Gene expression profile of the third pharyngeal pouch reveals role of mesenchymal MafB in embryonic thymus development

Blood

Volumn 113, Issue 13, 2009, Pages 2976-2987

  Sultana, Dil Afroz ^a   Tomita, Shuhei ^a   Hamada, Michito ^b   Iwanaga, Yasuyuki ^a,c   Kitahama, Yuki ^a   Van Khang, Nguyen ^a   Hirai, Shuichi ^a,c   Ohigashi, Izumi ^a   Nitta, Sachiko ^a   Amagai, Takashi ^d   Takahashi, Satoru ^b   Takahama, Yousuke ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c KAGAWA UNIVERSITY   (Japan)

^d MEIJI UNIVERSITY OF INTEGRATIVE MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CCL25 CHEMOKINE; CD45 ANTIGEN; CHEMOKINE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; TRANSCRIPTION FACTOR MAFB; UNCLASSIFIED DRUG; WNT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; FETUS; GENE EXPRESSION PROFILING; MESENCHYME CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRE T LYMPHOCYTE; PRIMORDIUM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYMOCYTE; THYMUS;

EID: 63849090193     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-06-164921     Document Type: Article

References (70)

1. Miller JFAP. The thymus and the development of immunologic responsiveness. Science. 1964;144:1544-1551.
2. Kisielow P, von Boehmer H. Development and selection of T cells: facts and puzzles. Adv Immunol. 1995;58:87-209.
3. Scollay R, Wilson A, D'Amico A, et al. Developmental status and reconstitution potential of sub-populations of murine thymocytes. Immunol Rev.1988;104:81-120.
4. Petrie HT. Cell migration and the control of postnatal T-cell lymphopoiesis in the thymus. Nat Rev Immunol. 2003;3:859-866.
5. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol. 2006;6:127-135.
6. Hollander G, Gill J, Zuklys S, Iwanami N, Liu C, TakahamaY. Cellular and molecular events during early thymus development. Immunol Rev.2006;209:28-46.
7. Cordier A, Haumont S. Development of thymus, parathyroids and ultimo-branchial bodies in NMR1 and nude mice. Am J Anat. 1980;157:227-263.
8. Manley NR. Thymus organogenesis and molecular mechanisms of thymic epithelial cell differentiation. Sem Immunol. 2000;12:421-428.
9. Yamagishi H, Maeda J, Hu T, et al. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 2003;17:269-281.
10. Xu H, Cerrato F, Baldini A. Timed mutation and cell-fate mapping reveal reiterated roles of Tbx1 during embryogenesis, and a crucial function during segmentation of the pharyngeal system via regulation of endoderm expansion. Development. 2005;132:4387-4395.
11. Lindsay EA, Vitelli F, Su H, et al. Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice. Nature. 2001;410:97-101.
12. Jerome LA, Papaioannou VE. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet. 2001;27:286-291.
13. Manley NR, Capecchi MR. The role of Hoxa-3 in mouse thymus and thyroid development. Development. 1995;121:1989-2003.
14. Manley NR, Capecchi MR. Hox group 3 paralogs regulate the development and migration of the thymus, thyroid and parathyroid glands. Dev Biol.1998;195:1-15.
15. Su D, Ellis S, Napier A, Lee K, Manley NR. Hoxa3 and pax1 regulate epithelial cell death and proliferation during thymus and parathyroid organogenesis. Dev Biol. 2001;236:316-329.
16. Wallin J, Eibel H, Neubuser A, Wilting J, Koseki H, Balling R. Pax1 is expressed during development of the thymus epithelium and is required for normal Tcell maturation. Development. 1996;122:23-30.
17. Peters H, Neubuser A, Kratochwil K, Balling R. Pax-9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev. 1998;12:2735-2747.
18. Zou D, Silvius D, Davenport J, Grifone R, Maire P, Xu PX. Patterning of the third pharyngeal pouch into thymus/parathyroid by Six and Eya1. Dev Biol. 2006;293:499-512.
19. Gordon J, Bennett AR, Blackburn CC, Manley NR. Gcm2 and Foxn1 mark early parathyroid and thymus-specific domains in the developing third pharyngeal pouch. Mech Dev. 2001;103:141-143.
20. Nehls M, Kyewski B, Messerle M, et al. Two genetically separable steps in the differentiation of thymic epithelium. Science. 1996;272:886-889.
21. Su DM, Navarre S, Oh WJ, Condie BG, Manley NR. Adomain of Foxn1 required for crosstalk-dependent thymic epithelial cell differentiation. Nat Immunol. 2003;4:1128-1135.
22. Itoi M, Kawamoto H, Katsura Y, Amagai T. Two distinct steps of immigration of hematopoietic progenitors into the early thymus anlage. Int Immunol. 2001;13:1203-1211.
23. 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.
24. Itoi M, Tsukamoto N, Amagai T. Expression of Dll4 and CCL25 in Foxn1-negative epithelial cells in the post-natal thymus. Int Immunol. 2007;19:127-132.
25. Tsukamoto N, Itoi M, Nishikawa M, Amagai T. Lack of Delta like 1 and 4 expressions in nude thymus anlages. Cell Immunol. 2005;234:77-80.
26. 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.
27. Balciunaite G, Keller MP, Balciunaite E, et al. Wnt glycoproteins regulate the expression of FoxN1, the gene defective in nude mice. Nat Immunol. 2002;3:1102-1108.
28. Bleul CC, Boehm T. BMP signaling is required for normal thymus development. J Immunol. 2005;175:5213-5221.
29. Erickson M, Morkowski S, Lehar S, et al. Regulation of thymic epithelium by keratinocyte growth factor. Blood. 2002;100:3269-3278.
30. Rossi SW, Jeker LT, Ueno T, et al. Keratinocyte growth factor (KGF) enhances postnatal T-cell development via enhancements in proliferation and function of thymic epithelial cells. Blood. 2007;109:3803-3811.
31. Moriguchi T, Hamada M, Morito N, et al. MafB is essential for renal development and F4/80 expression in macrophages. Mol Cell Biol. 2006;26:5715-5727.
32. Gray DH, Chidgey AP, Boyd RL. Analysis of thymic stromal cell populations using flow cytometry. J Immunol Methods. 2002;260:15-28.
33. Ueno T, Liu C, Nitta T, Takahama Y. Development of T-lymphocytes in mouse fetal thymus organ culture. Methods Mol Biol. 2005;290:117-133.
34. Gray DH, Tull D, Ueno T, et al. Aunique thymic fibroblast population revealed by the monoclonal antibody MTS-15. J Immunol. 2007;178:4956-4965.
35. T) method. Methods. 2001;25:402-408.
36. Vilet V, Melis EM, van Ewijk W. Monoclonal antibodies to stromal cell types of the mouse thymus. Eur J Immunol. 1984;14:524-529.
37. National Center for Biotechnology Information. BLAST database. Available at: http://www.ncbi.nih.gov. Accessed January 2008.
38. JAX Laboratories. Mouse Genome Informatics (MGI) database. Available at: http://www.informatics.jax.org. Accessed September 2008.
39. European Molecular Biology Laboratory. InterPro Database. Available at: http://www.ebi.ac.uk/interpro. Accessed November 2007.
40. National Center for Biotechnology Information. Conserved Domain Database (CDD). Available at: http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi. Accessed January 2008.
41. European Molecular Biology Laboratory. SMART tool. Available at: http://smart.embl-heidelberg.de.Accessed December 2006.
42. Günther T, Chen ZF, Kim J, et al. Genetic ablation of parathyroid glands reveals another source of parathyroid hormone. Nature. 2000;406:199-203.
43. Ho C, Conner DA, Pollak MR, et al. A mouse model of human familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism. Nat Genet. 1995;11:389-394.
44. Miao D, He B, Karaplis AC, Goltzman D. Parathyroid hormone is essential for normal fetal bone formation. J Clin Invest. 2002;109:1173-1182.
45. 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.
46. Von FJU, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredun-dant cytokine. J Exp Med. 1995;181:1519-26.
47. Jenkinson WE, Simona WR, Sonia MP, Jenkinson EJ, Anderson G. PDGFRα-expressing mesenchyme regulates thymus growth and the availability of intrathymic niches. Blood. 2007;109:954-960.
48. Bleul CC, Boehm T. Laser capture microdissection-based expression profiling identifies PD1-ligand as a target of the nude locus gene product. Eur J Immunol. 2001;31:2497-2503.
49. Le Douarin NM, Jotereau FV. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 1975;142:17-40.
50. Yamazaki H, Sakata E, Yamane T, et al. Presence and distribution of neural crest-derived cells in the murine developing thymus and their potential for differentiation. Int Immunol. 2005;17:549-558.
51. Foster K, Julie Sheridan J, Veiga-Fernandes H, et al. Contribution of neural crest-derived cells in the embryonic and adult thymus. J Immunol. 2008;180:3183-3189.
52. Blanchi B, Kelly LM, Viemari JC, et al. MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat Neuro-sci. 2003;6:1091-1100.
53. Jenkinson WE, Simona WR, Parnell SM, et al. Chemokine receptor expression defines heterogeneity in the earliest thymic migrants. Eur J Immunol. 2007;37:2090-2096.
54. Kataoka K, Fujiwara KT, Noda M, Nishizawa M. MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol Cell Biol. 1994;14:7581-7591.
55. Cordes SP, Barsh GS. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell. 1994;79:1025-1034.
56. Lumsden A, Sprawson N, Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development. 1991;113:1281-1291.
57. Li MA, Alls JD, Avancini RM, Koo K, Godt D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol. 2003;5:994-1000.
58. Mulroy T, McMahon JA, Burakoff SJ, McMahon AP, Sen J. Wnt-1 and Wnt-4 regulate thymic cellularity. Eur J Immunol. 2002;32:967-971. 59. Liang H, Coles AH, Zhu Z, et al. Noncanonical Wnt signaling promotes apoptosis in thymocyte development. J Exp Med. 2007;204:3077-3084.
59. Pongracz J, Hare K, Harman B, Anderson G, Jenkinson EJ. Thymic epithelial cells provide Wnt signals to developing thymocytes. Eur J Immunol.2003;33:1949- 1956.
60. Tsai PT, Lee RA, Wu H. BMP4 acts upstream of FGF in modulating thymic stroma and regulating thymopoiesis. Blood. 2003;102:3947-3953.
61. Patel SR, Gordon J, Mahbub F, Blackburn CC, Manley NR. Bmp4 and Noggin expression during early thymus and parathyroid organogenesis. Gene Expr Patterns. 2006;6:794-799.
62. Anderson G, Jenkinson WE, Jones T, et al. Establishment and functioning of intrathymic micro-environments. Immunol Rev. 2006;209:10-27.
63. 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.
64. Graf D, Nethisinghe S, Palmer DB, Fisher AG, Merkenschlager M. The developmentally regulated expression of Twisted gastrulation reveals a role for bone morphogenetic proteins in the control of T cell development. J Exp Med. 2002;196:163-171.
65. Revest JM, Suniara RK, Kerr K, Owen JJ, Dickson C. Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J Immunol. 2001;167:1954-1961.
66. Rossi S, Blazar BR, Farrell CL, et al. Keratinocyte growth factor preserves normal thymopoiesis and thymic microenvironment during experimental graft-versus-host disease. Blood. 2002;100:682-691.
67. Havran WL, Allison JP. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature. 1988;335:443-445.
68. Itoi M, Tsukamoto N, Yoshida H, Amagai T. Mesenchymal cells are required for functional development of thymic epithelial cells. Int Immunol. 2007;19:953-964.
69. Matsuoka TA, Zhao L, Artner I, et al. Members of the large Maf transcription family regulate insulin gene transcription in islet beta cells. Mol Cell Biol.2003;23:6049-6062.
70. Tsuchiya M, Taniguchi S, Yasuda K, et al. Potential roles of large mafs in cell lineages and developing pancreas. Pancreas. 2006;32:408-416.