Noninvasive and quantitative live imaging reveals a potential stress-responsive enhancer in the failing heart

FASEB Journal

Volumn 28, Issue 4, 2014, Pages 1870-1879

  Matsuoka, Ken ^a   Asano, Yoshihiro ^a   Higo, Shuichiro ^a   Tsukamoto, Osamu ^a   Yan, Yi ^a   Yamazaki, Satoru ^b   Matsuzaki, Takashi ^a   Kioka, Hidetaka ^a   Kato, Hisakazu ^a   Uno, Yoshihiro ^a   Asakura, Masanori ^b   Asanuma, Hiroshi ^c   Minamino, Tetsuo ^a   Aburatani, Hiroyuki ^d   Kitakaze, Masafumi ^b   Komuro, Issei ^a   Takashima, Seiji ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

In vivo assessment; Natriuretic peptide; Transcriptional regulation

Indexed keywords

FIREFLY LUCIFERASE; RNA POLYMERASE II;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; AUTOSOME; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; ENHANCER REGION; EPIGENETICS; GENE; GENE EXPRESSION; GENE LOCUS; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; IMAGING SYSTEM; IN VIVO STUDY; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; NONINVASIVE AND QUANTITATIVE LIVE IMAGING SYSTEM; NPPA GENE; NPPB GENE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; TRANSCRIPTION INITIATION SITE;

IN VIVO ASSESSMENT; NATRIURETIC PEPTIDE; TRANSCRIPTIONAL REGULATION;

5' FLANKING REGION; ADRENERGIC ALPHA-1 RECEPTOR AGONISTS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; HEART FAILURE; HUMANS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NATRIURETIC PEPTIDE, BRAIN; NATRIURETIC PEPTIDE, C-TYPE; PROTEIN PRECURSORS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL;

EID: 84901020480     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-245522     Document Type: Article

References (38)

1. Spitz, F., and Furlong, E. E. (2012) Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 13, 613-626
2. Chien, K. R., Domian, I. J., and Parker, K. K. (2008) Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 322, 1494-1497
3. Olson, E. N. (2006) Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927
4. Burley, D. S., and Baxter, G. F. (2007) B-type natriuretic peptide at early reperfusion limits infarct size in the rat isolated heart. Basic Res. Cardiol. 102, 529-541
5. Holtwick, R., van Eickels, M., Skryabin, B. V., Baba, H. A., Bubikat, A., Begrow, F., Schneider, M. D., Garbers, D. L., and Kuhn, M. (2003) Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J. Clin. Invest. 111, 1399-1407
6. Kitakaze, M., Asakura, M., Kim, J., Shintani, Y., Asanuma, H., Hamasaki, T., Seguchi, O., Myoishi, M., Minamino, T., Ohara, T., Nagai, Y., Nanto, S., Watanabe, K., Fukuzawa, S., Hirayama, A., Nakamura, N., Kimura, K., Fujii, K., Ishihara, M., Saito, Y., Tomoike, H., and Kitamura, S. (2007) Human atrial natriuretic peptide and nicorandil as adjuncts to reperfusion treatment for acute myocardial infarction (J-WIND): two randomised trials. Lancet 370, 1483-1493
7. Li, P., Wang, D., Lucas, J., Oparil, S., Xing, D., Cao, X., Novak, L., Renfrow, M. B., and Chen, Y. F. (2008) Atrial natriuretic peptide inhibits transforming growth factor beta-induced Smad signaling and myofibroblast transformation in mouse cardiac fibroblasts. Circ. Res. 102, 185-192
8. Tamura, N., Ogawa, Y., Chusho, H., Nakamura, K., Nakao, K., Suda, M., Kasahara, M., Hashimoto, R., Katsuura, G., Mukoyama, M., Itoh, H., Saito, Y., Tanaka, I., Otani, H., and Katsuki, M. (2000) Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc. Natl. Acad. Sci. U. S. A. 97, 4239-4244
9. De Lange, F. J., Moorman, A. F., and Christoffels, V. M. (2003) Atrial cardiomyocyte-specific expression of Cre recombinase driven by an Nppa gene fragment. Genesis 37, 1-4
10. Habets, P. E., Moorman, A. F., Clout, D. E., van Roon, M. A., Lingbeek, M., van Lohuizen, M., Campione, M., and Christoffels, V. M. (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
11. Horsthuis, T., Houweling, A. C., Habets, P. E., de Lange, F. J., el Azzouzi, H., Clout, D. E., Moorman, A. F., and Christoffels, V. M. (2008) Distinct regulation of developmental and heart diseaseinduced atrial natriuretic factor expression by two separate distal sequences. Circ. Res. 102, 849-859
12. Knowlton, K. U., Rockman, H. A., Itani, M., Vovan, A., Seidman, C. E., and Chien, K. R. (1995) Divergent pathways mediate the induction of ANF transgenes in neonatal and hypertrophic ventricular myocardium. J. Clin. Invest. 96, 1311-1318
13. Small, E. M., and Krieg, P. A. (2003) Transgenic analysis of the atrialnatriuretic factor (ANF) promoter: Nkx2-5 and GATA-4 binding sites are required for atrial specific expression of ANF. Dev. Biol. 261, 116-131
14. Warren, S. A., Terada, R., Briggs, L. E., Cole-Jeffrey, C. T., Chien, W. M., Seki, T., Weinberg, E. O., Yang, T. P., Chin, M. T., Bungert, J., and Kasahara, H. (2011) Differential role of Nkx2-5 in activation of the atrial natriuretic factor gene in the developing versus failing heart. Mol. Cell. Biol. 31, 4633-4645
15. Simpson, P., McGrath, A., and Savion, S. (1982) Myocyte hypertrophy in neonatal rat heart cultures and its regulation by serum and by catecholamines. Circ. Res. 51, 787-801
16. Siepel, A., Bejerano, G., Pedersen, J. S., Hinrichs, A. S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L. W., Richards, S., Weinstock, G. M., Wilson, R. K., Gibbs, R. A., Kent, W. J., Miller, W., and Haussler, D. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050
17. Blanchette, M., Kent, W. J., Riemer, C., Elnitski, L., Smit, A. F., Roskin, K. M., Baertsch, R., Rosenbloom, K., Clawson, H., Green, E. D., Haussler, D., and Miller, W. (2004) Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708-715
18. Pollard, K. S., Hubisz, M. J., Rosenbloom, K. R., and Siepel, A. (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res. 20, 110-121
19. Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., and Liu, X. S. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137
20. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002) Capturing chromosome conformation. Science 295, 1306-1311
21. Hagege, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W., and Forne, T. (2007) Quantitative analysis of chromosome conformation capture assays (3CqPCR). Nat. Protoc. 2, 1722-1733
22. Liao, Y., Ishikura, F., Beppu, S., Asakura, M., Takashima, S., Asanuma, H., Sanada, S., Kim, J., Ogita, H., Kuzuya, T., Node, K., Kitakaze, M., and Hori, M. (2002) Echocardiographic assessment of LV hypertrophy and function in aortic-banded mice: necropsy validation. Am. J. Physiol. Heart Circ. Physiol. 282, H1703-H1708
23. Saadane, N., Alpert, L., and Chalifour, L. E. (1999) Expression of immediate early genes, GATA-4, and Nkx-2.5 in adrenergicinduced cardiac hypertrophy and during regression in adult mice. Brit. J. Pharmacol. 127, 1165-1176
24. Vecchione, C., Fratta, L., Rizzoni, D., Notte, A., Poulet, R., Porteri, E., Frati, G., Guelfi, D., Trimarco, V., Mulvany, M. J., Agabiti-Rosei, E., Trimarco, B., Cotecchia, S., and Lembo, G. (2002) Cardiovascular influences of -1 -adrenergic receptor defect in mice. Circulation 105, 1700-1707
25. Nobrega, M. A., Ovcharenko, I., Afzal, V., and Rubin, E. M. (2003) Scanning human gene deserts for long-range enhancers. Science 302, 413 (Pubitemid 37296259)
26. Thomas, J. W., Touchman, J. W., Blakesley, R. W., Bouffard, G. G., Beckstrom-Sternberg, S. M., Margulies, E. H., Blanchette, M., Siepel, A. C., Thomas, P. J., McDowell, J. C., Maskeri, B., Hansen, N. F., Schwartz, M. S., Weber, R. J., Kent, W. J., Karolchik, D., Bruen, T. C., Bevan, R., Cutler, D. J., Schwartz, S., Elnitski, L., Idol, J. R., Prasad, A. B., Lee-Lin, S. Q., Maduro, V. V., Summers, T. J., Portnoy, M. E., Dietrich, N. L., Akhter, N., Ayele, K., Benjamin, B., Cariaga, K., Brinkley, C. P., Brooks, S. Y., Granite, S., Guan, X., Gupta, J., Haghighi, P., Ho, S. L., Huang, M. C., Karlins, E., Laric, P. L., Legaspi, R., Lim, M. J., Maduro, Q. L., Masiello, C. A., Mastrian, S. D., McCloskey, J. C., Pearson, R., Stantripop, S., Tiongson, E. E., Tran, J. T., Tsurgeon, C., Vogt, J. L., Walker, M. A., Wetherby, K. D., Wiggins, L. S., Young, A. C., Zhang, L. H., Osoegawa, K., Zhu, B., Zhao, B., Shu, C. L., De Jong, P. J., Lawrence, C. E., Smit, A. F., Chakravarti, A., Haussler, D., Green, P., Miller, W., and Green, E. D. (2003) Comparative analyses of multi-species sequences from targeted genomic regions. Nature 424, 788-793
27. Woolfe, A., Goodson, M., Goode, D. K., Snell, P., McEwen, G. K., Vavouri, T., Smith, S. F., North, P., Callaway, H., Kelly, K., Walter, K., Abnizova, I., Gilks, W., Edwards, Y. J., Cooke, J. E., and Elgar, G. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 3, e7
28. Bell, A. C., West, A. G., and Felsenfeld, G. (1999) The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98, 387-396
29. Felsenfeld, G., Burgess-Beusse, B., Farrell, C., Gaszner, M., Ghirlando, R., Huang, S., Jin, C., Litt, M., Magdinier, F., Mutskov, V., Nakatani, Y., Tagami, H., West, A., and Yusufzai, T. (2004) Chromatin boundaries and chromatin domains. Cold Spring Harb. Symp. Quant. Biol. 69, 245-250
30. Shen, Y., Yue, F., McCleary, D. F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V. V., and Ren, B. (2012) A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116-120
31. Birney, E., Stamatoyannopoulos, J. A., Dutta, A., Guigo, R., Gingeras, T. R., Margulies, E. H., Weng, Z., Snyder, M., Dermitzakis, E. T., Thurman, R. E., Kuehn, M. S., Taylor, C. M., Neph, S., Koch, C. M., Asthana, S., Malhotra, A., Adzhubei, I., Greenbaum, J. A., Andrews, R. M., Flicek, P., Boyle, P. J., Cao, H., Carter, N. P., Clelland, G. K., Davis, S., Day, N., Dhami, P., Dillon, S. C., Dorschner, M. O., Fiegler, H., Giresi, P. G., Goldy, J., Hawrylycz, M., Haydock, A., Humbert, R., James, K. D., Johnson, B. E., Johnson, E. M., Frum, T. T., Rosenzweig, E. R., Karnani, N., Lee, K., Lefebvre, G. C., Navas, P. A., Neri, F., Parker, S. C., Sabo, P. J., Sandstrom, R., Shafer, A., Vetrie, D., Weaver, M., Wilcox, S., Yu, M., Collins, F. S., Dekker, J., Lieb, J. D., Tullius, T. D., Crawford, G. E., Sunyaev, S., Noble, W. S., Dunham, I., Denoeud, F., Reymond, A., Kapranov, P., Rozowsky, J., Zheng, D., Castelo, R., Frankish, A., Harrow, J., Ghosh, S., Sandelin, A., Hofacker, I. L., Baertsch, R., Keefe, D., Dike, S., Cheng, J., Hirsch, H. A., Sekinger, E. A., Lagarde, J., Abril, J. F., Shahab, A., Flamm, C., Fried, C., Hackermuller, J., Hertel, J., Lindemeyer, M., Missal, K., Tanzer, A., Washietl, S., Korbel, J., Emanuelsson, O., Pedersen, J. S., Holroyd, N., Taylor, R., Swarbreck, D., Matthews, N., Dickson, M. C., Thomas, D. J., Weirauch, M. T., Gilbert, J., Drenkow, J., Bell, I., Zhao, X., Srinivasan, K. G., Sung, W. K., Ooi, H. S., Chiu, K. P., Foissac, S., Alioto, T., Brent, M., Pachter, L., Tress, M. L., Valencia, A., Choo, S. W., Choo, C. Y., Ucla, C., Manzano, C., Wyss, C., Cheung, E., Clark, T. G., Brown, J. B., Ganesh, M., Patel, S., Tammana, H., Chrast, J., Henrichsen, C. N., Kai, C., Kawai, J., Nagalakshmi, U., Wu, J., Lian, Z., Lian, J., Newburger, P., Zhang, X., Bickel, P., Mattick, J. S., Carninci, P., Hayashizaki, Y., Weissman, S., Hubbard, T., Myers, R. M., Rogers, J., Stadler, P. F., Lowe, T. M., Wei, C. L., Ruan, Y., Struhl, K., Gerstein, M., Antonarakis, S. E., Fu, Y., Green, E. D., Karaoz, U., Siepel, A., Taylor, J., Liefer, L. A., Wetterstrand, K. A., Good, P. J., Feingold, E. A., Guyer, M. S., Cooper, G. M., Asimenos, G., Dewey, C. N., Hou, M., Nikolaev, S., Montoya-Burgos, J. I., Loytynoja, A., Whelan, S., Pardi, F., Massingham, T., Huang, H., Zhang, N. R., Holmes, I., Mullikin, J. C., Ureta-Vidal, A., Paten, B., Seringhaus, M., Church, D., Rosenbloom, K., Kent, W. J., Stone, E. A., Batzoglou, S., Goldman, N., Hardison, R. C., Haussler, D., Miller, W., Sidow, A., Trinklein, N. D., Zhang, Z. D., Barrera, L., Stuart, R., King, D. C., Ameur, A., Enroth, S., Bieda, M. C., Kim, J., Bhinge, A. A., Jiang, N., Liu, J., Yao, F., Vega, V. B., Lee, C. W., Ng, P., Shahab, A., Yang, A., Moqtaderi, Z., Zhu, Z., Xu, X., Squazzo, S., Oberley, M. J., Inman, D., Singer, M. A., Richmond, T. A., Munn, K. J., Rada-Iglesias, A., Wallerman, O., Komorowski, J., Fowler, J. C., Couttet, P., Bruce, A. W., Dovey, O. M., Ellis, P. D., Langford, C. F., Nix, D. A., Euskirchen, G., Hartman, S., Urban, A. E., Kraus, P., Van Calcar, S., Heintzman, N., Kim, T. H., Wang, K., Qu, C., Hon, G., Luna, R., Glass, C. K., Rosenfeld, M. G., Aldred, S. F., Cooper, S. J., Halees, A., Lin, J. M., Shulha, H. P., Zhang, X., Xu, M., Haidar, J. N., Yu, Y., Ruan, Y., Iyer, V. R., Green, R. D., Wadelius, C., Farnham, P. J., Ren, B., Harte, R. A., Hinrichs, A. S., Trumbower, H., Clawson, H., Hillman-Jackson, J., Zweig, A. S., Smith, K., Thakkapallayil, A., Barber, G., Kuhn, R. M., Karolchik, D., Armengol, L., Bird, C. P., de Bakker, P. I., Kern, A. D., Lopez-Bigas, N., Martin, J. D., Stranger, B. E., Woodroffe, A., Davydov, E., Dimas, A., Eyras, E., Hallgrimsdottir, I. B., Huppert, J., Zodyf, J., Gnerre, S., Jaffe, D. B., Chang, J. L., Lindblad-Toh, K., Lander, E. S., Koriabine, M., Nefedov, M., Osoegawa, K., Yoshinaga, Y., Zhu, B., and de Jong, P. J. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799-816
32. Blow, M. J., McCulley, D. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., Afzal, V., Bristow, J., Ren, B., Black, B. L., Rubin, E. M., Visel, A., and Pennacchio, L. A. (2010) ChIP-Seq identification of weakly conserved heart enhancers. Nat. Genet. 42, 806-810
33. Koch, F., Jourquin, F., Ferrier, P., and Andrau, J. C. (2008) Genome-wide RNA polymerase II: not genes only!. Trends Biochem. Sci. 33, 265-273
34. Szutorisz, H., Dillon, N., and Tora, L. (2005) The role of enhancers as centres for general transcription factor recruitment. Trends Biochem. Sci. 30, 593-599
35. Sei, C. A., Irons, C. E., Sprenkle, A. B., McDonough, P. M., Brown, J. H., and Glembotski, C. C. (1991) The -adrenergic stimulation of atrial natriuretic factor expression in cardiac myocytes requires calcium influx, protein kinase C, and calmodulin-regulated pathways. J. Biol. Chem. 266, 15910-15916
36. Iaccarino, G., Dolber, P. C., Lefkowitz, R. J., and Koch, W. J. (1999) B -adrenergic receptor kinase-1 levels in catecholamineinduced myocardial hypertrophy: regulation by beta-but not alpha1-adrenergic stimulation. Hypertension 33, 396-401
37. Seidman, C. E., Wong, D. W., Jarcho, J. A., Bloch, K. D., and Seidman, J. G. (1988) Cis-acting sequences that modulate atrial natriuretic factor gene expression. Proc. Natl. Acad. Sci. U. S. A. 85, 4104-4108
38. Thuerauf, D. J., and Glembotski, C. C. (1997) Differential effects of protein kinase C, Ras, and Raf-1 kinase on the induction of the cardiac B-type natriuretic peptide gene through a critical promoter-proximal M-CAT element. J. Biol. Chem. 272, 7464-7472