Engineering the human thymic microenvironment to support thymopoiesis in vivo

Stem Cells

Volumn 32, Issue 9, 2014, Pages 2386-2396

  Chung, Brile ^a   Montel Hagen, Amélie ^a   Ge, Shundi ^a   Blumberg, Garrett ^a   Kim, Kenneth ^a   Klein, Sam ^a   Zhu, Yuhua ^a   Parekh, Chintan ^a   Balamurugan, Arumugam ^a,b   Yang, Otto O ^a,b   Crooks, Gay M ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c AIDS HEALTHCARE FOUNDATION   (United States)

Author keywords

T cell development; Thymic microenvironment; Thymus; Thymus transplantation; Tissue engineering; Vascular endothelial growth factor

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; AUTOIMMUNE REGULATOR PROTEIN; CD3 ANTIGEN; CD34 ANTIGEN; CD4 ANTIGEN; CD5 ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; CYTOKERATIN 14; CYTOKERATIN 5; DNA NUCLEOTIDYLEXOTRANSFERASE; ENDOGLIN; EPITHELIAL CELL ADHESION MOLECULE; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 2; HERMES ANTIGEN; KERATINOCYTE GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN P63; T LYMPHOCYTE RECEPTOR; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL COMPOSITION; CELL EXPANSION; CELL GROWTH; CELL MIGRATION; CELL POPULATION; EX VIVO STUDY; GENE; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFANT; INGUINAL REGION; LENTIVIRINAE; LYMPHOCYTE DIFFERENTIATION; MESENCHYME; MICROENVIRONMENT; MOUSE; NEWBORN; NONHUMAN; THYMIC EPITHELIAL CELL; THYMIC MESENCHYME; THYMOCYTE; THYMOPOIESIS; THYMUS; TISSUE ENGINEERING; UMBILICAL CORD BLOOD; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; LYMPHOPOIESIS; METABOLISM; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; PROCEDURES; SCID MOUSE; TUMOR MICROENVIRONMENT;

ANIMALS; CELL PROLIFERATION; CELLULAR MICROENVIRONMENT; GENE EXPRESSION; HUMANS; LYMPHOPOIESIS; MICE; MICE, INBRED NOD; MICE, SCID; THYMUS GLAND; TISSUE ENGINEERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84906254181     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1731     Document Type: Article

References (46)

1. Chung B, Barbara-Burnham L, Barsky L, et al. Radiosensitivity of thymic interleukin-7 production and thymopoiesis after bone marrow transplantation. Blood 2001; 98: 1601-1606.
2. Douek DC, McFarland RD, Keiser PH, et al. Changes in thymic function with age and during the treatment of HIV infection. Nature 1998; 396: 690-695.
3. Hakim FT, Memon SA, Cepeda R, et al. Age-dependent incidence, time course, and consequences of thymic renewal in adults. J Clin Invest 2005; 115: 930-939.
4. Mackall CL, Fleisher TA, Brown MR, et al. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 1995; 332: 143-149.
5. Weinberg K, Blazar BR, Wagner JE, et al. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood 2001; 97: 1458-1466.
6. Markert ML, Hummell DS, Rosenblatt HM, et al. Complete DiGeorge syndrome: Persistence of profound immunodeficiency. J Pediatr 1998; 132: 15-21.
7. Brehm MA, Jouvet N, Greiner DL, et al. Humanized mice for the study of infectious diseases. Curr Opin Immunol 2013.
8. Brehm MA, Shultz LD, Greiner DL,. Humanized mouse models to study human diseases. Curr Opin Endocrinol Diabetes Obes 2010; 17: 120-125.
9. 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.
10. Shultz LD, Ishikawa F, Greiner DL,. Humanized mice in translational biomedical research. Nat Rev Immunol 2007; 7: 118-130.
11. McCune JM, Namikawa R, Kaneshima H, et al. The SCID-hu mouse: Murine model for the analysis of human hematolymphoid differentiation and function. Science 1988; 241: 1632-1639.
12. Lapidot T, Pflumio F, Doedens M, et al. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science 1992; 255: 1137-1141.
13. Nolta JA, Hanley MB, Kohn DB,. Sustained human hematopoiesis in immunodeficient mice by cotransplantation of marrow stroma expressing human interleukin-3: Analysis of gene transduction of long-lived progenitors. Blood 1994; 83: 3041-3051.
14. Ishikawa F, Yasukawa M, Lyons B, et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 2005; 106: 1565-1573.
15. Ito M, Hiramatsu H, Kobayashi K, et al. NOD/SCID/gamma(c)(null) mouse: An excellent recipient mouse model for engraftment of human cells. Blood 2002; 100: 3175-3182.
16. Lepus CM, Gibson TF, Gerber SA, 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.
17. Pearson T, Shultz LD, Miller D, et al. Non-obese diabetic-recombination activating gene-1 (NOD-Rag1 null) interleukin (IL)-2 receptor common gamma chain (IL2r gamma null) null mice: A radioresistant model for human lymphohaematopoietic engraftment. Clin Exp Immunol 2008; 154: 270-284.
18. Traggiai E, Chicha L, Mazzucchelli L, et al. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 2004; 304: 104-107.
19. Wege AK, Melkus MW, Denton PW, et al. Functional and phenotypic characterization of the humanized BLT mouse model. Curr Top Microbiol Immunol 2008; 324: 149-165.
20. Kalscheuer H, Danzl N, Onoe T, et al. A model for personalized in vivo analysis of human immune responsiveness. Sci Transl Med 2012; 4: 125ra130.
21. Melkus MW, Estes JD, Padgett-Thomas A, et al. Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med 2006; 12: 1316-1322.
22. Tonomura N, Habiro K, Shimizu A, et al. Antigen-specific human T-cell responses and T cell-dependent production of human antibodies in a humanized mouse model. Blood 2008; 111: 4293-4296.
23. Cuddihy AR, Ge S, Zhu J, et al. VEGF-mediated cross-talk within the neonatal murine thymus. Blood 2009; 113: 2723-2731.
24. Cuddihy AR, Suterwala BT, Ge S, et al. Rapid thymic reconstitution following bone marrow transplantation in neonatal mice is VEGF-dependent. Biol Blood Marrow Transplant 2012; 18: 683-689.
25. Ropke C, Elbroend J,. Human thymic epithelial cells in serum-free culture: Nature and effects on thymocyte cell lines. Dev Immunol 1992; 2: 111-121.
26. Haas DL, Case SS, Crooks GM, et al. Critical factors influencing stable transduction of human CD34(+) cells with HIV-1-derived lentiviral vectors. Mol Ther 2000; 2: 71-80.
27. Balamurugan A, Ng HL, Yang OO,. Rapid T cell receptor delineation reveals clonal expansion limitation of the magnitude of the HIV-1-specific CD8+ T cell response. J Immunol 2010; 185: 5935-5942.
28. Anderson G, Jenkinson EJ,. Investigating central tolerance with reaggregate thymus organ cultures. Methods Mol Biol 2007; 380: 185-196.
29. Akiyama T, Shimo Y, Yanai H, et al. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-tolerance. Immunity 2008; 29: 423-437.
30. Poliani PL, Facchetti F, Ravanini M, et al. Early defects in human T-cell development severely affect distribution and maturation of thymic stromal cells: Possible implications for the pathophysiology of Omenn syndrome. Blood 2009; 114: 105-108.
31. Dooley J, Erickson M, Larochelle WJ, et al. FGFR2IIIb signaling regulates thymic epithelial differentiation. Dev Dyn 2007; 236: 3459-3471.
32. Itoi M, Tsukamoto N, Yoshida H, et al. Mesenchymal cells are required for functional development of thymic epithelial cells. Int Immunol 2007; 19: 953-964.
33. Revest JM, Suniara RK, Kerr K, et al. Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J Immunol 2001; 167: 1954-1961.
34. Spits H,. Development of alphabeta T cells in the human thymus. Nat Rev Immunol 2002; 2: 760-772.
35. Gardner JM, Fletcher AL, Anderson MS, et al. AIRE in the thymus and beyond. Curr Opin Immunol 2009; 21: 582-589.
36. Yano M, Kuroda N, Han H, et al. Aire controls the differentiation program of thymic epithelial cells in the medulla for the establishment of self-tolerance. J Exp Med 2008; 205: 2827-2838.
37. Koch U, Fiorini E, Benedito R, et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med 2008; 205: 2515-2523.
38. Mohtashami M, Zuniga-Pflucker JC,. Three-dimensional architecture of the thymus is required to maintain delta-like expression necessary for inducing T cell development. J Immunol 2006; 176: 730-734.
39. Schmitt TM, Zuniga-Pflucker JC,. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 2002; 17: 749-756.
40. Zuniga-Pflucker JC,. T-cell development made simple. Nat Rev Immunol 2004; 4: 67-72.
41. Anderson G, Jenkinson EJ, Moore NC, et al. MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 1993; 362: 70-73.
42. Gray D, Abramson J, Benoist C, et al. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire. J Exp Med 2007; 204: 2521-2528.
43. Seach N, Hammett M, Chidgey A,. Isolation, characterization, and reaggregate culture of thymic epithelial cells. Methods Mol Biol 2013; 945: 251-272.
44. Jenkinson WE, Rossi SW, Parnell SM, et al. PDGFRalpha-expressing mesenchyme regulates thymus growth and the availability of intrathymic niches. Blood 2007; 109: 954-960.
45. Jenkinson WE, Jenkinson EJ, Anderson G,. Differential requirement for mesenchyme in the proliferation and maturation of thymic epithelial progenitors. J Exp Med 2003; 198: 325-332.
46. Markert ML, Devlin BH, Alexieff MJ, et al. Review of 54 patients with complete DiGeorge anomaly enrolled in protocols for thymus transplantation: Outcome of 44 consecutive transplants. Blood 2007; 109: 4539-4547.