High diversity of the immune repertoire in humanized NOD.SCID.γc -/- mice

European Journal of Immunology

Volumn 39, Issue 8, 2009, Pages 2136-2145

  Marodon, Gilles ^a,b   Desjardins, Delphine ^a,b   Mercey, Laetitia ^a,b   Baillou, Claude ^a,b   Parent, Pierric ^a,b   Manuel, Manuarii ^c,d   Caux, Christophe ^d   Bellier, Bertrand ^a,b   Pasqual, Nicolas ^c   Klatzmann, David ^a,b  

^a CNRS   (France)

^b INSERM   (France)

^c CEA GRENOBLE   (France)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

Animal models; Immune responses; T cells; Vaccination; VDJ recombination

Indexed keywords

ADENOVIRUS VECTOR; GENOMIC DNA; IMMUNOGLOBULIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN J CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; VIRUS GLYCOPROTEIN; CD45 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; GENE REARRANGEMENT; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNIZATION; MOUSE; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; NONOBESE DIABETIC MOUSE; PHENOTYPE; PRIORITY JOURNAL; SCID MOUSE; THYMUS; ANIMAL; CELL CLONE; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GENETICS; HEPATITIS C VIRUS; IMMUNOLOGY; IMMUNOPHENOTYPING; MALE; METABOLISM; METHODOLOGY; MOUSE MUTANT; NEWBORN; POLYMERASE CHAIN REACTION; T LYMPHOCYTE;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD45; CLONE CELLS; FEMALE; FLOW CYTOMETRY; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; HEPACIVIRUS; HUMANS; IMMUNITY, CELLULAR; IMMUNIZATION; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOPHENOTYPING; MALE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 70249093644     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939480     Document Type: Article

References (37)

1. Ito, M., Hiramatsu, H., Kobayashi, K., Suzue, K., Kawahata, M., Hioki, K., Ueyama, Y. et al., NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002. 100: 3175-3182. (Pubitemid 35217065)
2. Traggiai, E., Chicha, L., Mazzucchelli, L., Bronz, L., Piffaretti, J. C., Lanzavecchia, A. and Manz, M. G., Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 2004. 304: 104-107. (Pubitemid 38451466)
3. Shultz, L. D., Ishikawa, F. and Greiner, D. L., Humanized mice in translational biomedical research. Nat. Rev. Immunol. 2007. 7: 118-130.
4. Baenziger, S., Tussiwand, R., Schlaepfer, E., Mazzucchelli, L., Heikenwalder, M., Kurrer, M. O., Behnke, S. et al., Disseminated and sustained HIV infection in CD34+cord blood cell-transplanted Rag2-/-γc-/- mice. Proc Natl Acad Sci. USA 2006. 103: 15951-15956.
5. Berges, B. K., Wheat, W. H., Palmer, B. E., Connick, E. and Akkina, R., HIV-1 infection and CD4 T cell depletion in the humanized Rag2-/-gammac-/- (RAG-hu) mouse model. Retrovirology 2006. 3: 76. (Pubitemid 44742668)
6. Gorantla, S., Sneller, H., Walters, L., Sharp, J. G., Pirruccello, S. J., West, J. T., Wood, C. et al., Human immunodeficiency virus type 1 pathobiology studied in humanized BALB/c-Rag2-/-γc-/- mice. J. Virol. 2007. 81: 2700-2712.
7. Zhang, L., Kovalev, G. I. and Su, L., HIV-1 infection and pathogenesis in a novel humanized mouse model. Blood 2007. 109: 2978-2981. (Pubitemid 46482096)
8. Watanabe, S., Terashima, K., Ohta, S., Horibata, S., Yajima, M., Shiozawa, Y., Dewan, M. Z. et al., Hematopoietic stem cell-engrafted NOD/SCID/IL2Rγnull mice develop human lymphoid systems and induce long-lasting HIV-1 infection with specific humoral immune responses. Blood 2007. 109: 212-218. (Pubitemid 46070123)
9. Nakata, H., Maeda, K., Miyakawa, T., Shibayama, S., Matsuo, M., Takaoka, Y., Ito, M. et al., Potent anti-R5 human immunodeficiency virus type 1 effects of a CCR5 antagonist, AK602/ONO4128/GW873140, in a novel human peripheral blood mononuclear cell nonobese diabetic-SCID, interleukin-2 receptor gamma-chain-knocked-out AIDS mouse model. J. Virol. 2005. 79: 2087-2096. (Pubitemid 40204566)
10. Nikolich-Zugich, J., Slifka, M. K. and Messaoudi, I., The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 2004. 4: 123-132.
11. Gorochov, G., Neumann, A. U., Kereveur, A., Parizot, C., Li, T., Katlama, C., Karmochkine, M. et al., Perturbation of CD4+and CD8+T-cell repertoires during progression to AIDS and regulation of the CD4+repertoire during antiviral therapy. Nat. Med. 1998. 4: 215-221.
12. Yahata, T., Ando, K., Nakamura, Y., Ueyama, Y., Shimamura, K., Tamaoki, N., Kato, S. et al., Functional human T lymphocyte development from cord blood CD34+cells in nonobese diabetic/Shi-scid, IL-2 receptor gamma null mice. J. Immunol. 2002. 169: 204-209.
13. Hiramatsu, H., Nishikomori, R., Heike, T., Ito, M., Kobayashi, K., Katamura, K. and Nakahata, T., Complete reconstitution of human lymphocytes from cord blood CD34+cells using the NOD/SCID/γcnull mice model. Blood 2003. 102: 873-880.
14. Pannetier, C., Cochet, M., Darche, S., Casrouge, A., Zoller, M. and Kourilsky, P., The sizes of the CDR3 hypervariable regions of the murine T-cell receptor beta chains vary as a function of the recombined germline segments. Proc. Natl. Acad. Sci. USA 1993. 90: 4319-4323.
15. Shultz, L. D., Lyons, B. L., Burzenski, L. M., Gott, B., Chen, X., Chaleff, S., Kotb, M. et al., Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2Rγnull mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 2005. 174: 6477-6489. (Pubitemid 40663843)
16. Ishikawa, F., Yasukawa, M., Lyons, B., Yoshida, S., Miyamoto, T., Yoshimoto, G., Watanabe, T. et al., Development of functional human blood and immune systems in NOD/SCID/IL2 receptor γ chain(null) mice. Blood 2005. 106: 1565-1573. (Pubitemid 41208567)
17. Melkus, M. W., Estes, J. D., Padgett-Thomas, A., Gatlin, J., Denton, P. W., Othieno, F. A., Wege, A. K. et al., Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat. Med. 2006. 12: 1316-1322.
18. Tonomura, N., Habiro, K., Shimizu, A., Sykes, M. and Yang, Y.-G., Antigen-specific human T-cell responses and T cell-dependent production of human antibodies in a humanized mouse model. Blood 2008. 111: 4293-4296.
19. Gurer, C., Strowig, T., Brilot, F., Pack, M., Trumpfheller, C., Arrey, F., Park, C. G. et al., Targeting the nuclear antigen 1 of Epstein-Barr virus to the human endocytic receptor DEC-205 stimulates protective T-cell responses. Blood 2008. 112: 1231-1239.
20. Pasqual, N., Gallagher, M., Aude-Garcia, C., Loiodice, M., Thuderoz, F., Demongeot, J., Ceredig, R. et al., Quantitative and qualitative changes in V-J alpha rearrangements during mouse thymocytes differentiation: implication for a limited T cell receptor alpha chain repertoire. J. Exp. Med. 2002. 196: 1163-1173.
21. Colonna, M., Trinchieri, G. and Liu, Y.-J., Plasmacytoid dendritic cells in immunity. Nat. Immunol. 2004. 5: 1219-1226.
22. Mackall, C. L., Bare, C. V., Granger, L. A., Sharrow, S. O., Titus, J. A. and Gress, R. E., Thymic-independent T cell regeneration occurs via antigen-driven expansion of peripheral T cells resulting in a repertoire that is limited in diversity and prone to skewing. J. Immunol. 1996. 156: 4609-4616.
23. La Gruta, N. L., Driel, I. R. and Gleeson, P. A., Peripheral T. cell expansion in lymphopenic mice results in a restricted T cell repertoire. Eur. J. Immunol. 2000. 30: 3380-3386.
24. Zamisch, M., Moore-Scott, B., Su, D. M., Lucas, P. J., Manley, N. and Richie, E. R., Ontogeny and regulation of IL-7-expressing thymic epithelial cells. J. Immunol. 2005. 174: 60-67. (Pubitemid 40007392)
25. Sportes, C., Hakim, F. T., Memon, S. A., Zhang, H., Chua, K. S., Brown, M. R., Fleisher, T. A. et al., Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J. Exp. Med. 2008. 205: 1701-1714.
26. King, C., Ilic, A., Koelsch, K. and Sarvetnick, N., Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 2004. 117: 265-277. (Pubitemid 38496245)
27. Arruvito, L., Sanz, M., Banham, A. H. and Fainboim, L., Expansion of CD4 (+)CD25(+) and FOXP3(+) regulatory T cells during the follicular phase of the menstrual cycle: Implications for human reproduction. J. Immunol. 2007. 178: 2572-2578. (Pubitemid 46233460)
28. Mutis, T., van Rijn, R. S., Simonetti, E. R., Aarts-Riemens, T., Emmelot, M. E., van Bloois, L., Martens, A. et al., Human regulatory T cells control xenogeneic graft-versus-host disease induced by autologous T cells in RAG2-/-gammac-/- immunodeficient mice. Clin. Cancer Res. 2006. 12: 5520-5525.
29. Legrand, N., Cupedo, T., van Lent, A. U., Ebeli, M. J., Weijer, K., Hanke, T. and Spits, H., Transient accumulation of human mature thymocytes and regulatory T cells with CD28 superagonist in human immune system Rag2-/-gammac-/- mice. Blood 2006. 108: 238-245.
30. Jiang, Q., Zhang, L., Wang, R., Jeffrey, J., Washburn, M. L., Brouwer, D., Barbour, S. et al., FoxP3+CD4+regulatory T cells play an important role in acute HIV-1 infection in humanized Rag2-/-γC-/- mice in vivo. Blood 2008. 112: 2858-2868.
31. Sun, Z., Denton, P. W., Estes, J. D., Othieno, F. A., Wei, B. L., Wege, A. K., Melkus, M. W. et al., Intrarectal transmission, systemic infection, and CD4+T cell depletion in humanized mice infected with HIV-1. J. Exp. Med. 2007. 204: 705-714.
32. Cupedo, T., Crellin, N. K., Papazian, N., Rombouts, E. J., Weijer, K., Grogan, J. L., Fibbe, W. E. et al., Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+CD127+natural killer-like cells. Nat. Immunol. 2009. 10: 66-74.
33. Manz, M. G., Human-hemato-lymphoid-system mice: opportunities and challenge. Immunity 2007. 26: 537-541.
34. Desjardins, D., Huret, C., Dalba, C., Kreppel, F., Kochanek, S., Cosset, F. L., Tangy, F. et al., Recombinant retrovirus-like particle forming DNA vaccines in prime-boost immunization and their use for hepatitis C virus vaccine development. J. Gene Med. 2009. 11: 313-325.
35. Lauer, G. M., Lucas, M., Timm, J., Ouchi, K., Kim, A. Y., Day, C. L., zur Wiesch, J. S. et al., Full-breadth analysis of CD8+T-cell responses in acute hepatitis C virus infection and early therapy. J. Virol. 2005. 79: 12979-12988.
36. Missale, G., Bertoni, R., Lamonaca, V., Valli, A., Massari, M., Mori, C., Rumi, M. G. et al., Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J. Clin. Invest. 1996. 98: 706-714.
37. Scheeren, F. A., Nagasawa, M., Weijer, K., Cupedo, T., Kirberg, J., Legrand, N. and Spits, H., T cell-independent development and induction of somatic hypermutation in human IgM+IgD+CD27+B cells. J. Exp. Med. 2008. 205: 2033-2042.