Quantitative analyses link modulation of sonic hedgehog signaling to continuous variation in facial growth and shape

Development

Volumn 137, Issue 20, 2010, Pages 3405-3409

  Young, Nathan M ^a   Chong, H Jonathan ^b   Hu, Diane ^a   Hallgrímsson, Benedikt ^c   Marcucio, Ralph S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Cell signaling; Chick; Cranial neural crest cells; Geometric morphometrics; Population variation

Indexed keywords

SONIC HEDGEHOG PROTEIN; PRIMER DNA;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MORPHOLOGY; EMBRYO; EXPERIMENTAL STUDY; FACE; FACE GROWTH; GENE EXPRESSION; MAXILLA; MITOSIS; MODULATION; NONHUMAN; NONLINEAR SYSTEM; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE GENETICS; SIGNAL TRANSDUCTION; TISSUE GROWTH; ANIMAL; CELL PROLIFERATION; CHICK EMBRYO; EMBRYOLOGY; FACIAL BONE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MORPHOMETRICS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ERINACEIDAE; VERTEBRATA;

ANIMALS; BODY WEIGHTS AND MEASURES; CELL PROLIFERATION; CHICK EMBRYO; DNA PRIMERS; FACIAL BONES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77957666583     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.052340     Document Type: Article

References (38)

1. Allen, B. L., Tenzen, T. and McMahon, A. P. (2007). The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 21, 1244-1257. (Pubitemid 46789881)
2. Balk, K. and Biesecker, L. G. (2008). The clinical atlas of Greig cephalopolysyndactyly syndrome. Am. J. Med. Genet. 146A, 548-557.
3. Bookstein, F. L. (1996). Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press.
4. Boughner, J. C., Wat, S., Diewert, V. M., Young, N. M., Browder, L. W. and Hallgrímsson, B. (2008). Short-faced mice and the developmental interactions between the brain and the face. J. Anat. 213, 646-662.
5. Cohen, M. M. and Sulik, K. K. (1992). Perspectives on holoprosencephaly, Part II: Central nervous system, craniofacial anatomy, syndrome commentary, diagnostic approach, and experimental studies. J. Craniofac. Genet. Dev. Biol. 12, 196-224.
6. Cooper, W. J. and Albertson, R. C. (2008). Quantification and variation in experimental studies of morphogenesis. Dev. Biol. 321, 295-302.
7. Cordero, D., Marcucio, R., Hu, D., Gaffield, W., Tapadia, M. and Helms, J. A. (2004). Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes. J. Clin. Invest. 114, 485-494.
8. DeMeyer, W. E., Zeman, W. and Palmer, C. G. (1964). The face predicts the brain: diagnostic significance of median facial anomalies for holoprosencephaly (arhinencephaly). Pediatrics 34, 256-263.
9. Dipple, K. M. and McCabe, E. R. (2000). Phenotypes of patients with 'simple' Mendelian disorders are complex traits: thresholds, modifiers, and systems dynamics. Am. J. Hum. Genet. 66, 1729-1735.
10. Eldar, A., Rosin, D., Shilo, B. Z. and Naama, B. (2003). Self-enhanced ligand degradation underlies robustness of morphogen gradients. Dev. Cell 5, 635-646.
11. Etheridge, L. A., Crawford, T. Q., Zhang, S. and Roelink, H. (2010). Evidence for a role of vertebrate Disp1 in long-range Shh signaling. Development 137, 133-140.
12. Hardy, J. and Singleton, A. (2009). Genomewide association studies and human disease. New Engl. J. Med. 360, 1759-1768.
13. Hooper, J. E. and Scott, M. P. (2005). Communicating with Hedgehogs. Nat. Rev. Mol. Cell. Biol. 6, 306-317.
14. Hu, D. and Marcucio, R. S. (2009). A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136, 107-116.
15. 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.
16. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
17. Lai, K., Robertson, M. J. and Schaffer, D. V. (2004). The sonic hedgehog signaling system as a bistable genetic switch. Biophys. J. 86, 2748-2757.
18. Manolio, T. A., Brooks, L. D. and Collins, F. S. (2009). A HapMap harvest of insights into the genetics of common disease. J. Clin. Invest. 118, 1590-1605.
19. Marcucio, R. S., Cordero, D. and Helms, J. A. (2005). Molecular interactions coordinating the development of the forebrain and face. Dev. Biol. 284, 48-61.
20. McMahon, A. P., Ingham, P. W. and Tabin, C. J. (2003). Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53, 1-114. (Pubitemid 137639458)
21. Ming, J. E. and Muenke, M. (2002). Multiple hits during early embryonic development: digenic diseases and holoprosencephaly. Am. J. Hum. Genet. 71, 1017-1032.
22. Muenke, M. and Beachy, P. A. (2000). Genetics of ventral forebrain development and holoprosencephaly. Curr. Opin. Genet. Dev. 10, 262-269.
23. Muenke, M. and Cohen, M. M. (2000). Genetic approaches to understanding brain development: holoprosencephaly as a model. Ment. Retard. Dev. Disab. Res. Rev. 6, 15-21.
24. Oates, A. C., Gorfinkiel, N., Gozález-Gaitán, M. and Heisenberg, C. P. (2009). Quantitative approaches in developmental biology. Nat. Rev. Genet. 10, 517-530.
25. Parsons, T. E., Kristensen, E., Hornung, L., Diewert, V. M., Boyd, S. K., German, R. Z. and Hallgrímsson, B. (2008). Phenotypic variability and craniofacial dysmorphology: increased shape variance in a mouse model for cleft lip. J. Anat. 212, 135-143.
26. Saha, K. and Schaffer, D. V. (2006). Signal dynamics in Sonic hedgehog tissue patterning. Development 133, 1411-1411.
27. Seppala, M., Depew, M. J., Martinelli, D. C., Fan, C. M., Sharpe, P. T. and Cobourne, M. T. (2007). Gas1 is a modifier for holoprosencephaly and genetically interacts with sonic hedgehog. J. Clin. Invest. 117, 1575-1584.
28. Taipale, J., Cooper, M. K., Maiti, T. and Beachy, P. A. (2002). Patched acts catalytically to suppress the activity of Smoothened. Nature 418, 892-897.
29. Tenzen, T., Allen, B. L., Cole, F., Kang, J. S., Krauss, R. S. and McMahon, A. P. (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.
30. Tian, H., Tenzen, T. and McMahon, A. P. (2004). Dose dependency of Disp1 and other hedgehog signaling components in the mouse. Development 131, 4021-4033.
31. Tian, H., Jeong, J., Harfe, B. D., Tabin, C. J. and McMahon, A. P. (2005). Mouse Disp1 is required in sonic hedgehog-expressing cells for paracrine activity of the cholesterol-modified ligand. Development 132, 133-142. (Pubitemid 40207973)
32. Tobin, J. L., Di Franco, M., Eichers, E., May-Simera, H., Garcia, M., Yan, J., Qunlan, R., Justice, M. J., Hennekam, R. C., Briscoe, J. et al. (2008). Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschprung's disease in Bardet-Biedl syndrome. Proc. Natl. Acad. Sci. USA 105, 6714-6719.
33. Ulloa, F. and Briscoe, J. (2007). Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6, 2640-2649.
34. Wiley, D. F., Amenta, N., Alacantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., Harcourt-Smith, W., Rohlf, F. J., St. John, K. and Hamann, B. (2005). Evolutionary Morphing. In Proceedings of IEEE Visualization 2005. Minneapolis, MN: IDAV.
35. Yamamoto, Y., Byerly, M. S., Jackman, W. R. and Jeffery, W. R. (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.
36. Young, N. M., Wat, S., Diewert, V. M., Browder, L. W. and Hallgrímsson, B. (2007). Comparative morphometrics of embryonic facial morphogenesis: implications for cleft-lip etiology. Anat. Rec. 290, 123-139.
37. Zelditch, M. L., Swiderski, D. L., Sheets, H. D. and Fink, W. L. (2004). Geometric Morphometrics for Biologists: a Primer. New York: Academic Press.
38. Zhang, W., Kang, J. S., Cole, F., Yi, M. J. and Krauss, R. S. (2006). Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev. Cell 10, 657-665.