A novel role for APOBEC3: Susceptibility to sexual transmission of murine acquired immunodeficiency virus (mAIDS) is aggravated in APOBEC3 deficient mice

Retrovirology

Volumn 9, Issue , 2012, Pages

  Jones, Philip H ^a   Mehta, Harshini V ^a   Okeoma, Chioma M ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

APOBEC3; Female; LP BM5 virus; Male; MLV; MURINE AIDS

Indexed keywords

HYDROLASE; PROTEIN APOBEC3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOBEC3 GENE; ARTICLE; CONTROLLED STUDY; FEMALE; FEMALE GENITAL TRACT INFECTION; GENE; GENE MUTATION; INFECTION SENSITIVITY; MALE; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEMINAL PLASMA; SEXUAL TRANSMISSION; TISSUE DISTRIBUTION; VIRUS LOAD; VIRUS TRANSMISSION;

ANIMALS; CYTIDINE DEAMINASE; DISEASE SUSCEPTIBILITY; FEMALE; GENITALIA; GERM CELLS; LEUKEMIA VIRUS, MURINE; MALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; RNA, MESSENGER; SEXUALLY TRANSMITTED DISEASES, VIRAL; SPLENOMEGALY; VIRAL LOAD;

MOUSE MAMMARY TUMOR VIRUS; MURINAE; MUS;

EID: 84861980048     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-50     Document Type: Article

References (88)

1. Cameron DW, Simonsen JN, D'Costa LJ, Ronald AR, Maitha GM, Gakinya MN, Cheang M, Ndinya-Achola JO, Piot P, Brunham RC, et al. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet 1989, 2:403-407.
2. Clumeck N, Taelman H, Hermans P, Piot P, Schoumacher M, De Wit S. A cluster of HIV infection among heterosexual people without apparent risk factors. N Engl J Med 1989, 321:1460-1462. 10.1056/NEJM198911233212107, 2811959.
3. Royce RA, Sena A, Cates W, Cohen MS. Sexual transmission of HIV. N Engl J Med 1997, 336:1072-1078. 10.1056/NEJM199704103361507, 9091805.
4. Vernazza PL, Eron JJ, Fiscus SA, Cohen MS. Sexual transmission of HIV: infectiousness and prevention. AIDS 1999, 13:155-166. 10.1097/00002030-199902040-00003, 10202821.
5. Byrn RA, Zhang D, Eyre R, McGowan K, Kiessling AA. HIV-1 in semen: an isolated virus reservoir. Lancet 1997, 350:1141. 10.1016/S0140-6736(97)24042-0, 9343504.
6. Delwart EL, Mullins JI, Gupta P, Learn GH, Holodniy M, Katzenstein D, Walker BD, Singh MK. Human immunodeficiency virus type 1 populations in blood and semen. J Virol 1998, 72:617-623. 109415, 9420266.
7. Kroodsma KL, Kozal MJ, Hamed KA, Winters MA, Merigan TC. Detection of drug resistance mutations in the human immunodeficiency virus type 1 (HIV-1) pol gene: differences in semen and blood HIV-1 RNA and proviral DNA. J Infect Dis 1994, 170:1292-1295. 10.1093/infdis/170.5.1292, 7963730.
8. Taylor S, Boffito M, Vernazza PL. Antiretroviral therapy to reduce the sexual transmission of HIV. J HIV Ther 2003, 8:55-66.
9. Boden D, Hurley A, Zhang L, Cao Y, Guo Y, Jones E, Tsay J, Ip J, Farthing C, Limoli K, Parkin N, Markowitz M. HIV-1 drug resistance in newly infected individuals. JAMA 1999, 282:1135-1141. 10.1001/jama.282.12.1135, 10501116.
10. Little SJ, Daar ES, D'Aquila RT, Keiser PH, Connick E, Whitcomb JM, Hellmann NS, Petropoulos CJ, Sutton L, Pitt JA, Rosenberg ES, Koup RA, Walker BD, Richman DD. Reduced antiretroviral drug susceptibility among patients with primary HIV infection. JAMA 1999, 282:1142-1149. 10.1001/jama.282.12.1142, 10501117.
11. Hecht FM, Grant RM, Petropoulos CJ, Dillon B, Chesney MA, Tian H, Hellmann NS, Bandrapalli NI, Digilio L, Branson B, Kahn JO. Sexual transmission of an HIV-1 variant resistant to multiple reverse-transcriptase and protease inhibitors. N Engl J Med 1998, 339:307-311. 10.1056/NEJM199807303390504, 9682043.
12. Cu-Uvin S, DeLong AK, Venkatesh KK, Hogan JW, Ingersoll J, Kurpewski J, De Pasquale MP, D'Aquila R, Caliendo AM. Genital tract HIV-1 RNA shedding among women with below detectable plasma viral load. AIDS 2010, 24:2489-2497. 10.1097/QAD.0b013e32833e5043, 20736815.
13. Cu-Uvin S, Caliendo AM. Genital tract HIV-1 RNA shedding among women with below detectable plasma viral load. AIDS 2011, 25:880-881. 10.1097/QAD.0b013e328344ccf8, 21412068.
14. Mosier DE. Animal models for retrovirus-induced immunodeficiency disease. Immunol Invest 1986, 15:233-261. 10.3109/08820138609026687, 3019879.
15. Chattopadhyay SK, Morse HC, Makino M, Ruscetti SK, Hartley JW. Defective virus is associated with induction of murine retrovirus-induced immunodeficiency syndrome. Proc Natl Acad Sci U S A 1989, 86:3862-3866. 10.1073/pnas.86.10.3862, 287241, 2542949.
16. Chattopadhyay SK, Sengupta DN, Fredrickson TN, Morse HC, Hartley JW. Characteristics and contributions of defective, ecotropic, and mink cell focus-inducing viruses involved in a retrovirus-induced immunodeficiency syndrome of mice. J Virol 1991, 65:4232-4241. 248860, 1649328.
17. Jolicoeur P. Murine acquired immunodeficiency syndrome (MAIDS): an animal model to study the AIDS pathogenesis. FASEB J 1991, 5:2398-2405.
18. Morse HC, Yetter RA, Via CS, Hardy RR, Cerny A, Hayakawa K, Hugin AW, Miller MW, Holmes KL, Shearer GM. Functional and phenotypic alterations in T cell subsets during the course of MAIDS, a murine retrovirus-induced immunodeficiency syndrome. J Immunol 1989, 143:844-850.
19. Morse HC, Chattopadhyay SK, Makino M, Fredrickson TN, Hugin AW, Hartley JW. Retrovirus-induced immunodeficiency in the mouse: MAIDS as a model for AIDS. AIDS 1992, 6:607-621.
20. Yetter RA, Buller RM, Lee JS, Elkins KL, Mosier DE, Fredrickson TN, Morse HC. CD4+ T cells are required for development of a murine retrovirus-induced immunodeficiency syndrome (MAIDS). J Exp Med 1988, 168:623-635. 10.1084/jem.168.2.623, 2189016, 2842430.
21. Cerny A, Hugin AW, Hardy RR, Hayakawa K, Zinkernagel RM, Makino M, Morse HC. B cells are required for induction of T cell abnormalities in a murine retrovirus-induced immunodeficiency syndrome. J Exp Med 1990, 171:315-320. 10.1084/jem.171.1.315, 2187666, 1967300.
22. Cerny A, Hugin AW, Holmes KL, Morse HC. CD4+ T cells in murine acquired immunodeficiency syndrome: evidence for an intrinsic defect in the proliferative response to soluble antigen. Eur J Immunol 1990, 20:1577-1581. 10.1002/eji.1830200725, 1974851.
23. Hartley JW, Fredrickson TN, Yetter RA, Makino M, Morse HC. Retrovirus-induced murine acquired immunodeficiency syndrome: natural history of infection and differing susceptibility of inbred mouse strains. J Virol 1989, 63:1223-1231. 247818, 2536830.
24. Pozsgay JM, Beilharz MW, Wines BD, Hess AD, Pitha PM. The MA (p15) and p12 regions of the gag gene are sufficient for the pathogenicity of the murine AIDS virus. J Virol 1993, 67:5989-5999. 238020, 7690416.
25. Fraternale A, Casabianca A, Tonelli A, Vallanti G, Chiarantini L, Brandi G, Celeste AG, Magnani M. Inhibition of murine AIDS by alternate administration of azidothymidine and fludarabine monophosphate. J Acquir Immune Defic Syndr 2000, 23:209-220.
26. Fraternale A, Tonelli A, Casabianca A, Chiarantini L, Schiavano GF, Celeste AG, Magnani M. New treatment protocol including lympholytic and antiretroviral drugs to inhibit murine AIDS. J Acquir Immune Defic Syndr 2000, 23:107-113.
27. Mayhew CN, Sumpter R, Inayat M, Cibull M, Phillips JD, Elford HL, Gallicchio VS. Combination of inhibitors of lymphocyte activation (hydroxyurea, trimidox, and didox) and reverse transcriptase (didanosine) suppresses development of murine retrovirus-induced lymphoproliferative disease. Antiviral Res 2005, 65:13-22. 10.1016/j.antiviral.2004.09.003, 15652967.
28. Beilharz MW, Sammels LM, Paun A, Shaw K, van Eeden P, Watson MW, Ashdown ML. Timed ablation of regulatory CD4+ T cells can prevent murine AIDS progression. J Immunol 2004, 172:4917-4925.
29. Dias AS, Bester MJ, Britz RF, Apostolides Z. Animal models used for the evaluation of antiretroviral therapies. Curr HIV Res 2006, 4:431-446. 10.2174/157016206778560045, 17073618.
30. Patterson BK, Landay A, Siegel JN, Flener Z, Pessis D, Chaviano A, Bailey RC. Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol 2002, 161:867-873. 10.1016/S0002-9440(10)64247-2, 1867269, 12213715.
31. Johansson EL, Rudin A, Wassen L, Holmgren J. Distribution of lymphocytes and adhesion molecules in human cervix and vagina. Immunology 1999, 96:272-277. 10.1046/j.1365-2567.1999.00675.x, 2326729, 10233705.
32. Olaitan A, Johnson MA, MacLean A, Poulter LW. The distribution of immunocompetent cells in the genital tract of HIV-positive women. AIDS 1996, 10:759-764.
33. Edwards JN, Morris HB. Langerhans' cells and lymphocyte subsets in the female genital tract. Br J Obstet Gynaecol 1985, 92:974-982. 10.1111/j.1471-0528.1985.tb03080.x, 2931100.
34. Hladik F, Lentz G, Delpit E, McElroy A, McElrath MJ. Coexpression of CCR5 and IL-2 in human genital but not blood T cells: implications for the ontogeny of the CCR5+ Th1 phenotype. J Immunol 1999, 163:2306-2313.
35. Zhang L, He T, Talal A, Wang G, Frankel SS, Ho DD. In vivo distribution of the human immunodeficiency virus/simian immunodeficiency virus coreceptors: CXCR4, CCR3, and CCR5. J Virol 1998, 72:5035-5045. 110066, 9573273.
36. Prakash M, Kapembwa MS, Gotch F, Patterson S. Higher levels of activation markers and chemokine receptors on T lymphocytes in the cervix than peripheral blood of normal healthy women. J Reprod Immunol 2001, 52:101-111. 10.1016/S0165-0378(01)00114-0, 11600181.
37. Pichlmair A, Reis E, Sousa C. Innate recognition of viruses. Immunity 2007, 27:370-383. 10.1016/j.immuni.2007.08.012, 17892846.
38. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138:576-591. 10.1016/j.cell.2009.06.015, 2747301, 19631370.
39. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 2009, 10:1065-1072. 10.1038/ni.1779, 19609254.
40. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009, 27:229-265. 10.1146/annurev.immunol.021908.132715, 19302040.
41. Bhattacharya C, Aggarwal S, Kumar M, Ali A, Matin A. Mouse apolipoprotein B editing complex 3 (APOBEC3) is expressed in germ cells and interacts with dead-end (DND1). PLoS One 2008, 3:e2315. 10.1371/journal.pone.0002315, 2384002, 18509452.
42. Koning FA, Newman EN, Kim EY, Kunstman KJ, Wolinsky SM, Malim MH. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 2009, 83:9474-9485. 10.1128/JVI.01089-09, 2738220, 19587057.
43. LaRue RS, Jonsson SR, Silverstein KA, Lajoie M, Bertrand D, El-Mabrouk N, Hotzel I, Andresdottir V, Smith TP, Harris RS. The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals. BMC Mol Biol 2008, 9:104. 10.1186/1471-2199-9-104, 2612020, 19017397.
44. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 2004, 101:6062-6067. 10.1073/pnas.0400782101, 395923, 15075390.
45. Okeoma CM, Lovsin N, Peterlin BM, Ross SR. APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 2007, 445:927-930. 10.1038/nature05540, 17259974.
46. Okeoma CM, Low A, Bailis W, Fan HY, Peterlin BM, Ross SR. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J Virol 2009, 83:3486-3495. 10.1128/JVI.02347-08, 2663286, 19153238.
47. Okeoma CM, Huegel AL, Lingappa J, Feldman MD, Ross SR. APOBEC3 proteins expressed in mammary epithelial cells are packaged into retroviruses and can restrict transmission of milk-borne virions. Cell Host Microbe 2010, 8:534-543. 10.1016/j.chom.2010.11.003, 3023938, 21147467.
48. Cullen BR. HIV-1 Vif: counteracting innate antiretroviral defenses. Mol Ther 2003, 8:525-527. 10.1016/j.ymthe.2003.08.010, 14565218.
49. Chiu YL, Greene WC. Multifaceted antiviral actions of APOBEC3 cytidine deaminases. Trends Immunol 2006, 27:291-297. 10.1016/j.it.2006.04.003, 16678488.
50. Malim MH. APOBEC proteins and intrinsic resistance to HIV-1 infection. Philos Trans R Soc Lond B Biol Sci 2009, 364:675-687. 10.1098/rstb.2008.0185, 2660912, 19038776.
51. Okeoma CM, Petersen J, Ross SR. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J Virol 2009, 83:3029-3038. 10.1128/JVI.02536-08, 2655539, 19153233.
52. Low A, Okeoma CM, Lovsin N, De Las Heras M, Taylor TH, Peterlin BM, Ross SR, Fan H. Enhanced replication and pathogenesis of Moloney murine leukemia virus in mice defective in the murine APOBEC3 gene. Virology 2009, 385:455-463. 10.1016/j.virol.2008.11.051, 3124558, 19150103.
53. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 2004, 14:1392-1396. 10.1016/j.cub.2004.06.057, 15296758.
54. Bishop KN, Holmes RK, Sheehy AM, Malim MH. APOBEC-mediated editing of viral RNA. Science 2004, 305:645. 10.1126/science.1100658, 15286366.
55. Holmes RK, Koning FA, Bishop KN, Malim MH. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem 2007, 282:2587-2595.
56. Aguiar RS, Lovsin N, Tanuri A, Peterlin BM. Vpr.A3A chimera inhibits HIV replication. J Biol Chem 2008, 283:2518-2525.
57. Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650. 10.1038/nature00939, 12167863.
58. Conticello SG, Harris RS, Neuberger MS. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 2003, 13:2009-2013. 10.1016/j.cub.2003.10.034, 14614829.
59. Marin M, Rose KM, Kozak SL, Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 2003, 9:1398-1403. 10.1038/nm946, 14528301.
60. Takeda E, Tsuji-Kawahara S, Sakamoto M, Langlois MA, Neuberger MS, Rada C, Miyazawa M. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J Virol 2008, 82:10998-11008. 10.1128/JVI.01311-08, 2573259, 18786991.
61. Langlois MA, Neuberger MS. Human APOBEC3G can restrict retroviral infection in avian cells and acts independently of both UNG and SMUG1. J Virol 2008, 82:4660-4664. 10.1128/JVI.02469-07, 2293047, 18272574.
62. Huang M, Simard C, Jolicoeur P. Immunodeficiency and clonal growth of target cells induced by helper-free defective retrovirus. Science 1989, 246:1614-1617. 10.1126/science.2480643, 2480643.
63. Simard C, Huang M, Jolicoeur P. Murine AIDS is initiated in the lymph nodes draining the site of inoculation, and the infected B cells influence T cells located at distance, in noninfected organs. J Virol 1994, 68:1903-1912. 236652, 8107250.
64. Huang M, Jolicoeur P. Myristylation of Pr60gag of the murine AIDS-defective virus is required to induce disease and notably for the expansion of its target cells. J Virol 1994, 68:5648-5655. 236966, 8057445.
65. Huang M, Simard C, Kay DG, Jolicoeur P. The majority of cells infected with the defective murine AIDS virus belong to the B-cell lineage. J Virol 1991, 65:6562-6571. 250712, 1658361.
66. Iwashiro M, Messer RJ, Peterson KE, Stromnes IM, Sugie T, Hasenkrug KJ. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc Natl Acad Sci U S A 2001, 98:9226-9230. 10.1073/pnas.151174198, 55402, 11459933.
67. Okeoma CM, Shen M, Ross SR. A novel block to mouse mammary tumor virus infection of lymphocytes in B10.BR mice. J Virol 2008, 82:1314-1322. 10.1128/JVI.01848-07, 2224452, 18003725.
68. Pilcher CD, Shugars DC, Fiscus SA, Miller WC, Menezes P, Giner J, Dean B, Robertson K, Hart CE, Lennox JL, Eron JJ, Hicks CB. HIV in body fluids during primary HIV infection: implications for pathogenesis, treatment and public health. AIDS 2001, 15:837-845. 10.1097/00002030-200105040-00004, 11399956.
69. Pilcher CD, Eron JJ, Vemazza PL, Battegay M, Harr T, Yerly S, Vom S, Perrin L. Sexual transmission during the incubation period of primary HIV infection. JAMA 2001, 286:1713-1714. 10.1001/jama.286.14.1713, 11594895.
70. Whitney JB, Luedemann C, Hraber P, Rao SS, Mascola JR, Nabel GJ, Letvin NL. T-cell vaccination reduces simian immunodeficiency virus levels in semen. J Virol 2009, 83:10840-10843. 10.1128/JVI.01202-09, 2753121, 19640980.
71. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, Meehan MO, Lutalo T, Gray RH. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000, 342:921-929. 10.1056/NEJM200003303421303, 10738050.
72. Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F, Lutalo T, Li X, vanCott T, Quinn TC. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001, 357:1149-1153. 10.1016/S0140-6736(00)04331-2, 11323041.
73. Okada Y, Abe E, Komuro K, Mizuochi T. Heterosexual transmission of a murine AIDS virus. J Virol 1998, 72:2541-2543. 109560, 9499121.
74. Roan NR, Muller JA, Liu H, Chu S, Arnold F, Sturzel CM, Walther P, Dong M, Witkowska HE, Kirchhoff F, Munch J, Greene WC. Peptides released by physiological cleavage of semen coagulum proteins form amyloids that enhance HIV infection. Cell Host Microbe 2011, 10:541-550. 10.1016/j.chom.2011.10.010, 22177559.
75. van Leeuwen E, de Vries JW, Jurriaans S, Verhoeve HR, Prins JM, Repping S, van der Veen F. Intra uterine insemination with processed sperm for HIV serodiscordant couples in whom the man is HIV positive. Ned Tijdschr Geneeskd 2005, 149:423-424.
76. Mermin JH, Holodniy M, Katzenstein DA, Merigan TC. Detection of human immunodeficiency virus DNA and RNA in semen by the polymerase chain reaction. J Infect Dis 1991, 164:769-772. 10.1093/infdis/164.4.769, 1680138.
77. Nuovo GJ, Becker J, Simsir A, Margiotta M, Khalife G, Shevchuk M. HIV-1 nucleic acids localize to the spermatogonia and their progeny. A study by polymerase chain reaction in situ hybridization. Am J Pathol 1994, 144:1142-1148. 1887452, 8203455.
78. Bagasra O, Farzadegan H, Seshamma T, Oakes JW, Saah A, Pomerantz RJ. Detection of HIV-1 proviral DNA in sperm from HIV-1-infected men. AIDS 1994, 8:1669-1674. 10.1097/00002030-199412000-00005, 7888115.
79. Bagasra O, Freund M, Weidmann J, Harley G. Interaction of human immunodeficiency virus with human sperm in vitro. J Acquir Immune Defic Syndr 1988, 1:431-435.
80. Bagasra O, Patel D, Bobroski L, Abbasi JA, Bagasra AU, Baidouri H, Harris T, El-Roeiy A, Lengvarszky Z, Farzadegan H, Wood C. Localization of human herpesvirus type 8 in human sperms by in situ PCR. J Mol Histol 2005, 36:401-412.
81. Doehle BP, Schafer A, Wiegand HL, Bogerd HP, Cullen BR. Differential sensitivity of murine leukemia virus to APOBEC3-mediated inhibition is governed by virion exclusion. J Virol 2005, 79:8201-8207. 10.1128/JVI.79.13.8201-8207.2005, 1143768, 15956565.
82. Abudu A, Takaori-Kondo A, Izumi T, Shirakawa K, Kobayashi M, Sasada A, Fukunaga K, Uchiyama T. Murine retrovirus escapes from murine APOBEC3 via two distinct novel mechanisms. Curr Biol 2006, 16:1565-1570. 10.1016/j.cub.2006.06.055, 16890533.
83. Dey A, Mantri CK, Pandhare-Dash J, Liu B, Pratap S, Dash C. Downregulation of APOBEC3G by xenotropic murine leukemia-virus related virus (XMRV) in prostate cancer cells. Virol J 2011, 8:531. 10.1186/1743-422X-8-531, 3268770, 22152111.
84. Mosier DE, Yetter RA, Morse HC. Functional T lymphocytes are required for a murine retrovirus-induced immunodeficiency disease (MAIDS). J Exp Med 1987, 165:1737-1742. 10.1084/jem.165.6.1737, 2188367, 3035057.
85. Cook WJ, Green KA, Obar JJ, Green WR. Quantitative analysis of LP-BM5 murine leukemia retrovirus RNA using real-time RT-PCR. J Virol Methods 2003, 108:49-58. 10.1016/S0166-0934(02)00256-2, 12565153.
86. Jones PH, Mehta HV, Maric M, Roller RJ, Okeoma CM. Bone marrow stromal cell antigen 2 (BST-2) restricts mouse mammary tumor virus (MMTV) replication in vivo. Retrovirology 2012, 9:10. 10.1186/1742-4690-9-10, 3283513, 22284121.
87. Giese NA, Giese T, Morse HC. Murine AIDS is an antigen-driven disease: requirements for major histocompatibility complex class II expression and CD4+ T cells. J Virol 1994, 68:5819-5824. 236986, 7914549.
88. Lasheeb AS, King J, Ball JK, Curran R, Barratt CL, Afnan M, Pillay D. Semen characteristics in HIV-1 positive men and the effect of semen washing. Genitourin Med 1997, 73:303-305. 1195865, 9389956.