Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes

Journal of Clinical Investigation

Volumn 114, Issue 4, 2004, Pages 485-494

  Cordero, Dwight ^a,d   Marcucio, Ralph ^a   Hu, Diane ^a   Gaffield, William ^b   Tapadia, Minal ^a   Helms, Jill A ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

^c STANFORD UNIVERSITY   (United States)

^d Albert Einstein Medical College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETONE DERIVATIVE; SONIC HEDGEHOG PROTEIN; CYCLOPAMINE; TERATOGENIC AGENT; TRANSACTIVATOR PROTEIN; VERATRUM ALKALOID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIRD; CLEFT FACE; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYOTOXICITY; HOLOPROSENCEPHALY; HYPOTELORISM; HYPOTHESIS; MIDFACE HYPOPLASIA; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; CHICK EMBRYO; DOSE RESPONSE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MUTATION; PRENATAL DEVELOPMENT; TIME;

ANIMALS; APOPTOSIS; CHICK EMBRYO; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOLOPROSENCEPHALY; IN SITU HYBRIDIZATION; MUTATION; PHENOTYPE; TERATOGENS; TIME FACTORS; TRANS-ACTIVATORS; VARIATION (GENETICS); VERATRUM ALKALOIDS;

EID: 4344646698     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200419596     Document Type: Article

References (66)

1. Ming, J.E., et al. 2002. Mutations in PATCHED-1, the receptor for SONIC HEDGEHOG, are associated with holoprosencephaly. Hum. Genet. 110:297-301.
2. McKusick-Nathans Institute for Genetic Medicine, Johns Hopkins University (Baltimore, MD) and National Center for Biotechnology Information, National Library of Medicine (Bethesda, MD). 2000. Online Mendelian Inheritance in Man, OMIM. http://www.ncbi.nlm.nih.gov/omim/.
3. Muenke, M., and Beachy, P.A. 2000. Genetics of ventral forebrain development and holoprosencephaly. Curr. Opin. Genet. Dev. 10:262-269.
4. Gorlin, R.J., Cohen, M.M., and Levin, L.S. 1990. Syndromes of the head and neck. Oxford University Press. New York, New York, USA. 977 pp.
5. Roessler, E., and Muenke, M. 1999. The molecular genetics of holoprosencephaly: a model of brain development for the next century. Childs Nerv. Syst. 15:646-651.
6. Brown, S.A., et al. 1998. Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat. Genet. 20:180-183.
7. Wallis, D.E., et al. 1999. Mutations in the homeodomain of the human SIX3 gene cause holoprosencephaly. Nat. Genet. 22:196-198.
8. Gripp, K.W., et al. 2000. Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination. Nat. Genet. 25:205-208.
9. Chiang, C., et al. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 383:407-413.
10. Roessler, E., et al. 1996. Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat. Genet. 14:357-360.
11. Belloni, E., et al. 1996. Identification of Sonic hedgehog as a candidate gene in holoprosencephaly. Nat. Genet. 14:353-356.
12. Roessler, E., et al. 2003. Loss-of-function mutations in the human GLI2 gene are associated with pituitary anomalies and holoprosencephaly-like features. Proc. Natl. Acad. Sci. U. S. A. 100:13424-13429.
13. Nanni, L., et al. 1999. The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly. Hum. Mol. Genet. 8:2479-2488.
14. Ming, J.E., and Muenke, M. 2002. Multiple hits during early embryonic development: digenic diseases and holoprosencephaly. Am. J. Hum. Genet. 71:1017-1032.
15. 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.
16. Finnell, R.H., Waes, J.G., Eudy, J.D., and Rosenquist, T.H. 2002. Molecular basis of environmentally induced birth defects. Annu. Rev. Pharmacol. Toxicol. 42:181-208.
17. Cohen, M.M., Jr., and Shiota, K. 2002. Teratogenesis of holoprosencephaly. Am. J. Med. Genet. 109:1-15.
18. Barr, M., Jr., et al. 1983. Holoprosencephaly in infants of diabetic mothers. J. Pediatr. 102:565-568.
19. Lammer, E.J., et al. 1985. Retinoic acid embryopathy. N. Engl. J. Med. 313:837-841.
20. Bonnemann, C., and Meinecke, P. 1990. Holoprosencephaly as a possible embryonic alcohol effect: another observation. Am. J. Med. Genet. 37:431-432.
21. Ronen, G.M., and Andrews, W.L. 1991. Holoprosencephaly as a possible embryonic alcohol effect. Am. J. Med. Genet. 40:151-154.
22. Sulik, K.K., and Johnston, M.C. 1982. Embryonic origin of holoprosencephaly: interrelationship of the developing brain and face. Scan. Electron Microsc. Pt 1:309-322.
23. Edison, R., and Muenke, M. 2003. The interplay of genetic and environmental factors in craniofacial morphogenesis: holoprosencephaly and the role of cholesterol. Congenit. Anom. (Kyoto). 43:1-21.
24. Coventry, S., Kapur, R.P., and Siebert, J.R. 1998. Cyclopamine-induced holoprosencephaly and associated craniofacial malformations in the golden hamster: anatomic and molecular events. Pediatr. Dev. Pathol. 1:29-41.
25. Chen, J.K., Taipale, J., Cooper, M.K., and Beachy, P.A. 2002. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16:2743-2748.
26. Chen, J.K., Taipale, J., Young, K.E., Maiti, T., and Beachy, P.A. 2002. Small molecule modulation of Smoothened activity. Proc. Natl. Acad. Sci. U. S. A. 99:14071-14076.
27. Taipale, J., et al. 2000. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature. 406:1005-1009.
28. Incardona, J.P., Gaffield, W., Kapur, R.P., and Roelink, H. 1998. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development. 125:3553-3562.
29. Gunhaga, L., Jessell, T.M., and Edlund, T. 2000. Sonic hedgehog signaling at gastrula stages specifies ventral telencephalic cells in the chick embryo. Development. 127:3283-3293.
30. Keeler, R.F. 1975. Teratogenic effects of cyclopamine and jervine in rats, mice and hamsters. Proc. Soc. Exp. Biol. Med. 149:302-306.
31. Omnell, M.L., Sim, F., Keeler, R.F., Harne, L.C., and Brown, K.S. 1990. Expression of Veratrum alkaloid teratogenicity in the mouse. Teratology. 42:105-119.
32. Binns, W., Shupe, J.L., Keeler, R.F., and James, L.F. 1965. Chronologic evaluation of teratogenicity in sheep fed Veratrum californicum. J. Am. Vet. Med. Assoc. 147:839-842.
33. Bryden, M.M., and Keeler, R.F. 1973. Proceedings: Effects of alkaloids of Veratrum californicum on developing embryos. J. Anat. 116:464.
34. Bryden, M.M., Perry, C., and Keeler, R.F. 1973. Effects of alkaloids of Veratrum californicum on chick embryos. Teratology. 8:19-25.
35. Keeler, R.F., and Binns, W. 1968. Teratogenic compounds of Veratrum californicum (Durand). V. Comparison of cyclopian effects of steroidal alkaloids from the plant and structurally related compounds from other sources. Teratology. 1:5-10.
36. Keeler, R.F. 1973. Teratogenic compounds of Veratrum californicum (Durand). XIV. Limb deformities produced by cyclopamine. Proc. Soc. Exp. Biol. Med. 142:1287-1291.
37. Cooper, M.K., Porter, J.A., Young, K.E., and Beachy, P.A. 1998. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science. 280:1603-1607.
38. Ahlgren, S.C., and Bronner-Fraser, M. 1999. Inhibition of sonic hedgehog signaling in vivo results in craniofacial neural crest cell death. Curr. Biol. 9:1304-1314.
39. 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.
40. Shen, H., et al. 1997. Chicken transcription factor AP-2: cloning, expression and its role in outgrowth of facial prominences and limb buds. Dev. Biol. 188:248-266.
41. DeMyer, W. 1964. The face predicts the brain: diagnostic significance of median facial anomalies for holoprosencephaly (arhinencephaly). Pediatrics. 34:256-263.
42. Cohen, M.M.J., 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. 12:196-244.
43. Hartman, J.L., 4th, Garvik, B., and Hartwell, L. 2001. Principles for the buffering of genetic variation. Science. 291:1001-1004.
44. Scriver, C.R. 2002. Why mutation analysis does not always predict clinical consequences: explanations in the era of genomics. J. Pediatr. 140:502-506.
45. St.-Jacques, B., Hammerschmidt, M., and McMahon, A.P. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13:2072-2086.
46. Bitgood, M.J., Shen, L., and McMahon, A.P. 1996. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr. Biol. 6:298-304.
47. Pola, R., et al. 2001. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat. Med. 7:706-711.
48. Kanda, S., et al. 2003. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J. Biol. Chem. 278:8244-8249.
49. Hammerschmidt, M., Brook, A., and McMahon, A.P. 1997. The world according to hedgehog. Trends Genet. 13:14-21.
50. Nybakken, K., and Perrimon, N. 2002. Hedgehog signal transduction: recent findings. Curr. Opin. Genet. Dev. 12:503-511.
51. Helms, J.A., and Schneider, R.A. 2003. Cranial skeletal biology. Nature. 423:326-331.
52. Kenney, A.M., and Rowitch, D.H. 2000. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20:9055-9067.
53. Lai, K., Kaspar, B.K., Gage, F.H., and Schaffer, D.V. 2003. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6:21-27.
54. Ahlgren, S.C., Thakur, V., and Bronner-Fraser, M. 2002. Sonic hedgehog rescues cranial neural crest from cell death induced by ethanol exposure. Proc. Natl. Acad. Sci. U. S. A. 99:10476-10481.
55. Coumoul, X., and Deng, C.X. 2003. Roles of FGF receptors in mammalian development and congenital diseases. Birth Defects Res. Part C Embryo Today. 69:286-304.
56. ten Berge, D., et al. 2001. Prx1 and Prx2 are upstream regulators of sonic hedgehog and control cell proliferation during mandibular arch morphogenesis. Development. 128:2929-2938.
57. Bai, C.B., Stephen, D., and Joyner, A.L. 2004. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell. 6:103-115.
58. Schneider, R.A., and Helms, J.A. 2003. The cellular and molecular origins of beak morphology. Science. 299:565-568.
59. Hu, D., and Helms, J.A. 1999. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development. 126:4873-4884.
60. Sanz-Ezquerro, J.J., and Tickle, C. 2000. Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development. Development. 127:4811-4823.
61. Couly, G., Creuzet, S., Bennaceur, S., Vincent, C., and Le Douarin, N.M. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development. 129:1061-1073.
62. Muenke, M., and Cohen, M.M., Jr. 2000. Genetic approaches to understanding brain development: holoprosencephaly as a model. Ment. Retard. Dev. Disabil. Res. Rev. 6:15-21.
63. Gaffield, W., Benson, M., Lundin, R.E., and Keeler, R.F. 1986. Carbon-13 and proton nuclear magnetic resonance spectra of Veratrum alkaloids. J. Nat. Prod. 49:286-292.
64. Gaffield, W., Incardona, J.P., Kapur, R.P., and Roelink, H. 1999. A looking glass perspective: thalidomide and cyclopamine. Cell. Mol. Biol. 45:579-588.
65. Hamburger, V., and Hamilton, H.L. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88:49-92.
66. Albrecht, U.E.G., Helms, J.A., and Lin, H. 1997. Visualization of gene expression patterns by in situ hybridization. In Molecular and cellular methods in developmental toxicology. G.P. Daston, editor. CRC Press. Boca Raton, Florida, USA. 23-48.