Pitx2 defines alternate pathways acting through MyoD during limb and somitic myogenesis

Development

Volumn 137, Issue 22, 2010, Pages 3847-3856

  L'Honoré, Aurore ^a   Ouimette, Jean François ^a   Lavertu Jolin, Marisol ^a   Drouin, Jacques ^a  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Differentiation; Mouse; Muscle; Myod1; Regulatory networks

Indexed keywords

MUTANT PROTEIN; MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIC FACTOR 4; MYOGENIC FACTOR 5; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; MYOD1 MYOGENIC DIFFERENTIATION PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FORELIMB; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INACTIVATION; HINDLIMB; HOMEOBOX; MOLECULAR MECHANICS; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY MECHANISM; SKELETAL MUSCLE; SOMITE; TRANSCRIPTION REGULATION; ANIMAL; LIMB; LIMB BUD; METABOLISM; PRENATAL DEVELOPMENT;

ANIMALS; EXTREMITIES; HOMEODOMAIN PROTEINS; LIMB BUDS; MICE; MUSCLE DEVELOPMENT; MYOD PROTEIN; SOMITES; TRANSCRIPTION FACTORS;

EID: 78149238325     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.053421     Document Type: Article

References (70)

1. Asakura, A., Lyons, G. E. and Tapscott, S. J. (1995). The regulation of MyoD gene expression: conserved elements mediate expression in embryonic axial muscle. Dev. Biol. 171, 386-398.
2. Bajard, L., Relaix, F., Lagha, M., Rocancourt, D., Daubas, P. and Buckingham, M. E. (2006). A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20, 2450-2464.
3. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. and Birchmeier, C. (1995). Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768-771.
4. Braun, T., Rudnicki, M. A., Arnold, H. H. and Jaenisch, R. (1992). Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369-382.
5. Chen, J. C. and Goldhamer, D. J. (2004). The core enhancer is essential for proper timing of MyoD activation in limb buds and branchial arches. Dev. Biol. 265, 502-512.
6. Chen, J. C., Ramachandran, R. and Goldhamer, D. J. (2002). Essential and redundant functions of the MyoD distal regulatory region revealed by targeted mutagenesis. Dev. Biol. 245, 213-223. (Pubitemid 34461815)
7. Christ, B. and Ordahl, C. P. (1995). Early stages of chick somite development. Anat. Embryol. (Berl.) 191, 381-396.
8. Christ, B. and Brand-Saberi, B. (2002). Limb muscle development. Int. J. Dev. Biol. 46, 905-914.
9. Christ, B., Jacob, M. and Jacob, H. J. (1983). On the origin and development of the ventrolateral abdominal muscles in the avian embryo. An experimental and ultrastructural study. Anat. Embryol. (Berl.) 166, 87-101.
10. Cossu, G., Kelly, R., Tajbakhsh, S., Di Donna, S., Vivarelli, E. and Buckingham, M. (1996). Activation of different myogenic pathways: myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122, 429-437.
11. Coulon, V., L'Honoré, A., Ouimette, J. F., Dumontier, É., van den Munckhof, P. and Drouin, J. (2007). A muscle-specific promoter directs Pitx3 gene expression in early muscle cells. J. Biol. Chem. 282, 33192-33200.
12. Dastjerdi, A., Robson, L., Walker, R., Hadley, J., Zhang, Z., Rodriguez-Niedenfuhr, M., Ataliotis, P., Baldini, A., Scambler, P. and Francis-West, P. (2007). Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm. Dev. Dyn. 236, 353-363.
13. Denetclaw, W. F., Jr, Christ, B. and Ordahl, C. P. (1997). Location and growth of epaxial myotome precursor cells. Development 124, 1601-1610.
14. Diehl, A. G., Zareparsi, S., Qian, M., Khanna, R., Angeles, R. and Gage, P. J. (2006). Extraocular muscle morphogenesis and gene expression are regulated by Pitx2 gene dose. Invest. Ophthalmol. Vis. Sci. 47, 1785-1793. (Pubitemid 46768255)
15. Dong, F., Sun, X., Liu, W., Ai, D., Klysik, E., Lu, M. F., Hadley, J., Antoni, L., Chen, L., Baldini, A. et al. (2006). Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development 133, 4891-4899.
16. Faerman, A., Goldhamer, D. J., Puzis, R., Emerson, C. P., Jr and Shani, M. (1995). The distal human myoD enhancer sequences direct unique muscle-specific patterns of lacZ expression during mouse development. Dev. Biol. 171, 27-38.
17. Frankel, N., Davis, G. K., Vargas, D., Wang, S., Payre, F. and Stern, D. L. (2010). Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466, 490-493.
18. Gage, P. J., Suh, H. Y. and Camper, S. A. (1999). Dosage requirement of Pitx2 for development of multiple organs. Development 126, 4643-4651.
19. Goldhamer, D. J., Faerman, A., Shani, M. and Emerson, C. P., Jr (1992). Regulatory elements that control the lineage-specific expression of myoD. Science 256, 538-542.
20. Goldhamer, D. J., Brunk, B. P., Faerman, A., King, A., Shani, M. and Emerson, C. P., Jr (1995). Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121, 637-649.
21. Grifone, R., Demignon, J., Houbron, C., Souil, E., Niro, C., Seller, M. J., Hamard, G. and Maire, P. (2005). Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132, 2235-2249.
22. Grifone, R., Demignon, J., Giordani, J., Niro, C., Souil, E., Bertin, F., Laclef, C., Xu, P. X. and Maire, P. (2007). Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev. Biol. 302, 602-616.
23. Hasty, P., Bradley, A., Hsi Morris, J., Edmondson, D. G., Venuti, J. M., Olson, E. N. and Klein, W. H. (1993). Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506.
24. Hu, P., Geles, K. G., Paik, J. H., DePinho, R. A. and Tjian, R. (2008). Codependent activators direct myoblast-specific MyoD transcription. Dev. Cell 15, 534-546.
25. Hughes, S. M., Taylor, J. M., Tapscott, S. J., Gurley, C. M., Carter, W. J. and Peterson, C. A. (1993). Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118, 1137-1147.
26. Kablar, B., Krastel, K., Ying, C., Asakura, A., Tapscott, S. J. and Rudnicki, M. A. (1997). MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729-4738.
27. Kablar, B., Krastel, K., Ying, C., Tapscott, S. J., Goldhamer, D. J. and Rudnicki, M. A. (1999). Myogenic determination occurs independently in somites and limb buds. Dev. Biol. 206, 219-231.
28. Kablar, B., Krastel, K., Tajbakhsh, S. and Rudnicki, M. A. (2003). Myf5 and MyoD activation define independent myogenic compartments during embryonic development. Dev. Biol. 258, 307-318.
29. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466-471.
30. Kassar-Duchossoy, L., Giacone, E., Gayraud-Morel, B., Jory, A., Gomes, D. and Tajbakhsh, S. (2005). Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426-1431.
31. Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J. et al. (2002). Identification of a Wnt/Dvl/b-cateninrPitx2 pathway mediating cell-type-specific proliferation during development. Cell 111, 673-685.
32. Kitamura, K., Miura, H., Miyagawa-Tomita, S., Yanazawa, M., Katoh-Fukui, Y., Suzuki, R., Ohuchi, H., Suehiro, A., Motegi, Y., Nakahara, Y. et al. (1999). Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126, 5749-5758.
33. Kucharczuk, K. L., Love, C. M., Dougherty, N. M. and Goldhamer, D. J. (1999). Fine-scale transgenic mapping of the MyoD core enhancer: MyoD is regulated by distinct but overlapping mechanisms in myotomal and non-myotomal muscle lineages. Development 126, 1957-1965.
34. L'Honoré, A., Lamb, N. J., Vandromme, M., Turowski, P., Carnac, G. and Fernandez, A. (2003). MyoD distal regulatory region contains an SRF binding CArG element required for MyoD expression in skeletal myoblasts and during muscle regeneration. Mol. Biol. Cell 14, 2151-2162.
35. L'Honoré, A., Coulon, V., Marcil, A., Lebel, M., Lafrance-Vanasse, J., Gage, P. J., Camper, S. A. and Drouin, J. (2007). Sequential expression and redundancy of Pitx2 and Pitx3 genes during muscle development. Dev. Biol. 307, 421-433.
36. Lamolet, B., Pulichino, A. M., Lamonerie, T., Gauthier, Y., Brue, T., Enjalbert, A. and Drouin, J. (2001). A pituitary cell-restricted T-box factor, Tpit, activates POMC transcription in cooperation with Pitx homeoproteins. Cell 104, 849-859.
37. Lanctôt, C., Gauthier, Y. and Drouin, J. (1999). Pituitary homeobox 1 (Ptx1) is differentially expressed during pituitary development. Endocrinology 140, 1416-1422.
38. Lewandoski, M., Sun, X. and Martin, G. R. (2000). Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26, 460-463.
39. Lin, C. R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, R., Izpisua Belmonte, J. C. and Rosenfeld, M. G. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphegenesis. Nature 401, 279-282.
40. Lu, M. F., Pressman, C., Dyer, R., Johnson, R. L. and Martin, J. F. (1999). Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401, 276-278.
41. Mackenzie, S., Walsh, F. S. and Graham, A. (1998). Migration of hypoglossal myoblast precursors. Dev. Dyn. 213, 349-358.
42. Mankoo, B. S., Collins, N. S., Ashby, P., Grigorieva, E., Pevny, L. H., Candia, A., Wright, C. V., Rigby, P. W. and Pachnis, V. (1999). Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400, 69-73.
43. Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S. and Nonaka, I. (1993). Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535.
44. Noden, D. M. (1983). The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev. Biol. 96, 144-165.
45. Noden, D. M. and Francis-West, P. (2006). The differentiation and morphogenesis of craniofacial muscles. Dev. Dyn. 235, 1194-1218.
46. Nudi, M., Ouimette, J. F. and Drouin, J. (2005). Bone morphogenic protein (Smad)-mediated repression of proopiomelanocortin transcription by interference with Pitx/Tpit activity. Mol. Endocrinol. 19, 1329-1342. (Pubitemid 40594128)
47. Ordahl, C. P. and Williams, B. A. (1998). Knowing chops from chuck: roasting myoD redundancy. BioEssays 20, 357-362.
48. Ott, M. O., Bober, E., Lyons, G., Arnold, H. and Buckingham, M. (1991). Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097-1107.
49. Poulin, G., Lebel, M., Chamberland, M., Paradis, F. W. and Drouin, J. (2000). Specific protein:protein interaction between basic Helix-Loop-Helix transcription factors and homeoproteins of the Pitx family. Mol. Cell. Biol. 20, 4826-4837.
50. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953. (Pubitemid 40896320)
51. Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H. H. and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
52. Sambasivan, R., Gayraud-Morel, B., Dumas, G., Cimper, C., Paisant, S., Kelly, R. G. and Tajbakhsh, S. (2009). Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev. Cell 16, 810-821.
53. Sassoon, D., Lyons, G. E., Wright, W. E., Lin, V., Lassar, A., Weintraub, H. and Buckingham, M. (1989). Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341, 303-307.
54. Semina, E. V., Reiter, R., Leysens, N. J., Alward, W. L., Small, K. W., Datson, N. A., Siegel-Bartelt, J., Bierke-Nelson, D., Bitoun, P., Zabel, B. U. et al. (1996). Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat. Genet. 14, 392-399.
55. Shang, Y., Yoshida, T., Amendt, B. A., Martin, J. F. and Owens, G. K. (2008). Pitx2 is functionally important in the early stages of vascular smooth muscle cell differentiation. J. Cell Biol. 181, 461-473.
56. Shih, H. P., Gross, M. K. and Kioussi, C. (2007a). Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc. Natl. Acad. Sci. USA 104, 5907-5912.
57. Shih, H. P., Gross, M. K. and Kioussi, C. (2007b). Expression pattern of the homeodomain transcription factor Pitx2 during muscle development. Gene Expr. Patterns 7, 441-451.
58. Szeto, D. P., Ryan, A. K., O'Connell, S. M. and Rosenfeld, M. G. (1996). P-OTX: a PIT-1-interacting homeodomain factor expressed during anterior pituitary gland development. Proc. Natl. Acad. Sci. USA 93, 7706-7710.
59. Tajbakhsh, S. and Buckingham, M. E. (1994). Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5. Proc. Natl. Acad. Sci. USA 91, 747-751.
60. Tajbakhsh, S. and Cossu, G. (1997). Establishing myogenic identity during somitogenesis. Curr. Genetics Dev. 7, 634-641.
61. Tajbakhsh, S., Bober, E., Babinet, C., Pournin, S., Arnold, H. and Buckingham, M. (1996a). Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle. Dev. Dyn. 206, 291-300.
62. Tajbakhsh, S., Rocancourt, D. and Buckingham, M. (1996b). Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 384, 266-270.
63. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
64. Tapscott, S. J., Lassar, A. B. and Weintraub, H. (1992). A novel myoblast enhancer element mediates MyoD transcription. Mol. Cell. Biol. 12, 4994-5003.
65. Tremblay, J. J. and Drouin, J. (1999). Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx1 and SF-1 to enhance luteinizing hormone b gene transcription. Mol. Cell. Biol. 19, 2567-2576.
66. Tremblay, J. J., Lanctôt, C. and Drouin, J. (1998). The pan-pituitary activator of transcription, Ptx-1 (pituitary homeobox1), acts in synergy with SF-1 and Pit1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3. Mol. Endocrinol. 12, 428-441.
67. Tremblay, J. J., Goodyer, C. G. and Drouin, J. (2000). Transcriptional properties of Ptx1 and Ptx2 isoforms. Neuroendocrinol. 71, 277-286.
68. Underhill, D. A., Vogan, K. J. and Gros, P. (1995). Analysis of the mouse Splotch-delayed mutation indicates that the Pax-3 paired domain can influence homeodomain DNA-binding activity. Proc. Natl. Acad. Sci. USA 92, 3692-3696.
69. Vadlamudi, U., Espinoza, H. M., Ganga, M., Martin, D. M., Liu, X., Engelhardt, J. F. and Amendt, B. A. (2005). PITX2, beta-catenin and LEF-1 interact to synergistically regulate the LEF-1 promoter. J. Cell Sci. 118, 1129-1137.
70. Wright, W. E., Sassoon, D. A. and Lin, V. K. (1989). Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56, 607-617.