MOZ Regulates the Tbx1 Locus, and Moz Mutation Partially Phenocopies DiGeorge Syndrome

Developmental Cell

Volumn 23, Issue 3, 2012, Pages 652-663

  Voss, Anne K ^a,b   Vanyai, Hannah K ^a,b   Collin, Caitlin ^a   Dixon, Mathew P ^a   McLennan, Tamara J ^a   Sheikh, Bilal N ^a,b   Scambler, Peter ^c   Thomas, Tim ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRK LIKE PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE MOZ; HISTONE H3; MESSENGER RNA; RETINOIC ACID; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXC1; TRANSCRIPTION FACTOR FOXC2; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR PITX2; TRANSCRIPTION FACTOR TBX1; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIGEORGE SYNDROME; EMBRYO; GENE INTERACTION; GENE LOCUS; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; HEART DEVELOPMENT; HISTONE ACETYLATION; HISTONE MODIFICATION; HOMOZYGOSITY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; DIGEORGE SYNDROME; HISTONE ACETYLTRANSFERASES; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; MUTATION; PHENOTYPE; T-BOX DOMAIN PROTEINS;

MUS;

EID: 84866025303     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.07.010     Document Type: Article

References (51)

1. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001, 410:120-124.
2. Borrow J., Stanton V.P., Andresen J.M., Becher R., Behm F.G., Chaganti R.S., Civin C.I., Disteche C., Dubé I., Frischauf A.M., et al. The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat. Genet. 1996, 14:33-41.
3. Botto L.D., May K., Fernhoff P.M., Correa A., Coleman K., Rasmussen S.A., Merritt R.K., O'Leary L.A., Wong L.Y., Elixson E.M., et al. A population-based study of the 22q11.2 deletion: phenotype, incidence, and contribution to major birth defects in the population. Pediatrics 2003, 112:101-107.
4. Chang S., McKinsey T.A., Zhang C.L., Richardson J.A., Hill J.A., Olson E.N. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol. 2004, 24:8467-8476.
5. Davenport T.G., Jerome-Majewska L.A., Papaioannou V.E. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development 2003, 130:2263-2273.
6. Doyon Y., Cayrou C., Ullah M., Landry A.J., Côté V., Selleck W., Lane W.S., Tan S., Yang X.J., Côté J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 2006, 21:51-64.
7. Estève P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., Carey M.F., Pradhan S. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 2006, 20:3089-3103.
8. Goodship J., Cross I., Scambler P., Burn J. Monozygotic twins with chromosome 22q11 deletion and discordant phenotype. J. Med. Genet. 1995, 32:746-748.
9. Gottlieb P.D., Pierce S.A., Sims R.J., Yamagishi H., Weihe E.K., Harriss J.V., Maika S.D., Kuziel W.A., King H.L., Olson E.N., et al. Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet. 2002, 31:25-32.
10. Guris D.L., Fantes J., Tara D., Druker B.J., Imamoto A. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat. Genet. 2001, 27:293-298.
11. Jerome L.A., Papaioannou V.E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet. 2001, 27:286-291.
12. Katsumoto T., Aikawa Y., Iwama A., Ueda S., Ichikawa H., Ochiya T., Kitabayashi I. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev. 2006, 20:1321-1330.
13. Kobrynski L.J., Sullivan K.E. Velocardiofacial syndrome, DiGeorge syndrome: the chromosome 22q11.2 deletion syndromes. Lancet 2007, 370:1443-1452.
14. Lachner M., O'Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001, 410:116-120.
15. 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., Lott I.T., et al. Retinoic acid embryopathy. N. Engl. J. Med. 1985, 313:837-841.
16. Liao J., Kochilas L., Nowotschin S., Arnold J.S., Aggarwal V.S., Epstein J.A., Brown M.C., Adams J., Morrow B.E. Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet. 2004, 13:1577-1585.
17. Lickert H., Takeuchi J.K., Von Both I., Walls J.R., McAuliffe F., Adamson S.L., Henkelman R.M., Wrana J.L., Rossant J., Bruneau B.G. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004, 432:107-112.
18. Lindsay E.A. Chromosomal microdeletions: dissecting del22q11 syndrome. Nat. Rev. Genet. 2001, 2:858-868.
19. Lindsay E.A., Baldini A. Recovery from arterial growth delay reduces penetrance of cardiovascular defects in mice deleted for the DiGeorge syndrome region. Hum. Mol. Genet. 2001, 10:997-1002.
20. Lindsay E.A., Vitelli F., Su H., Morishima M., Huynh T., Pramparo T., Jurecic V., Ogunrinu G., Sutherland H.F., Scambler P.J., et al. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 2001, 410:97-101.
21. 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. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 2001, 104:619-629.
22. Montgomery R.L., Davis C.A., Potthoff M.J., Haberland M., Fielitz J., Qi X., Hill J.A., Richardson J.A., Olson E.N. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev. 2007, 21:1790-1802.
23. Naiche L.A., Papaioannou V.E. Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 2003, 130:2681-2693.
24. Nimura K., Ura K., Shiratori H., Ikawa M., Okabe M., Schwartz R.J., Kaneda Y. A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 2009, 460:287-291.
25. Nowotschin S., Liao J., Gage P.J., Epstein J.A., Campione M., Morrow B.E. Tbx1 affects asymmetric cardiac morphogenesis by regulating Pitx2 in the secondary heart field. Development 2006, 133:1565-1573.
26. Paylor R., Glaser B., Mupo A., Ataliotis P., Spencer C., Sobotka A., Sparks C., Choi C.H., Oghalai J., Curran S., et al. Tbx1 haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22q11 deletion syndrome. Proc. Natl. Acad. Sci. USA 2006, 103:7729-7734.
27. Randall V., McCue K., Roberts C., Kyriakopoulou V., Beddow S., Barrett A.N., Vitelli F., Prescott K., Shaw-Smith C., Devriendt K., et al. Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J. Clin. Invest. 2009, 119:3301-3310.
28. Reifsnyder C., Lowell J., Clarke A., Pillus L. Yeast SAS silencing genes and human genes associated with AML and HIV-1 Tat interactions are homologous with acetyltransferases. Nat. Genet. 1996, 14:42-49.
29. Roberts C., Ivins S.M., James C.T., Scambler P.J. Retinoic acid down-regulates Tbx1 expression in vivo and in vitro. Dev. Dyn. 2005, 232:928-938.
30. Shirai M., Osugi T., Koga H., Kaji Y., Takimoto E., Komuro I., Hara J., Miwa T., Yamauchi-Takihara K., Takihara Y. The Polycomb-group gene Rae28 sustains Nkx2.5/Csx expression and is essential for cardiac morphogenesis. J. Clin. Invest. 2002, 110:177-184.
31. Singh S.M., Murphy B., O'Reilly R. Monozygotic twins with chromosome 22q11 deletion and discordant phenotypes: updates with an epigenetic hypothesis. J. Med. Genet. 2002, 39:e71.
32. Stankunas K., Hang C.T., Tsun Z.Y., Chen H., Lee N.V., Wu J.I., Shang C., Bayle J.H., Shou W., Iruela-Arispe M.L., Chang C.P. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev. Cell 2008, 14:298-311.
33. Stoller J.Z., Epstein J.A. Identification of a novel nuclear localization signal in Tbx1 that is deleted in DiGeorge syndrome patients harboring the 1223delC mutation. Hum. Mol. Genet. 2005, 14:885-892.
34. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
35. Thomas T., Voss A.K. The diverse biological roles of MYST histone acetyltransferase family proteins. Cell Cycle 2007, 6:696-704.
36. Thomas T., Corcoran L.M., Gugasyan R., Dixon M.P., Brodnicki T., Nutt S.L., Metcalf D., Voss A.K. Monocytic leukemia zinc finger protein is essential for the development of long-term reconstituting hematopoietic stem cells. Genes Dev. 2006, 20:1175-1186.
37. Thomas T., Loveland K.L., Voss A.K. The genes coding for the MYST family histone acetyltransferases, Tip60 and Mof, are expressed at high levels during sperm development. Gene Expr. Patterns 2007, 7:657-665.
38. Torres-Juan L., Rosell J., Morla M., Vidal-Pou C., García-Algas F., de la Fuente M.A., Juan M., Tubau A., Bachiller D., Bernues M., et al. Mutations in TBX1 genocopy the 22q11.2 deletion and duplication syndromes: a new susceptibility factor for mental retardation. Eur. J. Hum. Genet. 2007, 15:658-663.
39. Vitelli F., Morishima M., Taddei I., Lindsay E.A., Baldini A. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet. 2002, 11:915-922.
40. Voss A.K., Thomas T. MYST family histone acetyltransferases take center stage in stem cells and development. Bioessays 2009, 31:1050-1061.
41. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127:1-11.
42. Voss A.K., Collin C., Dixon M.P., Thomas T. Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev. Cell 2009, 17:674-686.
43. Voss A.K., Dixon M.P., McLennan T., Kueh A.J., Thomas T. Chromatin immunoprecipitation of mouse embryos. Methods Mol. Biol. 2012, 809:335-352.
44. Wang Z., Zhai W., Richardson J.A., Olson E.N., Meneses J.J., Firpo M.T., Kang C., Skarnes W.C., Tjian R. Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev. 2004, 18:3106-3116.
45. Xu H., Morishima M., Wylie J.N., Schwartz R.J., Bruneau B.G., Lindsay E.A., Baldini A. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 2004, 131:3217-3227.
46. Xu H., Cerrato F., Baldini A. Timed mutation and cell-fate mapping reveal reiterated roles of Tbx1 during embryogenesis, and a crucial function during segmentation of the pharyngeal system via regulation of endoderm expansion. Development 2005, 132:4387-4395.
47. Yagi H., Furutani Y., Hamada H., Sasaki T., Asakawa S., Minoshima S., Ichida F., Joo K., Kimura M., Imamura S., et al. Role of TBX1 in human del22q11.2 syndrome. Lancet 2003, 362:1366-1373.
48. Yamagishi H., Maeda J., Hu T., McAnally J., Conway S.J., Kume T., Meyers E.N., Yamagishi C., Srivastava D. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 2003, 17:269-281.
49. Zhang Z., Baldini A. In vivo response to high-resolution variation of Tbx1 mRNA dosage. Hum. Mol. Genet. 2008, 17:150-157.
50. Zhang Z., Baldini A. Manipulation of endogenous regulatory elements and transgenic analyses of the Tbx1 gene. Mamm. Genome 2010, 21:556-564.
51. Zweier C., Sticht H., Aydin-Yaylagül I., Campbell C.E., Rauch A. Human TBX1 missense mutations cause gain of function resulting in the same phenotype as 22q11.2 deletions. Am. J. Hum. Genet. 2007, 80:510-517.