Differential Role of Nkx2-5 in activation of the atrial natriuretic factor gene in the developing versus failing heart

Molecular and Cellular Biology

Volumn 31, Issue 22, 2011, Pages 4633-4645

  Warren, Sonisha A ^a   Terada, Ryota ^a   Briggs, Laura E ^a   Cole Jeffrey, Colleen T ^a   Chien, Wei Ming ^b   Seki, Tsugio ^c   Weinberg, Ellen O ^d   Yang, Thomas P ^a   Chin, Michael T ^b   Bungert, Jörg ^a   Kasahara, Hideko ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN HEY2; REPRESSOR PROTEIN; TAMOXIFEN; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANF GENE; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; EMBRYO; GENE; GENE ACTIVATION; GENE EXPRESSION; HEART ATRIUM; HEART DEVELOPMENT; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE CELL; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; NEWBORN; NKX2-5 GENE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; TRANSACTIVATION;

ANIMALS; ATRIAL NATRIURETIC FACTOR; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART FAILURE; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MYOCARDIUM; MYOCYTES, CARDIAC; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 83255186740     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05940-11     Document Type: Article

References (55)

1. Bar, H., J. Kreuzer, A. Cojoc, and L. Jahn. 2003. Upregulation of embryonic transcription factors in right ventricular hypertrophy. Basic Res. Cardiol. 98:285-294.
2. Beltrami, A. P., et al. 2003. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776.
3. Briggs, L. E., et al. 2008. Perinatal loss of Nkx2-5 results in rapid conduction and contraction defects. Circ. Res. 103:580-590.
4. Bruneau, B. G., et al. 2001. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106:709-721.
5. Chan, J. Y., et al. 2008. Identification of cardiac-specific myosin light chain kinase. Circ. Res. 102:571-580.
6. Chen, C. Y., et al. 1996. Activation of the cardiac alpha-actin promoter depends upon serum response factor, Tinman homologue, Nkx-2.5, and intact serum response elements. Dev. Genet. 19:119-130.
7. Christoffels, V. M., et al. 2000. Chamber formation and morphogenesis in the developing mammalian heart. Dev. Biol. 223:266-278.
8. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science 295:1306-1311.
9. Durocher, D., F. Charron, R. Warren, R. J. Schwartz, and M. Nemer. 1997. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J. 16:5687-5696.
10. Fischer, A., et al. 2005. Hey basic helix-loop-helix transcription factors are repressors of GATA4 and GATA6 and restrict expression of the GATA target gene ANF in fetal hearts. Mol. Cell Biol. 25:8960-8970.
11. Habets, P. E., et al. 2002. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev. 16:1234-1246.
12. Hayashi, S., and A. P. McMahon. 2002. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244:305-318.
13. Horsthuis, T., et al. 2008. Distinct regulation of developmental and heart disease-induced atrial natriuretic factor expression by two separate distal sequences. Circ. Res. 102:849-859.
14. Houweling, A. C., M. M. van Borren, A. F. Moorman, and V. M. Christoffels. 2005. Expression and regulation of the atrial natriuretic factor encoding gene Nppa during development and disease. Cardiovasc. Res. 67:583-593.
15. Iso, T., et al. 2001. HERP, a novel heterodimer partner of HES/E(spl) in Notch signaling. Mol. Cell Biol. 21:6080-6089.
16. Jenni, R., E. Oechslin, J. Schneider, C. Attenhofer Jost, and P. A. Kaufmann. 2001. Echocardiographic and pathoanatomical characteristics of isolated left ventricular non-compaction: a step towards classification as a distinct cardiomyopathy. Heart 86:666-671.
17. Kasahara, H., S. Bartunkova, M. Schinke, M. Tanaka, and S. Izumo. 1998. Cardiac and extracardiac expression of Csx/Nkx2.5 homeodomain protein. Circ. Res. 82:936-946.
18. Kasahara, H., et al. 2001. Characterization of homo- and heterodimerization of cardiac Csx/Nkx2.5 homeoprotein. J. Biol. Chem. 276:4570-4580.
19. Kathiriya, I. S., et al. 2004. Hairy-related transcription factors inhibit GATA-dependent cardiac gene expression through a signal-responsive mechanism. J. Biol. Chem. 279:54937-54943.
20. Knowlton, K. U., et al. 1995. Divergent pathways mediate the induction of ANF transgenes in neonatal and hypertrophic ventricular myocardium. J. Clin. Invest. 96:1311-1318.
21. Koibuchi, N., and M. T. Chin. 2007. CHF1/Hey2 plays a pivotal role in left ventricular maturation through suppression of ectopic atrial gene expression. Circ. Res. 100:850-855.
22. Komuro, I., and S. Izumo. 1993. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc. Natl. Acad. Sci. U. S. A. 90:8145-8149.
23. Kuwahara, K., and K. Nakao. 2010. Regulation and significance of atrial and brain natriuretic peptides as cardiac hormones. Endocr. J. 57:555-565.
24. Kuwahara, K., et al. 2001. The neuron-restrictive silencer element-neuronrestrictive silencer factor system regulates basal and endothelin 1-inducible atrial natriuretic peptide gene expression in ventricular myocytes. Mol. Cell Biol. 21:2085-2097.
25. LaPointe, M. C. 2005. Molecular regulation of the brain natriuretic peptide gene. Peptides 26:944-956.
26. Lee, Y., et al. 1998. The cardiac tissue-restricted homeobox protein Csx/ Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol. Cell Biol. 18:3120-3129.
27. Li, Q., G. Barkess, and H. Qian. 2006. Chromatin looping and the probability of transcription. Trends Genet. 22:197-202.
28. Lints, T. J., L. M. Parsons, L. Hartley, I. Lyons, and R. P. Harvey. 1993. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:419-431.
29. Liu, Y., M. Yu, L. Wu, and M. T. Chin. 2010. The bHLH transcription factor CHF1/Hey2 regulates susceptibility to apoptosis and heart failure after pressure overload. Am. J. Physiol. Heart Circ. Physiol. 298:H2082-H2092.
30. Lyons, I., et al. 1995. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9:1654-1666.
31. Mayer, B., et al. 2002. Molecular cloning and functional characterization of the upstream rat atrial natriuretic peptide promoter. J. Hypertens. 20:219-228.
32. McBride, K., and M. Nemer. 2001. Regulation of the ANF and BNP promoters by GATA factors: lessons learned for cardiac transcription. Can. J. Physiol. Pharmacol. 79:673-681.
33. McGrath, M. F., M. L. de Bold, and A. J. de Bold. 2005. The endocrine function of the heart. Trends Endocrinol. Metab. 16:469-477.
34. Molkentin, J. D., Q. Lin, S. A. Duncan, and E. N. Olson. 1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061-1072.
35. Moorman, A. F., A. C. Houweling, P. A. de Boer, and V. M. Christoffels. 2001. Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J. Histochem Cytochem. 49:1-8.
36. Oka, T., J. Xu, and J. D. Molkentin. 2007. Re-employment of developmental transcription factors in adult heart disease. Semin. Cell Dev. Biol. 18:117-131.
37. Pacher, P., T. Nagayama, P. Mukhopadhyay, S. Batkai, and D. A. Kass. 2008. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat. Protoc. 3:1422-1434.
38. Palstra, R. J., et al. 2003. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35:190-194.
39. Rockman, H. A., et al. 1991. Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 88:8277-8281.
40. Saadane, N., L. Alpert, and L. E. Chalifour. 1999. Expression of immediate early genes, GATA-4, and Nkx-2.5 in adrenergic-induced cardiac hypertrophy and during regression in adult mice. Br. J. Pharmacol. 127:1165-1176.
41. Sakata, Y., et al. 2002. Ventricular septal defect and cardiomyopathy in mice lacking the transcription factor CHF1/Hey2. Proc. Natl. Acad. Sci. U. S. A. 99:16197-16202.
42. Sedmera, D., et al. 2003. Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 274:773-777.
43. Seki, T., K. H. Hong, and S. P. Oh. 2006. Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab. Invest. 86:116-129.
44. Seki, T., J. Yun, and S. P. Oh. 2003. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ. Res. 93:682-689.
45. Shibata, R., et al. 2004. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10:1384-1389.
46. Singh, A. M., et al. 2007. Chibby, an antagonist of the Wnt/beta-catenin pathway, facilitates cardiomyocyte differentiation of murine embryonic stem cells. Circulation 115:617-626.
47. Takeda, M., et al. 2009. Slow progressive conduction and contraction defects in loss of Nkx2-5 mice after cardiomyocyte terminal differentiation. Lab. Invest. 89:983-993.
48. Tanaka, M., Z. Chen, S. Bartunkova, N. Yamasaki, and S. Izumo. 1999. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126:1269-1280.
49. Temsah, R., and M. Nemer. 2005. GATA factors and transcriptional regulation of cardiac natriuretic peptide genes. Regul. Pept. 128:177-185.
50. Terada, R., et al. 2011. Ablation of Nkx2-5 at mid-embryonic stage results in premature lethality and cardiac malformation. Cardiovasc. Res. 91:289-299.
51. Thompson, J. T., M. S. Rackley, and T. X. O'Brien. 1998. Upregulation of the cardiac homeobox gene Nkx2-5 (CSX) in feline right ventricular pressure overload. Am. J. Physiol. 274:H1569-H1573.
52. Watt, A. J., M. A. Battle, J. Li, and S. A. Duncan. 2004. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl. Acad. Sci. U. S. A. 101:12573-12578.
53. Xiang, F., et al. 2006. Transcription factor CHF1/Hey2 suppresses cardiac hypertrophy through an inhibitory interaction with GATA4. Am. J. Physiol. Heart Circ. Physiol. 290:H1997-H2006.
54. Xin, M., et al. 2007. Essential roles of the bHLH transcription factor Hrt2 in repression of atrial gene expression and maintenance of postnatal cardiac function. Proc. Natl. Acad. Sci. U. S. A. 104:7975-7980.
55. Yuasa, S., et al. 2010. Zac1 is an essential transcription factor for cardiac morphogenesis. Circ. Res. 106:1083-1091.