Essential role of the zinc finger transcription factor Casz1 for mammalian cardiac morphogenesis and development

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29801-29816

  Liu, Zhihui ^a   Li, Wenling ^c   Ma, Xuefei ^d   Ding, Nancy ^a   Spallotta, Francesco ^e   Southon, Eileen ^b   Tessarollo, Lino ^b   Gaetano, Carlo ^e   Mukouyama, Yoh Suke ^c   Thiele, Carol J ^a  

^a Neuro Oncology Branch   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Laboratory of Stem Cell and Neuro vascular Biology   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLOGY; DISEASES; HEART; MAMMALS; MORPHOLOGY; STEM CELLS; TRANSCRIPTION FACTORS; ZINC;

CARDIAC ARRHYTHMIA; CONGENITAL HEART DISEASE; EMBRYONIC STEM CELLS; MUSCLE CONTRACTIONS; TRANSCRIPTIONAL REGULATION; TRANSCRIPTOME ANALYSIS; VENTRICULAR SEPTAL DEFECT; ZINC FINGER TRANSCRIPTION FACTOR;

TRANSCRIPTION;

ION CHANNEL; PROTEIN CASZ1; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

1P36 DELETION SYNDROME; ABCC9 GENE; ACTA1 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CACNA1D GENE; CELL PROLIFERATION; CHROMOSOME 1P; CHROMOSOME 1P36; CHROMOSOME DELETION; CKM GENE; CONGENITAL HEART DISEASE; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GENETIC CODE; HEART ARRHYTHMIA; HEART DEVELOPMENT; HEART DISEASE; HEART VENTRICLE SEPTUM DEFECT; KNOCKOUT MOUSE; MALE; MAMMAL; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA ANALYSIS; TNNI2 GENE; TNNT1 GENE; TRANSCRIPTION REGULATION; VENTRICULAR NONCOMPACTION; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CELL CYCLE; DEFICIENCY; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; LYMPHATIC SYSTEM; METABOLISM; MORPHOGENESIS; PATHOLOGY; PHENOTYPE; REPRODUCIBILITY; SARCOMERE;

ANIMALS; CELL CYCLE; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HUMANS; LYMPHATIC SYSTEM; MICE; MODELS, BIOLOGICAL; MORPHOGENESIS; MYOCARDIUM; MYOCYTES, CARDIAC; PHENOTYPE; REPRODUCIBILITY OF RESULTS; SARCOMERES; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84908180993     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570416     Document Type: Article

References (61)

1. Hoffman, J. I., and Kaplan, S. (2002) The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39, 1890-1900
2. Fahed, A. C., Gelb, B. D., Seidman, J. G., and Seidman, C. E. (2013) Genetics of congenital heart disease: the glass half empty. Circ. Res. 112, 707-720
3. Bruneau, B. G. (2013) Signaling and transcriptional networks in heart development and regeneration. Cold Spring Harb. Perspect. Biol. 5, a008292
4. Srivastava, D. (2006) Making or breaking the heart: from lineage determination to morphogenesis. Cell 126, 1037-1048
5. Olson, E. N. (2006) Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927
6. Srivastava, D., and Olson, E. N. (2000) A genetic blueprint for cardiac development. Nature 407, 221-226
7. McCulley, D. J., and Black, B. L. (2012) Transcription factor pathways and congenital heart disease. Curr. Top. Dev. Biol. 100, 253-277
8. Cui, X., and Doe, C. Q. (1992) ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943-952
9. Mellerick, D. M., Kassis, J. A., Zhang, S. D., and Odenwald, W. F. (1992) Castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron 9, 789-803
10. Vacalla, C. M., and Theil, T. (2002) Cst, a novel mouse gene related to Drosophila Castor, exhibits dynamic expression patterns during neurogenesis and heart development. Mech. Dev. 118, 265-268
11. Liu, Z., Yang, X., Tan, F., Cullion, K., and Thiele, C. J. (2006) Molecular cloning and characterization of human Castor, a novel human gene upregulated during cell differentiation. Biochem. Biophys. Res. Commun. 344, 834-844
12. Liu, Z., Naranjo, A., and Thiele, C. J. (2011) CASZ1b, the short isoform of CASZ1 gene, coexpresses with CASZ1a during neurogenesis and suppresses neuroblastoma cell growth. PLoS One 6, e18557
13. Liu, Z., Yang, X., Li, Z., McMahon, C., Sizer, C., Barenboim-Stapleton, L., Bliskovsky, V., Mock, B., Ried, T., London, W. B., Maris, J., Khan, J., and Thiele, C. J. (2011) CASZ1, a candidate tumor-suppressor gene, suppresses neuroblastoma tumor growth through reprogramming gene expression. Cell Death Differ. 18, 1174-1183
14. Virden, R. A., Thiele, C. J., and Liu, Z. (2012) Characterization of critical domains within the tumor suppressor CASZ1 required for transcriptional regulation and growth suppression. Mol. Cell. Biol. 32, 1518-1528
15. Henrich, K. O., Schwab, M., and Westermann, F. (2012) 1p36 tumor suppression: a matter of dosage? Cancer Res. 72, 6079-6088
16. Gajecka, M., Mackay, K. L., and Shaffer, L. G. (2007) Monosomy 1p36 deletion syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 145C, 346-356
17. Christine, K. S., and Conlon, F. L. (2008) Vertebrate CASTOR is required for differentiation of cardiac precursor cells at the ventral midline. Dev. Cell 14, 616-623
18. Charpentier, M. S., Christine, K. S., Amin, N. M., Dorr, K. M., Kushner, E. J., Bautch, V. L., Taylor, J. M., and Conlon, F. L. (2013) CASZ1 promotes vascular assembly and morphogenesis through the direct regulation of an EGFL7/RhoA-mediated pathway. Dev. Cell 25, 132-143
19. Reid, S. W., and Tessarollo, L. (2009) Isolation, microinjection and transfer of mouse blastocysts. Methods Mol. Biol. 530, 269-285
20. Gerety, S. S., and Anderson, D. J. (2002) Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129, 1397-1410
21. Vecellio, M., Spallotta, F., Nanni, S., Colussi, C., Cencioni, C., Derlet, A., Bassetti, B., Tilenni, M., Carena, M. C., Farsetti, A., Sbardella, G., Castellano, S., Mai, A., Martelli, F., Pompilio, G., Capogrossi, M. C., Rossini, A., Dimmeler, S., Zeiher, A., and Gaetano, C. (2014) The histone acetylase activator pentadecylidenemalonate 1b rescues proliferation and differentiation in the human cardiac mesenchymal cells of type 2 diabetic patients. Diabetes 63, 2132-2147
22. Rossini, A., Frati, C., Lagrasta, C., Graiani, G., Scopece, A., Cavalli, S., Musso, E., Baccarin, M., Di Segni, M., Fagnoni, F., Germani, A., Quaini, E., Mayr, M., Xu, Q., Barbuti, A., DiFrancesco, D., Pompilio, G., Quaini, F., Gaetano, C., and Capogrossi, M. C. (2011) Human cardiac and bone marrow stromal cells exhibit distinctive properties related to their origin. Cardiovasc. Res. 89, 650-660
23. Claycomb, W. C., Lanson, N. A., Jr., Stallworth, B. S., Egeland, D. B., Delcarpio, J. B., Bahinski, A., and Izzo, N. J., Jr. (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc. Natl. Acad. Sci. U.S.A. 95, 2979-2984
24. Greenberg, C. C., Connelly, P. S., Daniels, M. P., and Horowits, R. (2008) Krp1 (Sarcosin) promotes lateral fusion of myofibril assembly intermediates in cultured mouse cardiomyocytes. Exp. Cell Res. 314, 1177-1191
25. Ma, X., Jana, S. S., Conti, M. A., Kawamoto, S., Claycomb, W. C., and Adelstein, R. S. (2010) Ablation of nonmuscle myosin II-B and II-C reveals a role for nonmuscle myosin II in cardiac myocyte karyokinesis. Mol. Biol. Cell 21, 3952-3962
26. Li, W., Kohara, H., Uchida, Y., James, J. M., Soneji, K., Cronshaw, D. G., Zou, Y. R., Nagasawa, T., and Mukouyama, Y. S. (2013) Peripheral nerve-derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev. Cell 24, 359-371
27. Li, W., and Mukouyama, Y. S. (2011) Whole-mount immunohistochemical analysis for embryonic limb skin vasculature: a model system to study vascular branching morphogenesis in embryo. J. Vis. Exp. pii, 2620
28. Spallotta, F., Cencioni, C., Straino, S., Nanni, S., Rosati, J., Artuso, S., Manni, I., Colussi, C., Piaggio, G., Martelli, F., Valente, S., Mai, A., Capogrossi, M. C., Farsetti, A., and Gaetano, C. (2013)Anitric oxide-dependent cross-talk between class I and III histone deacetylases accelerates skin repair. J. Biol. Chem. 288, 11004-11012
29. Barone, V., and Heisenberg, C. P. (2012) Cell adhesion in embryo morphogenesis. Curr. Opin. Cell Biol. 24, 148-153
30. Lecuit, T., and Lenne, P. F. (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644
31. Larsen, M., Artym, V. V., Green, J. A., and Yamada, K. M. (2006) The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18, 463-471
32. Corda, S., Samuel, J. L., and Rappaport, L. (2000) Extracellular matrix and growth factors during heart growth. Heart Fail Rev. 5, 119-130
33. Gumbiner, B. M. (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634
34. Nakamura, S., Kawai, T., Kamakura, T., and Ookura, T. (2010) TGF-β3 is expressed in taste buds and inhibits proliferation of primary cultured taste epithelial cells. In Vitro Cell. Dev. Biol. Anim. 46, 36-44
35. Iordanskaia, T., and Nawshad, A. (2011) Mechanisms of transforming growth factor β induced cell cycle arrest in palate development. J. Cell. Physiol. 226, 1415-1424
36. Little, N. A., and Jochemsen, A. G. (2002) p63. Int. J. Biochem. Cell Biol. 34, 6-9
37. Allocati, N., Di Ilio, C., and De Laurenzi, V. (2012) p63/p73 in the control of cell cycle and cell death. Exp. Cell Res. 318, 1285-1290
38. Mosca, B., Delbono, O., Laura Messi, M., Bergamelli, L., Wang, Z. M., Vukcevic, M., Lopez, R., Treves, S., Nishi, M., Takeshima, H., Paolini, C., Martini, M., Rispoli, G., Protasi, F., and Zorzato, F. (2013) Enhanced dihydropyridine receptor calcium channel activity restores muscle strength in JP45/CASQ1 double knockout mice. Nat. Commun. 4, 1541
39. Clarkson, E., Costa, C. F., and Machesky, L. M. (2004) Congenital myopathies: diseases of the actin cytoskeleton. J. Pathol. 204, 407-417
40. Robaszkiewicz, K., and Moraczewska, J. (2011) [Congenital myopathies: skeletal muscle diseases related to disorder of actin filament structure and functions]. Postepy. Hig. Med. Dosw. (Online) 65, 347-356
41. Kimber, E., Tajsharghi, H., Kroksmark, A. K., Oldfors, A., and Tulinius, M. (2006) A mutation in the fast skeletal muscle troponin I gene causes myopathy and distal arthrogryposis. Neurology 67, 597-601
42. Hein, S., Kostin, S., Heling, A., Maeno, Y., and Schaper, J. (2000) The role of the cytoskeleton in heart failure. Cardiovasc. Res. 45, 273-278
43. Chang, A. N., and Potter, J. D. (2005) Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail. Rev. 10, 225-235
44. Solaro, R. J., and de Tombe, P. P. (2008) Review focus series: sarcomeric proteins as key elements in integrated control of cardiac function. Cardiovasc. Res. 77, 616-618
45. Frank, D., and Frey, N. (2011) Cardiac Z-disc signaling network. J. Biol. Chem. 286, 9897-9904
46. Kim, S. Y., Park, Y. E., Kim, H. S., Lee, C. H., Yang, D. H., and Kim, D. S. (2011) Nemaline myopathy and non-fatal hypertrophic cardiomyopathy caused by a novel ACTA1 E239K mutation. J. Neurol. Sci. 307, 171-173
47. Tsoutsman, T., Bagnall, R. D., and Semsarian, C. (2008) Impact of multiple gene mutations in determining the severity of cardiomyopathy and heart failure. Clin. Exp. Pharmacol. Physiol. 35, 1349-1357
48. Lombardi, R., and Marian, A. J. (2011) Molecular genetics and pathogenesis of arrhythmogenic right ventricular cardiomyopathy: a disease of cardiac stem cells. Pediatr. Cardiol. 32, 360-365
49. Beffagna, G., Occhi, G., Nava, A., Vitiello, L., Ditadi, A., Basso, C., Bauce, B., Carraro, G., Thiene, G., Towbin, J. A., Danieli, G. A., and Rampazzo, A. (2005) Regulatory mutations in transforming growth factor-β3 gene cause arrhythmogenic right ventricular cardiomyopathy type 1. Cardiovasc. Res. 65, 366-373
50. Nichols, C. G., Singh, G. K., and Grange, D. K. (2013) KATP channels and cardiovascular disease: suddenly a syndrome. Circ. Res. 112, 1059-1072
51. Giudicessi, J. R., and Ackerman, M. J. (2012) Potassium-channel mutations and cardiac arrhythmias: diagnosis and therapy. Nat. Rev. Cardiol. 9, 319-332
52. Cerrone, M., Napolitano, C., and Priori, S. G. (2012) Genetics of ion-channel disorders. Curr. Opin. Cardiol. 27, 242-252
53. Venetucci, L., Denegri, M., Napolitano, C., and Priori, S. G. (2012) Inherited calcium channelopathies in the pathophysiology of arrhythmias. Nat. Rev. Cardiol. 9, 561-575
54. Hatcher, C. J., and Basson, C. T. (2009) Specification of the cardiac conduction system by transcription factors. Circ. Res. 105, 620-630
55. Bienengraeber, M., Olson, T. M., Selivanov, V. A., Kathmann, E. C., O'Cochlain, F., Gao, F., Karger, A. B., Ballew, J. D., Hodgson, D. M., Zingman, L. V., Pang, Y. P., Alekseev, A. E., and Terzic, A. (2004) ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. Nat. Genet. 36, 382-387
56. Maitra, M., Schluterman, M. K., Nichols, H. A., Richardson, J. A., Lo, C. W., Srivastava, D., and Garg, V. (2009) Interaction of Gata4 and Gata6 with Tbx5 is critical for normal cardiac development. Dev. Biol. 326, 368-377
57. Stennard, F. A., and Harvey, R. P. (2005) T-box transcription factors and their roles in regulatory hierarchies in the developing heart. Development 132, 4897-4910
58. Molkentin, J. D., Lin, Q., Duncan, S. A., and Olson, E. N. (1997) Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11, 1061-1072
59. Zhu, X., Zhang, Y., Wang, J., Yang, J. F., Yang, Y. F., and Tan, Z. P. (2013) 576 kb deletion in 1p36.33-p36.32 containing SKI is associated with limb malformation, congenital heart disease and epilepsy. Gene 528, 352-355
60. Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J. D., Romano-Adesman, A., Bjornson, R. D., Breitbart, R. E., Brown, K. K., Carriero, N. J., Cheung, Y. H., Deanfield, J., DePalma, S., Fakhro, K. A., Glessner, J., Hakonarson, H., Italia, M. J., Kaltman, J. R., Kaski, J., Kim, R., Kline, J. K., Lee, T., Leipzig, J., Lopez, A., Mane, S. M., Mitchell, L. E., Newburger, J. W., Parfenov, M., Pe'er, I., Porter, G., Roberts, A. E., Sachidanandam, R., Sanders, S. J., Seiden, H. S., State, M. W., Subramanian, S., Tikhonova, I. R., Wang, W., Warburton, D., White, P. S., Williams, I. A., Zhao, H., Seidman, J. G., Brueckner, M., Chung, W. K., Gelb, B. D., Goldmuntz, E., Seidman, C. E., and Lifton, R. P. (2013) De novo mutations in histone-modifying genes in congenital heart disease. Nature 498, 220-223
61. Wang, C., Liu, Z., Woo, C. W., Li, Z., Wang, L., Wei, J. S., Marquez, V. E., Bates, S. E., Jin, Q., Khan, J., Ge, K., and Thiele, C. J. (2012) EZH2 Mediates epigenetic silencing of neuroblastoma suppressor genes CASZ1, CLU, RUNX3, and NGFR. Cancer Res. 72, 315-324