Combinatorial roles for BMPs and endothelin 1 in patterning the dorsal-ventral axis of the craniofacial skeleton

Development

Volumn 138, Issue 23, 2011, Pages 5135-5146

  Alexander, Courtney ^a   Zuniga, Elizabeth ^b   Blitz, Ira L ^a   Wada, Naoyuki ^a,c   le Pabic, Pierre ^a   Javidan, Yashar ^a   Zhang, Tailin ^a   Cho, Ken W ^a   Crump, J Gage ^b   Schilling, Thomas F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Branchial arch; Craniofacial; Neural crest; Pharyngeal arch; Xenopus; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; CELL PROTEIN; DLX6A PROTEIN; EDN1 PROTEIN; ENDOTHELIN 1; FGF8A PROTEIN; HAND2 PROTEIN; JAG1B PROTEIN; MESSENGER RNA; NOGGIN; PITX2CA PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; ECTODERM; EMBRYO; ENDODERM; GASTRULA; GENE EXPRESSION; HETEROZYGOTE; HOMOZYGOTE; HYOID BONE; MANDIBLE; NEURAL CREST CELL; NONHUMAN; PALATE; PHARYNX; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TRANSGENIC ORGANISM; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; BRANCHIAL REGION; CELL MOVEMENT; ENDOTHELIN-1; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; NEURAL CREST; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 80755148792     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.067801     Document Type: Article

References (72)

1. Aberg, T., Wozney, J. and Thesleff, I. (1997). Expression patterns of bone morphogenetic proteins (Bmps) in the developing mouse tooth suggest roles in morphogenesis and cell differentiation. Dev. Dyn. 210, 383-396.
2. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. and Westerfield, M. (1994). Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475-3486.
3. Aybar, M. J. and Mayor, R. (2002). Early induction of neural crest cells: lessons learned from frog, fish and chick. Curr. Opin. Genet. Dev. 12, 452-458.
4. Beverdam, A., Merlo, G. R., Paleari, L., Mantero, S., Genova, F., Barbieri, O., Janvier, P. and Levi, G. (2002). Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis 34, 221-227.
5. Bouallegue, A., Daou, G. B. and Srivastava, A. K. (2007). Endothelin-1-induced signaling pathways in vascular smooth muscle cells. Curr. Vasc. Pharmacol. 5, 45-52.
6. Canalis, E., Deregowski, V., Pereira, R. C. and Gazzerro, E. (2005). Signals that determine the fate of osteoblastic cells. J. Endocrinol. Invest. 28, 3-7.
7. Chai, Y., Ito, Y. and Han, J. (2003). TGF-beta signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit. Rev. Oral Biol. Med. 14, 78-88.
8. Charite, J., McFadden, D. G., Merlo, G., Levi, G., Clouthier, D. E., Yanagisawa, M., Richardson, J. A. and Olson, E. N. (2001). Role of Dlx6 in regulation of an endothelin-1-dependent, dHAND branchial arch enhancer. Genes Dev. 15, 3039-3049.
9. Christiansen, J. H., Coles, E. G. and Wilkinson, D. G. (2000). Molecular control of neural crest formation, migration and differentiation. Curr. Opin. Cell Biol. 12, 719-724.
10. Clouthier, D. E., Hosoda, K., Richardson, J. A., Williams, S. C., Yanagisawa, H., Kuwaki, T., Kumada, M., Hammer, R. E. and Yanagisawa, M. (1998). Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development 125, 813-824.
11. Clouthier, D. E., Williams, S. C., Yanagisawa, H., Wieduwilt, M., Richardson, J. A. and Yanagisawa, M. (2000). Signaling pathways crucial for craniofacial development revealed by endothelin-A receptor-deficient mice. Dev. Biol. 217, 10-24.
12. Clouthier, D. E., Garcia, E. and Schilling, T. F. (2010). Regulation of facial morphogenesis by endothelin signaling: Insights from mice and fish. Am. J. Med. Genet. A 152A, 2962-2973.
13. David, N. B., Saint-Etienne, L., Tsang, M., Schilling, T. F. and Rosa, F. M. (2002). Requirement for endoderm and FGF3 in ventral head skeleton formation. Development 129, 4457-4468.
14. Dawson, L. A., Maitland, N. J., Berry, P., Turner, A. J. and Usmani, B. A. (2006). Expression and localization of endothelin-converting enzyme-1 in human prostate cancer. Exp. Biol. Med. 231, 1106-1110.
15. Depew, M. J., Lufkin, T., Rubenstein, J. L. (2002). Specification of jaw subdivisions by Dlx genes. Science 298, 381-385.
16. Dorai, H., Vukicevic, S. and Sampath, T. K. (2000). Bone morphogenetic protein-7 (osteogenic protein-1) inhibits smooth muscle cell proliferation and stimulates the expression of markers that are characteristic of SMC phenotype in vitro. J. Cell. Physiol. 184, 37-45.
17. Dudas, M., Sridurongrit, S., Nagy, A., Okazaki, K. and Kaartinen, V. (2004). Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mech. Dev. 121, 173-182.
18. Eberhart, J. K., Swartz, M. E., Crump, J. G. and Kimmel, C. B. (2006). Early Hedgehog signaling from neural to oral epithelium organizes anterior craniofacial development. Development 133, 1069-1077.
19. Guise, T. A., Yin, J. J. and Mohammad, K. S. (2003). Role of endothelin-1 in osteoblastic bone metastases. Cancer 97, 779-784.
20. Holzschuh, J., Wada, N., Wada, C., Schaffer, A., Javidan, Y., Tallafuss, A., Bally-Cuif, L. and Schilling, T. F. (2005). Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development 132, 3731-3742.
21. Howard, M. J., Stanke, M., Schneider, C., Wu, X. and Rohrer, H. (2000). The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 127, 4073-4081.
22. Hu, D., Marcucio, R. S. and Helms, J. A. (2003). A zone of frontonasal ectoderm regulates patterning and growth in the face. Development 130, 1749-1758.
23. Ishii, M., Han, J., Yen, H. Y., Sucov, H. M., Chai, Y. and Maxson, R. E., Jr (2005). Combined deficiencies of Msx1 and Msx2 cause impaired patterning and survival of the cranial neural crest. Development 132, 4937-4950.
24. Javidan, Y. and Schilling, T. F. (2004). Development of cartilage and bone. Methods Cell Biol. 76, 415-436.
25. Kaartinen, V., Dudas, M., Nagy, A., Sridurongrit, S., Lu, M. M. and Epstein, J. A. (2004). Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development 131, 3481-3490.
26. Kimmel, C. B., Ullmann, B., Walker, M., Miller, C. T. and Crump, J. G. (2003). Endothelin-1 mediated regulation of pharyngeal bone development. Development 130, 1339-1351.
27. Kimmel, C. B., Walker, M. B. and Miller, C. T. (2007). Morphing the hyomandibular skeleton in development and evolution. J. Exp. Zool. B Mol. Dev. Evol. 308, 609-624.
28. Knecht, A. K. and Bronner-Fraser, M. (2002). Induction of the neural crest: a multigene process. Nat. Rev. Genet. 3, 453-461.
29. Knight, R. D. and Schilling, T. F. (2006). Cranial neural crest and development of the head skeleton. Adv. Exp. Med. Biol. 589, 120-133.
30. Ko, S. O., Chung, I. H., Xu, X., Oka, S., Zhao, H., Cho, E. S., Deng, C. and Chai, Y. (2007). Smad4 is required to regulate the fate of cranial neural crest cells. Dev. Biol. 312, 435-447.
31. Kuraku, S., Takio, Y., Sugahara, F., Takechi, M. and Kuratani, S. (2010). Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Dev. Biol. 341, 315-323.
32. Le Bras, A., Vijayaraj, P. and Oettgen, P. (2010). Molecular mechanisms of endothelial differentiation. Vasc. Med. 15, 321-331.
33. Liu, W., Sun, X., Braut, A., Mishina, Y., Behringer, R. R., Mina, M. and Martin, J. F. (2005). Distinct functions for Bmp signaling in lip and palate fusion in mice. Development 132, 1453-1461.
34. Maemura, K., Kurihara, H., Kurihara, Y., Oda, H., Ishikawa, T., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Yazaki, Y. (1996). Sequence analysis, chromosomal location, and developmental expression of the mouse preproendothelin-1 gene. Genomics 31, 177-184.
35. Martinez-Barbera, J. P., Toresson, H., Da Rocha, S. and Krauss, S. (1997). Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene 198, 53-59.
36. Miller, C. T., Schilling, T. F., Lee, K., Parker, J. and Kimmel, C. B. (2000). sucker encodes a zebrafish Endothelin-1 required for ventral pharyngeal arch development. Development 127, 3815-3828.
37. Miller, C. T., Yelon, D., Stainier, D. Y. and Kimmel, C. B. (2003). Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130, 1353-1365.
38. Miller, C. T., Swartz, M. E., Khuu, P. A., Walker, M. B., Eberhart, J. K. and Kimmel, C. B. (2007). mef2ca is required in cranial neural crest to effect Endothelin1 signaling in zebrafish. Dev. Biol. 308, 144-157.
39. Nair, S., Li, W., Cornell, R. and Schilling, T. F. (2007). Requirements for Endothelin type-A receptors and Endothelin-1 signaling in the facial ectoderm for the patterning of skeletogenic neural crest cells in zebrafish. Development 134, 335-345.
40. Neidert, A. H., Virupannavar, V., Hooker, G. W. and Langeland, J. A. (2001). Lamprey Dlx genes and early vertebrate evolution. Proc. Natl. Acad. Sci. USA 98, 1665-1670.
41. Nie, X., Luukko, K. and Kettunen, P. (2006). BMP signalling in craniofacial development. Int. J. Dev. Biol. 50, 511-521.
42. Oka, K., Oka, S., Sasaki, T., Ito, Y., Bringas, P., Nonaka, K. and Chai, Y. (2007). The role of TGF-beta signaling in regulating chondrogenesis and osteogenesis during mandibular development. Dev. Biol. 303, 391-404.
43. Ozeki, H., Kurihara, Y., Tonami, K., Watatani, S. and Kurihara, H. (2004). Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mech. Dev. 121, 387-395.
44. Pyati, U. J., Webb, A. E. and Kimelman, D. (2005). Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132, 2333-2343.
45. Ruest, L. B., Xiang, X., Lim, K. C., Levi, G. and Clouthier, D. E. (2004). Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity. Development 131, 4413-4423.
46. Sato, T., Kawamura, Y., Asai, R., Amano, T., Uchijima, Y., Dettlaff-Swiercz, D. A., Offermanns, S., Kurihara, Y. and Kurihara, H. (2008). Recombinasemediated cassette exchange reveals the selective use of Gq/G11-dependent and -independent endothelin 1/endothelin type A receptor signaling in pharyngeal arch development. Development 135, 755-765.
47. Schilling, T. F., Prince, V. and Ingham, P. W. (2001). Plasticity in zebrafish hox expression in the hindbrain and cranial neural crest. Dev. Biol. 231, 201-216.
48. Stottmann, R. W., Anderson, R. M. and Klingensmith, J. (2001). The BMP antagonists Chordin and Noggin have essential but redundant roles in mouse mandibular outgrowth. Dev. Biol. 240, 457-473.
49. Talbot, J. C., Johnson, S. L. and Kimmel, C. B. (2010). hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development 137, 2507-2517.
50. Thesleff, I. and Sharpe, P. (1997). Signalling networks regulating dental development. Mech. Dev. 67, 111-123.
51. Thisse, C., Thisse, B., Schilling, T. F. and Postlethwait, J. H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.
52. Thomas, T., Kurihara, H., Yamagishi, H., Kurihara, Y., Yazaki, Y., Olson, E. N. and Srivastava, D. (1998). A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125, 3005-3014.
53. Trainor, P. A. and Krumlauf, R. (2000). Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 1, 116-124.
54. Tucker, A. S., Al Khamis, A. and Sharpe, P. T. (1998a). Interactions between Bmp-4 and Msx-1 act to restrict gene expression to odontogenic mesenchyme. Dev. Dyn. 212, 533-539.
55. Tucker, A. S., Matthews, K. L. and Sharpe, P. T. (1998b). Transformation of tooth type induced by inhibition of BMP signaling. Science 282, 1136-1138.
56. Tucker, A. S., Yamada, G., Grigoriou, M., Pachnis, V. and Sharpe, P. T. (1999). Fgf-8 determines rostral-caudal polarity in the first branchial arch. Development 126, 51-61.
57. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
58. von Bubnoff, A., Peiffer, D. A., Blitz, I. L., Hayata, T., Ogata, S., Zeng, Q., Trunnell, M. and Cho, K. W. (2005). Phylogenetic footprinting and genome scanning identify vertebrate BMP response elements and new target genes. Dev. Biol. 281, 210-226.
59. Wada, N., Javidan, Y., Nelson, S., Carney, T. J., Kelsh, R. N. and Schilling, T. F. (2005). Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 132, 3977-3988.
60. Walker, M. B. and Kimmel, C. B. (2007). A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 82, 23-28.
61. Westerfield, M. (2000). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4th edn. Eugene, OR: University of Oregon Press.
62. Whyteside, A. R., Hinsley, E. E., Lambert, L. A., McDermott, P. J. and Turner, A. J. (2010). ECE-1 influences prostate cancer cell invasion via ET-1-mediated FAK phosphorylation and ET-1-independent mechanisms. Can. J. Physiol. Pharmacol. 88, 850-854.
63. Wilson, J. and Tucker, A. S. (2004). Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev. Biol. 266, 138-150.
64. Wu, X. and Howard, M. J. (2002). Transcripts encoding HAND genes are differentially expressed and regulated by BMP4 and GDNF in developing avian gut. Gene Expr. 10, 279-293.
65. Yanagisawa, H., Hammer, R. E., Richardson, J. A., Williams, S. C., Clouthier, D. E. and Yanagisawa, M. (1998a). Role of Endothelin-1/Endothelin-A receptor-mediated signaling pathway in the aortic arch patterning in mice. J. Clin. Invest. 102, 22-33.
66. Yanagisawa, H., Yanagisawa, M., Kapur, R. P., Richardson, J. A., Williams, S. C., Clouthier, D. E., de Wit, D., Emoto, N. and Hammer, R. E. (1998b). Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 125, 825-836.
67. Yanagisawa, H., Clouthier, D. E., Richardson, J. A., Charite, J. and Olson, E. N. (2003). Targeted deletion of a branchial arch-specific enhancer reveals a role of dHAND in craniofacial development. Development 130, 1069-1078.
68. Yao, L. C., Blitz, I. L., Peiffer, D. A., Phin, S., Wang, Y., Ogata, S., Cho, K. W., Arora, K. and Warrior, R. (2006). Schnurri transcription factors from Drosophila and vertebrates can mediate Bmp signaling through a phylogenetically conserved mechanism. Development 133, 4025-4034.
69. Ye, L., Lewis-Russell, J. M., Kyanaston, H. G. and Jiang, W. G. (2007). Bone morphogenetic proteins and their receptor signaling in prostate cancer. Histol. Histopathol. 22, 1129-1147.
70. Yelon, D., Ticho, B., Halpern, M. E., Ruvinsky, I., Ho, R. K., Silver, L. M. and Stainier, D. Y. (2000). The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127, 2573-2582.
71. Zuniga, E., Stellabotte, F. and Crump, J. G. (2010). Jagged-Notch signaling ensures dorsal skeletal identity in the vertebrate face. Development 137, 1843-1852.
72. Zuniga, E., Rippen, M., Alexander, C., Schilling, T. F. and Crump, J. G. (2011). Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton. Development 138, 5147-5156.