Satb2, modularity, and the evolvability of the vertebrate jaw

Evolution and Development

Volumn 13, Issue 6, 2011, Pages 549-564

  Fish, Jennifer L ^b,d   Villmoare, Brian ^b   Köbernick, Katja ^c,e   Compagnucci, Claudia ^a   Britanova, Olga ^c,f   Tarabykin, Victor ^c,g   Depew, Michael J ^a,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d Department of Orthopaedic Surgery ^*  (United States)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; MATRIX ATTACHMENT REGION BINDING PROTEIN; MESSENGER RNA; SATB2 PROTEIN, MOUSE; SATB2 PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

EVOLUTIONARY BIOLOGY; FROG; GENETIC VARIATION; HYPOTHESIS TESTING; MORPHOLOGY; SIZE; TOOTH;

ANIMAL; ARTICLE; BIOSYNTHESIS; CHICKEN; EVOLUTION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MANDIBLE; MESODERM; METABOLISM; MOUSE; PRENATAL DEVELOPMENT; XENOPUS; ZEBRA FISH;

ANIMALS; BIOLOGICAL EVOLUTION; CHICKENS; FIBROBLAST GROWTH FACTOR 8; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; MANDIBLE; MATRIX ATTACHMENT REGION BINDING PROTEINS; MESODERM; MICE; RNA, MESSENGER; TRANSCRIPTION FACTORS; XENOPUS; ZEBRAFISH; ZEBRAFISH PROTEINS;

MUS; VERTEBRATA;

EID: 84859028595     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2011.00511.x     Document Type: Article

References (69)

1. Ahn, H. J., Park, Y., Kim, S., Park, H. C., Seo, S. K., Yeo, S. Y. et al. 2010. The expression profile and function of Satb2 in zebrafish embryonic development. Mol. Cells. 30:377-382.
2. Alkuraya, F. S., Saadi, I., Lund, J. J., Turbe-Doan, A., Morton, C. C., and Maas, R. L. 2006. SUMO1 haploinsufficiency leads to cleft lip and palate. Science 313:1751.
3. Andreou, A. M., Pauws, E., Jones, M. C., Singh, M. K., Bussen, M., Doudney, K., et al. 2007 TBX22 missense mutations found in patients with X-linked cleft palate affect DNA binding, sumoylation, and transcriptional repression. Am. J. Hum. Genet. 81: 700-712.
4. Atchley, W. R., and Hall, B. K. 1991. A model for development and evolution of complex morphological structures. Biol. Rev. Cambridge Phil. Soc. 66: 101-157.
5. Atchley, W. R., Plummer, A. A., and Riska, B. 1985. Genetics of mandible form in the mouse. Genetics. 111: 555-577.
6. Barghusen, H. R. and Hopson, A. 1979. The endoskeleton: the com- parative anatomy of the skull and visceral skeleton. In M. Wake (ed.). Hyman's Comparative Anatomy. University of Chicago Press, Chicago, IL: pp. 265-326.
7. Britanova, O., Akopov, S., Lukyanov, S., Gruss, P., and Tarabykin, V. 2005. Novel transcription factor Satb2 interacts with matrix attach- ment region DNA elements in a tissue-specific manner and demon- strates cell-type-dependent expression in the developing mouse CNS. Eur. J. Neurosci. 21: 658-668
8. Britanova, O., Depew, M. J., Schwark, M., Thomas, B .L., Miletich, I., Sharpe, P., et al. 2006. Satb2 haploinsufficiency phenocopies 2q32-q33 deletions, whereas loss suggests a fundamental role in the coordina- tion of jaw development. Am. J. Hum. Genet. 79: 668-678.
9. Cheverud, J. M. 1982. Phenotypic, genetic, and environmental integra- tion in the cranium. Evolution 36: 499-516.
10. Cheverud, J. M. 1988. A comparison of genetic and phenotypic corre- lations. Evolution 42: 958-968.
11. Cheverud, J. M. 1995. Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. Am. Nat. 145: 63-89.
12. Cheverud, J. M. 1996. Developmental integration and the evolution of pleiotropy. Am. Zool. 36: 44-50.
13. Cheverud, J. M., Hartman, S. E., Richtsmeier, J. T., and Atchley, W. R. 1991. A quantitative genetic analysis of localized morphology in mandibles of inbred mice using finite-element scaling analysis. J. Craniofac. Genet. Dev. Biol. 11: 122-137.
14. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D., and Kintner, C. 1995. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375: 761-766.
15. Fish et al. Satb2, modularity, and jaw evolvability 563
16. de Beer, G. 1985. The Development of the Vertebrate Skull. University of Chicago Press, Chicago.
17. Depew, M. J. 2008. Analysis of skeletal ontogenesis through differential staining of bone and cartilage. In: P. T. Sharpe and I. Mason (eds.). Molecular Embryology - Methods and Protocols. Humana Press, Totowa, NJ, pp. 37-45.
18. Depew, M. J., and Compagnucci, C. 2008. Tweaking the Hinge and Caps: testing a model of the organization of jaws. J. Exp. Zool. 310B, 315-335.
19. Depew, M. J., Liu, J. K., Long, J. E., Presley, R., Meneses, J. J., Pedersen, R. A., and Rubenstein, J. L. 1999. Dlx5 regulates regional develop- ment of the branchial arches and sensory capsules. Development 126, 3831-3846.
20. Depew, M. J., Lufkin, T., and Rubenstein, J. L. R. 2002. Specification of jaw subdivisions by Dlx genes. Science. 298: 381-385.
21. Depew, M. J., and Simpson, C.A. 2006. 21st century neontology and the comparative development of the vertebrate skull. Dev. Dyn. 235: 1256-1291.
22. Depew, M. J., Simpson, C., Marosso, M., and Rubenstein, J.L.R. 2005. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J. Anatomy. 207: 501-561.
23. Dobreva, G., Chahrour, M., Dautzenberg, M., Chirivella, L., Kanzler, B., Farinas, I., et al. 2006. Satb2 is a multifunctional determinant of craniofacial patterning and osteoblast differentiation. Cell 125: 971-986.
24. Dobreva, G., Dambacher, J., and Grosschedl, R. 2003. SUMO modifica- tion of a novel MAR-binding protein, Satb2, modulates immunoglob- ulin mu gene expression. Genes. Dev. 17: 3048-3061.
25. Ferguson, C. A., Tucker, A. S., and Sharpe, P. T. 2000. Temporospatial cell interactions regulating mandibular and maxillary arch patterning. Development 127: 403-412.
26. FitzPatrick, D. R., Carr, I. M., McLaren, L., Leek, J. P., Wightman, P., Williamson, K., et al. 2003. Identification of Satb2 as the cleft palate gene on 2q32-q33. Hum. Mol. Genet. 12: 2491-2501.
27. Flatt, T. 2005. The evolutionary genetics of canalization. Q. Rev. Biol. 80: 287-316.
28. Goodrich, E. S. 1958. Studies on the Structure and Development of Ver- tebrates. Dover Publications, New York.
29. Gupta, V., and Bei, M. 2006. Modification of Msx1 by SUMO-1. Biochem. Biophys. Res. Commun. 345: 74-77.
30. Hall, B. K. 1999. The Neural Crest in Development and Evolution. Springer, New York.
31. Hall, B. K. 2003. Unlocking the black box between genotype and phe- notype: cell condensations as morphogenetic (modular) units. Biol. Phil. 18: 219-247.
32. Hallgrimsson, B., Jamniczky, H., Young, N., Rolian, C., Parsons, T., Boughner, J., et al. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic co- variation. Evol. Biol. 36: 355-376.
33. Hendrikse, J. L., Parsons, T. E., and Hallgri{dotless}msson, B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evol. Dev. 9: 393-401.
34. Kirschner, M., and Gerhart, J. 1998. Evolvability. Proc. Natl. Acad. Sci. U.S. A. 95: 8420-8427.
35. Klingenberg, C. P. 2005. Developmental constraints, modules and evolv- ability. In: B. Hallgri{dotless}msson and B.K. Hall (eds.). Variation: A Central Concept in Biology, Elsevier Burlington, MA, pp. 219-247.
36. Klingenberg, C. P., Mebus, K., and Auffray, J. C. 2003. Develop- mental integration in a complex morphological structure: how dis- tinct are the modules in the mouse mandible? Evol. Dev. 5: 522-531.
37. Klingenberg, C. P., and Nijhout, H. F.1999. Genetics of fluctuating asymmetry: a developmental model of developmental instability. Evo- lution. 53: 358-375.
38. 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.
39. Kuratani, S. 2003. Evolution of the vertebrate jaw: homology and devel- opmental constraints. Paleontol. Res. 7: 89-102.
40. Kuratani, S. 2004. Evolution of the vertebrate jaw: comparative embry- ology and molecular developmental biology reveal the factors behind evolutionary novelty. J. Anat. 205: 335-347.
41. Kuratani, S. 2005. Developmental studies of the lamprey and hierarchi- cal evolutionary steps towards the acquisition of the jaw. J. Anat.207: 489-499.
42. Lande, R. 1980. The genetic covariance between characters maintained by pleiotropic mutations. Genetics. 94: 203-215.
43. Le Douarin, N., and Kalcheim, C. 1999. The Neural Crest. Cambridge University Press, Cambridge; New York, NY.
44. Leamy, L. J. 1984. Morphometric studies in inbred and hybrid house mice. Directional and fluctuating asymmetry. Am. Natural. 123: 579-593.
45. Leoyklang, P., Suphapeetiporn, K., Siriwan, P., Desudchit, T., Chaowanapanja, P., Gahl, W. A., et al. 2007. Heterozygous non- sense mutation Satb2 associated with cleft palate, osteoporosis, and cognitive defects. Hum. Mutat. 28: 732-738.
46. Macdonald, M. E., and Hall, B. K. 2001. Altered timing of the extracellular-matrix-mediated epithelial-mesenchymal interaction that initiates mandibular skeletogenesis in three inbred strains of mice: development, heterochrony, and evolutionary change in morphology. J. Exp Zool. 291: 258-273.
47. Masel, J., and Trotter, M. V. 2010. Robustness and evolvability. Trends Genet. 26: 406-414.
48. Miller, C. T., Yelon, D., Stainier, D. Y. R., and Kimmel, C. B. 2003. Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130, 1353-1365.
49. Moore, W. J. 1981. The Mammalian Skull. Cambridge University Press, Cambridge, New York, NY.
50. Neübuser, A., Peters, H., Balling, R., and Martin, G. R. 1997. Antag- onistic interactions between FGF and BMP signaling path-ways: a mechanism for positioning the sites of tooth formation. Cell 90: 247-255.
51. O'Higgins, P., and Jones, N. 1998. Facial growth in Cercocebus:an application of three-dimensional geometric morphometric techniques to the study of morphological variation. J. Anat. 193: 251-272.
52. Olson, E. C., and Miller, R. A. 1958. Morphological Integration. Uni- versity of Chicago Press, Chicago.
53. Pauws, E., and Stainer, P. 2007. FGF signalling and SUMO modifica- tion: new players in the aetiology of cleft lip and/or palate. Trends Genetics 23: 631-640.
54. Raff, R. A. 1996. The Shape of Life: Genes, Development and the Evolu- tion of Animal Form. University of Chicago Press, Chicago, IL.
55. Raff, E. C., and Raff, R. A. 2000. Dissociability, modularity, evolvability. Evol. Dev. 2: 235-237.
56. Rupp, R. A., Snider, L., and Weintraub, H. 1994. Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8: 1311-1323.
57. Schlosser, G., and Wagner, G.P. 2004. Introduction: the modularity concept in developmental and evolutionary biology. In: G. Schlosser and G.P. Wagner (eds.) Modularity in Development and Evolution. The University of Chicago Press, Chicago, pp. 1-18.
58. Sheehan-Rooney, K., Pálinkášová, B., Eberhart, J. K., and Dixon, M. J. 2010. A cross-species analysis of Satb2 expression suggests deep conservation across vertebrate lineages. Dev. Dyn. 239: 3481-3491.
59. Trumpp, A., Depew, M. J., Rubenstein, J. L., Bishop, J. M., and Martin, G. R. 1999. Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 13: 3136-3148.
60. Tucker, A., Watson, R. P., Lettice, L. A., Yamada, G., and Hill, R. E. 2004. Bapx1 regulates patterning in the middle ear: altered regulatory rolein the transition from the proximal jaw during vertebrate evolution. Development 131: 1235-1245.
61. Van Buggenhout, G., Van Ravenswaaij-Arts, C., Mc Maas, N., Thoelen, R., Vogels, A., Smeets, D., et al. 2005. The del(2)(q32.2q33) deletion syndrome defined by clinical and molecular characterization of four patients. Eur. J. Med. Genet. 48: 276-289.
62. Waddington, C. H., and Robertson, E. 1966. Selection for developmental canalisation. Genet. Res. 7: 303-312.
63. Wagner, G. P. 1995. Adaptation and the modular design of or- ganisms. In F. Moran, A. Moran, J. J. Merelo, and P. Chacon (eds.) Advances in Artificial Life. Springer Verlag, Berlin, pp. 317-328.
64. Wagner, G. P. 1996. Homologues, natural kinds and the evolution of modularity. Am. Zool. 36: 36-43.
65. Wagner, G. P. 1998. Complexity matters. Science 279: 1158-1159.
66. Wagner, G. P., Booth, G., and Bagheri-Chaichian, H. 1997. A population genetic theory of canalization. Evolution 51: 329-347.
67. Wagner, G. P., Pavlicev, M., and Cheverud, J. M. 2007. The road to modularity. Nat. Rev. Genet. 8: 921-931.
68. Zelditch, M. L., Wood, A. R, Bonett, R. M., and Swiderski, D. L. 2008. Modularity of the rodent mandible: integrating bones, muscles, and teeth. Evol. Dev. 10: 756-768.
69. Zelditch, M. L., Wood, A. R., and Swiderski, D. L. 2009. Building developmental integration into functional systems: function induced integration of mandibular shape. Evol. Biol. 36: 71-87