Genetically altered mutant mouse models of guanylyl cyclase/natriuretic peptide receptor-A exhibit the cardiac expression of proinflammatory mediators in a gene-dose-dependent manner

Endocrinology

Volumn 155, Issue 3, 2014, Pages 1045-1056

  Vellaichamy, Elangovan ^a   Das, Subhankar ^a   Subramanian, Umadevi ^a   Maeda, Nobuyo ^b   Pandey, Kailash N ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; CYTOKINE; GAMMA INTERFERON; GLYCOPROTEIN GP 130; GUANYLATE CYCLASE; HLA B ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; MESSENGER RNA; NATRIURETIC PEPTIDE RECEPTOR A; PROTEIN C FOS; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL WALL THICKENING; ARTICLE; BINDING AFFINITY; BODY WEIGHT; CELL INFILTRATION; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; GENE DISRUPTION; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION; GENE REPRESSION; GENETIC ASSOCIATION; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; IMMUNOREACTIVITY; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SYSTOLIC BLOOD PRESSURE; UPREGULATION;

ANIMALS; BODY WEIGHT; CELL NUCLEUS; CYCLIC GMP; CYTOKINES; CYTOSOL; FIBROSIS; GUANYLATE CYCLASE; HEART; HEART VENTRICLES; HYPERTROPHY; INFLAMMATION; MALE; MICE; MICE, TRANSGENIC; MYOCARDIUM; NF-KAPPA B; ORGAN SIZE; RECEPTORS, ATRIAL NATRIURETIC FACTOR; SYSTOLE; TRANSCRIPTION FACTOR AP-1;

EID: 84896842673     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1416     Document Type: Article

References (69)

1. de Bold AJ. Atrial natriuretic factor: a hormone produced by the heart. Science. 1985;230(4727):767-770.
2. Garbers DL. Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell. 1992;71(1):1-4.
3. Levin ER, Gardner DG, Samson WK. Natriuretic peptides. N Engl J Med. 1998;339(5):321-328. (Pubitemid 28366422)
4. Pandey KN. The functional genomics of guanylyl cyclase/natriuretic peptide receptor-A: perspectives and paradigms. FEBS J. 2011;278(11):1792-1807.
5. Pandey KN. Biology of natriuretic peptides and their receptors. Peptides. 2005;26(6):901-932. (Pubitemid 40725366)
6. Drewett JG, Garbers DL. The family of guanylyl cyclase receptors and their ligands. Endocr Rev. 1994;15(2):135-162. (Pubitemid 24129181)
7. Pandey KN, Singh S. Molecular cloning and expression of murine guanylate cyclase/atrial natriuretic factor receptor cDNA. J Biol Chem. 1990;265(21):12342-12348.
8. Garg R, Oliver PM, Maeda N, Pandey KN. Genomic structure, organization, and promoter region analysis of murine guanylyl cyclase/atrial natriuretic peptide receptor-A gene. Gene. 2002;291(1-2):123-133. (Pubitemid 34722383)
9. Calderone A, Thaik CM, Takahashi N, Chang DL, Colucci WS. Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J Clin Invest. 1998;101(4):812-818. (Pubitemid 28096078)
10. Pandey KN, Nguyen HT, Li M, Boyle JW. Natriuretic peptide receptor-A negatively regulates mitogen-activated protein kinase and proliferation of mesangial cells: role of cGMP-dependent protein kinase. Biochem Biophys Res Commun. 2000;271(2):374-379. (Pubitemid 30444734)
11. Ellmers LJ, Scott NJ, Piuhola J, et al. Npr1-regulated gene pathways contributing to cardiac hypertrophy and fibrosis. J Mol Endocrinol. 2007;38(1-2):245-257. (Pubitemid 46351607)
12. Li P, Wang D, Lucas J, et al. Atrial natriuretic peptide inhibits transforming growth factor β-induced Smad signaling and myofibroblast transformation in mouse cardiac fibroblasts. Circ Res. 2008;102(2):185-192. (Pubitemid 351651122)
13. Oliver PM, Fox JE, Kim R, et al. Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc Natl Acad Sci U S A. 1997;94(26):14730-14735. (Pubitemid 28041442)
14. Vellaichamy E, Khurana ML, Fink J, Pandey KN. Involvement of the NF-κB/matrix metalloproteinase pathway in cardiac fibrosis of mice lacking guanylyl cyclase/natriuretic peptide receptor A. J Biol Chem. 2005;280(19):19230-19242. (Pubitemid 41379630)
15. Oliver PM, John SW, Purdy KE, et al. Natriuretic peptide receptor 1 expression influences blood pressures of mice in a dose-dependent manner. Proc Natl Acad Sci U S A. 1998;95(5):2547-2551. (Pubitemid 28145979)
16. Zahabi A, Picard S, Fortin N, Reudelhuber TL, Deschepper CF. Expression of constitutively active guanylate cyclase in cardiomyocytes inhibits the hypertrophic effects of isoproterenol and aortic constriction on mouse hearts. J Biol Chem. 2003;278(48):47694-47699. (Pubitemid 37523215)
17. Zhao D, Das S, Pandey KN. Interactive roles of NPR1 gene-dosage and salt diets on cardiac angiotensin II, aldosterone and pro-inflammatory cytokines levels in mutant mice. J Hypertens. 2013;31(1):134-144.
18. He JG, Chen YL, Chen BL, et al. B-type natriuretic peptide attenuates cardiac hypertrophy via the transforming growth factor-β1/smad7 pathway in vivo and in vitro. Clin Exp Pharmacol Physiol. 2010;37(3):283-289.
19. Lin KF, Chao J, Chao L. Atrial natriuretic peptide gene delivery attenuates hypertension, cardiac hypertrophy, and renal injury in salt-sensitive rats. Hum Gene Ther. 1998;9(10):1429-1438. (Pubitemid 28379082)
20. Knowles JW, Erickson LM, Guy VK, Sigel CS, Wilder JC, Maeda N. Common variations in noncoding regions of the human natriuretic peptide receptorAgene have quantitative effects. Hum Genet. 2003;112(1):62-70. (Pubitemid 36869117)
21. Rubattu S, Bigatti G, Evangelista A, et al. Association of atrial natriuretic peptide and type a natriuretic peptide receptor gene polymorphisms with left ventricular mass in human essential hypertension. J Am Coll Cardiol. 2006;48(3):499-505. (Pubitemid 44093966)
22. Karayannis G, Tsezou A, Giannatou E, Papanikolaou V, Giamouzis G, Triposkiadis F. Polymorphisms of renin-angiotensin system and natriuretic peptide receptor A genes in patients of Greek origin with a history of myocardial infarction. Angiology. 2010;61(8):737-743.
23. Newton-Cheh C, Larson MG, Vasan RS, et al. Association of common variants in NPPA and NPPB with circulating natriuretic peptides and blood pressure. Nat Genet. 2009;41(3):348-353.
24. Del Greco MF, Pattaro C, Luchner A, et al. Genome-wide association analysis and fine mapping of NT-proBNP level provide novel insight into the role of the MTHFR-CLCN6-NPPA-NPPB gene cluster. Hum Mol Genet. 2011;20(8):1660-1671.
25. Hirota H, Yoshida K, Kishimoto T, Taga T. Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc Natl Acad Sci U S A. 1995;92(11):4862-4866.
26. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med. 1990;323(4):236-241. (Pubitemid 20225044)
27. Testa M, Yeh M, Lee P, et al. Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension. J Am Coll Cardiol. 1996;28(4):964-971.
28. Vanderheyden M, Paulus WJ, Voss M, et al. Myocardial cytokine gene expression is higher in aortic stenosis than in idiopathic dilated cardiomyopathy. Heart. 2005;91(7):926-931. (Pubitemid 40874083)
29. Baumgarten G, Knuefermann P, Kalra D, et al. Load-dependent and -independent regulation of proinflammatory cytokine and cytokine receptor gene expression in the adult mammalian heart. Circulation. 2002;105(18):2192-2197. (Pubitemid 34517164)
30. Palmieri EA, Benincasa G, Di Rella F, et al. Differential expression of TNF-α, IL-6, and IGF-1 by graded mechanical stress in normal rat myocardium. AmJ Physiol Heart Circ Physiol. 2002;282(3):H926-H934. (Pubitemid 34654929)
31. Krown KA, Page MT, Nguyen C, et al. Tumor necrosis factor α-induced apoptosis in cardiac myocytes. Involvement of the sphingolipid signaling cascade in cardiac cell death. J Clin Invest. 1996;98(12):2854-2865.
32. Sano M, Fukuda K, Kodama H, et al. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem. 2000;275(38):29717-29723. (Pubitemid 32043853)
33. Gray MO, Long CS, Kalinyak JE, Li HT, Karliner JS. Angiotensin II stimulates cardiac myocyte hypertrophy via paracrine release of TGF-β 1 and endothelin-1 from fibroblasts. Cardiovasc Res. 1998;40(2):352-363. (Pubitemid 28506046)
34. Sekiguchi K, Li X, Coker M, et al. Cross-regulation between the renin-angiotensin system and inflammatory mediators in cardiac hypertrophy and failure. Cardiovasc Res. 2004;63(3):433-442. (Pubitemid 38970187)
35. Thaik CM, Calderone A, Takahashi N, Colucci WS. Interleukin-1β modulates the growth and phenotype of neonatal rat cardiac myocytes. J Clin Invest. 1995;96(2):1093-1099.
36. Tsukagoshi H, Shimizu Y, Kawata T, et al. Atrial natriuretic peptide inhibits tumor necrosis factor-α production by interferon-γ- activated macrophages via suppression of p38 mitogen-activated protein kinase and nuclear factor-κB activation. Regul Pept. 2001;99(1):21-29. (Pubitemid 32232124)
37. Vellaichamy E, Zhao D, Somanna N, Pandey KN. Genetic disruption of guanylyl cyclase/natriuretic peptide receptor-A upregulates ACEandAT1receptor gene expression and signaling: role in cardiac hypertrophy. Physiol Genomics. 2007;31(2):193-202. (Pubitemid 350014397)
38. Pandey KN, Oliver PM, Maeda N, Smithies O. Hypertension associated with decreased testosterone levels in natriuretic peptide receptor-A gene-knockout and gene-duplicated mutant mouse models. Endocrinology. 1999;140(11):5112-5119.
39. Shi SJ, Vellaichamy E, Chin SY, Smithies O, Navar LG, Pandey KN. Natriuretic peptide receptor A mediates renal sodium excretory responses to blood volume expansion. Am J Physiol Renal Physiol. 2003;285(4):F694-F702. (Pubitemid 37140253)
40. Das S, Periyasamy R, Pandey KN. Activation of IKK/NF-κB provokes renal inflammatory responses in guanylyl cyclase/natriuretic peptide receptor-A gene-knockout mice. Physiol Genomics. 2012;44(7):430-442.
41. Kumar P, Garg R, Bolden G, Pandey KN. Interactive roles of Ets-1, Sp1, and acetylated histones in the retinoic acid-dependent activation of guanylyl cyclase/atrial natriuretic peptide receptor-A gene transcription. J Biol Chem. 2010;285(48):37521-37530.
42. Khurana ML, Pandey KN. Catalytic activation of guanylate cyclase/atrial natriuretic factor receptor by combined effects of ANF and GTPγS in plasma membranes of Leydig tumor cells: involvement of G-proteins. Arch Biochem Biophys. 1995;316(1):392-398.
43. Leitman DC, Agnost VL, Tuan JJ, Andresen JW, Murad F. Atrial natriuretic factor and sodium nitroprusside increase cyclic GMP in cultured rat lung fibroblasts by activating different forms of guanylate cyclase. Biochem J. 1987;244(1):69-74. (Pubitemid 17098810)
44. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic acids research. 1983;11(5):1475-1489.
45. Prabhu SD. Cytokine-induced modulation of cardiac function. Circ Res. 2004;95(12):1140-1153. (Pubitemid 39648205)
46. Das S, Au E, Krazit ST, Pandey KN. Targeted disruption of guanylyl cyclase-A/natriuretic peptide receptor-A gene provokes renal fibrosis and remodeling in null mutant mice: role of proinflammatory cytokines. Endocrinology. 2010;151(12):5841-5850.
47. Kong X, Wang X, Xu W, et al. Natriuretic peptide receptor a as a novel anticancer target. Cancer Res. 2008;68(1):249-256. (Pubitemid 351380126)
48. Oral H, Sivasubramanian N, Dyke DB, et al. Myocardial proinflammatory cytokine expression and left ventricular remodeling in patients with chronic mitral regurgitation. Circulation. 2003;107(6):831-837. (Pubitemid 36241040)
49. Chandrasekar B, Mitchell DH, Colston JT, Freeman GL. Regulation of CCAAT/enhancer binding protein, interleukin-6, interleukin-6 receptor, and gp130 expression during myocardial ischemia/reperfusion. Circulation. 1999;99(3):427-433. (Pubitemid 29051270)
50. Ghorbel MT, Sharman G, Leroux M, et al. Microarray analysis reveals interleukin-6 as a novel secretory product of the hypothalamo-neurohypophyseal system. J Biol Chem. 2003;278(21):19280-19285. (Pubitemid 36799320)
51. Lemke R, Härtig W, Rossner S, Bigl V, Schliebs R. Interleukin-6 is not expressed in activated microglia and in reactive astrocytes in response to lesion of rat basal forebrain cholinergic system as demonstrated by combined in situ hybridization and immunocytochemistry. J Neurosci Res. 1998;51(2):223-236. (Pubitemid 28073030)
52. Ma F, Li Y, Jia L, et al. Macrophage-stimulated cardiac fibroblast production of IL-6 is essential for TGF β/Smad activation and cardiac fibrosis induced by angiotensin II. PloS One. 2012;7(5):e35144.
53. Ono K, Matsumori A, Shioi T, Furukawa Y, Sasayama S. Cytokine gene expression after myocardial infarction in rat hearts: possible implication in left ventricular remodeling. Circulation. 1998;98(2):149-156. (Pubitemid 28317895)
54. Kurrelmeyer KM, Michael LH, Baumgarten G, et al. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci U S A. 2000;97(10):5456-5461. (Pubitemid 30313740)
55. Li YY, Feng YQ, Kadokami T, et al. Myocardial extracellular matrix remodeling in transgenic mice overexpressing tumor necrosis factor α can be modulated by anti-tumor necrosis factor α therapy. Proc Natl Acad Sci U S A. 2000;97(23):12746-12751.
56. Villarreal FJ, Dillmann WH. Cardiac hypertrophy-induced changes in mRNA levels for TGF-β1, fibronectin, and collagen. Am J Physiol. 1992;262(6 Pt 2):H1861-H1866.
57. Morgan HE, Baker KM. Cardiac hypertrophy. Mechanical, neural, and endocrine dependence. Circulation. 1991;83(1):13-25.
58. Sadoshima J, Izumo S. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol. 1997;59:551-571. (Pubitemid 27142455)
59. -/- mice with cardiac hypertrophy and fibrosis. Am J Physiol Heart Circ Physiol. 2002;283(2):H707-H714.
60. Knowles JW, Esposito G, Mao L, et al. Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest. 2001;107(8):975-984. (Pubitemid 32328002)
61. Takimoto E, Champion HC, Li M, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med. 2005;11(2):214-222. (Pubitemid 40321358)
62. Lee DI, Kass DA. Phosphodiesterases and cyclic GMP regulation in heart muscle. Physiology (Bethesda). 2012;27(4):248-258.
63. Kumar R, Cartledge WA, Lincoln TM, Pandey KN. Expression of guanylyl cyclase-A/atrial natriuretic peptide receptor blocks the activation of protein kinase C in vascular smooth muscle cells. Role of cGMP and cGMP-dependent protein kinase. Hypertension. 1997;29(1 Pt 2):414-421. (Pubitemid 27074077)
64. Tripathi S, Pandey KN. Guanylyl cyclase/natriuretic peptide receptor-A signaling antagonizes the vascular endothelial growth factor-stimulated MAPKs and downstream effectors AP-1 and CREB in mouse mesangial cells. Mol Cell Biochem. 2012;368(1-2):47-59.
65. Purcell NH, Molkentin JD. Is nuclear factor κB an attractive therapeutic target for treating cardiac hypertrophy? Circulation. 2003;108(6):638-640. (Pubitemid 36999241)
66. Frantz S, Fraccarollo D, Wagner H, et al. Sustained activation of nuclear factor κB and activator protein 1 in chronic heart failure. Cardiovasc Res. 2003;57(3):749-756. (Pubitemid 36254868)
67. Li Y, Ha T, Gao X, et al. NF-κB activation is required for the development of cardiac hypertrophy in vivo. Am J Physiol Heart Circ Physiol. 2004;287(4):H1712-H1720. (Pubitemid 39313278)
68. Ladetzki-Baehs K, Keller M, Kiemer AK, et al. Atrial natriuretic peptide, a regulator of nuclear factor-κB activation in vivo. Endocrinology. 2007;148(1):332-336. (Pubitemid 46021466)
69. Kiemer AK, Weber NC, Vollmar AM. Induction of IκB: atrial natriuretic peptide as a regulator of the NF-κB pathway. Biochem Biophys Res Commun. 2002;295(5):1068-1076.