Mechanisms that underlie co-variation of the brain and face

Genesis

Volumn 49, Issue 4, 2011, Pages 177-189

  Marcucio, Ralph S ^a   Young, Nathan M ^a   Hu, Diane ^a   Hallgrimsson, Benedikt ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bmp; Craniofacial; Disease; Evolution; FEZ; Fgf8; Neural crest; Shh

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 8; OSTEOGENIC PROTEIN 1; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN;

BRAIN; BRAIN DEVELOPMENT; CRANIOFACIAL DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; FACE; FACE DEVELOPMENT; FACE MALFORMATION; GENE EXPRESSION; GROWTH REGULATION; HUMAN; MORPHOLOGY; NEURAL CREST; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRAIN; EPITHELIAL CELLS; FACE; FACIAL BONES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MESODERM; MORPHOGENESIS; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 79954599478     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20710     Document Type: Review

References (97)

1. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. 2004. Bmp4 and morphological variation of beaks in Darwin's finches. Science 305: 1462-1465.
2. Abzhanov A, Rodda SJ, McMahon AP, Tabin CJ. 2007. Regulation of skeletogenic differentiation in cranial dermal bone. Development 134: 3133-3144.
3. Abzhanov A, Tabin CJ. 2004. Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev Biol 273: 134-148.
4. Ahituv N, Rubin EM, Nobrega MA. 2004. Exploiting human-fish genome comparisons for deciphering gene regulation. Hum Mol Genet 13: R261-R266.
5. Ahlgren SC, Bronner-Fraser M. 1999. Inhibition of sonic hedgehog signaling in vivo results in craniofacial neural crest cell death. Curr Biol 9: 1304-1314.
6. Aldridge K, Kane AA, Marsh JL, Yan P, Govier D, Richtsmeier JT. 2005. Relationship of brain and skull in pre- and postoperative sagittal synostosis. J Anat 206: 373-385.
7. Allen BL, Tenzen T, McMahon AP. 2007. The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev 21: 1244-1257.
8. Ashique AM, Fu K, Richman JM. 2002a. Endogenous bone morphogenetic proteins regulate outgrowth and epithelial survival during avian lip fusion. Development 129: 4647-4660.
9. Ashique AM, Fu K, Richman JM. 2002b. Signalling viatype IA and type IB bone morphogenetic protein receptors (BMPR) regulates intramembranous bone formation, chondrogenesis and feather formation in the chicken embryo. Int J Dev Biol 46: 243-253.
10. Atchley WR, Hall BK. 1991. A model for development and evolution of complex morphological structures. Biol Rev Camb Philos Soc 66: 101-157.
11. Balk K, Biesecker LG. 2008. The clinical atlas of Greig cephalopolysyndactyly syndrome. Am J Med Genet A 146: 548-557.
12. Barlow AJ, Francis-West PH. 1997. Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia. Development 124: 391-398.
13. Bennett JH, Hunt P, Thorogood P. 1995. Bone morphogenetic protein-2 and -4 expression during murine orofacial development. Arch Oral Biol 40: 847-854.
14. Biegert J. 1963. The evaluation of characteristics of theskull, hands and feet for primate taxonomy. In Washburn SL, editor. Classification and human evolution. Chicago: Aldine. pp 116-145.
15. Boughner JC, Wat S, Diewert VM, Young NM, Browder LW, Hallgrimsson B. 2008. Short-faced mice and developmental interactions between the brain and the face. J Anat 213: 646-662.
16. Brito JM, Teillet MA, Le Douarin NM. 2006. An early role for sonic hedgehog from foregut endoderm in jaw development: Ensuring neural crest cell survival. Proc Natl Acad Sci USA 103: 11607-11612.
17. Brito JM, Teillet MA, Le Douarin NM. 2008. Induction of mirror-image supernumerary jaws in chicken mandibular mesenchyme by Sonic Hedgehog-producing cells. Development 135: 2311-2319.
18. Chai Y, Maxson REJr. 2006. Recent advances in craniofacial morphogenesis. Dev Dyn 235: 2353-2375.
19. Cordero D, Marcucio R, Hu D, Gaffield W, Tapadia M, Helms JA. 2004. Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes. J Clin Invest 114: 485-494.
20. Creuzet SE. 2009a. Neural crest contribution to forebrain development. Semin Cell Dev Biol 20: 751-759.
21. Creuzet SE. 2009b. Regulation of pre-otic brain development by the cephalic neural crest. Proc Natl Acad Sci USA 106: 15774-15779.
22. Creuzet SE, Martinez S, Le Douarin NM. 2006. The cephalic neural crest exerts a critical effect on forebrain and midbrain development. Proc Natl Acad Sci USA 103: 14033-14038.
23. Dahmane N, Lee J, Robins P, Heller P, Ruiz I, Altaba A. 1997. Activation of the transcription factor Gli 1 and the Sonic hedgehog signalling pathway in skin tumors. Nature 389: 876-881.
24. DeBeer G. 1937. The development of the vertebrate skull. London: Oxford University Press.
25. DeMyer W. 1964. The face predicts the brain: Diagnostic significance of median facial anomialies for holoprosencephaly (arhinencephay). Pediatrics 34: 256-263.
26. Depew MJ, Compagnucci C. 2008. Tweaking the hinge and caps: Testing a model of the organization of jaws. J Exp Zool B Mol Dev Evol 310: 315-335.
27. Diewert VM. 1983. A morphometric analysis of craniofacial growth and changes in spatial relations during secondary palatal development in human embryos and fetuses. Am J Anat 167: 495-522.
28. Diewert VM. 1985. Growth movements during prenatal development of human facial morphology. Prog Clin Biol Res 187: 57-66.
29. Diewert VM, Lozanoff S. 1993a. A morphometric analysis of human embryonic craniofacial growth in the median plane during primary palate formation. J Craniofac Genet Dev Biol 13: 147-161.
30. Diewert VM, Lozanoff S, Choy V. 1993b. Computer reconstructions of human embryonic craniofacial morphology showing changes in relations between the face and brain during primary palate formation. J Craniofac Genet Dev Biol 13: 193-201.
31. Donoghue PC, Graham A, Kelsh RN. 2008. The origin and evolution of the neural crest. Bioessays 30: 530-541.
32. Dorus S, Anderson JR, Vallender EJ, Gilbert SL, Zhang L, Chemnick LG, Ryder OA, Li W, Lahn BT. 2006. Sonic Hedgehog, a key development gene, experienced intensified molecular evolution in primates. Hum Mol Genet 15: 2031-2037.
33. Eberhart JK, He X, Swartz ME, Yan YL, Song H, Boling TC, Kunerth AK, Walker MB, Kimmel CB, Postlethwait JH. 2008. MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat Genet 40: 290-298.
34. Eberhart JK, Swartz ME, Crump JG, Kimmel CB. 2006. Early Hedgehog signaling from neural to oral epithelium organizes anterior craniofacial development. Development 133: 1069-1077.
35. Epstein DJ, Martinu L, Michaud JL, Losos KM, Fan C, Joyner AL. 2000. Members of the bHLH-PAS family regulate Shh transcription in forebrain regions of the mouse CNS. Development 127: 4701-4709.
36. Epstein DJ, McMahon AP, Joyner AL. 1999. Regionalization of Sonic hedgehog transcription along the anteroposterior axis of the mouse central nervous system is regulated by Hnf3-dependent and-independent mechanisms. Development 126: 281-292.
37. Etheridge LA, Crawford TQ, Zhang S, Roelink H. 2010. Evidence for a role of vertebrate Disp1 in long-range Shh signaling. Development 137: 133-140.
38. Evans DJ, Noden DM. 2006. Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev Dyn 235: 1310-1325.
39. Firnberg N, Neubuser A. 2002. FGF signaling regulates expression of Tbx2, Erm, Pea3, and Pax3 in the early nasal region. Dev Biol 247: 237-250.
40. Foppiano S, Hu D, Marcucio RS. 2007. Signaling by bone morphogenetic proteins directs formation of an ectodermal signaling center that regulates craniofacial development. Dev Biol 312: 103-114.
41. Francis-West P, Ladher R, Barlow A, Graveson A. 1998. Signalling interactions during facial development. Mech Dev 75: 3-28.
42. 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.
43. Geetha-Loganathan P, Nimmagadda S, Antoni L, Fu K, Whiting CJ, Francis-West P, Richman JM. 2009. Expression of WNT signalling pathway genes during chicken craniofacial development. Dev Dyn 238: 1150-1165.
44. Geng X, Speirs C, Lagutin O, Inbal A, Liu W, Solnica-Krezel L, Jeong Y, Epstein DJ, Oliver G. 2008. Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev Cell 15: 236-247.
45. Golden JA, Bracilovic A, McFadden KA, Beesley JS, Rubenstein JL, Grinspan JB. 1999. Ectopic bone morphogenetic proteins 5 and 4 in the chicken forebrain lead to cyclopia and holoprosencephaly. Proc Natl Acad Sci USA 96: 2439-2444.
46. Goodrich LV, Scott MP. 1998. Hedgehog and patched in neural development and disease. Neuron 21: 1243-1257.
47. Graham A, Okabe M, Quinlan R. 2005. The role of the endoderm in the development and evolution of the pharyngeal arches. J Anat 207: 479-487.
48. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Hober B, Hoffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PL, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Paabo S. A draft sequence of the Neandertal genome. Science 328: 710-722.
49. Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS. 2009. Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolut Biol 36: 355-376.
50. Hallgrimsson B, Lieberman DE. 2008. Mouse models and the evolutionary developmental biology of the skull. Integr Comp Biol 48: 373-384.
51. Hallgrimsson B, Lieberman DE, Liu W, Ford-Hutchinson AF, Jirik FR. 2007a. Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol Dev 9: 76-91.
52. Hallgrimsson B, Lieberman DE, Young NM, Parsons T, Wat S. 2007b. Evolution of covariance in the mammalian skull. Novartis Found Symp 284: 164-185; discussion 185-190.
53. Hamburger V, Hamilton HL. 1951. A series of developmental stages in development of the chick embryo. J Morphol 88: 49-92.
54. Hu D, Colnot C, Marcucio RS. 2008. Effect of bone morphogenetic protein signaling on development of the jaw skeleton. Dev Dyn 237: 3727-3737.
55. Hu D, Marcucio RS. 2009a. A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136: 107-116.
56. Hu D, Marcucio RS. 2009b. Unique organization of the frontonasal ectodermal zone in birds and mammals. Dev Biol 325: 200-210.
57. Hu D, Marcucio R, Helms JA. 2003. A zone of frontonasal ectoderm regulates patterning and growth in the face. Development 130: 1749-1758.
58. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev 15: 3059-3087.
59. Jeong Y, El-Jaick K, Roessler E, Muenke M, Epstein DJ. 2006. A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development 133: 761-772.
60. Jeong Y, Epstein DJ. 2003. Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130: 3891-3902.
61. Jeong Y, Leskow FC, El-Jaick K, Roessler E, Muenke M, Yocum A, Dubourg C, Li X, Geng X, Oliver G, Epstein DJ. 2008. Regulation of a remote Shh forebrain enhancer by the Six3 homeoprotein. Nat Genet 40: 1348-1353.
62. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP. 2004. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18: 937-951.
63. Le Douarin NM, Brito JM, Creuzet S. 2007. Role of the neural crest in face and brain development. Brain Res Rev 55: 237-247.
64. Lieberman DE, Hallgrimsson B, Liu W, Parsons TE, Jamniczky HA. 2008. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: Testing a new model using mice. J Anat 212: 720-735.
65. Marcucio RS, Cordero DR, Hu D, Helms JA. 2005. Molecular interactions coordinating the development of the forebrain and face. Dev Biol 284: 48-61.
66. Martinez-Abadias N, Esparza M, Sjovold T, Gonzalez-Jose R, Santos M, Hernandez M. 2009. Heritability of human cranial dimensions: Comparing the evolvability of different cranial regions. J Anat 214: 19-35.
67. Menuet A, Alunni A, Joly JS, Jeffery WR, Retaux S. 2007. Expanded expression of Sonic Hedgehog in Astyanax cavefish: Multiple consequences on forebrain development and evolution. Development 134: 845-855.
68. Muenke M, Beachy PA. 2000. Genetics of ventral forebrain development and holoprosencephaly. Curr Opin Genet Dev 10: 262-269.
69. Muenke M, Cohen MMJr, 2000. Genetic approaches to understanding brain development: Holoprosencephaly as a model. Ment Retard Dev Disabil Res Rev 6: 15-21.
70. Odent S, Atti-Bitach T, Blayau M, Mathieu M, Aug J, de Delezo AL, Gall JY, Le Marec B, Munnich A, David V, Vekemans M. 1999. Expression of the Sonic hedgehog (SHH) gene during early human development and phenotypic expression of new mutations causing holoprosencephaly. Hum Mol Genet 8: 1683-1689.
71. Ohkubo Y, Chiang C, Rubenstein JL. 2002. Coordinate regulation and synergistic actions of BMP4. SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111: 1-17.
72. Reid B, Yang H, Melvin VS, Teketo MM, Williams T. 2011. Ectodermal Wnt/β-catenin signaling shapes the mouse face. Dev Biol 349:261-269.
73. Richman JM, Lee SH. 2003. About face: Signals and genes controlling jaw patterning and identity in vertebrates. Bioessays 25: 554-568.
74. Richtsmeier JT, Aldridge K, DeLeon VB, Panchal J, Kane AA, Marsh JL, Yan P, Cole TMIII. 2006. Phenotypic integration of neurocranium and brain. J Exp Zool B Mol Dev Evol 306: 360-378.
75. Richtsmeier JT, Deleon VB. 2009. Morphological integration of the skull in craniofacial anomalies. Orthod Craniofac Res 12: 149-158.
76. Rosen V. 2006. BMP and BMP inhibitors in bone. Ann NY Acad Sci 1068: 19-25.
77. Ross C, Henneberg M. 1995. Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. Am J Phys Anthropol 98: 575-593.
78. Ross CF, Ravosa MJ. 1993. Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am J Phys Anthropol 91: 305-324.
79. Ruiz i Altaba A. 1997. Catching a Gli-mpse of Hedgehog. Cell 90: 193-196.
80. Saha K, Schaffer DV. 2006. Signal dynamics in Sonic hedgehog tissue patterning. Development 133: 889-900.
81. Schneider RA, Helms JA. 2003. The cellular and molecular origins of beak morphology. Science 299: 565-568.
82. Schneider RA, Hu D, Rubenstein JL, Maden M, Helms JA. 2001. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128: 2755-2767.
83. Seppala M, Depew MJ, Martinelli DC, Fan CM, Sharpe PT, Cobourne MT. 2007. Gas1 is a modifier for holoprosencephaly and genetically interacts with sonic hedgehog. J Clin Invest 117: 1575-1584.
84. Szabo-Rogers HL, Geetha-Loganathan P, Nimmagadda S, Fu KK, Richman JM. 2008. FGF signals from the nasal pit are necessary for normal facial morphogenesis. Dev Biol 318: 289-302.
85. Szabo-Rogers HL, Geetha-Loganathan P, Whiting CJ, Nimmagadda S, Fu K, Richman JM. 2009a. Novel skeletogenic patterning roles for the olfactory pit. Development 136: 219-229.
86. Szabo-Rogers HL, Smithers LE, Yakob W, Liu KJ. 2009b. New directions in craniofacial morphogenesis. Dev Biol 34: 84-94.
87. Tenzen T, Allen BL, Cole F, Kang JS, Krauss RS, McMahon AP. 2006. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev Cell 10: 647-656.
88. Tian H, Jeong J, Harfe BD, Tabin CJ, McMahon AP. 2005. Mouse Disp1 is required in sonic hedgehog-expressing cells for paracrine activity of the cholesterol-modified ligand. Development 132: 133-142.
89. Tian H, Tenzen T, McMahon AP. 2004. Dose dependency of Disp1 and genetic interaction between Disp1 and other hedgehog signaling components in the mouse. Development 131: 4021-4033.
90. Tobin JL, Di Franco M, Eichers E, May-Simera H, Garcia M, Yan J, Quinlan R, Justice MJ, Hennekam RC, Briscoe J, Tada M, Mayor R, Burns AJ, Lupski JR, Hammond P, Beales PL. 2008. Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschsprung's disease in Bardet-Biedl syndrome. Proc Natl Acad Sci USA 105: 6714-6719.
91. Welsh IC, O'Brien TP. 2009. Signaling integration in the rugae growth zone directs sequential SHH signaling center formation during the rostral outgrowth of the palate. Dev Biol 336: 53-67.
92. Wu P, Jiang TX, Shen JY, Widelitz RB, Chuong CM. 2006. Morphoregulation of avian beaks: Comparative mapping of growth zone activities and morphological evolution. Dev Dyn 235: 1400-1412.
93. Wu P, Jiang TX, Suksaweang S, Widelitz RB, Chuong CM. 2004. Molecular shaping of the beak. Science 305: 1465-1466.
94. Yamamoto Y, Byerly MS, Jackman WR, Jeffery WR. 2009. Pleiotropic functions of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution. Dev Biol 330: 200-211.
95. Young NM, Chong HJ, Hu D, Hallgrimsson B, Marcucio RS. 2010. Quantitative analyses link modulation of sonic hedgehog signaling to continuous variation in facial growth and shape. Development 137: 3405-3409.
96. Zhang W, Kang JS, Cole F, Yi MJ, Krauss RS. 2006. Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev Cell 10: 657-665.
97. Weinberg SM, Andreasen NC, Nopoulos P. 2009. J Anat 214: 926-936.