Boc modifies the holoprosencephaly spectrum of Cdo mutant mice

DMM Disease Models and Mechanisms

Volumn 4, Issue 3, 2011, Pages 368-380

  Zhang, Wei ^a,c   Hong, Mingi ^a   Bae, Gyu Un ^a,b   Kang, Jong Sun ^b   Krauss, Robert S ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Sungkyunkwan University School of Medicine   (South Korea)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; DEVELOPMENTAL STAGE; DISEASE SEVERITY; EMBRYO; EVOLUTION; FEMALE; GENE EXPRESSION; GENE TARGETING; HOLOPROSENCEPHALY; MALE; MAMMAL; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BONE DEVELOPMENT; CELL ADHESION MOLECULES; EMBRYO, MAMMALIAN; EXTREMITIES; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOLOPROSENCEPHALY; HUMANS; IMMUNOGLOBULIN G; MICE; MICE, MUTANT STRAINS; PALATE; PHENOTYPE; POLYMERASE CHAIN REACTION; PROSENCEPHALON; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

ERINACEIDAE; HEXAPODA; MAMMALIA; MUS;

EID: 79956110764     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.005744     Document Type: Article

References (58)

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. Aoto, K., Nishimura, T., Eto, K. and Motoyama, J. (2002). Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev. Biol. 251, 320-332.
3. Aoto, K., Shikata, Y., Imai, H., Matsumaru, D., Tokunaga, T., Shioda, S., Yamada, G. and Motoyama, J. (2009). Mouse Shh is required for prechordal plate maintenance during brain and craniofacial morphogenesis. Dev. Biol. 327, 106-120.
4. Camp, D., Currie, K., Labbé, A., van Meyel, D. J. and Charron, F. (2010). Ihog and Boi are essential for Hedgehog signaling in Drosophila. Neural Dev. 5, 28.
5. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
6. Cohen, M. M., Jr (1989). Perspectives on holoprosencephaly: Part I. Epidemiology, genetics, and syndromology. Teratology 40, 211-235.
7. Cohen, M. M., Jr (2006). Holoprosencephaly: clinical, anatomic, and molecular dimensions. Birth Defects Res. Part A Clin. Mol. Teratol. 76, 658-673.
8. Cohen, M. M., Jr and Shiota, K. (2002). Teratogenesis of holoprosencephaly. Am. J. Med. Genet. 109, 1-15.
9. Cole, F. and Krauss, R. S. (2003). Microform holoprosencephaly in mice that lack the Ig superfamily member Cdon. Curr. Biol. 13, 411-415.
10. 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.
11. Domené, S., Roessler, E., El-Jaick, K. B., Snir, M., Brown, J. L., Vélez, J. I., Bale, S., Lacbawan, F., Muenke, M. and Feldman, B. (2008). Mutations in the human SIX3 gene in holoprosencephaly are loss of function. Hum. Mol. Genet. 17, 3919-3928.
12. Dubourg, C., Bendavid, C., Pasquier, L., Henry, C., Odent, S. and David, V. (2007). Holoprosencephaly. Orphanet. J. Rare Dis. 2, 8.
13. Fernandes, M. and Hébert, J. M. (2008). The ups and downs of holoprosencephaly: dorsal versus ventral patterning forces. Clin. Genet. 73, 413-423.
14. Geng, X. and Oliver, G. (2009). Pathogenesis of holoprosencephaly. J. Clin. Invest. 119, 1403-1413.
15. Geng, X., Speirs, C., Lagutin, O., Inbal, A., Liu, W., Solnica-Krezel, L., Jeong, Y., Epstein, D. J. and Oliver, G. (2008). Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev. Cell 15, 236-247.
16. Gritli-Linde, A. (2008). The etiopathogenesis of cleft lip and cleft palate usefulness and caveats of mouse models. Curr. Top. Dev. Biol. 84, 37-138.
17. Gutin, G., Fernandes, M., Palazzolo, L., Paek, H., Yu, K., Ornitz, D. M., McConnell, S. K. and Hebert, J. M. (2006). FGF signalling generates ventral telencephalic cells independently of SHH. Development 133, 2937-2946.
18. Hébert, J. M. and Fishell, G. (2008). The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9, 678-685.
19. Helms, J. A., Cordero, D. and Tapadia, M. D. (2005). New insights into craniofacial morphogenesis. Development 132, 851-861.
20. Hu, D. and Helms, J. A. (1999). The role of Sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development 126, 4873-4884.
21. 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.
22. Ingham, P. W. and McMahon, A. P. (2009). Hedgehog signalling: Kif7 is not that fishy after all. Curr. Biol. 19, R729-R731.
23. Jeong, J. and McMahon, A. P. (2005). Growth and pattern of the mammalian neural tube are governed by partially overlapping feedback activities of the hedgehog antagonists patched 1 and Hhip1. Development 132, 143-154. (Pubitemid 40207974)
24. Jiang, J. and Hui, C. C. (2008). Hedgehog signaling in development and cancer. Dev. Cell 15, 801-812.
25. Kang, J. S., Zhang, W. and Krauss, R. S. (2007). Hedgehog signaling: cooking with Gas1. Sci. STKE 403, pe50.
26. Kiecker, C. and Niehrs, C. (2001). The role of prechordal mesendoderm in neural patterning. Curr. Opin. Neurobiol. 11, 27-33.
27. Krauss, R. S. (2007). Holoprosencephaly: new models, new insights. Expert Rev. Mol. Med. 9, 1-17.
28. Lan, Y. and Jiang, R. (2009). Sonic hedgehog signaling regulates reciprocal epithelialmesenchymal interactions controlling palatal outgrowth. Development 136, 1387-1396.
29. Marcucio, R. S., Cordero, D. R., Hu, D. and Helms, J. A. (2005). Molecular interactions coordinating the development of the forebrain and face. Dev. Biol. 284, 48-61.
30. Martinelli, D. C. and Fan, C. M. (2007). Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev. 21, 1231-1243.
31. McLellan, J. S., Yao, S., Zheng, X., Geisbrecht, B. V., Ghirlando, R., Beachy, P. A. and Leahy, D. J. (2006). Structure of a heparin-dependent complex of Hedgehog and Ihog. Proc. Natl. Acad. Sci. USA 103, 17208-17213.
32. McLellan, J. S., Zheng, X., Hauk, G., Ghirlando, R., Beachy, P. A. and Leahy, D. J. (2008). The mode of Hedgehog binding to Ihog homologues is not conserved across different phyla. Nature 455, 979-983.
33. 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.
34. Ming, J. E. and Muenke, M. (2002). Multiple hits during early embryonic development: digenic diseases and holoprosencephaly. Am. J. Hum. Genet. 71, 1017-1032.
35. Muenke, M. and Beachy, P. A. (2000). Genetics of ventral forebrain development and holoprosencephaly. Curr. Opin. Genet. Dev. 10, 262-269.
36. Muenke, M. and Beachy, P. A. (2001). Holoprosencephaly. In The Metabolic and Molecular Bases of Inherited Disease, Vol. IV (ed. C. R. Scriver, A. L. Beaudet, W. S. Sly and D. Valle), pp. 6203-6230. New York: McGraw-Hill.
37. Mulieri, P. J., Okada, A., Sassoon, D. A., McConnell, S. K. and Krauss, R. S. (2000). Developmental expression pattern of the cdo gene. Dev. Dyn. 219, 40-49.
38. Mulieri, P. M., Kang, J.-S., Sassoon, D. A. and Krauss, R. S. (2002). Expression of the boc gene during murine embryogenesis. Dev. Dyn. 223, 379-388.
39. Ohkubo, Y., Chiang, C. and Rubenstein, J. L. (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.
40. Okada, A., Charron, F., Morin, S., Shin, D. S., Wong, K., Fabre, P. J., Tessier-Lavigne, M. and McConnell, S. K. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
41. Okada, T., Okumura, Y., Motoyama, J. and Ogawa, M. (2008). FGF8 signaling patterns the telencephalic midline by regulating putative key factors of midline development. Dev. Biol. 320, 92-101.
42. Petryk, A., Anderson, R. M., Jarcho, M. P., Leaf, I., Carlson, C. S., Klingensmith, J., Shawlot, W. and O'Connor, M. B. (2004). The mammalian twisted gastrulation gene functions in foregut and craniofacial development. Dev. Biol. 267, 374-386.
43. Rice, R., Spencer-Dene, B., Connor, E. C., Gritli-Linde, A., McMahon, A. P., Dickson, C., Thesleff, I. and Rice, D. P. (2004). Disruption of Fgf10/Fgfr2b-coordinated epithelial-mesenchymal interactions causes cleft palate. J. Clin. Invest. 113, 1692-1700.
44. Roessler, E., El-Jaick, K. B., Dubourg, C., Vélez, J. I., Solomon, B. D., Pineda-Alvarez, D. E., Lacbawan, F., Zhou, N., Ouspenskaia, M., Paulussen, A. et al. (2009a). The mutational spectrum of holoprosencephaly- associated changes within the SHH gene in humans predicts loss-of-function through either key structural alterations of the ligand or its altered synthesis. Hum. Mutat. 30, E921-E935.
45. Roessler, E., Lacbawan, F., Dubourg, C., Paulussen, A., Herbergs, J., Hehr, U., Bendavid, C., Zhou, N., Ouspenskaia, M., Bale, S. et al. (2009b). The full spectrum of holoprosencephaly-associated mutations within the ZIC2 gene in humans predicts loss-of-function as the predominant disease mechanism. Hum. Mutat. 30, E541-E554.
46. Roessler, E., Pei, W., Ouspenskaia, M. V., Karkera, J. D., Veléz, J. I., Banerjee-Basu, S., Gibney, G., Lupo, P. J., Mitchell, L. E., Towbin, J. A. et al. (2009c). Cumulative ligand activity of NODAL mutations and modifiers are linked to human heart defects and holoprosencephaly. Mol. Genet. Metab. 98, 225-234.
47. Rubenstein, J. L. and Beachy, P. A. (1998). Patterning of the embryonic forebrain. Curr. Opin. Neurobiol. 8, 18-26.
48. Singh, S., Tokhunts, R., Baubet, V., Goetz, J. A., Huang, Z. J., Schilling, N. S., Black, K. E., MacKenzie, T. A., Dahmane, N. and Robbins, D. J. (2009). Sonic hedgehog mutations identified in holoprosencephaly patients can act in a dominant negative manner. Hum. Genet. 125, 95-103.
49. Spandidos, A., Wang, X., Wang, H. and Seed, B. (2010). PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 38, D792-D799.
50. Storm, E. E., Garel, S., Borello, U., Hebert, J. M., Martinez, S., McConnell, S. K., Martin, G. R. and Rubenstein, J. L. (2006). Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133, 1831-1844.
51. 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.
52. Varjosalo, M. and Taipale, J. (2008). Hedgehog: functions and mechanisms. Genes Dev. 22, 2454-2472.
53. Wilson, S. W. and Houart, C. (2004). Early steps in the development of the forebrain. Dev. Cell 6, 167-181. (Pubitemid 38190359)
54. Yamada, S., Uwabe, C., Fujii, S. and Shiota, K. (2004). Phenotypic variability in human embryonic holoprosencephaly in the Kyoto Collection. Birth Defects Res. Part A Clin. Mol. Teratol. 70, 495-508.
55. Yao, S., Lum, L. and Beachy, P. (2006). The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell 125, 343-357.
56. 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.
57. Zhang, Y., Rath, N., Hannenhalli, S., Wang, Z., Cappola, T., Kimura, S., Atochina-Vasserman, E., Lu, M. M., Beers, M. F. and Morrisey, E. E. (2007). GATA and Nkx factors synergistically regulate tissue-specific gene expression and development in vivo. Development 134, 189-198.
58. Zheng, X., Mann, R. K., Sever, N. and Beachy, P. A. (2010). Genetic and biochemical definition of the Hedgehog receptor. Genes Dev. 24, 57-71.