Atrial natriuretic peptide exerts protective action against angiotensin II-induced cardiac remodeling by attenuating inflammation via endothelin-1/endothelin receptor A cascade

Heart and Vessels

Volumn 28, Issue 5, 2013, Pages 646-657

  Fujita, Shuichi ^a   Shimojo, Naoshi ^a,b,c   Terasaki, Fumio ^a   Otsuka, Kaoru ^a   Hosotani, Noriko ^a   Kohda, Yuka ^a   Tanaka, Takao ^d   Nishioka, Tomohiro ^b   Yoshida, Toshimichi ^b,c   Hiroe, Michiaki ^e   Kitaura, Yasushi ^a   Ishizaka, Nobukazu ^a   Imanaka Yoshida, Kyoko ^b,c  

^a OSAKA MEDICAL COLLEGE   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c MIE UNIVERSITY   (Japan)

^d BAIKA WOMEN'S UNIVERSITY   (Japan)

^e NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

Author keywords

ANP; Cardiac remodeling; Endothelin 1; Inflammation; Tenascin C

Indexed keywords

ANGIOTENSIN II; ATRIAL NATRIURETIC FACTOR; BOSENTAN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CYCLO(DEXTRO TRYPTOPHYL DEXTRO ASPARTYLPROLYL DEXTRO VALYLLEUCYL); ENDOTHELIN 1; MESSENGER RNA; N (2,6 DIMETHYLPIPERIDINOCARBONYL) 4 METHYLLEUCYL DEXTRO (1 METHOXYCARBONYLTRYPTOPHANYL) DEXTRO NORLEUCINE; TENASCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CARDIOVASCULAR RESPONSE; CARDITIS; CELL INFILTRATION; CELL SIZE; CONTROLLED STUDY; ET 1 GENE; GENE; GENE EXPRESSION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART RATE; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; IMMUNOREACTIVITY; MACROPHAGE; MALE; MUSCLE CELL; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SYSTOLIC BLOOD PRESSURE; TN C GENE; UPREGULATION;

ANGIOTENSIN II; ANIMALS; ANTI-INFLAMMATORY AGENTS; ATRIAL NATRIURETIC FACTOR; CARDIOMEGALY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; FIBRILLAR COLLAGENS; FIBROBLASTS; FIBROSIS; HEART DISEASES; INFLAMMATION; INFLAMMATION MEDIATORS; INFUSIONS, INTRAVENOUS; MACROPHAGES; MALE; MITRAL VALVE; MYOCARDIAL CONTRACTION; MYOCARDIUM; RATS; RATS, INBRED WKY; RECEPTOR, ENDOTHELIN A; SIGNAL TRANSDUCTION; STROKE VOLUME; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84884673822     PISSN: 09108327     EISSN: 16152573     Source Type: Journal    
DOI: 10.1007/s00380-012-0311-0     Document Type: Article

References (62)

1. Levin ER, Gardner DG, Samson WK (1998) Natriuretic peptides. N Engl J Med 339:321-328
2. Schultz HD, Gardner DG, Deschepper CF, Coleridge HM, Coleridge JC (1998) Vagal C-fiber blockade abolishes sympathetic inhibition by atrial natriuretic factor. Am J Physiol 255:R6-R13
3. Ehara S, Nakamura Y, Matsumoto K, Hasegawa T, Shimada K, Takagi M, Hanatani A, Izumi Y, Terashima M, Yoshiyama M (2012) Effects of intravenous atrial natriuretic peptide and nitroglycerin on coronary vasodilation and flow velocity determined using 3 T magnetic resonance imaging in patients with nonischemic heart failure. Heart Vessels. doi: 10.1007/s00380-012-0292-z
4. Kasamaki Y, Izumi Y, Ozawa Y, Ohta M, Tano A, Watanabe I, Hirayama A, Nakayama T, Kawamura H, Himit D, Mahemuti M, Sezai A (2012) Relationship between status of plasma atrial natriuretic peptide and heart rate variability in human subjects. Heart Vessels. doi: 10.1007/s00380-012-0237-6
5. Kasama S, Furuya M, Toyama T, Ichikawa S, Kurabayashi M (2008) Effect of atrial natriuretic peptide on left ventricular remodeling in patients with acute myocardial infarction. Eur Heart J 29:1485-1494
6. Saito Y (2010) Roles of atrial natriuretic peptide and its therapeutic use. J Cardiol 56:262-270
7. Ishikawa C, Tsutamoto M, Wada A, Fujii M, Ohno K, Sakai H, Yamamoto T, Horie M (2005) Inhibition of aldosterone and endothelin-1 by carperitide was attenuated with more than 1 week of infusion in patients with congestive heart failure. J Cardiovasc Pharmacol 46:513-518
8. Tanaka T, Tsutamoto T, Sakai H, Nishiyama K, Fujii M, Yamamoto T, Horie M (2008) Effect of atrial natriuretic peptide on adiponectin in patients with heart failure. Eur J Heart Fail 10:360-366
9. Tsukamoto O, Fujita M, Kato M, Yamazaki S, Asano Y, Ogai A, Okazaki H, Asai M, Nagamachi Y, Maeda N, Shintani Y, Minamino T, Asakura M, Kishimoto I, Funahashi T, Tomoike H, Kitakaze M (2009) Natriuretic peptides enhance the production of adiponectin in human adipocytes and in patients with chronic heart failure. J Am Coll Cardiol 53:2070-2077
10. Hattori H, Minami Y, Mizuno M, Yumino D, Hoshi H, Arashi H, Nuki T, Sashida Y, Higashitani M, Serizawa N, Yamada N, Yamaguchi J, Mori F, Shiga T, Hagiwara N (2012) Differences in hemodynamic responses between intravenous carperitide and nicorandil in patients with acute heart failure syndromes. Heart Vessels. doi: 1007/s00380-012-0252-7
11. Yamaji M, Tsutamoto T, Tanaka T, Kawahara C, Nishiyama K, Yamamoto T, Fujii M, Horie M (2009) Effect of carperitide on plasma adiponectin levels in acute decompensated heart failure patients with diabetes mellitus. Circ J 73:2264-2269
12. Nomura F, Kurobe N, Mori Y, Hikita A, Kawai M, Suwa M, Okutani Y (2008) Multicenter prospective investigation on efficacy and safety of carperitide as a first-line drug for acute heart failure syndrome with preserved blood pressure: COMPASS: carperitide effects observed through monitoring dyspnea in acute decompensated heart failure study. Circ J 72:1777-1786
13. Hata N, Seino Y, Tsutamoto T, Hiramitsu S, Kaneko N, Yoshikawa T, Yokoyama H, Tanaka K, Mizuno K, Nejima J, Kinoshita M (2008) Effects of carperitide on the long-term prognosis of patients with acute decompensated chronic heart failure: the PROTECT multicenter randomized controlled study. Circ J 72:1787-1793
14. Kuga H, Ogawa K, Oida A, Taguchi I, Nakatsugawa M, Hoshi T, Sugimura H, Abe S, Kaneko A (2003) Administration of atrial natriuretic peptide attenuates reperfusion phenomena and preserves left ventricular regional wall motion after direct coronary angioplasty for acute myocardial infarction. Circ J 67:443-448
15. Kasama S, Toyama T, Hatori T, Sumino H, Kumakura H, Takayama Y, Ichikawa S, Suzuki T, Kurabayashi M (2007) Effects of intravenous atrial natriuretic peptide on cardiac sympathetic nerve activity and left ventricular remodeling in patients with first anterior acute myocardial infarction. J Am Coll Cardiol 49:667-674
16. 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, Kitamura S; J-WIND investigators (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
17. Hayashi M, Tsutamoto T, Wada A, Maeda K, Mabuchi N, Tsutsui T, Horie M, Ohnishi M, Kinoshita M (2001) Intravenous atrial natriuretic peptide prevents left ventricular remodeling in patients with first anterior acute myocardial infarction. J Am Coll Cardiol 37:1820-1826
18. Tsuneyoshi H, Nishina T, Nomoto T, Kanemitsu H, Kawakami R, Unimonh O, Nishimura K, Komeda M (2004) Atrial natriuretic peptide helps prevent late remodeling after left ventricular aneurysm repair. Circulation 110:II174-II179
19. Tanaka K, Ito M, Kodama M, Hoyano M, Kimura S, Mitsuwa W, Hirono S, Adachi T, Watanabe K, Nakazawa M, Aizawa Y (2009) Long-term carperitide treatment attenuates left ventricular remodeling in rats with heart failure after autoimmune myocarditis. J Cardiovasc Pharmacol 54:232-239
20. Fiebeler A, Nussberger J, Shagdarsuren E, Rong S, Hilfenhaus G, Al-Saadi N, Dechend R, Wellner M, Meiners S, Maser-Gluth C, Jeng AY, Webb RL, Luft FC, Muller DN (2005) Aldosterone synthase inhibitor ameliorates angiotensin II-induced organ damage. Circulation 111:3087-3094
21. Kuwahara F, Kai H, Tokuda K, Takeya M, Takeshita A, Egashira K, Imaizumi T (2004) Hypertensive myocardial fibrosis and diastolic dysfunction: another model of inflammation? Hypertension 43:739-745
22. Rocha R, Rudolph AE, Frierdich GE, Nachowiak DA, Kekec BK, Blomme EA, McMahon EG, Delyani JA (2004) Aldosterone induces a vascular inflammatory phenotype in the rat heart. Am J Physiol 283:H1802-H1810
23. Endemann DH, Touyz RM, Iglarz M, Savoia C, Schiffrin EL (2004) Eplerenone prevents salt induced vascular remodeling and cardiac fibrosis in stroke-prone spontaneously hypertensive rats. Hypertension 43:1252-1257
24. Frangogiannis NG, Shimoni S, Chang SM, Ren G, Dewald O, Gersch C, Shan K, Aggeli C, Reardon M, Letsou GV, Espada R, Ramchandani M, Entman ML, Zoghbi WA (2002) Active interstitial remodeling: an important process in the hibernating human myocardium. J Am Coll Cardiol 39:1468-1474
25. Imanaka-Yoshida K, Hiroe M, Yasutomi Y, Toyozaki T, Tsuchiya T, Noda N, Maki T, Nishikawa T, Sakakura T, Yoshida T (2002) Tenascin-C is a useful marker for disease activity in myocarditis. J Pathol 197:388-394
26. Imanaka-Yoshida K, Matsumoto K, Hara M, Sakakura T, Yoshida T (2003) The dynamic expression of tenascin-C and tenascin-X during early heart development in the mouse. Differentiation 71:291-298
27. Morimoto S, Imanaka-Yoshida K, Hiramitsu S, Kato S, Ohtsuki M, Uemura A, Kato Y, Nishikawa T, Toyozaki T, Hishida H, Yoshida T, Hiroe M (2005) Diagnostic utility of tenascin-C for evaluation of the activity of human acute myocarditis. J Pathol 205:460-467
28. Nishioka T, Suzuki M, Onishi K, Takakura N, Inada H, Yoshida T, Hiroe M, Imanaka-Yoshida K (2007) Eplerenone attenuates myocardial fibrosis in the angiotensin II-induced hypertensive mouse: involvement of tenascin-C induced by aldosterone-mediated inflammation. J Cardiovasc Pharmacol 49:261-268
29. Tamura A, Kusachi S, Nogami K, Yamanishi A, Kajikawa Y, Hirohata S, Tsuji T (1996) Tenascin expression in endomyocardial biopsy specimens in patients with dilated cardiomyopathy: distribution along margin of fibrotic lesions. Heart 75:291-294
30. Tsukada B, Terasaki F, Shimomura H, Otsuka K, Otsuka K, Katashima T, Fujita S, Imanaka-Yoshida K, Yoshida T, Hiroe M, Kitaura Y (2009) High prevalence of chronic myocarditis in dilated cardiomyopathy referred for left ventriculoplasty: expression of tenascin-C as a possible marker for inflammation. Human Pathol 40:1015-1022
31. Okamoto H, Imanaka-Yoshida K (2012) Matricellular proteins: new molecular targets to prevent heart failure. Cardiovasc Ther 30:198-209
32. Imanaka-Yoshida K (2012) Tenascin-C in cardiovascular tissue remodeling. From development to inflammation and repair. Circ J 76:2513-2520
33. Imanaka-Yoshida K, Hiroe M, Nishikawa T, Ishiyama S, Shimojo T, Ohta Y, Sakakura T, Yoshida T (2001) Tenascin-C modulates adhesion of cardiomyocytes to extracellular matrix during tissue remodeling after myocardial infarction. Lab Invest 81:1015-1024
34. Tamaoki M, Imanaka-Yoshida K, Yokoyama K, Nishioka T, Inada H, Hiroe M, Sakakura T, Yoshida T (2005) Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury. Am J Pathol 167:71-80
35. Calderone A, Thaik CM, Takahashi N, Chang DL, Colucci WS (1998) Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J Clin Invest 101:812-818
36. Hayashi D, Kudoh S, Shiojima I, Zou Y, Harada K, Shimoyama M, Imai Y, Monzen K, Yamazaki T, Yazaki Y, Nagai R, Komuro I (2004) Atrial natriuretic peptide inhibits cardiomyocyte hypertrophy through mitogen-activated protein kinase phosphatase-1. Biochem Biophys Res Commun 322:310-319
37. Holtwick R, van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, 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
38. Oliver PM, Fox JE, Kim R, Rockman HA, Kim HS, Reddick RL, Pandey KN, Milgram SL, Smithies O, Maeda N (1997) Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc Natl Acad Sci USA 94:14730-14735
39. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, Rockman HA, Maeda N (2001) Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest 107:975-984
40. Kishimoto I, Rossi K, Garbers DL (2001) A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc Natl Acad Sci USA 98:2703-2706
41. Manabe I (2011) Chronic inflammation links cardiovascular, metabolic and renal diseases. Circ J 75:2739-2748
42. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG (2010) The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 48:504-511
43. Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503-506
44. Bornstein P, Sage EH (2002) Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 14:608-616
45. Midwood KS, Hussenet T, Langlois B, Orend G (2011) Advances in tenascin-C biology. Cell Mol Life Sci 68:3175-3199
46. Chiquet-Ehrismann R, Tucker RP (2011) Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 3
47. Kanayama M, Morimoto J, Matsui Y, Ikesue M, Danzaki K, Kurotaki D, Ito K, Yoshida T, Uede T (2011) α9β1 integrin-mediated signaling serves as an intrinsic regulator of pathogenic Th17 cell generation. J Immunol 187:5851-5864
48. Udalova IA, Ruhmann M, Thomson SJ, Midwood KS (2011) Expression and immune function of tenascin-C. Crit Rev Immunol 31:115-145
49. El-Karef A, Yoshida T, Gabazza EC, Nishioka T, Inada H, Sakakura T, Imanaka-Yoshida K (2007) Deficiency of tenascin-C attenuates liver fibrosis in immune-mediated chronic hepatitis in mice. J Pathol 211:86-94
50. Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, Drexler S, Sofat N, Kashiwagi M, Orend G, Brennan F, Foxwell B (2009) Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 15:774-780
51. Nishioka T, Onishi K, Shimojo N, Nagano Y, Matsusaka H, Ikeuchi M, Ide T, Tsutsui H, Hiroe M, Yoshida T, Imanaka-Yoshida K (2010) Tenascin-C may aggravate left ventricular remodeling and function after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 298:H1072-H1078
52. Moriyama N, Taniguchi M, Miyano K, Miyoshi M, Watanabe T (2006) ANP inhibits LPS-induced stimulation of rat microglial cells by suppressing NF-kappaB and AP-1 activations. Biochem Biophys Res Commun 350:322-328
53. Ladetzki-Baehs K, Keller M, Kiemer AK, Koch E, Zahler S, Wendel A, Vollmar AM (2007) Atrial natriuretic peptide, a regulator of nuclear factor-kappa B activation in vivo. Endocrinology 148:332-336
54. Kiemer AK, Hartung T, Vollmar AM (2000) cGMP-mediated inhibition of TNF-alpha production by the atrial natriuretic peptide in murine macrophages. J Immunol 165:175-181
55. Leask A (2010) Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 106:1675-1680
56. Fujisaki H, Ito H, Hirata Y, Tanaka M, Hata M, Lin M, Adachi S, Akimoto H, Marumo F, Hiroe M (1995) Natriuretic peptides inhibit angiotensin II-induced proliferation of rat cardiac fibroblasts by blocking endothelin-1 gene expression. J Clin Invest 96:1059-1065
57. Glenn DJ, Rahmutula D, Nishimito M, Liang F, Gardner DG (2009) Atrial natriuretic peptide suppresses endothelin gene expression and proliferation in cardiac fibroblasts through a GATA4-dependent mechanism. Cardiovasc Res 84:209-217
58. Lange K, Kammerer M, Hegi ME, Grotegut S, Dittmann A, Huang W, Fluri E, Yip GW, Gotte M, Ruiz C, Orend G (2007) Endothelin receptor type B counteracts tenascin-C-induced endothelin receptor type A-dependent focal adhesion and actin stress fiber disorganization. Cancer Res 67:6163-6173
59. Nagaharu K, Zhang X, Yoshida T, Katoh D, Hanamura N, Kozuka Y, Ogawa T, Shiraishi T, Imanaka-Yoshida K (2011) Tenascin C induces epithelial-mesenchymal transition-like change accompanied by SRC activation and focal adhesion kinase phosphorylation in human breast cancer cells. Am J Pathol 178:754-763
60. Ishigaki T, Imanaka-Yoshida K, Shimojo N, Matsushima S, Taki W, Yoshida T (2011) Tenascin-C enhances crosstalk signaling of integrin αvβ3/ PDGFR-β complex by SRC recruitment promoting PDGF-induced proliferation and migration in smooth muscle cells. J Cell Physiol 226:2617-2624
61. Ito H, Hirata Y, Hiroe M, Tsujino M, Adachi S, Takamoto T, Nitta M, Taniguchi K, Marumo F (1991) Endothelin-1 induces hypertrophy with enhanced expression of muscle-specific genes in cultured neonatal rat cardiomyocytes. Circ Res 69:209-215
62. Ito H, Hirata Y, Adachi S, Tanaka M, Tsujino M, Koike A, Nogami A, Marumo F, Hiroe M (1993) Endothelin-1 is an autocrine/paracrine factor in the mechanism of angiotensin Il-induced hypertrophy in cultured rat cardiomyocytes. J Clin Invest 92:398-403