The utilization of humanized mouse models for the study of human retroviral infections

Retrovirology

Volumn 6, Issue , 2009, Pages 76-

  Van Duyne, Rachel ^a   Pedati, Caitlin ^a   Guendel, Irene ^a   Carpio, Lawrence ^a   Kehn Hall, Kylene ^a   Saifuddin, Mohammed ^b   Kashanchi, Fatah ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; RAG2 PROTEIN, MOUSE;

ANIMAL; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; MOUSE; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; RETROVIRUS INFECTION; REVIEW;

ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HIV-1; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; RETROVIRIDAE INFECTIONS;

EID: 70349918640     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-6-76     Document Type: Review

References (163)

1. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 1983, 220:868-71.
2. Gallo RC, Sarin PS, Gelmann EP, Robert-Guroff M, Richardson E, Kalyanaraman VS, Mann D, Sidhu GD, Stahl RE, Zolla-Pazner S. Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science 1983, 220:865-7.
3. Stevenson M. HIV-1 pathogenesis. Nat Med 2003, 9:853-60.
4. Kahn JO, Walker BD. Acute human immunodeficiency virus type 1 infection. N Engl J Med 1998, 339:33-9.
5. Perrin L. Primary HIV infection. Antivir Ther 1999, 3:13-8.
6. Mosier DE. How HIV changes its tropism: evolution and adaptation?. Curr Opin HIV AIDS 2009, 4:125-30.
7. Regoes RR, Bonhoeffer S. The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol 2005, 13:269-77.
8. Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, Luzuriaga K, Robinson J, Burton DR, Bell J, Simmonds P. Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology 2008, 5:5. 2268948, 18205925.
9. Centlivre M, Sala M, Wain-Hobson S, Berkhout B. In HIV-1 pathogenesis the die is cast during primary infection. Aids 2007, 21:1-11.
10. Derdeyn CA, Silvestri G. Viral and host factors in the pathogenesis of HIV infection. Curr Opin Immunol 2005, 17:366-73.
11. Benito JM, Lopez M, Soriano V. The role of CD8+ T-cell response in HIV infection. AIDS Rev 2004, 6:79-88.
12. Saksena NK, Wu JQ, Potter SJ, Wilkinson J, Wang B. Human immunodeficiency virus interactions with CD8+ T lymphocytes. Curr HIV Res 2008, 6:1-9.
13. Petrovas C, Mueller YM, Katsikis PD. HIV-specific CD8+ T cells: serial killers condemned to die?. Curr HIV Res 2004, 2:153-62.
14. Picker LJ, Watkins DI. HIV pathogenesis: the first cut is the deepest. Nat Immunol 2005, 6:430-2.
15. Han Y, Wind-Rotolo M, Yang HC, Siliciano JD, Siliciano RF. Experimental approaches to the study of HIV-1 latency. Nat Rev Microbiol 2007, 5:95-106.
16. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990, 61:213-22.
17. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA. HIV-1 replication is controlled at the level of T cell activation and proviral integration. Embo J 1990, 9:1551-60. 551849, 2184033.
18. Vatakis DN, Kim S, Kim N, Chow SA, Zack JA. Human immunodeficiency virus integration efficiency and site selection in quiescent CD4+ T cells. J Virol 2009, 83:6222-33.
19. Jeeninga RE, Westerhout EM, ML VG, Berkhout B. HIV-1 latency in actively dividing human T cell lines. Retrovirology 2008, 5:37. 2387167, 18439275.
20. Yamashita M, Emerman M. Retroviral infection of non-dividing cells: old and new perspectives. Virology 2006, 344:88-93.
21. Douek DC. Disrupting T-cell homeostasis: how HIV-1 infection causes disease. AIDS Rev 2003, 5:172-7.
22. Preston BD, Poiesz BJ, Loeb LA. Fidelity of HIV-1 reverse transcriptase. Science 1988, 242:1168-71.
23. Menendez-Arias L. Molecular basis of fidelity of DNA synthesis and nucleotide specificity of retroviral reverse transcriptases. Prog Nucleic Acid Res Mol Biol 2002, 71:91-147.
24. Chen R, Quinones-Mateu ME, Mansky LM. Drug resistance, virus fitness and HIV-1 mutagenesis. Curr Pharm Des 2004, 10:4065-70.
25. Chen R, Quinones-Mateu ME, Mansky LM. HIV-1 mutagenesis during antiretroviral therapy: implications for successful drug treatment. Front Biosci 2005, 10:743-50.
26. Mansky LM. HIV mutagenesis and the evolution of antiretroviral drug resistance. Drug Resist Updat 2002, 5:219-23.
27. Martinez-Picado J, Martinez MA. HIV-1 reverse transcriptase inhibitor resistance mutations and fitness: a view from the clinic and ex vivo. Virus Res 2008, 134:104-23.
28. Re MC, Bon I, Monari P, Gorini R, Schiavone P, Gibellini D, La Placa M. Drug failure during HIV-1 treatment. New Microbiol 2003, 26:405-13.
29. Daar ES, Richman DD. Confronting the emergence of drug-resistant HIV type 1: impact of antiretroviral therapy on individual and population resistance. AIDS Res Hum Retroviruses 2005, 21:343-57.
30. Zoeteweij JP, Blauvelt A. HIV-Dendritic cell interactions promote efficient viral infection of T cells. J Biomed Sci 1998, 5:253-9.
31. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996, 382:722-5.
32. Kedzierska K, Crowe SM. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr Med Chem 2002, 9:1893-903.
33. Tuttle DL, Harrison JK, Anders C, Sleasman JW, Goodenow MM. Expression of CCR5 increases during monocyte differentiation and directly mediates macrophage susceptibility to infection by human immunodeficiency virus type 1. J Virol 1998, 72:4962-9. 110058, 9573265.
34. Kohler JJ, Tuttle DL, Coberley CR, Sleasman JW, Goodenow MM. Human immunodeficiency virus type 1 (HIV-1) induces activation of multiple STATs in CD4+ cells of lymphocyte or monocyte/macrophage lineages. J Leukoc Biol 2003, 73:407-16.
35. Swingler S, Brichacek B, Jacque JM, Ulich C, Zhou J, Stevenson M. HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 2003, 424:213-9.
36. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008, 1:23-30.
37. Dandekar S. Pathogenesis of HIV in the gastrointestinal tract. Curr HIV/AIDS Rep 2007, 4:10-5.
38. Kelleher AD, Zaunders JJ. Decimated or missing in action: CD4+ T cells as targets and effectors in the pathogenesis of primary HIV infection. Curr HIV/AIDS Rep 2006, 3:5-12.
39. Mehandru S, Tenner-Racz K, Racz P, Markowitz M. The gastrointestinal tract is critical to the pathogenesis of acute HIV-1 infection. J Allergy Clin Immunol 2005, 116:419-22.
40. Paiardini M, Frank I, Pandrea I, Apetrei C, Silvestri G. Mucosal immune dysfunction in AIDS pathogenesis. AIDS Rev 2008, 10:36-46.
41. van Marle G, Gill MJ, Kolodka D, McManus L, Grant T, Church DL. Compartmentalization of the gut viral reservoir in HIV-1 infected patients. Retrovirology 2007, 4:87. 2217557, 18053211.
42. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-71.
43. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, Taylor H, Hermankova M, Chadwick K, Margolick J, Quinn TC. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 1997, 387:183-8.
44. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-7.
45. Mehandru S, Poles MA, Tenner-Racz K, Manuelli V, Jean-Pierre P, Lopez P, Shet A, Low A, Mohri H, Boden D. Mechanisms of gastrointestinal CD4+ T-cell depletion during acute and early human immunodeficiency virus type 1 infection. J Virol 2007, 81:599-612. 1797467, 17065209.
46. Rutjens E, Balla-Jhagjhoorsingh S, Verschoor E, Bogers W, Koopman G, Heeney J. Lentivirus infections and mechanisms of disease resistance in chimpanzees. Front Biosci 2003, 8:d1134-45.
47. Boberg A, Brave A, Johansson S, Wahren B, Hinkula J, Rollman E. Murine models for HIV vaccination and challenge. Expert Rev Vaccines 2008, 7:117-30.
48. Zarling JM, Ledbetter JA, Sias J, Fultz P, Eichberg J, Gjerset G, Moran PA. HIV-infected humans, but not chimpanzees, have circulating cytotoxic T lymphocytes that lyse uninfected CD4+ cells. J Immunol 1990, 144:2992-8.
49. Joag SV. Primate models of AIDS. Microbes Infect 2000, 2:223-9.
50. Hu SL. Non-human primate models for AIDS vaccine research. Curr Drug Targets Infect Disord 2005, 5:193-201. 1488817, 15975024.
51. Abel K. The rhesus macaque pediatric SIV infection model - a valuable tool in understanding infant HIV-1 pathogenesis and for designing pediatric HIV-1 prevention strategies. Curr HIV Res 2009, 7:2-11.
52. Li J, Lord CI, Haseltine W, Letvin NL, Sodroski J. Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus that expresses the HIV-1 envelope glycoproteins. J Acquir Immune Defic Syndr 1992, 5:639-46.
53. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley M, Schumacher-Stankey J, Wroblewski E, Mosser A, Raphael J, Kamenya S, Lonsdorf EV, Travis DA, Mlengeya T, Kinsel MJ, Else JG, Silvestri G, Goodall J, Sharp PM, Shaw GM, Pusey AE, Hahn BH. Increased mortality and AIDS-like immunopathology in wild chimpazees infected with SIVcpz. Nature 2009, 460:515-519.
54. Uhl EW, Martin M, Coleman JK, Yamamoto JK. Advances in FIV vaccine technology. Vet Immunol Immunopathol 2008, 123:65-80.
55. Burkhard MJ, Dean GA. Transmission and immunopathogenesis of FIV in cats as a model for HIV. Curr HIV Res 2003, 1:15-29.
56. Goffinet C, Michel N, Allespach I, Tervo HM, Hermann V, Krausslich HG, Greene WC, Keppler OT. Primary T-cells from human CD4/CCR5-transgenic rats support all early steps of HIV-1 replication including integration, but display impaired viral gene expression. Retrovirology 2007, 4:53. 1971067, 17655755.
57. Michel N, Goffinet C, Ganter K, Allespach I, Kewalramani VN, Saifuddin M, Littman DR, Greene WC, Goldsmith MA, Keppler OT. Human cyclin T1 expression ameliorates a T-cell-specific transcriptional limitation for HIV in transgenic rats, but is not sufficient for a spreading infection of prototypic R5 HIV-1 strains ex vivo. Retrovirology 2009, 6:2. 2631513, 19144136.
58. Tervo HM, Goffinet C, Keppler OT. Mouse T-cells restrict replication of human immunodeficiency virus at the level of integration. Retrovirology 2008, 5:58. 2557013, 18611257.
59. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983, 301:527-30.
60. McCune JM. Development and applications of the SCID-hu mouse model. Semin Immunol 1996, 8:187-96.
61. McCune JM, Namikawa R, Kaneshima H, Shultz LD, Lieberman M, Weissman IL. The SCID-hu mouse: murine model for the analysis of human hematolymphoid differentiation and function. Science 1988, 241:1632-9.
62. Mosier DE, Gulizia RJ, Baird SM, Wilson DB. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature 1988, 335:256-9.
63. Tary-Lehmann M, Saxon A, Lehmann PV. The human immune system in hu-PBL-SCID mice. Immunol Today 1995, 16:529-33.
64. Christianson SW, Greiner DL, Hesselton RA, Leif JH, Wagar EJ, Schweitzer IB, Rajan TV, Gott B, Roopenian DC, Shultz LD. Enhanced human CD4+ T cell engraftment in beta2-microglobulin-deficient NOD-scid mice. J Immunol 1997, 158:3578-86.
65. Greiner DL, Shultz LD, Yates J, Appel MC, Perdrizet G, Hesselton RM, Schweitzer I, Beamer WG, Shultz KL, Pelsue SC. Improved engraftment of human spleen cells in NOD/LtSz-scid/scid mice as compared with C. Am J Pathol 1995, 146:888-902. 1869266, 7717456.
66. Hesselton RM, Greiner DL, Mordes JP, Rajan TV, Sullivan JL, Shultz LD. High levels of human peripheral blood mononuclear cell engraftment and enhanced susceptibility to human immunodeficiency virus type 1 infection in NOD/LtSz-scid/scid mice. J Infect Dis 1995, 172:974-82.
67. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, Tennent B, McKenna S, Mobraaten L, Rajan TV, Greiner DL. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 1995, 154:180-91.
68. Ito M, Kobayashi K, Nakahata T. NOD/Shi-scid IL2rgamma(null) (NOG) mice more appropriate for humanized mouse models. Curr Top Microbiol Immunol 2008, 324:53-76.
69. Pearson T, Greiner DL, Shultz LD. Humanized SCID mouse models for biomedical research. Curr Top Microbiol Immunol 2008, 324:25-51.
70. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G, Watanabe T, Akashi K, Shultz LD, Harada M. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 2005, 106:1565-73. 1895228, 15920010.
71. Ito M, Hiramatsu H, Kobayashi K, Suzue K, Kawahata M, Hioki K, Ueyama Y, Koyanagi Y, Sugamura K, Tsuji K. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002, 100:3175-82.
72. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 2005, 174:6477-89.
73. Traggiai E, Chicha L, Mazzucchelli L, Bronz L, Piffaretti JC, Lanzavecchia A, Manz MG. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 2004, 304:104-7.
74. Uittenbogaart CH, Anisman DJ, Tary-Lehmann M, Vollger LW, Breit TM, Van Dongen JJ, Saxon A. The SCID mouse environment causes immunophenotypic changes in human immature T-cell lines. Int J Cancer 1994, 56:546-51.
75. Sundell IB, Koka PS. Chimeric SCID-hu Model as a Human Hematopoietic Stem Cell Host That Recapitulates the Effects of HIV-1 on Bone Marrow Progenitors in Infected Patients. J Stem Cells 2006, 1:283-300. 2585495, 19030112.
76. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007, 7:118-30.
77. Koyanagi Y, Tanaka Y, Ito M, Yamamoto N. Humanized mice for human retrovirus infection. Curr Top Microbiol Immunol 2008, 324:133-48.
78. Denton PW, Garcia JV. Novel humanized murine models for HIV research. Curr HIV/AIDS Rep 2009, 6:13-9.
79. Koka PS, Fraser JK, Bryson Y, Bristol GC, Aldrovandi GM, Daar ES, Zack JA. Human immunodeficiency virus inhibits multilineage hematopoiesis in vivo. J Virol 1998, 72:5121-7. 110080, 9573283.
80. Koka PS, Jamieson BD, Brooks DG, Zack JA. Human immunodeficiency virus type 1-induced hematopoietic inhibition is independent of productive infection of progenitor cells in vivo. J Virol 1999, 73:9089-97. 112941, 10516015.
81. Goldstein H, Pettoello-Mantovani M, Katopodis NF, Kim A, Yurasov S, Kollmann TR. SCID-hu mice: a model for studying disseminated HIV infection. Semin Immunol 1996, 8:223-31.
82. Stoddart CA, Bales CA, Bare JC, Chkhenkeli G, Galkina SA, Kinkade AN, Moreno ME, Rivera JM, Ronquillo RE, Sloan B. Validation of the SCID-hu Thy/Liv mouse model with four classes of licensed antiretrovirals. PLoS One 2007, 2:e655. 1925140, 17668043.
83. Stoddart CA, Nault G, Galkina SA, Thibaudeau K, Bakis P, Bousquet-Gagnon N, Robitaille M, Bellomo M, Paradis V, Liscourt P. Albumin-conjugated C34 peptide HIV-1 fusion inhibitor: equipotent to C34 and T-20 in vitro with sustained activity in SCID-hu Thy/Liv mice. J Biol Chem 2008, 283:34045-52. 2590714, 18809675.
84. Stoddart CA, Joshi P, Sloan B, Bare JC, Smith PC, Allaway GP, Wild CT, Martin DE. Potent activity of the HIV-1 maturation inhibitor bevirimat in SCID-hu Thy/Liv mice. PLoS One 2007, 2:e1251. 2080775, 18043758.
85. Namikawa R, Kaneshima H, Lieberman M, Weissman IL, McCune JM. Infection of the SCID-hu mouse by HIV-1. Science 1988, 242:1684-6.
86. Stanley SK, McCune JM, Kaneshima H, Justement JS, Sullivan M, Boone E, Baseler M, Adelsberger J, Bonyhadi M, Orenstein J. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID-hu mouse. J Exp Med 1993, 178:1151-63. 2191215, 8376927.
87. Aldrovandi GM, Feuer G, Gao L, Jamieson B, Kristeva M, Chen IS, Zack JA. The SCID-hu mouse as a model for HIV-1 infection. Nature 1993, 363:732-6.
88. Bonyhadi ML, Rabin L, Salimi S, Brown DA, Kosek J, McCune JM, Kaneshima H. HIV induces thymus depletion in vivo. Nature 1993, 363:728-32.
89. Miles SA, Mitsuyasu RT, Moreno J, Baldwin G, Alton NK, Souza L, Glaspy JA. Combined therapy with recombinant granulocyte colony-stimulating factor and erythropoietin decreases hematologic toxicity from zidovudine. Blood 1991, 77:2109-17.
90. Withers-Ward ES, Amado RG, Koka PS, Jamieson BD, Kaplan AH, Chen IS, Zack JA. Transient renewal of thymopoiesis in HIV-infected human thymic implants following antiviral therapy. Nat Med 1997, 3:1102-9.
91. Isgro A, De Vita L, Mezzaroma I, Aiuti A, Aiuti F. Recovery of haematopoietic abnormalities in HIV-1 infected patients treated with HAART. Aids 1999, 13:2486-8.
92. McCune JM, Namikawa R, Shih CC, Rabin L, Kaneshima H. Pseudotypes in HIV-infected mice. Science 1990, 250:1152-4.
93. Kaneshima H, Shih CC, Namikawa R, Rabin L, Outzen H, Machado SG, McCune JM. Human immunodeficiency virus infection of human lymph nodes in the SCID-hu mouse. Proc Natl Acad Sci USA 1991, 88:4523-7. 51693, 1903543.
94. Greiner DL, Hesselton RA, Shultz LD. SCID mouse models of human stem cell engraftment. Stem Cells 1998, 16:166-77.
95. Nonoyama S, Smith FO, Bernstein ID, Ochs HD. Strain-dependent leakiness of mice with severe combined immune deficiency. J Immunol 1993, 150:3817-24.
96. Kollmann TR, Pettoello-Mantovani M, Zhuang X, Kim A, Hachamovitch M, Smarnworawong P, Rubinstein A, Goldstein H. Disseminated human immunodeficiency virus 1 (HIV-1) infection in SCID-hu mice after peripheral inoculation with HIV-1. J Exp Med 1994, 179:513-22. 2191362, 8294863.
97. Di Fabio S, Giannini G, Lapenta C, Spada M, Binelli A, Germinario E, Sestili P, Belardelli F, Proietti E, Vella S. Vaginal transmission of HIV-1 in hu-SCID mice: a new model for the evaluation of vaginal microbicides. Aids 2001, 15:2231-8.
98. Di Fabio S, Van Roey J, Giannini G, Mooter G, Spada M, Binelli A, Pirillo MF, Germinario E, Belardelli F, de Bethune MP. Inhibition of vaginal transmission of HIV-1 in hu-SCID mice by the non-nucleoside reverse transcriptase inhibitor TMC120 in a gel formulation. Aids 2003, 17:1597-604.
99. Santini SM, Rizza P, Logozzi MA, Sestili P, Gherardi G, Lande R, Lapenta C, Belardelli F, Fais S. The SCID mouse reaction to human peripheral blood mononuclear leukocyte engraftment. Transplantation 1995, 60:1306-14.
100. Tary-Lehmann M, Saxon A. Human mature T cells that are anergic in vivo prevail in SCID mice reconstituted with human peripheral blood. J Exp Med 1992, 175:503-16. 2119121, 1346272.
101. Hoffmann-Fezer G, Gall C, Zengerle U, Kranz B, Thierfelder S. Immunohistology and immunocytology of human T-cell chimerism and graft-versus-host disease in SCID mice. Blood 1993, 81:3440-8.
102. Reinhardt B, Torbett BE, Gulizia RJ, Reinhardt PP, Spector SA, Mosier DE. Human immunodeficiency virus type 1 infection of neonatal severe combined immunodeficient mice xenografted with human cord blood cells. AIDS Res Hum Retroviruses 1994, 10:131-41.
103. Kawano Y, Tanaka Y, Misawa N, Tanaka R, Kira JI, Kimura T, Fukushi M, Sano K, Goto T, Nakai M. Mutational analysis of human immunodeficiency virus type 1 (HIV-1) accessory genes: requirement of a site in the nef gene for HIV-1 replication in activated CD4+ T cells in vitro and in vivo. J Virol 1997, 71:8456-66. 192308, 9343202.
104. Koup RA, Safrit JT, Weir R, Gauduin MC. Defining antibody protection against HIV-1 transmission in Hu-PBL-SCID mice. Semin Immunol 1996, 8:263-8.
105. Picchio GR, Valdez H, Sabbe R, Landay AL, Kuritzkes DR, Lederman MM, Mosier DE. Altered viral fitness of HIV-1 following failure of protease inhibitor-based therapy. J Acquir Immune Defic Syndr 2000, 25:289-95.
106. Poignard P, Sabbe R, Picchio GR, Wang M, Gulizia RJ, Katinger H, Parren PW, Mosier DE, Burton DR. Neutralizing antibodies have limited effects on the control of established HIV-1 infection in vivo. Immunity 1999, 10:431-8.
107. Andrus L, Prince AM, Bernal I, McCormack P, Lee DH, Gorny MK, Zolla-Pazner S. Passive immunization with a human immunodeficiency virus type 1-neutralizing monoclonal antibody in Hu-PBL-SCID mice: isolation of a neutralization escape variant. J Infect Dis 1998, 177:889-97.
108. Okamoto Y, Eda Y, Ogura A, Shibata S, Amagai T, Katsura Y, Asano T, Kimachi K, Makizumi K, Honda M. In SCID-hu mice, passive transfer of a humanized antibody prevents infection and atrophic change of medulla in human thymic implant due to intravenous inoculation of primary HIV-1 isolate. J Immunol 1998, 160:69-76.
109. Yoshida A, Tanaka R, Murakami T, Takahashi Y, Koyanagi Y, Nakamura M, Ito M, Yamamoto N, Tanaka Y. Induction of protective immune responses against R5 human immunodeficiency virus type 1 (HIV-1) infection in hu-PBL-SCID mice by intrasplenic immunization with HIV-1-pulsed dendritic cells: possible involvement of a novel factor of human CD4(+) T-cell origin. J Virol 2003, 77:8719-28. 167224, 12885891.
110. Yoshida A, Tanaka R, Kodama A, Yamamoto N, Ansari AA, Tanaka Y. Identification of HIV-1 epitopes that induce the synthesis of a R5 HIV-1 suppression factor by human CD4+ T cells isolated from HIV-1 immunized hu-PBL SCID mice. Clin Dev Immunol 2005, 12:235-42. 2270741, 16584108.
111. Prochazka M, Gaskins HR, Shultz LD, Leiter EH. The nonobese diabetic scid mouse: model for spontaneous thymomagenesis associated with immunodeficiency. Proc Natl Acad Sci USA 1992, 89:3290-4. 48852, 1373493.
112. Ogasawara K, Hamerman JA, Hsin H, Chikuma S, Bour-Jordan H, Chen T, Pertel T, Carnaud C, Bluestone JA, Lanier LL. Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity 2003, 18:41-51.
113. Baxter AG, Cooke A. Complement lytic activity has no role in the pathogenesis of autoimmune diabetes in NOD mice. Diabetes 1993, 42:1574-8.
114. Lowry PA, Shultz LD, Greiner DL, Hesselton RM, Kittler EL, Tiarks CY, Rao SS, Reilly J, Leif JH, Ramshaw H. Improved engraftment of human cord blood stem cells in NOD/LtSz-scid/scid mice after irradiation or multiple-day injections into unirradiated recipients. Biol Blood Marrow Transplant 1996, 2:15-23.
115. Pflumio F, Izac B, Katz A, Shultz LD, Vainchenker W, Coulombel L. Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood 1996, 88:3731-40.
116. Legrand N, Weijer K, Spits H. Experimental models to study development and function of the human immune system in vivo. J Immunol 2006, 176:2053-8.
117. Koyanagi Y, Tanaka Y, Kira J, Ito M, Hioki K, Misawa N, Kawano Y, Yamasaki K, Tanaka R, Suzuki Y. Primary human immunodeficiency virus type 1 viremia and central nervous system invasion in a novel hu-PBL-immunodeficient mouse strain. J Virol 1997, 71:2417-24. 191352, 9032379.
118. Wege AK, Melkus MW, Denton PW, Estes JD, Garcia JV. Functional and phenotypic characterization of the humanized BLT mouse model. Curr Top Microbiol Immunol 2008, 324:149-65.
119. Denton PW, Estes JD, Sun Z, Othieno FA, Wei BL, Wege AK, Powell DA, Payne D, Haase AT, Garcia JV. Antiretroviral pre-exposure prophylaxis prevents vaginal transmission of HIV-1 in humanized BLT mice. PLoS Med 2008, 5:e16. 2194746, 18198941.
120. Watanabe S, Terashima K, Ohta S, Horibata S, Yajima M, Shiozawa Y, Dewan MZ, Yu Z, Ito M, Morio T. Hematopoietic stem cell-engrafted NOD/SCID/IL2Rgamma null mice develop human lymphoid systems and induce long-lasting HIV-1 infection with specific humoral immune responses. Blood 2007, 109:212-8.
121. Watanabe S, Ohta S, Yajima M, Terashima K, Ito M, Mugishima H, Fujiwara S, Shimizu K, Honda M, Shimizu N. Humanized NOD/SCID/IL2Rgamma(null) mice transplanted with hematopoietic stem cells under nonmyeloablative conditions show prolonged life spans and allow detailed analysis of human immunodeficiency virus type 1 pathogenesis. J Virol 2007, 81:13259-64. 2169100, 17881441.
122. Goldman JP, Blundell MP, Lopes L, Kinnon C, Di Santo JP, Thrasher AJ. Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain. Br J Haematol 1998, 103:335-42.
123. Mazurier F, Fontanellas A, Salesse S, Taine L, Landriau S, Moreau-Gaudry F, Reiffers J, Peault B, Di Santo JP, de Verneuil H. A novel immunodeficient mouse model - RAG2 × common cytokine receptor gamma chain double mutants - requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J Interferon Cytokine Res 1999, 19:533-41.
124. Gimeno R, Weijer K, Voordouw A, Uittenbogaart CH, Legrand N, Alves NL, Wijnands E, Blom B, Spits H. Monitoring the effect of gene silencing by RNA interference in human CD34+ cells injected into newborn RAG2-/- gammac-/- mice: functional inactivation of p53 in developing T cells. Blood 2004, 104:3886-93.
125. Baenziger S, Tussiwand R, Schlaepfer E, Mazzucchelli L, Heikenwalder M, Kurrer MO, Behnke S, Frey J, Oxenius A, Joller H. Disseminated and sustained HIV infection in CD34+ cord blood cell-transplanted Rag2-/-gamma c-/- mice. Proc Natl Acad Sci USA 2006, 103:15951-6. 1635108, 17038503.
126. Berges BK, Wheat WH, Palmer BE, Connick E, Akkina R. HIV-1 infection and CD4 T cell depletion in the humanized Rag2-/-gamma c-/- (RAG-hu) mouse model. Retrovirology 2006, 3:76. 1635423, 17078891.
127. Zhang L, Kovalev GI, Su L. HIV-1 infection and pathogenesis in a novel humanized mouse model. Blood 2007, 109:2978-81. 1852218, 17132723.
128. Jiang Q, Zhang L, Wang R, Jeffrey J, Washburn ML, Brouwer D, Barbour S, Kovalev GI, Unutmaz D, Su L. FoxP3+CD4+ regulatory T cells play an important role in acute HIV-1 infection in humanized Rag2-/-gammaC-/- mice in vivo. Blood 2008, 112:2858-68.
129. Gorantla S, Sneller H, Walters L, Sharp JG, Pirruccello SJ, West JT, Wood C, Dewhurst S, Gendelman HE, Poluektova L. Human immunodeficiency virus type 1 pathobiology studied in humanized BALB/c-Rag2-/-gammac-/- mice. J Virol 2007, 81:2700-12. 1865995, 17182671.
130. An DS, Poon B, Ho Tsong Fang R, Weijer K, Blom B, Spits H, Chen IS, Uittenbogaart CH. Use of a novel chimeric mouse model with a functionally active human immune system to study human immunodeficiency virus type 1 infection. Clin Vaccine Immunol 2007, 14:391-6. 1865603, 17314230.
131. Van Duyne R, Cardenas J, Easley R, Wu W, Kehn-Hall K, Klase Z, Mendez S, Zeng C, Chen H, Saifuddin M. Effect of transcription peptide inhibitors on HIV-1 replication. Virology 2008, 376:308-22.
132. ter Brake O, Legrand N, von Eije KJ, Centlivre M, Spits H, Weijer K, Blom B, Berkhout B. Evaluation of safety and efficacy of RNAi against HIV-1 in the human immune system (Rag-2(-/-)gammac(-/-)) mouse model. Gene Ther 2009, 16:148-53.
133. Berges BK, Akkina SR, Folkvord JM, Connick E, Akkina R. Mucosal transmission of R5 and X4 tropic HIV-1 via vaginal and rectal routes in humanized Rag2-/- gammac -/- (RAG-hu) mice. Virology 2008, 373:342-51.
134. Hofer U, Baenziger S, Heikenwalder M, Schlaepfer E, Gehre N, Regenass S, Brunner T, Speck RF. RAG2-/- gamma(c)-/- mice transplanted with CD34+ cells from human cord blood show low levels of intestinal engraftment and are resistant to rectal transmission of human immunodeficiency virus. J Virol 2008, 82:12145-53. 2593344, 18842716.
135. Verdonck K, Gonzalez E, Van Dooren S, Vandamme AM, Vanham G, Gotuzzo E. Human T-lymphotropic virus 1: recent knowledge about an ancient infection. Lancet Infect Dis 2007, 7:266-81.
136. Yasunaga J, Matsuoka M. Human T-cell leukemia virus type I induces adult T-cell leukemia: from clinical aspects to molecular mechanisms. Cancer Control 2007, 14:133-40.
137. Takatsuki K. Discovery of adult T-cell leukemia. Retrovirology 2005, 2:16. 555581, 15743528.
138. Yoshida M, Satou Y, Yasunaga J, Fujisawa J, Matsuoka M. Transcriptional control of spliced and unspliced human T-cell leukemia virus type 1 bZIP factor (HBZ) gene. J Virol 2008, 82:9359-68. 2546946, 18653454.
139. Kashanchi F, Brady JN. Transcriptional and post-transcriptional gene regulation of HTLV-1. Oncogene 2005, 24:5938-51.
140. Faris M. Potential for molecular targeted therapy for adult T-cell leukemia/lymphoma. Int Rev Immunol 2008, 27:71-8.
141. Murata K, Yamada Y. The state of the art in the pathogenesis of ATL and new potential targets associated with HTLV-1 and ATL. Int Rev Immunol 2007, 26:249-68.
142. Usui T, Yanagihara K, Tsukasaki K, Murata K, Hasegawa H, Yamada Y, Kamihira S. Characteristic expression of HTLV-1 basic zipper factor (HBZ) transcripts in HTLV-1 provirus-positive cells. Retrovirology 2008, 5:34. 2386809, 18426605.
143. Saito M, Matsuzaki T, Satou Y, Yasunaga J, Saito K, Arimura K, Matsuoka M, Ohara Y. In vivo expression of the HBZ gene of HTLV-1 correlates with proviral load, inflammatory markers and disease severity in HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP). Retrovirology 2009, 6:19. 2653460, 19228429.
144. Shimoyama M. Diagnostic criteria and classification of clinical subtypes of adult T-cell leukaemia-lymphoma. Br J Haematol 1991, 79:1984-87.
145. Feuer G, Fraser JK, Zack JA, Lee F, Feuer R, Chen IS. Human T-cell leukemia virus infection of human hematopoietic progenitor cells: maintenance of virus infection during differentiation in vitro and in vivo. J Virol 1996, 70:4038-44. 190282, 8648741.
146. Nadella MV, Shu ST, Dirksen WP, Thudi NK, Nadella KS, Fernandez SA, Lairmore MD, Green PL, Rosol TJ. Expression of parathyroid hormone-related protein during immortalization of human peripheral blood mononuclear cells by HTLV-1: implications for transformation. Retrovirology 2008, 5:46. 2435116, 18541021.
147. Matsuoka M, Jeang KT. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 2007, 7:270-80.
148. Peloponese JM, Kinjo T, Jeang KT. Human T-cell leukemia virus type 1 Tax and cellular transformation. Int J Hematol 2007, 86:101-6.
149. Agbottah E, Yeh WI, Berro R, Klase Z, Pedati C, Kehn-Hall K, Wu W, Kashanchi F. Two specific drugs, BMS-345541 and purvalanol A induce apoptosis of HTLV-1 infected cells through inhibition of the NF-kappaB and cell cycle pathways. AIDS Res Ther 2008, 5:12. 2483717, 18544167.
150. Feuer G, Zack JA, Harrington WJ, Valderama R, Rosenblatt JD, Wachsman W, Baird SM, Chen IS. Establishment of human T-cell leukemia virus type I T-cell lymphomas in severe combined immunodeficient mice. Blood 1993, 82:722-31.
151. Kondo A, Imada K, Hattori T, Yamabe H, Tanaka T, Miyasaka M, Okuma M, Uchiyama T. A model of in vivo cell proliferation of adult T-cell leukemia. Blood 1993, 82:2501-9.
152. Liu Y, Dole K, Stanley JR, Richard V, Rosol TJ, Ratner L, Lairmore M, Feuer G. Engraftment and tumorigenesis of HTLV-1 transformed T cell lines in SCID/bg and NOD/SCID mice. Leuk Res 2002, 26:561-7.
153. Tanaka M, Sun B, Fang J, Nitta T, Yoshida T, Kohtoh S, Kikukawa H, Hanai S, Uchida K, Miwa M. Human T-cell leukemia virus type 1 (HTLV-1) infection of mice: proliferation of cell clones with integrated HTLV-1 provirus in lymphoid organs. J Virol 2001, 75:4420-3. 114189, 11287593.
154. Miyazato P, Yasunaga J, Taniguchi Y, Koyanagi Y, Mitsuya H, Matsuoka M. De novo human T-cell leukemia virus type 1 infection of human lymphocytes in NOD-SCID, common gamma-chain knockout mice. J Virol 2006, 80:10683-91. 1641804, 16943297.
155. Takajo I, Umeki K, Morishita K, Yamamoto I, Kubuki Y, Hatakeyama K, Kataoka H, Okayama A. Engraftment of peripheral blood mononuclear cells from human T-lymphotropic virus type 1 carriers in NOD/SCID/gammac(null) (NOG) mice. Int J Cancer 2007, 121:2205-11.
156. Ohsugi T, Kumasaka T, Ishida A, Ishida T, Horie R, Watanabe T, Umezawa K, Yamaguchi K. In vitro and in vivo antitumor activity of the NF-kappaB inhibitor DHMEQ in the human T-cell leukemia virus type I-infected cell line, HUT-102. Leuk Res 2006, 30:90-7.
157. Ohsugi T, Kumasaka T, Okada S, Ishida T, Yamaguchi K, Horie R, Watanabe T, Umezawa K. Dehydroxymethylepoxyquinomicin (DHMEQ) therapy reduces tumor formation in mice inoculated with tax-deficient adult T-cell leukemia-derived cell lines. Cancer Lett 2007, 257:206-15.
158. Shu ST, Nadella MV, Dirksen WP, Fernandez SA, Thudi NK, Werbeck JL, Lairmore MD, Rosol TJ. A novel bioluminescent mouse model and effective therapy for adult T-cell leukemia/lymphoma. Cancer Res 2007, 67:11859-66.
159. Nitta T, Tanaka M, Sun B, Sugihara E, Kimura M, Kamada Y, Takahashi H, Hanai S, Jiang SW, Fujisawa J. Reduction of human T-cell leukemia virus type-1 infection in mice lacking nuclear factor-kappaB-inducing kinase. Cancer Sci 2008, 99:872-8.
160. Chen J, Zhang M, Ju W, Waldmann TA. Effective treatment of a murine model of adult T-cell leukemia using depsipeptide and its combination with unmodified daclizumab directed toward CD25. Blood 2009, 113:1287-93.
161. Dittmer D, Stoddart C, Renne R, Linquist-Stepps V, Moreno ME, Bare C, McCune JM, Ganem D. Experimental transmission of Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) to SCID-hu Thy/Liv mice. J Exp Med 1999, 190:1857-68. 2195708, 10601360.
162. Gobbi A, Stoddart CA, Locatelli G, Santoro F, Bare C, Linquist-Stepps V, Moreno ME, Abbey NW, Herndier BG, Malnati MS. Coinfection of SCID-hu Thy/Liv mice with human herpesvirus 6 and human immunodeficiency virus type 1. J Virol 2000, 74:8726-31. 116384, 10954574.
163. Alfonzo M, Blanc D, Troadec C, Huerre M, Eliaszewicz M, Gonzalez G, Koyanagi Y, Scott-Algara D. Temporary restoration of immune response against Toxoplasma gondii in HIV-infected individuals after HAART, as studied in the hu-PBMC-SCID mouse model. Clin Exp Immunol 2002, 129:411-9. 1906477, 12197881.