Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm

Developmental Dynamics

Volumn 236, Issue 2, 2007, Pages 353-363

  Dastjerdi, Akbar ^a   Robson, Lesley ^b   Walker, Rebecca ^a   Hadley, Julia ^a   Zhang, Zhen ^c   Rodriguez Niedenführ, Marc ^a,e   Ataliotis, Paris ^d,f   Baldini, Antonio ^c,g   Scambler, Peter ^d   Francis West, Philippa ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^f ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^g TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Craniofacial mesoderm; DiGeorge syndrome; Limb; Muscle; T box

Indexed keywords

COMPLEMENTARY DNA; GENOMIC DNA; SULFUR 35; VIRUS DNA;

ARTICLE; CHICK EMBRYO; CRANIOFACIAL DEVELOPMENT; DIGEORGE SYNDROME; EMBRYO; HEART MUSCLE CELL; IN SITU HYBRIDIZATION; LIMB DEVELOPMENT; MESODERM; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS INFECTION;

ANIMALS; CHICK EMBRYO; EMBRYONIC DEVELOPMENT; EXTREMITIES; FACIAL MUSCLES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; IN SITU HYBRIDIZATION; MESODERM; MICE; MICE, KNOCKOUT; MYOBLASTS, SKELETAL; RETROVIRIDAE; T-BOX DOMAIN PROTEINS; TRANSFECTION;

MUS;

EID: 33846904563     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21010     Document Type: Article

References (76)

1. Agulnik SI, Papaioannou VE, Silver LM. 1998. Cloning, mapping, and expression analysis of TBX15, a new member of the T-Box gene family. Genomics 51:68-75.
2. Anakwe K, Robson L, Hadley J, Buxton P, Church V, Allen S, Hartmann C, Harfe B, Nohno T, Brown AM, Evans DJ, Francis-West P. 2003. Wnt signalling regulates myogenic differentiation in the developing avian wing. Development 130:3503-3514.
3. Arnold JS, Werling U, Braunstein EM, Liao J, Nowotschin S, Edelmann W, Hebert JM, Morrow BE. 2006. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133:977-987.
4. Ataliotis P, Ivins S, Mohun TJ, Scambler PJ. 2005. XTbx1 is a transcriptional activator involved in head and pharyngeal arch development in Xenopus laevis. Dev Dyn 232:979-991.
5. Bober E, Franz T, Arnold HH, Gruss P, Tremblay P. 1994. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120:603-612.
6. Botto LD, May K, Fernhoff PM, Correa A, Coleman K, Rasmussen SA, Merritt RK, O'Leary LA, Wong LY, Elixson EM, Mahle WT, Campbell RM. 2003. A population-based study of the 22q11.2 deletion: phenotype, incidence, and contribution to major birth defects in the population. Pediatrics 112:101-107.
7. Brohmann H, Jagla K, Birchmeier C. 2000. The role of Lbx1 in migration of muscle precursor cells. Development 127:437-445.
8. Brown CB, Wenning JM, Lu MM, Epstein DJ, Meyers EN, Epstein JA. 2004. Cre-mediated excision of Fgf8 in the Tbx1 expression domain reveals a critical role for Fgf8 in cardiovascular development in the mouse. Dev Biol 267:190-202.
9. Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F. 2003. The formation of skeletal muscle: from somite to limb. J Anat 202:59-68.
10. Chapman DL, Papaioannou VE. 1998. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391:695-697.
11. Chapman DL, Garvey N, Hancock S, Alexiou M, Agulnik SI, Gibson-Brown JJ, Cebra-Thomas J, Bollag RJ, Silver LM, Papaioannou VE. 1996. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206:379-390.
12. Chen AE, Ginty DD, Fan CM. 2005. Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433:317-322.
13. Church V, Nohno T, Linker C, Marcelle C, Francis-West P. 2002. Wnt regulation of chondrocyte differentiation. J Cell Sci 115:4809-4818.
14. Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129:1061-1073.
15. Davis RL, Weintraub H, Lassar AB. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987-1000.
16. Duprez D, Bell EJ, Richardson MK, Archer CW, Wolpert L, Brickell PM, Francis-West PH. 1996. Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech Dev 57:145-157.
17. Evans DJ, Noden DM. 2006. Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev Dyn 235:1310-1325.
18. Francis-West PH, Tatla T, Brickell PM. 1994. Expression patterns of the bone morphogenetic protein genes Bmp-4 and Bmp-2 in the developing chick face suggest a role in outgrowth of the primordia. Dev Dyn 201:168-178.
19. Francis-West PH, Antoni L, Anakwe K. 2003. Regulation of myogenic differentiation in the developing limb bud. J Anat 202:69-81.
20. Garg V, Yamagishi C, Hu T, Kathiriya IS, Yamagishi H, Srivastava D. 2001. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev Biol 235:62-73.
21. Gibson-Brown JJ, I Aqulnik S, Silver LM, Papaioannou VE. 1998. Expression of T-box genes Tbx2-Tbx5 during chick organogenesis. Mech Dev 74:165-169.
22. Goulding M, Lumsden A, Paquette AJ. 1994. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120:957-971.
23. Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, Goulding M. 2000. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127:413-424.
24. Guris DL, Duester G, Papaioannou VE, Imamoto A. 2006. Dose-dependent interaction of Tbx1 and Crk1 and locally aberrant RA signaling in a model of del22q11 syndrome. Dev Cell 10:81-92.
25. Haenig B, Schmidt C, Kraus F, Pfordt M, Kispert A. 2002. Cloning and expression analysis of the chick ortholog of TBX22, the gene mutated in X-linked cleft palate and ankyloglossia. Mech Dev 117:321-325.
26. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
27. Houzelstein D, Auda-Boucher G, Cheraud Y, Rouaud T, Blanc I, Tajbakhsh S, Buckingham ME, Fontaine-Perus J, Robert B. 1999. The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126:2689-2701.
28. Hu T, Yamagishi H, Maeda J, McAnally J, Yamagishi C, Srivastava D. 2004. Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development 131: 5491-5502.
29. Ivins S, Lammerts van Beuren K, Roberts C, James C, Lindsay E, Baldini A, Ataliotis P, Scambler PJ. 2005. Microarray analysis detects differentially expressed genes in the pharyngeal region of mice lacking Tbx1. Dev Biol 285:554-569.
30. Jerome LA, Papaioannou VE. 2001. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet 27:286-291.
31. Kelly RG, Jerome-Majewska LA, Papaioannou VE. 2004. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet 13:2829-2840.
32. Kispert A, Ortner H, Cooke J, Herrmann BG. 1995. The chick Brachyury gene: developmental expression pattern and response to axial induction by localized activin. Dev Biol 168:406-415.
33. Kochilas L, Merscher-Gomez S, Lu MM, Potluri V, Liao J, Kucherlapati R, Morrow B, Epstein JA. 2002. The role of neural crest during cardiac development in a mouse model of DiGeorge syndrome. Dev Biol 251:157-166.
34. Kochilas LK, Potluri V, Gitler A, Balasubramanian K, Chin AJ. 2003. Cloning and characterization of zebrafish tbx1. Gene Expr Patterns 3:645-651.
35. Kraus F, Haenig B, Kispert A. 2001a. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech Dev 100:83-86.
36. Kraus F, Haenig B, Kispert A. 2001b. Cloning and expression analysis of the mouse T-box gene tbx20. Mech Dev 100:87-91.
37. Ladher RK, Wright TJ, Moon AM, Mansour SL, Schoenwolf GC. 2005. FGF8 initiates inner ear induction in chick and mouse. Genes Dev 19:603-613.
38. Lin ZY, Dechesne CA, Eldridge J, Paterson BM. 1989. An avian muscle factor related to MyoD1 activates muscle-specific promoters in nonmuscle cells of different germ-layer origin and in BrdU-treated myoblasts. Genes Dev 3:986-996.
39. Lin GF, Geng X, Chen Y, Qu B, Wang F, Hu R, Ding X. 2003. T-box binding site mediates the dorsal activation of Myf5 in Xenopus gastrula embryos. Dev Dyn 226:51-58.
40. Lindsay EA, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, Jurecic V, Ogunrinu G, Sutherland HF, Scambler PJ, Bradley A, Baldini A. 2001. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410:97-101.
41. Logan C, Francis-West P. 1999. Gene transfer in avian embryos using replication-competent retroviruses. Methods Mol Biol 97:539-551.
42. Lu J, Webb R, Richardson JA, Olson EN. 1999. MyoR: a muscle-restricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc Natl Acad Sci U S A 96:552-557.
43. Lu JR, Bassel-Duby R, Hawkins A, Chang P, Valdez R, Wu H, Gan L, Shelton JM, Richardson JA, Olson EN. 2002. Control of facial muscle development by MyoR and capsulin. Science 298:2378-2381.
44. Mankoo BS, Collins NS, Ashby P, Grigorieva E, Pevny LH, Candia A, Wright CV, Rigby PW, Pachnis V. 1999. Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400:69-73.
45. McDonald-McGinn DM, LaRossa D, Goldmuntz E, Sullivan K, Eicher P, Gerdes M, Moss E, Wang P, Solot C, Schultz P, Lynch D, Bingham P, Keenan G, Weinzimer S, Ming JE, Driscoll D, Clark BJ III, Markowitz R, Cohen A, Moshang T, Pasquariello P, Randall P, Emanuel BS, Zackai EH. 1997. The 22q11.2 deletion: screening, diagnostic workup, and outcome of results; report on 181 patients. Genet Test 1:99-108.
46. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM, Xavier RJ, Demay MB, Russell RG, Factor S, Tokooya K, Jore BS, Lopez M, Pandita RK, Lia M, Carrion D, Xu H, Schorle H, Kobler JB, Scambler P, Wynshaw-Boris A, Skoultchi AI, Morrow BE, Kucherlapati R. 2001. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104:619-629.
47. Mitani Y, Takahashi H, Satoh N. 1999. An ascidian T-box gene As-T2 is related to the Tbx6 subfamily and is associated with embryonic muscle cell differentiation. Dev Dyn 215:62-68.
48. Mitani Y, Takahashi H, Satoh N. 2001. Regulation of the muscle-specific expression and function of an ascidian T-box gene, As-T2. Development 128:3717-3728.
49. Moraes F, Novoa A, Jerome-Majewska LA, Papaioannou VE, Mallo M. 2005. Tbx1 is required for proper neural crest migration and to stabilize spatial patterns during middle and inner ear development. Mech Dev 122:199-212.
50. Noden DM, Francis-West P. 2006. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194-1218.
51. Noden DM, Marcucio R, Borycki AG, Emerson CP, Jr. 1999. Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. Dev Dyn 216:96-112.
52. Packham EA, Brook JD. 2003. T-box genes in human disorders. Hum Mol Genet 12 Spec No 1:R37-R44.
53. Papaioannou VE, Silver LM. 1998. The T-box gene family. Bioessays 20:9-19.
54. Paylor R, Glaser B, Mupo A, Ataliotis P, Spencer C, Sobotka A, Sparks C, Choi CH, Oghalai J, Curran S, Murphy KC, Monks S, Williams N, O'Donovan MC, Owen MJ, Scambler PJ, Lindsay E. 2006. Tbx1 haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22q11 deletion syndrome. Proc Natl Acad Sci U S A 103:7729-7734.
55. Piotrowski T, Ahn DG, Schilling TF, Nair S, Ruvinsky I, Geisler R, Rauch GJ, Haffter P, Zon LI, Zhou Y, Foott H, Dawid IB, Ho RK. 2003. The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130:5043-5052.
56. Pownall ME, Emerson CP Jr. 1992. Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev Biol 151:67-79.
57. Raft S, Nowotschin S, Liao J, Morrow BE. 2004. Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131:1801-1812.
58. Ryan AK, Goodship JA, Wilson DI, Philip N, Levy A, Seidel H, Schuffenhauer S, Oechsler H, Belohradsky B, Prieur M, Aurias A, Raymond FL, Clayton-Smith J, Hatchwell E, McKeown C, Beemer FA, Dallapiccola B, Novelli G, Hurst JA, Ignatius J, Green AJ, Winter RM, Brueton L, Brondum-Nielsen K, Scambler PJ. 1997. Spectrum of clinical features associated with interstitial chromosome 22q11 deletions: a European collaborative study. J Med Genet 34:798-804.
59. Saga Y, Hata N, Kobayashi S, Magnuson T, Seldin MF, Taketo MM. 1996. MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 122:2769-2778.
60. Sauka-Spengler T, Le Mentec C, Lepage M, Mazan S. 2002. Embryonic expression of Tbx1, a DiGeorge syndrome candidate gene, in the lamprey Lampetra fluviatilis. Gene Expr Patterns 2:99-103.
61. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100:431-440.
62. Schafer K, Braun T. 1999. Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat Genet 23:213-216.
63. Smith SJ, Ataliotis P, Kotecha S, Towers N, Sparrow DB, Mohun TJ. 2005. The MLC1v gene provides a transgenic marker of myocardium formation within developing chambers of the Xenopus heart. Dev Dyn 232:1003-1012.
64. Tzahor E, Kempf H, Mootoosamy RC, Poon AC, Abzhanov A, Tabin CJ, Dietrich S, Lassar AB. 2003. Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev 17:3087-3099.
65. Vitelli F, Morishima M, Taddei I, Lindsay EA, Baldini A. 2002a. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum Mol Genet 11:915-922.
66. Vitelli F, Taddei I, Morishima M, Meyers EN, Lindsay EA, Baldini A. 2002b. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 129:4605-4611.
67. Vitelli F, Viola A, Morishima M, Pramparo T, Baldini A, Lindsay E. 2003. TBX1 is required for inner ear morphogenesis. Hum Mol Genet 12:2041-2048.
68. Vitelli F, Zhang Z, Huynh T, Sobotka A, Mupo A, Baldini A. 2006. Fgf8 expression in the Tbx1 domain causes skeletal abnormalities and modifies the aortic arch but not the outflow tract phenotype of Tbx1 mutants. Dev Biol 295:559-570.
69. von Scheven G, Bothe I, Ahmed MU, Alvares LE, Dietrich S. 2006. Protein and genomic organisation of vertebrate MyoR and Capsulin genes and their expression during avian development. Gene Expr Patterns 6:383-393.
70. Williams BA, Ordahl CP. 1994. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120:785-796.
71. Wilson DI, Burn J, Scambler P, Goodship J. 1993. DiGeorge syndrome: part of CATCH 22. J Med Genet 30:852-856.
72. Xu H, Morishima M, Wylie JN, Schwartz RJ, Bruneau BG, Lindsay EA, Baldini A. 2004. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131:3217-3227.
73. Xu H, Cerrato F, Baldini A. 2005. 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 132:4387-4395.
74. Yagi H, Furutani Y, Hamada H, Sasaki T, Asakawa S, Minoshima S, Ichida F, Joo K, Kimura M, Imamura S, Kamatani N, Momma K, Takao A, Nakazawa M, Shimizu N, Matsuoka R. 2003. Role of TBX1 in human del22q11.2 syndrome. Lancet 362:1366-1373.
75. Zhang Z, Cerrato F, Xu H, Vitelli F, Morishima M, Vincentz J, Furuta Y, Ma L, Martin JF, Baldini A, Lindsay E. 2005. Tbx1 expression in pharyngeal epithelia is necessary for pharyngeal arch artery development. Development 132:5307-5315.
76. Zhang Z, Huynh T, Baldini A. 2006. Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development 133:3587-3595.