22q11 Gene dosage establishes an adaptive range for sonic hedgehog and retinoic acid signaling during early development

Human Molecular Genetics

Volumn 22, Issue 2, 2013, Pages 300-312

  Maynard, Thomas M ^a   Gopalakrishna, Deepak ^b   Meechan, Daniel W ^a   Paronett, Elizabeth M ^a   Newbern, Jason M ^c   LaMantia, Anthony Samuel ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPAMINE; PROTEIN; RALDH2 PROTEIN; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME DELETION 22Q11; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; FEMALE; GENE DOSAGE; GENE LOSS; GENE MUTATION; GENETIC POLYMORPHISM; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL;

ADAPTATION, BIOLOGICAL; ANIMALS; BONE MORPHOGENETIC PROTEINS; DIGEORGE SYNDROME; FEMALE; FIBROBLAST GROWTH FACTORS; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; MORPHOGENESIS; NEURAL TUBE; PHENOTYPE; SIGNAL TRANSDUCTION; TRETINOIN;

ERINACEIDAE;

EID: 84871546292     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds429     Document Type: Article

References (72)

1. Shaikh, T.H., Kurahashi, H., Saitta, S.C., O'Hare, A.M., Hu, P., Roe, B.A., Driscoll, D.A., McDonald-McGinn, D.M., Zackai, E.H., Budarf, M.L. et al. (2000) Chromosome 22-specific low copy repeats and the 22q11.2 deletion syndrome: genomic organization and deletion endpoint analysis. Hum. Mol. Genet., 9, 489-501.
2. Ryan, A.K., Goodship, J.A., Wilson, D.I., Philip, N., Levy, A., Seidel, H., Schuffenhauer, S., Oechsler, H., Belohradsky, B., Prieur, M. et al. (1997) Spectrum of clinical features associated with interstitial chromosome 22q11 deletions: a European collaborative study. J. Med. Genet., 34, 798-804.
3. Shprintzen, R.J., Goldberg, R.B., Lewin, M.L., Sidoti, E.J., Berkman, M.D., Argamaso, R.V. and Young, D. (1978) A new syndrome involving cleft palate, cardiac anomalies, typical facies, and learning disabilities: velo-cardio-facial syndrome. Cleft Palate J., 15, 56-62.
4. Chaoui, R., Korner, H., Bommer, C. and Kalache, K.D. (2002) Fetal thymus and the 22q11.2 deletion. Prenat. Diagn., 22, 839-840.
5. Lindsay, E.A., Morris, M.A., Gos, A., Nestadt, G., Wolyniec, P.S., Lasseter, V.K., Shprintzen, R., Antonarakis, S.E., Baldini, A. and Pulver, A.E. (1995) Schizophrenia and chromosomal deletions within 22q11.2. Am. J. Hum. Genet., 56, 1502-1503.
6. Amati, F., Conti, E., Novelli, A., Bengala, M., Diglio, M.C., Marino, B., Giannotti, A., Gabrielli, O., Novelli, G. and Dallapiccola, B. (1999) Atypical deletions suggest five 22q11.2 critical regions related to the DiGeorge/velo-cardio-facial syndrome. Eur. J. Hum. Genet., 7, 903-909.
7. Fernandez, L., Nevado, J., Santos, F., Heine-Suner, D., Martinez-Glez, V., Garcia-Minaur, S., Palomo, R., Delicado, A., Pajares, I.L., Palomares, M. et al. (2009) A deletion and a duplication in distal 22q11.2 deletion syndrome region. Clinical implications and review. BMC Med. Genet., 10, 48.
8. LaMantia, A.S. (1999) Forebrain induction, retinoic acid, and vulnerability to schizophrenia: insights from molecular and genetic analysis in developing mice. Biol. Psychiatry, 46, 19-30.
9. Meechan, D.W., Tucker, E.S., Maynard, T.M. and LaMantia, A.S. (2009) Diminished dosage of 22q11 genes disrupts neurogenesis and cortical development in a mouse model of 22q11 deletion/DiGeorge syndrome. Proc. Natl Acad. Sci. USA, 106, 16434-16445.
10. Meechan, D.W., Maynard, T.M., Wu, Y., Gopalakrishna, D., Lieberman, J.A. and LaMantia, A.S. (2006) Gene dosage in the developing and adult brain in a mouse model of 22q11 deletion syndrome. Mol. Cell. Neurosci., 33, 412-428.
11. Maynard, T.M., Haskell, G.T., Peters, A.Z., Sikich, L., Lieberman, J.A. and LaMantia, A.S. (2003) A comprehensive analysis of 22q11 gene expression in the developing and adult brain. Proc. Natl Acad. Sci. USA, 100, 14433-14438.
12. Frank, D.U., Fotheringham, L.K., Brewer, J.A., Muglia, L.J., Tristani-Firouzi, M., Capecchi, M.R. and Moon, A.M. (2002) An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development, 129, 4591-4603.
13. Vermot, J., Niederreither, K., Garnier, J.M., Chambon, P. and Dolle, P. (2003) Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc. Natl Acad. Sci. USA, 100, 1763-1768.
14. Washington Smoak, I., Byrd, N.A., Abu-Issa, R., Goddeeris, M.M., Anderson, R., Morris, J., Yamamura, K., Klingensmith, J. and Meyers, E.N. (2005) Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev. Biol., 283, 357-372.
15. Bachiller, D., Klingensmith, J., Shneyder, N., Tran, U., Anderson, R., Rossant, J. and De Robertis, E.M. (2003) The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome. Development, 130, 3567-3578.
16. Garg, V., Yamagishi, C., Hu, T., Kathiriya, I.S., Yamagishi, H. and Srivastava, D. (2001) Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol., 235, 62-73.
17. Zhang, L., Zhong, T., Wang, Y., Jiang, Q., Song, H. and Gui, Y. (2006) TBX1, a DiGeorge syndrome candidate gene, is inhibited by retinoic acid. Int. J. Dev. Biol., 50, 55-61.
18. Guris, D.L., Duester, G., Papaioannou, V.E. and Imamoto, A. (2006) Dose-dependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome. Dev. Cell, 10, 81-92.
19. Arnold, J.S., Werling, U., Braunstein, E.M., Liao, J., Nowotschin, S., Edelmann, W., Hebert, J.M. and Morrow, B.E. (2006) Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development, 133, 977-987.
20. Braunstein, E.M., Monks, D.C., Aggarwal, V.S., Arnold, J.S. and Morrow, B.E. (2009) Tbx1 and Brn4 regulate retinoic acid metabolic genes during cochlear morphogenesis. BMC Dev. Biol., 9, 31.
21. Guo, T., McDonald-McGinn, D., Blonska, A., Shanske, A., Bassett, A.S., Chow, E., Bowser, M., Sheridan, M., Beemer, F., Devriendt, K. et al. (2011) Genotype and cardiovascular phenotype correlations with TBX1 in 1,022 velo-cardio-facial/DiGeorge/22q11.2 deletion syndrome patients. Hum. Mutat., 32, 1278-1289.
22. Randall, V., McCue, K., Roberts, C., Kyriakopoulou, V., Beddow, S., Barrett, A.N., Vitelli, F., Prescott, K., Shaw-Smith, C., Devriendt, K. et al. (2009) Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J. Clin. Invest., 119, 3301-3310.
23. Vitelli, F., Morishima, M., Taddei, I., Lindsay, E.A. and Baldini, A. (2002) Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet., 11, 915-922.
24. Rauch, R., Hofbeck, M., Zweier, C., Koch, A., Zink, S., Trautmann, U., Hoyer, J., Kaulitz, R., Singer, H. and Rauch, A. (2010) Comprehensive genotype-phenotype analysis in 230 patients with tetralogy of Fallot. J. Med. Genet., 47, 321-331.
25. Yagi, H., Furutani, Y., Hamada, H., Sasaki, T., Asakawa, S., Minoshima, S., Ichida, F., Joo, K., Kimura, M., Imamura, S. et al. (2003) Role of TBX1 in human del22q11.2 syndrome. Lancet, 362, 1366-1373.
26. Jerome, L.A. and Papaioannou, V.E. (2001) DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet., 27, 286-291.
27. Funke, B.H., Lencz, T., Finn, C.T., DeRosse, P., Poznik, G.D., Plocik, A.M., Kane, J., Rogus, J., Malhotra, A.K. and Kucherlapati, R. (2007) Analysis of TBX1 variation in patients with psychotic and affective disorders. Mol. Med., 13, 407-414.
28. Paylor, R., Glaser, B., Mupo, A., Ataliotis, P., Spencer, C., Sobotka, A., Sparks, C., Choi, C.H., Oghalai, J., Curran, S. et al. (2006) Tbx1 haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22q11 deletion syndrome. Proc. Natl Acad. Sci. USA, 103, 7729-7734.
29. Torres-Juan, L., Rosell, J., Morla, M., Vidal-Pou, C., Garcia-Algas, F., de la Fuente, M.A., Juan, M., Tubau, A., Bachiller, D., Bernues, M. et al. (2007) Mutations in TBX1 genocopy the 22q11.2 deletion and duplication syndromes: a new susceptibility factor for mental retardation. Eur. J. Hum. Genet., 15, 658-663.
30. Merscher, S., Funke, B., Epstein, J.A., Heyer, J., Puech, A., Lu, M.M., Xavier, R.J., Demay, M.B., Russell, R.G., Factor, S. et al. (2001) TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell, 104, 619-629.
31. Liao, J., Kochilas, L., Nowotschin, S., Arnold, J.S., Aggarwal, V.S., Epstein, J.A., Brown, M.C., Adams, J. and Morrow, B.E. (2004) Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet., 13, 1577-1585.
32. Lania, G., Zhang, Z., Huynh, T., Caprio, C., Moon, A.M., Vitelli, F. and Baldini, A. (2009) Early thyroid development requires a Tbx1-Fgf8 pathway. Dev. Biol., 328, 109-117.
33. Roberts, C., Ivins, S., Cook, A.C., Baldini, A. and Scambler, P.J. (2006) Cyp26 genes a1, b1 and c1 are down-regulated in Tbx1 null mice and inhibition of Cyp26 enzyme function produces a phenocopy of DiGeorge Syndrome in the chick. Hum. Mol. Genet., 15, 3394-3410.
34. Passman, J.N., Dong, X.R., Wu, S.P., Maguire, C.T., Hogan, K.A., Bautch, V.L. and Majesky, M.W. (2008) A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc. Natl Acad. Sci. USA, 105, 9349-9354.
35. Balkan, W., Colbert, M., Bock, C. and Linney, E. (1992) Transgenic indicator mice for studying activated retinoic acid receptors during development. Proc. Natl Acad. Sci. USA, 89, 3347-3351.
36. Miletich, I., Yu, W.Y., Zhang, R., Yang, K., Caixeta de Andrade, S., Pereira, S.F., Ohazama, A., Mock, O.B., Buchner, G., Sealby, J. et al. (2011) Developmental stalling and organ-autonomous regulation of morphogenesis. Proc. Natl Acad. Sci. USA, 108, 19270-19275.
37. Salazar-Ciudad, I. and Jernvall, J. (2010) A computational model of teeth and the developmental origins of morphological variation. Nature, 464, 583-586.
38. Lipinski, R.J., Hutson, P.R., Hannam, P.W., Nydza, R.J., Washington, I.M., Moore, R.W., Girdaukas, G.G., Peterson, R.E. and Bushman, W. (2008) Dose- and route-dependent teratogenicity, toxicity, and pharmacokinetic profiles of the hedgehog signaling antagonist cyclopamine in the mouse. Toxicol. Sci., 104, 189-197.
39. Mukai, J., Liu, H., Burt, R.A., Swor, D.E., Lai, W.S., Karayiorgou, M. and Gogos, J.A. (2004) Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat. Genet., 36, 725-731.
40. Baines, M.G., Duclos, A.J., de Fougerolles, A.R. and Gendron, R.L. (1996) Immunological prevention of spontaneous early embryo resorption is mediated by non-specific immunosimulation. Am. J. Reprod. Immunol., 35, 34-42.
41. Duclos, A.J., Haddad, E.K. and Baines, M.G. (1995) Presence of activated macrophages in a murine model of early embryo loss. Am. J. Reprod. Immunol., 33, 354-366.
42. 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.
43. Schimmang, T., Lemaistre, M., Vortkamp, A. and Ruther, U. (1992) Expression of the zinc finger gene Gli3 is affected in the morphogenetic mouse mutant extra-toes (Xt). Development, 116, 799-804.
44. Katoh, Y. and Katoh, M. (2009) Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr. Mol. Med., 9, 873-886.
45. Blaess, S., Corrales, J.D. and Joyner, A.L. (2006) Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development, 133, 1799-1809.
46. Niederreither, K., Vermot, J., Messaddeq, N., Schuhbaur, B., Chambon, P. and Dolle, P. (2001) Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development, 128, 1019-1031.
47. Nickel, R.E. and Magenis, R.E. (1996) Neural tube defects and deletions of 22q11. Am. J. Med. Genet., 66, 25-27.
48. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet., 21, 444-448.
49. Sulik, K.K., Cook, C.S. and Webster, W.S. (1988) Teratogens and craniofacial malformations: relationships to cell death. Development, 103 (suppl.), 213-231.
50. Johnston, M.C. and Bronsky, P.T. (1991) Animal models for human craniofacial malformations. J. Craniofac. Genet. Dev. Biol., 11, 277-291.
51. Roberts, C., Ivins, S.M., James, C.T. and Scambler, P.J. (2005) Retinoic acid down-regulates Tbx1 expression in vivo and in vitro. Dev. Dyn., 232, 928-938.
52. Bhasin, N., Maynard, T.M., Gallagher, P.A. and LaMantia, A.S. (2003) Mesenchymal/epithelial regulation of retinoic acid signaling in the olfactory placode. Dev. Biol., 261, 82-98.
53. Bockman, D.E., Redmond, M.E. and Kirby, M.L. (1989) Alteration of early vascular development after ablation of cranial neural crest. Anat. Rec., 225, 209-217.
54. Goddeeris, M.M., Schwartz, R., Klingensmith, J. and Meyers, E.N. (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development, 134, 1593-1604.
55. Dyer, L.A. and Kirby, M.L. (2009) Sonic hedgehog maintains proliferation in secondary heart field progenitors and is required for normal arterial pole formation. Dev. Biol., 330, 305-317.
56. Roberts, C., Sutherland, H.F., Farmer, H., Kimber, W., Halford, S., Carey, A., Brickman, J.M., Wynshaw-Boris, A. and Scambler, P.J. (2002) Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol. Cell. Biol., 22, 2318-2328.
57. Fuccillo, M., Joyner, A.L. and Fishell, G. (2006) Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat. Rev. Neurosci., 7, 772-783.
58. Mao, J., Kim, B.M., Rajurkar, M., Shivdasani, R.A. and McMahon, A.P. (2010) Hedgehog signaling controls mesenchymal growth in the developing mammalian digestive tract. Development, 137, 1721-1729.
59. Rhinn, M. and Dolle, P. (2012) Retinoic acid signalling during development. Development, 139, 843-858.
60. Lohnes, D., Mark, M., Mendelsohn, C., Dolle, P., Dierich, A., Gorry, P., Gansmuller, A. and Chambon, P. (1994) Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development, 120, 2723-2748.
61. Vaessen, M.J., Kootwijk, E., Mummery, C., Hilkens, J., Bootsma, D. and van Kessel, A.G. (1989) Preferential expression of cellular retinoic acid binding protein in a subpopulation of neural cells in the developing mouse embryo. Differentiation, 40, 99-105.
62. LaMantia, A.S., Colbert, M.C. and Linney, E. (1993) Retinoic acid induction and regional differentiation prefigure olfactory pathway formation in the mammalian forebrain. Neuron, 10, 1035-1048.
63. Sakai, Y., Meno, C., Fujii, H., Nishino, J., Shiratori, H., Saijoh, Y., Rossant, J. and Hamada, H. (2001) The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes. Dev., 15, 213-225.
64. Li, P., Pashmforoush, M. and Sucov, H.M. (2010) Retinoic acid regulates differentiation of the secondary heart field and TGFbeta-mediated outflow tract septation. Dev. Cell, 18, 480-485.
65. Soprano, D.R. and Soprano, K.J. (1995) Retinoids as teratogens. Annu. Rev. Nutr., 15, 111-132.
66. Caterino, M., Ruoppolo, M., Fulcoli, G., Huynth, T., Orru, S., Baldini, A. and Salvatore, F. (2009) Transcription factor TBX1 overexpression induces downregulation of proteins involved in retinoic acid metabolism: a comparative proteomic analysis. J. Proteome. Res., 8, 1515-1526.
67. Ribes, V., Wang, Z., Dolle, P. and Niederreither, K. (2006) Retinaldehyde dehydrogenase 2 (RALDH2)-mediated retinoic acid synthesis regulates early mouse embryonic forebrain development by controlling FGF and sonic hedgehog signaling. Development, 133, 351-361.
68. Ryckebusch, L., Wang, Z., Bertrand, N., Lin, S.C., Chi, X., Schwartz, R., Zaffran, S. and Niederreither, K. (2008) Retinoic acid deficiency alters second heart field formation. Proc. Natl Acad. Sci. USA, 105, 2913-2918.
69. Lo-Castro, A., Galasso, C., Cerminara, C., El-Malhany, N., Benedetti, S., Nardone, A.M. and Curatolo, P. (2009) Association of syndromic mental retardation and autism with 22q11.2 duplication. Neuropediatrics, 40, 137-140.
70. Portnoi, M.F. (2009) Microduplication 22q11.2: a new chromosomal syndrome. Eur. J. Med. Genet., 52, 88-93.
71. Cooper, M.K., Wassif, C.A., Krakowiak, P.A., Taipale, J., Gong, R., Kelley, R.I., Porter, F.D. and Beachy, P.A. (2003) A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat. Genet., 33, 508-513.
72. Lammer, E.J., Chen, D.T., Hoar, R.M., Agnish, N.D., Benke, P.J., Braun, J.T., Curry, C.J., Fernhoff, P.M., Grix, A.W. Jr., Lott, I.T. et al. (1985) Retinoic acid embryopathy. N. Engl. J. Med., 313, 837-841.