Conserved and divergent aspects of human T-cell development and migration in humanized mice

Immunology and Cell Biology

Volumn 93, Issue 8, 2015, Pages 716-726

  Halkias, Joanna ^a,b   Yen, Bonnie ^a   Taylor, Kayleigh T ^a   Reinhartz, Olaf ^b,c   Winoto, Astar ^a   Robey, Ellen A ^a   Melichar, Heather J ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL OAKLAND   (United States)

^c LUCILE PACKARD CHILDREN S HOSPITAL   (United States)

^d MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR FOXP3; BIOLOGICAL MARKER; HLA A2 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL MATURATION; CHIMERA; CONTROLLED STUDY; FETUS; GENE EXPRESSION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MICROENVIRONMENT; MOUSE; NEWBORN; NONHUMAN; STROMA; T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSGENE; ANIMAL; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; LYMPHOPOIESIS; METABOLISM; ORGANOGENESIS; PHENOTYPE; PHYSIOLOGY; REPORTER GENE; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TUMOR MICROENVIRONMENT;

ANIMALS; BIOMARKERS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MOVEMENT; CELLULAR MICROENVIRONMENT; GENE EXPRESSION; GENES, REPORTER; HLA-A2 ANTIGEN; HUMANS; IMMUNE SYSTEM; LYMPHOPOIESIS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; ORGANOGENESIS; PHENOTYPE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; THYMOCYTES; THYMUS GLAND;

EID: 84941878986     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2015.38     Document Type: Article

References (70)

1. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 2005; 106: 1565-1573.
2. Traggiai E, Chicha L, Mazzucchelli L, Bronz L, Piffaretti JC, Lanzavecchia A et al. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 2004; 304: 104-107.
3. Brehm MA, Cuthbert A, Yang C, Miller DM, DiIorio P, Laning J et al. Parameters for establishing humanized mouse models to study human immunity: analysis of human hematopoietic stem cell engraftment in three immunodeficient strains of mice bearing the IL2rgamma(null) mutation. Clin Immunol 2010; 135: 84-98.
4. Lepus CM, Gibson TF, Gerber SA, Kawikova I, Szczepanik M, Hossain J et al. Comparison of human fetal liver, umbilical cord blood, and adult blood hematopoietic stem cell engraftment in NOD-scid/gammac-/-, Balb/c-Rag1-/-gammac-/-, and C.B-17-scid/bg immunodeficient mice. Hum Immunol 2009; 70: 790-802.
5. Aryee KE, Shultz LD, Brehm MA. Immunodeficient mouse model for human hematopoietic stem cell engraftment and immune system development. Methods Mol Biol 2014; 1185: 267-278.
6. Lan P, Tonomura N, Shimizu A, Wang S, Yang YG. Reconstitution of a functional human immune system in immunodeficient mice through combined human fetal thymus/liver and CD34+ cell transplantation. Blood 2006; 108: 487-492.
7. 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: 1632-1639.
8. Melkus MW, Estes JD, Padgett-Thomas A, Gatlin J, Denton PW, Othieno FA et al. Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med 2006; 12: 1316-1322.
9. Plum J, De Smedt M, Leclercq G, Taghon T, Kerre T, Vandekerckhove B. Human intrathymic development: a selective approach. Semin Immunopathol 2008; 30: 411-423.
10. Shultz LD, Saito Y, Najima Y, Tanaka S, Ochi T, Tomizawa M et al. Generation of functional human T-cell subsets with HLA-restricted immune responses in HLA class I expressing NOD/SCID/IL2r gamma(null) humanized mice. Proc Natl Acad Sci USA 2010; 107: 13022-13027.
11. Jaiswal S, Pearson T, Friberg H, Shultz LD, Greiner DL, Rothman AL et al. Dengue virus infection and virus-specific HLA-A2 restricted immune responses in humanized NOD-scid IL2rgammanull mice. PLoS ONE 2009; 4: e7251.
12. Strowig T, Gurer C, Ploss A, Liu YF, Arrey F, Sashihara J et al. Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J Exp Med 2009; 206: 1423-1434.
13. Halkias J, Melichar HJ, Taylor KT, Ross JO, Yen B, Cooper SB et al. Opposing chemokine gradients control human thymocyte migration in situ. J Clin Invest 2013; 123: 2131-2142.
14. Gilhus NE, Matre R. HLA-DR antigens and Fc gamma receptors in fetal and infant thymus, examined by a double-marker technique. Acta Pathol Microbiol Immunol Scand C 1983; 91: 227-232.
15. Marinova T, Altankova I, Dimitrova D, Pomakov Y. Presence of HLA-DR immunopositive cells in human fetal thymus. Arch Physiol Biochem 2001; 109: 74-79.
16. Park SH, Bae YM, Kim TJ, Ha IS, Kim S, Chi JG et al. HLA-DR expression in human fetal thymocytes. Hum Immunol 1992; 33: 294-298.
17. Thulesen S, Jorgensen A, Gerwien J, Dohlsten M, Holst Nissen M, Odum N et al. Superantigens are presented by and activate thymocytes from infants. Exp Clin Immunogenet 1999; 16: 226-233.
18. Choi EY, Jung KC, Park HJ, Chung DH, Song JS, Yang SD et al. Thymocyte-thymocyte interaction for efficient positive selection and maturation of CD4 T cells. Immunity 2005; 23: 387-396.
19. Lee YJ, Jeon YK, Kang BH, Chung DH, Park CG, Shin HY et al. Generation of PLZF+ CD4+ T cells via MHC class II-dependent thymocyte-thymocyte interaction is a physiological process in humans. J Exp Med 2010; 207: 237-246.
20. Legrand N, Weijer K, Spits H. Experimental models to study development and function of the human immune system in vivo. J Immunol 2006; 176: 2053-2058.
21. Burt TD. Fetal regulatory T cells and peripheral immune tolerance in utero: implications for development and disease. Am J Reprod Immunol 2013; 69: 346-358.
22. Min HS, Lee YJ, Jeon YK, Kim EJ, Kang BH, Jung KC et al. MHC class II-restricted interaction between thymocytes plays an essential role in the production of innate CD8+ T cells. J Immunol 2011; 186: 5749-5757.
23. Yuan J, Nguyen CK, Liu X, Kanellopoulou C, Muljo SA. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 2012; 335: 1195-1200.
24. Gordon SM, Carty SA, Kim JS, Zou T, Smith-Garvin J, Alonzo ES et al. Requirements for eomesodermin and promyelocytic leukemia zinc finger in the development of innate-like CD8+ T cells. J Immunol 2011; 186: 4573-4578.
25. Weinreich MA, Odumade OA, Jameson SC, Hogquist KA. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat Immunol 2010; 11: 709-716.
26. Broussard C, Fleischacker C, Horai R, Chetana M, Venegas AM, Sharp LL et al. Altered development of CD8+ T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 2006; 25: 93-104.
27. Horai R, Mueller KL, Handon RA, Cannons JL, Anderson SM, Kirby MR et al. Requirements for selection of conventional and innate T lymphocyte lineages. Immunity 2007; 27: 775-785.
28. De Rosa SC, Andrus JP, Perfetto SP, Mantovani JJ, Herzenberg LA, Herzenberg LA et al. Ontogeny of gamma delta T cells in humans. J Immunol 2004; 172: 1637-1645.
29. Vermijlen D, Brouwer M, Donner C, Liesnard C, Tackoen M, Van Rysselberge M et al. Human cytomegalovirus elicits fetal gammadelta T cell responses in utero. J Exp Med 2010; 207: 807-821.
30. Havran WL, Allison JP. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 1988; 335: 443-445.
31. Haynes BF, Heinly CS. Early human T cell development: analysis of the human thymus at the time of initial entry of hematopoietic stem cells into the fetal thymic microenvironment. J Exp Med 1995; 181: 1445-1458.
32. Ikuta K, Kina T, MacNeil I, Uchida N, Peault B, Chien YH et al. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 1990; 62: 863-874.
33. Gimeno R, Weijer K, Voordouw A, Uittenbogaart CH, Legrand N, Alves NL et al. 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: 3886-3893.
34. Zhao Y, Dai ZP, Lv P, Gao XM. Phenotypic and functional analysis of human T lymphocytes in early second-and third-trimester fetuses. Clin Exp Immunol 2002; 129: 302-308.
35. Billerbeck E, Barry WT, Mu K, Dorner M, Rice CM, Ploss A. Development of human CD4 +FoxP3+ regulatory T cells in human stem cell factor-, granulocyte-macrophage colonystimulating factor-, and interleukin-3-expressing NOD-SCID IL2Rgamma(null) humanized mice. Blood 2011; 117: 3076-3086.
36. Aschenbrenner K, D'Cruz LM, Vollmann EH, Hinterberger M, Emmerich J, Swee LK et al. Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat Immunol 2007; 8: 351-358.
37. Cowan JE, Parnell SM, Nakamura K, Caamano JH, Lane PJ, Jenkinson EJ et al. The thymic medulla is required for Foxp3+ regulatory but not conventional CD4+ thymocyte development. J Exp Med 2013; 210: 675-681.
38. Lei Y, Ripen AM, Ishimaru N, Ohigashi I, Nagasawa T, Jeker LT et al. Aire-dependent production of XCL1 mediates medullary accumulation of thymic dendritic cells and contributes to regulatory T cell development. J Exp Med 2011; 208: 383-394.
39. Watanabe N, Wang YH, Lee HK, Ito T, Wang YH, Cao W et al. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 2005; 436: 1181-1185.
40. Cupedo T, Nagasawa M, Weijer K, Blom B, Spits H. Development and activation of regulatory T cells in the human fetus. Eur J Immunol 2005; 35: 383-390.
41. Darrasse-Jeze G, Marodon G, Salomon BL, Catala M, Klatzmann D. Ontogeny of CD4 +CD25+ regulatory/suppressor T cells in human fetuses. Blood 2005; 105: 4715-4721.
42. Michaelsson J, Mold JE, McCune JM, Nixon DF. Regulation of T cell responses in the developing human fetus. J Immunol 2006; 176: 5741-5748.
43. Halkias J, Melichar HJ, Taylor KT, Robey EA. Tracking migration during human T cell development. Cell Mol Life Sci 2014; 71: 3101-3117.
44. Bendriss-Vermare N, Barthelemy C, Durand I, Bruand C, Dezutter-Dambuyant C, Moulian N et al. Human thymus contains IFN-alpha-producing CD11c(-), myeloid CD11c(+), and mature interdigitating dendritic cells. J Clin Invest 2001; 107: 835-844.
45. Huntington ND, Alves NL, Legrand N, Lim A, Strick-Marchand H, Plet A et al. Autonomous and extrinsic regulation of thymopoiesis in human immune system (HIS) mice. Eur J Immunol 2011; 41: 2883-2893.
46. Ladi E, Schwickert TA, Chtanova T, Chen Y, Herzmark P, Yin X et al. Thymocytedendritic cell interactions near sources of CCR7 ligands in the thymic cortex. J Immunol 2008; 181: 7014-7023.
47. Le Borgne M, Ladi E, Dzhagalov I, Herzmark P, Liao YF, Chakraborty AK et al. The impact of negative selection on thymocyte migration in the medulla. Nat Immunol 2009; 10: 823-830.
48. Witt CM, Raychaudhuri S, Schaefer B, Chakraborty AK, Robey EA. Directed migration of positively selected thymocytes visualized in real time. PLoS Biol 2005; 3: e160.
49. Azar GA, Lemaitre F, Robey EA, Bousso P. Subcellular dynamics of T cell immunological synapses and kinapses in lymph nodes. Proc Natl Acad Sci USA 2010; 107: 3675-3680.
50. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004; 427: 154-159.
51. Miller MJ, Safrina O, Parker I, Cahalan MD. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J Exp Med 2004; 200: 847-856.
52. Sims TN, Soos TJ, Xenias HS, Dubin-Thaler B, Hofman JM, Waite JC et al. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse. Cell 2007; 129: 773-785.
53. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. Humanized mice for immune system investigation: progress, promise and challenges. Nat Rev Immunol 2012; 12: 786-798.
54. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007; 7: 118-130.
55. Apostolou I, Sarukhan A, Klein L, von Boehmer H. Origin of regulatory T cells with known specificity for antigen. Nat Immunol 2002; 3: 756-763.
56. Jordan MS, Boesteanu A, Reed AJ, Petrone AL, Holenbeck AE, Lerman MA et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001; 2: 301-306.
57. Kawahata K, Misaki Y, Yamauchi M, Tsunekawa S, Setoguchi K, Miyazaki J et al. Generation of CD4(+)CD25(+) regulatory T cells from autoreactive T cells simultaneously with their negative selection in the thymus and from nonautoreactive T cells by endogenous TCR expression. J Immunol 2002; 168: 4399-4405.
58. Ribot J, Romagnoli P, van Meerwijk JP. Agonist ligands expressed by thymic epithelium enhance positive selection of regulatory T lymphocytes from precursors with a normally diverse TCR repertoire. J Immunol 2006; 177: 1101-1107.
59. Coquet JM, Ribot JC, Babala N, Middendorp S, van der Horst G, Xiao Y et al. Epithelial and dendritic cells in the thymic medulla promote CD4+Foxp3+ regulatory T cell development via the CD27-CD70 pathway. J Exp Med 2013; 210: 715-728.
60. Legrand N, Cupedo T, van Lent AU, Ebeli MJ, Weijer K, Hanke T et al. 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.
61. Proietto AI, van Dommelen S, Zhou P, Rizzitelli A, D'Amico A, Steptoe RJ et al. Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci USA 2008; 105: 19869-19874.
62. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000; 12: 431-440.
63. Tai X, Cowan M, Feigenbaum L, Singer A. CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2. Nat Immunol 2005; 6: 152-162.
64. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002; 3: 673-680.
65. Reche PA, Soumelis V, Gorman DM, Clifford T, Liu M, Travis M et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 2001; 167: 336-343.
66. Melichar HJ, Ross JO, Herzmark P, Hogquist KA, Robey EA. Distinct temporal patterns of T cell receptor signaling during positive versus negative selection in situ. Sci Signal 2013; 6: 92.
67. Chen Q, Khoury M, Chen J. Expression of human cytokines dramatically improves reconstitution of specific human-blood lineage cells in humanized mice. Proc Natl Acad Sci USA 2009; 106: 21783-21788.
68. Huntington ND, Alves NL, Legrand N, Lim A, Strick-Marchand H, Mention JJ et al. IL-15 transpresentation promotes both human T-cell reconstitution and T-cell-dependent antibody responses in vivo. Proc Natl Acad Sci USA 2011; 108: 6217-6222.
69. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S et al. 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: 6477-6489.
70. Dzhagalov IL, Melichar HJ, Ross JO, Herzmark P, Robey EA. Two-photon imaging of the immune system. Curr Protoc Cytom 2012; Chapter 12: Unit12-Unit26.