J. Virol. 80:2206-2215.
87. Maeda, N., Palmarini, M., Murgia, C., et al. 2001. Direct transformation of rodent fibroblasts by jaagsiekte sheep retrovirus DNA. Proc. Natl. Acad. Sci. U S A. 98:4449-4454.
88. Mangeat, B., Turelli, P., Caron, G., et al. 2003. Broad antiretroviral defense by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103.
89. Mariani, R., Chen, D., Schrofelbauer, B., et al. 2003. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114:21-31.
90. Marin, M., Rose, K. M., Kozak, S. L., et al. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9:1398-1403.
91. Marrack, P., Kushnir, E., and Kappler, J. 1991. A maternally inherited superantigen encoded by mammary tumor virus. Nature 349:524-526.
92. Martin, P., Ruiz, S. R., Martinez del Hoyo, G., et al. 2002. Dramatic increase in lymph node dendritic cell numbers during infection by the mouse mammary tumor virus occurs by a CD62Ldependent blood-borne DC recruitment. Blood 99:1282-1288.
93. Matano, T., Odawara, T., Ohshima, M., et al. 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.
94. Mertz, J. A., Simper, M. S., Lozano, M. M., et al. 2005. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 79:14737-14747.
95. Mikl, M. C., Watt, I. N., Lu, M., et al. 2005. Mice deficient in APOBEC2 and APOBEC3. Mol. Cell. Biol. 25:7270-7277.
96. Miyazawa, M., Nishio, J., Wehrly, K., et al. 1992. Spontaneous recovery from Friend retrovirusinduced leukemia. Mapping of the Rfv-2 gene in the Q/TL region of mouse MHC. J. Immunol. 148:1964-1967.
97. Miyazawa, M., Tsuji-Kawahara, S., and Kanari, Y. 2008. Host genetic factors that control immune responses to retrovirus infections. Vaccine 26:2981-2996.
98. Moore, J. P., and Doms, R. W. 2003. The entry of entry inhibitors: A fusion of science and medicine. Proc. Natl. Acad. Sci. U S A. 100:10598-10602.
99. Morris, V. L., Medeiros, E., Ringold, G. M., et al. 1977. Comparison of mouse mammary tumor virus-specific DNA in inbred, wild and Asian mice, and in tumors and normal organs from inbred mice. J. Mol. Biol. 114:73-91.
100. Moyes, D., Griffiths, D. J., and Venables, P. J. 2007. Insertional polymorphisms: A new lease of life for endogenous retroviruses in human disease. Trends Genet. 23:326-333.
101. Murcia, P. R., Arnaud, F., and Palmarini, M. 2007. The transdominant endogenous retrovirus enJS56A1 associates with and blocks intracellular trafficking of Jaagsiekte sheep retrovirus Gag. J. Virol. 81:1762-1772.
102. Mustafa, F., Bhadra, S., Johnston, D., et al. 2003. The type B leukemogenic virus truncated superantigen is dispensable for T-cell lymphomagenesis. J. Virol. 77:3866-3870.
103. Nandi, S., Handin, M., Robinson, A., et al. 1966. Susceptibility of mammary tissues of "genetically resistant" strains of mice to mammary tumor virus. J. Natl. Cancer Inst. 36:783-80.
104. Nandi, S., and McGrath, C. M. 1973. Mammary neoplasia in mice. Adv. Canc. Res. 17:353-414.
105. Nishigaki, K., Thompson, D., Hanson, C., et al. 2001. The envelope glycoprotein of friend spleen focus-forming virus covalently interacts with and constitutively activates a truncated form of the receptor tyrosine kinase Stk. J. Virol. 75:7893-7903.
106. Nisole, S., Stoye, J. P., and Saib, A. 2005. Trim family proteins: retroviral restriction and antiviral defence. Nature Rev. Microbiol. 3:799-808.
107. Odaka, T., Ikeda, H., Moriwaki, K., et al. 1978. Genetic resistance in Japanese wild mice (Mus musculus molossinus) to an NB-tropic Friend murine leukemia virus. J. Natl. Cancer Inst. 61:1301-1306.
108. Odaka, T., Ikeda, H., Yoshikura, H., et al. 1981. Fv-4: Gene controlling resistance to NB-tropic Friend murine leukemia virus. Distribution in wild mice, introduction into genetic background of BALB/c mice, and mapping of chromosomes. J. Natl. Cancer Inst. 67:1123-1127.
109. Okeoma, C. M., Lovsin, N., Peterlin, B. M., et al. 2007. APOBEC3 inhibits mouse mammary tumor virus replication in vivo. Nature 445:927-930.
110. Okeoma, C. M., Shen, M., and Ross, S. R. 2008. A novel block to mouse mammary tumor virus infection of lymphocytes in B10.BR mice. J. Virol. 82:1314-1322.
111. Okeoma, C. M., Petersen, J., and Ross, S. R. 2009a. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J. Virol. 83:3029-3028.
112. Okeoma, C. M., Low, W., Bailis, W., et al. 2009b. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J. Virol. 83:3486-3495.
113. Okimoto, M. A., and Fan, H. 1999. Moloney murine leukemia virus infects cells of the developing hair follicle after neonatal subcutaneous inoculation in mice. J. Virol. 73:2509-2516.
114. Outzen, H. C., Morrow, D., and Shultz, L. D. 1985. Attenuation of exogenous murine mammary tumor virus virulence in the C3H/HeJ mouse substrain bearing the Lps mutation. J. Natl. Canc. Inst. 75:917-923.
115. Overbaugh, J., Miller, A. D., and Eiden, M. V. 2001. Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol. and Mol. Biol. Rev. 65:371-389.
116. Palmarini, M., Datta, S., Omid, R., et al. 2000. The long terminal repeat of Jaagsiekte sheep retrovirus is preferentially active in differentiated epithelial cells of the lungs. J. Virol. 74:5776-5787.
117. Palmarini, M., Maeda, N., Murgia, C., et al. 2001. A phosphatidylinositol 3-kinase docking site in the cytoplasmic tail of the Jaagsiekte sheep retrovirus transmembrane protein is essential for envelope-induced transformation of NIH 3T3 cells. J. Virol. 75:11002-11009.
118. Palmarini, M., Mura, M., and Spencer, T. E. 2004. Endogenous betaretroviruses of sheep: Teaching new lessons in retroviral interference and adaptation. J. Gen. Virol. 85:1-13.
119. Papiernik, M., Pontoux, C., and Golstin, P. 1995. Non-exclusive Fas control and age dependence of viral superantigen-induced clonal deletion in lupus-prone mice. Eur. J. Immunol. 25:1517-1523.
120. Pataer, A., Kamoto, T., Lu, L. M., et al. 1996. Two dominant host resistance genes to pre-B lymphoma in wild-derived inbred mouse strain MSM/Ms. Cancer Res. 56:3716-3720.
121. Paxton, W. A., Martin, S. R., Tse D., et al. 1996. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat. Med. 2:412-417.
122. Payne, L. N., Brown, S. R., Bumstead, N., et al. 1991. A novel subgroup of exogenous avian leukosis virus in chickens. J. Gen. Virol. 72:801-807.
123. Payne, S. H., and Elder, J. H. 2001. The role of retroviral dUTPases in replication and virulence. Curr. Protein. Pept. Sci. 2:381-388.
124. Persons, D. A., Paulson, R. F., Loyd, M. R., et al. 1999. Fv2 encodes a truncated form of the Stk receptor tyrosine kinase. Nature Genetics. 23:159-165.
125. Pion, M., Granelli-Piperno, A., Mangeat, B., et al. 2006. APOBEC3G/3F mediates intrinsic resistance of moncyte-derived dendritic cells to HIV-1 infection. J. Exp. Med. 203:2887-2893.
126. Pucillo, C., Cepeda, R., and Hodes, R. J. 1993. Expression of a MHC Class II transgene determines superantigenicity and susceptibility to mouse mammary tumor virus infection. J. Exp. Med. 178:1441-1445
127. Purdy, A., Case, L., Duvall, M., et al. 2003. Unique resistance of I/LnJ mice to a retrovirus is due to sustained IFN-gamma dependent production of virus-neutralizing antibodies. J. Exp. Med. 197:233-243.
128. Rai, S. K., Duh, F. M., Vigdorovich, V., et al. 2001. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc. Natl. Acad. Sci. U S A. 98:4443-4448.
129. Rassa, J. C., Meyers, J. L., Zhang, Y., et al. 2002. Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc Natl Acad Sci USA. 99:2281-2286.
130. Richardson, D. M. 1973. Spontaneous mammary tumor incidence in C3H/HeJ mice. Jax. Notes 413:1-3.
131. Ross, S. R., Schofield, J. J., Farr, C. J., et al. 2002. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. U S A. 99:12386-12390.
132. Ross, S. R. 2009. Are viruses inhibited by APOBEC3 molecules from their host species? PLoS Pathog.ens 5:e1000347. doi:10.1371/journal.ppat.1000347
133. Rulli, K., Lenz, J., and Levy, L. S. 2002. Disruption of hematopoiesis and thymopoiesis in the early premalignant stages of infection with SL3-3 murine leukemia virus. J. Virol. 76:2363-2374.
134. Rulli, S. J., Mirro, J., Hill, S. A., et al. 2008. Interactions of murine APOBEC3 and human APOBEC3G with murine leukemia viruses. J. Virol. 82: 6566-6575.
135. Ruscetti, S., Matthai, R., and Potter, M. 1985. Susceptibility of BALB/c mice carrying various DBA/2 genes to development of Friend murine leukemia virus-induced erythroleukemia. J. Exp. Med. 162:1579-1587.
136. Sarkar, N. H., Golovkina, T., and Uz-Zaman, T. 2004. RIII/Sa mice with a high incidence of mammary tumors express two exogenous strains and one potential endogenous strain of mouse mammary tumor virus. J. Virol. 78:1055-1062.
137. Santiago M L, Montano M, Benitez R, et al. (2008) Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science 321:1343-1346
138. Sheehy, A. M., Gaddis, N. C., Choi, J. D., et al. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
139. Shirakawa, K., Takaori-Kondo, A., Kobayashi, M., et al. 2006. Ubiquitination of APOBEC3 proteins by the Vif-Cullin5-ElonginB-ElonginC complex. Virology 344:263-266.
140. Silverman, R. H. 2007. Viral encounters with 2',5'-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81:12720-12729.
141. Simard, J., Dumont, M., Soucy, P., et al. 2002. Perspective: Prostate cancer susceptibility genes. Endocrinology 143:2029-2040.
142. Steeves, R., and Lilly, F. 1977. Interactions between host and viral genomes in mouse leukemia. Annu. Rev. Genet. 11:277-296.
143. Swanson, I., Jude, B. A., Zhang, A. R., et al. 2006. Sequences within the gag gene of mouse mammary tumor virus needed for mammary gland cell transformation. J. Virol. 80:3215-3224.
144. Takeda, E., Tsuji-Kawahara, S., Sakamoto, M., et al. 2008. Mouse APOBEC3 restricts Friend leukemia virus infection and pathogenesis in vivo. J. Virol. 82:10998-11008.
145. Talbot, S. J., and Crawford, D. H. 2004. Viruses and tumours-an update. Eur. J. Cancer 40:1998-2005.
146. Taylor, G. M., Gao, Y., and Sanders, D. A. 2001. Fv-4: Identification of the defect in Env and the mechanism of resistance to ecotropic murine leukemia virus. J. Virol. 75:11244-11248.
147. Towers, G. J. 2007. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 440.
148. Tsubura, A., Inaba, M., Imai, S., et al. 1988. Intervention of T-cells in transportation of mouse mammary tumor virus (milk factor) to mammary gland cells in vivo. Canc. Res. 48:6555-6559.
149. Urisman, A., Molinaro, R. J., Fischer, N., et al. 2006. Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog. 2:e25.
150. Vacheron, S., Luther, S. J., and Acha-Orbea, H. 2002. Preferential infection of immature dendritic cells and B cells by mouse mammary tumor virus. J. Immunol. 168:3470-3476.
151. Weiss, R. A. 1993. Cellular receptors and viral glycoproteins involved in retrovirus entry. In Retroviridae, ed. J. A. Levy, pp. 1-108. New York: Plenum Press
152. Weiss, R. A. 2001. Retroviruses and cancer. Curr. Sci. 81:528-534.
153. Wiegand, H. L., Doehle, B. P., Bogerd, H. P., et al. 2004. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO. J. 23:2451-2458.
154. Wrona, T., and Dudley, J. P. 1996. Major histocompatibility complex class II I-E independent transmission of C3H mouse mammary tumor virus. J. Virol. 70:1246-1249.
155. Wu, T., Yan, Y., and Kozak, C. A. 2005. Rmcf2, a xenotropic provirus in the Asian mouse species Mus castaneus, blocks infection by polytropic mouse gammaretroviruses. J. Virol. 79:96779696.
156. Xiao, Z., Ehrlich, E., Yu Y., et al. 2006. Assembly of HIV-1 Vif-Cul5 E3 ubiquitin ligase through a novel zinc-binding domain-stabilized hydrophobic interface in Vif. Virology 349:290-299.
157. Yang, W. K., Yang, D.-M., and Kiggans, J. O. J. 1980. Synthesis and circularization of N-and B-tropic retroviral DNA in Fv-1 permissive and restrictive mouse cells. Proc. Natl. Acad. Sci. U S A. 77:2294-2298.
158. Yang, Y. L., Guo, L., Xu, S., et al. 1999. Receptors for polytropic and xenotropic mouse leukaemia viruses encoded by a single gene at Rmc1. Nat. Genet. 21:216-219.
159. Yoshimoto, T., Nagase, H., Nakano, H., et al. 1994. A Vb8.2-specific superantigen from exogenous mouse mammary tumor virus carried by FM mice. Eur. J. Immunol. 24:1612-1619.
160. Zhang, L., Li, X., Ma, J., et al. 2008. The incorporation of APOBEC3 proteins into murine leukemia viruses. Virology 378:69-78.
161. Zhu, Q., Maitra, U., Johnston, D., et al. 2004. The homeodomain protein CDP regulates mammaryspecific gene transcription and tumorigenesis. Mol. Cell Biol. 24:4810-4823.