Lrrc10 is a novel cardiac-specific target gene of Nkx2-5 and GATA4

Journal of Molecular and Cellular Cardiology

Volumn 62, Issue , 2013, Pages 237-246

  Brody, Matthew J ^a,b   Cho, Eunjin ^a,b   Mysliwiec, Matthew R ^a   Kim, Tae gyun ^a,d   Carlson, Clayton D ^b,e   Lee, Kyu Ho ^c   Lee, Youngsook ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d Korea Food and Drug Administration   (South Korea)

^e United States of America   (United States)

Author keywords

Cardiac gene expression; GATA4; Lrrc10; Nkx2 5; Transcriptional regulation

Indexed keywords

LEUCINE RICH REPEAT CONTAINING 10 PROTEIN; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE; GENE EXPRESSION REGULATION; HEART DEVELOPMENT; HEART MUSCLE CELL; LEUCINE RICH REPEAT CONTAINING 10 GENE; MOUSE; MUTATIONAL ANALYSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REGULATORY SEQUENCE;

CARDIAC GENE EXPRESSION; GATA4; LRRC10; NKX2-5; TRANSCRIPTIONAL REGULATION;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; GATA4 TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MUSCLE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

EID: 84880938454     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.05.020     Document Type: Article

References (66)

1. Kim K.H., Kim T.G., Micales B.K., Lyons G.E., Lee Y. Dynamic expression patterns of leucine-rich repeat containing protein 10 in the heart. Dev Dyn 2007, 236:2225-2234.
2. Nakane T., Satoh T., Inada Y., Nakayama J., Itoh F., Chiba S. Molecular cloning and expression of HRLRRP, a novel heart-restricted leucine-rich repeat protein. Biochem Biophys Res Commun 2004, 314:1086-1092.
3. Kim K.H., Antkiewicz D.S., Yan L., Eliceiri K.W., Heideman W., Peterson R.E., et al. Lrrc10 is required for early heart development and function in zebrafish. Dev Biol 2007, 308:494-506.
4. Adameyko I.I., Mudry R.E., Houston-Cummings N.R., Veselov A.P., Gregorio C.C., Tevosian S.G. Expression and regulation of mouse SERDIN1, a highly conserved cardiac-specific leucine-rich repeat protein. Dev Dyn 2005, 233:540-552.
5. Brody M.J., Hacker T.A., Patel J.R., Feng L., Sadoshima J., Tevosian S.G., et al. Ablation of the cardiac-specific gene leucine-rich repeat containing 10 (Lrrc10) results in dilated cardiomyopathy. PLoS One 2012, 7:e51621.
6. Fan X., Yang Q., Wang Y., Zhang Y., Wang J., Yuan J., et al. Cloning and characterization of the cardiac-specific Lrrc10 promoter. BMB Rep 2011, 44:123-128.
7. Pashmforoush M., Lu J.T., Chen H., Amand T.S., Kondo R., Pradervand S., et al. Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 2004, 117:373-386.
8. Terada R., Warren S., Lu J.T., Chien K.R., Wessels A., Kasahara H. Ablation of Nkx2-5 at mid-embryonic stage results in premature lethality and cardiac malformation. Cardiovasc Res 2011, 91(2):289-299.
9. Tanaka M., Chen Z., Bartunkova S., Yamasaki N., Izumo S. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 1999, 126:1269-1280.
10. Briggs L.E., Takeda M., Cuadra A.E., Wakimoto H., Marks M.H., Walker A.J., et al. Perinatal loss of Nkx2-5 results in rapid conduction and contraction defects. Circ Res 2008, 103:580-590.
11. Takeda M., Briggs L.E., Wakimoto H., Marks M.H., Warren S.A., Lu J.T., et al. Slow progressive conduction and contraction defects in loss of Nkx2-5 mice after cardiomyocyte terminal differentiation. Lab Invest 2009, 89:983-993.
12. Moskowitz I.P., Kim J.B., Moore M.L., Wolf C.M., Peterson M.A., Shendure J., et al. A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell 2007, 129:1365-1376.
13. Jay P.Y., Harris B.S., Maguire C.T., Buerger A., Wakimoto H., Tanaka M., et al. Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system. J Clin Invest 2004, 113:1130-1137.
14. Schott J.J., Benson D.W., Basson C.T., Pease W., Silberbach G.M., Moak J.P., et al. Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science 1998, 281:108-111.
15. Lee Y., Shioi T., Kasahara H., Jobe S.M., Wiese R.J., Markham B.E., et al. 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 1998, 18:3120-3129.
16. Sepulveda J.L., Belaguli N., Nigam V., Chen C.Y., Nemer M., Schwartz R.J. GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol Cell Biol 1998, 18:3405-3415.
17. Sepulveda J.L., Vlahopoulos S., Iyer D., Belaguli N., Schwartz R.J. Combinatorial expression of GATA4, Nkx2-5, and serum response factor directs early cardiac gene activity. J Biol Chem 2002, 277:25775-25782.
18. Durocher D., Charron F., Warren R., Schwartz R.J., Nemer M. The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. EMBO J 1997, 16:5687-5696.
19. Shiojima I., Komuro I., Oka T., Hiroi Y., Mizuno T., Takimoto E., et al. Context-dependent transcriptional cooperation mediated by cardiac transcription factors Csx/Nkx-2.5 and GATA-4. J Biol Chem 1999, 274:8231-8239.
20. Chen C.Y., Croissant J., Majesky M., Topouzis S., McQuinn T., Frankovsky M.J., et al. Activation of the cardiac alpha-actin promoter depends upon serum response factor, tinman homologue, Nkx-2.5, and intact serum response elements. Dev Genet 1996, 19:119-130.
21. Chen C.Y., Schwartz R.J. Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol Cell Biol 1996, 16:6372-6384.
22. Linhares V.L., Almeida N.A., Menezes D.C., Elliott D.A., Lai D., Beyer E.C., et al. Transcriptional regulation of the murine connexin40 promoter by cardiac factors Nkx2-5, GATA4 and Tbx5. Cardiovasc Res 2004, 64:402-411.
23. Kim T.G., Chen J., Sadoshima J., Lee Y. Jumonji represses atrial natriuretic factor gene expression by inhibiting transcriptional activities of cardiac transcription factors. Mol Cell Biol 2004, 24:10151-10160.
24. van Berlo J.H., Elrod J.W., Aronow B.J., Pu W.T., Molkentin J.D. Serine 105 phosphorylation of transcription factor GATA4 is necessary for stress-induced cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A 2011, 108:12331-12336.
25. Garg V., Kathiriya I.S., Barnes R., Schluterman M.K., King I.N., Butler C.A., et al. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 2003, 424:443-447.
26. Haworth K.E., Kotecha S., Mohun T.J., Latinkic B.V. GATA4 and GATA5 are essential for heart and liver development in Xenopus embryos. BMC Dev Biol 2008, 8:74.
27. Rivera-Feliciano J., Lee K.H., Kong S.W., Rajagopal S., Ma Q., Springer Z., et al. Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 2006, 133:3607-3618.
28. Molkentin J.D., Lu J.R., Antos C.L., Markham B., Richardson J., Robbins J., et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 1998, 93:215-228.
29. Maitra M., Schluterman M.K., Nichols H.A., Richardson J.A., Lo C.W., Srivastava D., et al. Interaction of Gata4 and Gata6 with Tbx5 is critical for normal cardiac development. Dev Biol 2009, 326:368-377.
30. Belaguli N.S., Sepulveda J.L., Nigam V., Charron F., Nemer M., Schwartz R.J. Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol Cell Biol 2000, 20:7550-7558.
31. Moore M.L., Wang G.L., Belaguli N.S., Schwartz R.J., McMillin J.B. GATA-4 and serum response factor regulate transcription of the muscle-specific carnitine palmitoyltransferase I beta in rat heart. J Biol Chem 2001, 276:1026-1033.
32. Brown C.O., Chi X., Garcia-Gras E., Shirai M., Feng X.H., Schwartz R.J. The cardiac determination factor, Nkx2-5, is activated by mutual cofactors GATA-4 and Smad1/4 via a novel upstream enhancer. J Biol Chem 2004, 279:10659-10669.
33. Oka T., Maillet M., Watt A.J., Schwartz R.J., Aronow B.J., Duncan S.A., et al. Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 2006, 98:837-845.
34. Funke-Kaiser H., Lemmer J., Langsdorff C.V., Thomas A., Kovacevic S.D., Strasdat M., et al. Endothelin-converting enzyme-1 (ECE-1) is a downstream target of the homeobox transcription factor Nkx2-5. FASEB J 2003, 17:1487-1489.
35. Barth J.L., Clark C.D., Fresco V.M., Knoll E.P., Lee B., Argraves W.S., et al. Jarid2 is among a set of genes differentially regulated by Nkx2.5 during outflow tract morphogenesis. Dev Dyn 2010, 239:2024-2033.
36. Riazi A.M., Takeuchi J.K., Hornberger L.K., Zaidi S.H., Amini F., Coles J., et al. NKX2-5 regulates the expression of beta-catenin and GATA4 in ventricular myocytes. PLoS One 2009, 4:e5698.
37. Murphy A.M., Thompson W.R., Peng L.F., Jones L. Regulation of the rat cardiac troponin I gene by the transcription factor GATA-4. Biochem J 1997, 322(Pt 2):393-401.
38. Ip H.S., Wilson D.B., Heikinheimo M., Tang Z., Ting C.N., Simon M.C., et al. The GATA-4 transcription factor transactivates the cardiac muscle-specific troponin C promoter-enhancer in nonmuscle cells. Mol Cell Biol 1994, 14:7517-7526.
39. Bhalla S.S., Robitaille L., Nemer M. Cooperative activation by GATA-4 and YY1 of the cardiac B-type natriuretic peptide promoter. J Biol Chem 2001, 276:11439-11445.
40. Pikkarainen S., Tokola H., Majalahti-Palviainen T., Kerkela R., Hautala N., Bhalla S.S., et al. GATA-4 is a nuclear mediator of mechanical stretch-activated hypertrophic program. J Biol Chem 2003, 278:23807-23816.
41. Thuerauf D.J., Hanford D.S., Glembotski C.C. Regulation of rat brain natriuretic peptide transcription. A potential role for GATA-related transcription factors in myocardial cell gene expression. J Biol Chem 1994, 269:17772-17775.
42. Molkentin J.D., Kalvakolanu D.V., Markham B.E. Transcription factor GATA-4 regulates cardiac muscle-specific expression of the alpha-myosin heavy-chain gene. Mol Cell Biol 1994, 14:4947-4957.
43. Durocher D., Chen C.Y., Ardati A., Schwartz R.J., Nemer M. The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium. Mol Cell Biol 1996, 16:4648-4655.
44. Wang Y., Morishima M., Zheng M., Uchino T., Mannen K., Takahashi A., et al. Transcription factors Csx/Nkx2.5 and GATA4 distinctly regulate expression of Ca2+ channels in neonatal rat heart. J Mol Cell Cardiol 2007, 42:1045-1053.
45. Lim J.Y., Kim W.H., Kim J., Park S.I. Induction of Id2 expression by cardiac transcription factors GATA4 and Nkx2.5. J Cell Biochem 2008, 103:182-194.
46. Kim T.G., Kraus J.C., Chen J., Lee Y. Jumonji, a critical factor for cardiac development, functions as a transcriptional repressor. J Biol Chem 2003, 278:42247-42255.
47. Kim T.G., Jung J., Mysliwiec M.R., Kang S., Lee Y. Jumonji represses alpha-cardiac myosin heavy chain expression via inhibiting MEF2 activity. Biochem Biophys Res Commun 2005, 329:544-553.
48. Johansen F.E., Prywes R. Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol Cell Biol 1993, 13:4640-4647.
49. Mysliwiec M.R., Carlson C.D., Tietjen J., Hung H., Ansari A.Z., Lee Y. Jarid2 (jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J Biol Chem 2012, 287:1235-1241.
50. Mysliwiec M.R., Bresnick E.H., Lee Y. Endothelial Jarid2/jumonji is required for normal cardiac development and proper Notch1 expression. J Biol Chem 2011, 286(19):17193-17204.
51. Heinemeyer T., Wingender E., Reuter I., Hermjakob H., Kel A.E., Kel O.V., et al. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 1998, 26:362-367.
52. Loots G.G., Ovcharenko I., Pachter L., Dubchak I., Rubin E.M. rVista for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res 2002, 12:832-839.
53. Lyons I., Parsons L.M., Hartley L., Li R., Andrews J.E., Robb L., et al. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev 1995, 9:1654-1666.
54. Zhao R., Watt A.J., Battle M.A., Li J., Bondow B.J., Duncan S.A. Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Dev Biol 2008, 317:614-619.
55. Xin M., Davis C.A., Molkentin J.D., Lien C.L., Duncan S.A., Richardson J.A., et al. A threshold of GATA4 and GATA6 expression is required for cardiovascular development. Proc Natl Acad Sci U S A 2006, 103:11189-11194.
56. Mysliwiec M.R., Kim T.G., Lee Y. Characterization of zinc finger protein 496 that interacts with jumonji/Jarid2. FEBS Lett 2007, 581:2633-2640.
57. Clark C.D., Zhang B., Lee B., Evans S.I., Lassar A.B., Lee K.H. Evolutionary conservation of Nkx2.5 autoregulation in the second heart field. Dev Biol 2013, 374:198-209.
58. Latinkic B.V., Cooper B., Smith S., Kotecha S., Towers N., Sparrow D., et al. Transcriptional regulation of the cardiac-specific MLC2 gene during Xenopus embryonic development. Development 2004, 131:669-679.
59. Park J.S., Kim H.S., Kim J.D., Seo J., Chung K.S., Lee H.S., et al. Isolation of a ventricle-specific promoter for the zebrafish ventricular myosin heavy chain (vmhc) gene and its regulation by GATA factors during embryonic heart development. Dev Dyn 2009, 238:1574-1581.
60. Kuo H., Chen J., Ruiz-Lozano P., Zou Y., Nemer M., Chien K.R. Control of segmental expression of the cardiac-restricted ankyrin repeat protein gene by distinct regulatory pathways in murine cardiogenesis. Development 1999, 126:4223-4234.
61. Rivkees S.A., Chen M., Kulkarni J., Browne J., Zhao Z. Characterization of the murine A1 adenosine receptor promoter, potent regulation by GATA-4 and Nkx2.5. J Biol Chem 1999, 274:14204-14209.
62. Wang G.L., Moore M.L., McMillin J.B. A region in the first exon/intron of rat carnitine palmitoyltransferase Ibeta is involved in enhancement of basal transcription. Biochem J 2002, 362:609-618.
63. Maillet M., Gastineau M., Bochet P., Asselin-Labat M.L., Morel E., Laverriere J.N., et al. Functional studies of the 5'-untranslated region of human 5-HT4 receptor mRNA. Biochem J 2005, 387:463-471.
64. Zhang R., Xu X. Transient and transgenic analysis of the zebrafish ventricular myosin heavy chain (vmhc) promoter: an inhibitory mechanism of ventricle-specific gene expression. Dev Dyn 2009, 238:1564-1573.
65. Shang L.L., Dudley S.C. Tandem promoters and developmentally regulated 5'- and 3'-mRNA untranslated regions of the mouse Scn5a cardiac sodium channel. J Biol Chem 2005, 280:933-940.
66. Wilhide C.C., Jin Y., Guo Q., Li L., Li S.X., Rubin E., et al. The human integrin beta3 gene is 63kb and contains a 5'-UTR sequence regulating expression. Blood 1997, 90:3951-3961.