Maintenance of a normal thymic microenvironment and T-cell homeostasis require Smad4-mediated signaling in thymic epithelial cells

Blood

Volumn 112, Issue 9, 2008, Pages 3688-3695

  Jeker, Lukas T ^a   Barthlott, Thomas ^a   Keller, Marcel P ^a   Zuklys, Saulius ^a   Hauri Hohl, Mathias ^a   Deng, Chu Xia ^a   Holländer, Georg A ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; CHEMOKINE; COMPLEMENTARY DNA; SMAD4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL ISOLATION; EPITHELIUM CELL; FLOW CYTOMETRY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE DIFFERENTIATION; MICROENVIRONMENT; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; THYMUS; ANIMAL; CYTOLOGY; FEMALE; GENETIC TRANSCRIPTION; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; MALE; METABOLISM; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PREGNANCY; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CHEMOKINES; DNA, COMPLEMENTARY; EPITHELIAL CELLS; FEMALE; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; MALE; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; PREGNANCY; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION, GENETIC;

EID: 55749107446     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-04-150532     Document Type: Article

References (50)

1. Anderson G, Jenkinson WE, Jones T, et al. Establishment and functioning of intrathymic microenvironments. Immunol Rev. 2006;209:10-27.
2. Klug DB, Carter C, Crouch E, Roop D, Conti CJ, Richie ER. Interdependence of cortical thymic epithelial cell differentiation and T-lineage commitment. Proc Natl Acad Sci U S A. 1998;95: 11822-11827.
3. Bleul CC, Boehm T. Chemokines define distinct microenvironments in the developing thymus. Eur J Immunol. 2000;30:3371-3379.
4. Liu C, Ueno T, Kuse S, et al. The role of CCL21 in recruitment of T-precursor cells to fetal thymi. Blood. 2005;105:31-39.
5. Liu C, Saito F, Liu Z, et al. Coordination between CCR7- and CCR9-mediated chemokine signals in prevascular fetal thymus colonization. Blood. 2006;108:2531-2539.
6. Schwarz BA, Sambandam A, Maillard I, Harman BC, Love PE, Bhandoola A. Selective thymus settling regulated by cytokine and chemokine receptors. J Immunol. 2007;178:2008-2017.
7. Scimone ML, Aifantis I, Apostolou I, von Boehmer H, von Andrian UH. A multistep adhesion cascade for lymphoid progenitor cell homing to the thymus. Proc Natl Acad Sci U S A. 2006;103:7006-7011.
8. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol. 2002;168:2811-2819.
9. Candélas S, Muegge K, Durum SK. IL-7 receptor and VDJ recombination: trophic versus mechanistic actions. Immunity. 1997;6:501-508.
10. Massa S, Balciunaite G, Ceredig R, Rolink AG. Critical role for c-kit (CD117) in T cell lineage commitment and early thymocyte development in vitro. Eur J Immunol. 2006;36:526-532.
11. Rodewald HR, Ogawa M, Haller C, Waskow C, DiSanto JP. Pro-thymocyte expansion by c-kit and the common cytokine receptor gamma chain is essential for repertoire formation. Immunity. 1997;6:265-272.
12. Bhandoola A, von Boehmer H, Petrie HT, Zúñlga-Pflücker JC. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity. 2007; 26:678-689.
13. Ceredig R, Rolink T. A positive look at double-negative thymocytes. Nat Rev Immunol. 2002;2: 888-897.
14. Starr TK, Jameson SC, Hogquist KA. Positive and negative selection of T cells. Annu Rev Immunol. 2003;21:139-176.
15. Massagué J, Blain SW, Lo RS. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell. 2000;103:295-309.
16. Schier AF. Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol. 2003;19:589-621.
17. Whitman M. Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev. 1998;12:2445-2462
18. Licona-Limón P, Soldevila G. The role of TGF-beta superfamily during T-cell development: new insights. Immunol Lett. 2007;109:1-12.
19. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature. 2003;425:577-584.
20. Massagué J, Chen YG. Controlling TGF-beta signaling. Genes Dev. 2000;14:627-644.
21. Massagué J, Seoane J, Wotton D. Smad transcription factors. Genes Dev. 2005;19:2783-2810.
22. Park SH. Fine tuning and cross-talking of TGF-beta signal by inhibitory Smads. J Biochem Mol Biol. 2005;38:9-16.
23. Yang X, Li C, Herrera PL, Deng CX. Generation of Smad4/Dpc4 conditional knockout mice. Genesis. 2002;32:80-81.
24. Sirard C, de la Pompa JL, Elia A, et al. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 1998;12:107-119.
25. Yang X, Li C, Xu X, Deng C. The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci U S A. 1998;95:3667-3672.
26. Nehls M, Kyewski B, Messerle M, et al. Two genetically separable steps in the differentiation of thymic epithelium. Science. 1996;272:886-889.
27. Gray D, Abramson J, Benoist C, Mathis D. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire. J Exp Med. 2007;204: 2521-2528.
28. Jameson SC. T cell homeostasis: keeping useful T cells alive and live T cells useful. Semin Immunol. 2005;17:231-237.
29. Prockop SE, Petrie HT. Regulation of thymus size by competition for stromal niches among early T cell progenitors. J Immunol. 2004;173:1604-1611.
30. Schwarz BA, Bhandoola A. Circulating hematopoietic progenitors with T lineage potential. Nat Immunol. 2004;5:953-960.
31. Perry SS, Wang H, Pierce LJ, Yang AM, Tsai S, Spangrude GJ. L-selectin defines a bone marrow analog to the thymic early T-lineage progenitor. Blood. 2004;103:2990-2996.
32. Gray DH, Seach N, Ueno T, et al. Developmental kinetics, turnover, and stimulatory capacity of thymic epithelial cells. Blood. 2006;108:3777-3785.
33. Gui J, Zhu X, Dohkan J, Cheng L, Barnes PF, Su DM. The aged thymus shows normal recruitment of lymphohematopoietic progenitors but has defects in thymic epithelial cells. Int Immunol. 2007; 19:1201-1211.
34. Hsu HC, Li L, Zhang HG, Mountz JD. Genetic regulation of thymic involution. Mech Ageing Dev. 2005;126:87-97.
35. He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MA, Massagué J. Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell. 2006; 125:929-941.
36. Hager-Theodorides AL, Outram SV, Shah DK, et al. Bone morphogenetic protein 2/4 signaling regulates early thymocyte differentiation. J Immunol. 2002;169:5496-5504.
37. Licona P, Chimal-Monroy J, Soldevila G. Inhibins are the major activin ligands expressed during early thymocyte development. Dev Dyn. 2006; 235:1124-1132.
38. Schluns KS, Grutkoski PS, Cook JE, Engelmann GL, Le PT. Human thymic epithelial cells produce TGF-beta 3 and express TGF-beta receptors. Int Immunol. 1995;7:1681-1690.
39. Takahama Y, Letterio JJ, Suzuki H, Farr AG, Singer A. Early progression of thymocytes along the CD4/CD8 developmental pathway is regulated by a subset of thymic epithelial cells expressing transforming growth factor beta. J Exp Med. 1994;179:1495-1506.
40. He W, Li AG, Wang D, et al. Overexpression of Smad7 results in severe pathological alterations in multiple epithelial tissues. EMBO J. 2002;21: 2580-2590.
41. Mazars A, Lallemand F, Prunier C, et al. Evidence for a role of the JNK cascade in Smad7-mediated apoptosis. J Biol Chem. 2001;276:36797-36803.
42. Yu L, Hébert MC, Zhang YE. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J. 2002;21: 3749-3759.
43. Han G, Li AG, Liang YY, et al. Smad7-induced beta-catenin degradation alters epidermal appendage development. Dev Cell. 2006;11:301-312.
44. Bleul CC, Boehm T. BMP signaling is required for normal thymus development. J Immunol. 2005; 175:5213-5221.
45. Johnson K, Kirkpatrick H, Comer A, Hoffmann FM, Laughon A. Interaction of Smad complexes with tripartite DNA-binding sites. J Biol Chem. 1999;274:20709-20716.
46. Zawel L, Dai JL, Buckhaults P, et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell. 1998;1:611-617.
47. Calon A, Gross I, Lhermitte B, et al. Different effects of the Cdx1 and Cdx2 homeobox genes in a murine model of intestinal inflammation. Gut. 2007;56:1688-1695.
48. Ericsson A, Kotarsky K, Svensson M, Sigvardsson M, Agace W. Functional characterization of the CCL25 promoter in small intestinal epithelial cells suggests a regulatory role for caudal-related homeobox (Cdx) transcription factors. J Immunol. 2006;176:3642-3651.
49. Michaelidis TM, Lie DC. Wnt signaling and neural stem cells: caught in the Wnt web. Cell Tissue Res. 2008;331:193-210.
50. Nishita M, Hashimoto MK, Ogata S, et al. Interaction between Wnt and TGF-beta signalling path-ways during formation of Spemann's organizer. Nature. 2000;403:781-785.