The fire within: Cardiac inflammatory signaling in health and disease

Circulation Research

Volumn 110, Issue 1, 2012, Pages 116-125

  Coggins, Matthew ^a   Rosenzweig, Anthony ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

heart failure; ischemia; myocardial inflammation; signal transduction

Indexed keywords

CYTOKINE; ETANERCEPT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INFLIXIMAB; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN INTERACTING WITH PROTEIN KINASE C; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR;

ARTHRITIS; CELL METABOLISM; CELL SURVIVAL; HEART DISEASE; HEART FAILURE; HEMODYNAMIC STRESS; HUMAN; MOLECULAR INTERACTION; MYOCARDITIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW;

ANIMALS; CELL SURVIVAL; HEART DISEASES; HOMEOSTASIS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MODELS, ANIMAL; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION;

EID: 84855384344     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.243196     Document Type: Review

References (92)

1. Majno G. The healing hand; man and wound in the ancient world. Cambridge: Harvard University Press; 1975.
2. Brain P. Galen on bloodletting: a study of the origins, development and validity of his opinions, with a translation of the three works. Cambridge, Cambridgeshire, New York: Cambridge University Press; 1986.
3. Gordon JW, Shaw JA, Kirshenbaum LA. Multiple facets of NF-kappaB in the heart: to be or not to NF-kappaB. Circ Res. 2011;108:1122-1132.
4. Marchant D, Boyd J, Lin D, Granville D, Garmaroudi F, McManus B. Inflammation in myocardial diseases. Circ Res. 2012;110:126-144.
5. Frangogiannis NG. Regulation of the inflammatory response in cardiac repair. Circ Res. 2012;110:159-173.
6. Papaconstantinou J, Hsieh CC, DeFord JH. Signaling pathways in response to inflammation, senescence and aging in the heart. Circ Res. 2012;In press.
7. Kolattukudy PE. Inflammation, ER stress, and autophagy in cardiovascular diseases. Circ Res. 2012;110:174-189.
8. Kaya Z, Leib C, Katus HA. Autoantibodies in heart failure and cardiac dysfunction. Circ Res. 2012;110:145-158.
9. Nagai T, Anzai T, Kaneko H, Mano Y, Anzai A, Maekawa Y, Takahashi T, Meguro T, Yoshikawa T, Fukuda K. C-reactive protein overexpression exacerbates pressure overload-induced cardiac remodeling through enhanced inflammatory response. Hypertension. 2011;57:208-215.
10. Kuster GM, Kotlyar E, Rude MK, Siwik DA, Liao R, Colucci WS, Sam F. Mineralocorticoid receptor inhibition ameliorates the transition to myocardial failure and decreases oxidative stress and inflammation in mice with chronic pressure overload. Circulation. 2005;111: 420-427. (Pubitemid 40204425)
11. Song X, Kusakari Y, Xiao CY, Kinsella SD, Rosenberg MA, Scherrer-Crosbie M, Hara K, Rosenzweig A, Matsui T. mTOR attenuates the inflammatory response in cardiomyocytes and prevents cardiac dysfunction in pathological hypertrophy. Am J Physiol Cell Physiol. 2010; 299:C1256-C1266.
12. Damilano F, Franco I, Perrino C, Schaefer K, Azzolino O, Carnevale D, Cifelli G, Carullo P, Ragona R, Ghigo A, Perino A, Lembo G, Hirsch E. Distinct effects of leukocyte and cardiac phosphoinositide 3-kinase gamma activity in pressure overload-induced cardiac failure. Circulation. 2011;123:391-399.
13. Huang H, Tang QZ, Wang AB, Chen M, Yan L, Liu C, Jiang H, Yang Q, Bian ZY, Bai X, Zhu LH, Wang L, Li H. Tumor suppressor A20 protects against cardiac hypertrophy and fibrosis by blocking transforming growth factor-beta activated kinase 1-dependent signaling. Hypertension. 2010; 56:232-239.
14. Mann DL. The emerging role of innate immunity in the heart and vascular system: for whom the cell tolls. Circ Res. 2011;108:1133-1145.
15. Nishimura M, Naito S. Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol Pharm Bull. 2005;28: 886-892. (Pubitemid 40740661)
16. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, Lee RT, Kelly RA. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest. 1999;104:271-280.
17. Frantz S, Bauersachs J, Ertl G. Post-infarct remodelling: contribution of wound healing and inflammation. Cardiovasc Res. 2009;81:474-481.
18. Birks EJ, Felkin LE, Banner NR, Khaghani A, Barton PJ, Yacoub MH. Increased toll-like receptor 4 in the myocardium of patients requiring left ventricular assist devices. J Heart Lung Transplant. 2004;23:228-235. (Pubitemid 38175301)
19. Chao W, Shen Y, Zhu X, Zhao H, Novikov M, Schmidt U, Rosenzweig A. Lipopolysaccharide improves cardiomyocyte survival and function after serum deprivation. J Biol Chem. 2005;280:21997-22005. (Pubitemid 40827853)
20. Zhu X, Zhao H, Graveline AR, Buys ES, Schmidt U, Bloch KD, Rosenzweig A, Chao W. MyD88 and NOS2 are essential for toll-like receptor 4-mediated survival effect in cardiomyocytes. Am J Physiol Heart Circ Physiol. 2006;291:H1900-H1909. (Pubitemid 44497698)
21. Chao W. Toll-like receptor signaling: a critical modulator of cell survival and ischemic injury in the heart. Am J Physiol Heart Circu Physiol. 2009;296:H1-H12.
22. Kleinbongard P, Heusch G, Schulz R. TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther. 2010; 127:295-314.
23. Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med. 1997;336:1066-1071. (Pubitemid 27163860)
24. Chen LW, Egan L, Li ZW, Greten FR, Kagnoff MF, Karin M. The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemiareperfusion. Nat Med. 2003;9:575-581. (Pubitemid 36597104)
25. Luo JL, Kamata H, Karin M. IKK/NF-kappa B signaling: balancing life and death-a new approach to cancer therapy. J Clin Invest. 2005; 115(10):2625-2632. (Pubitemid 41434385)
26. Hettmann T, DiDonato J, Karin M, Leiden JM. An essential role for nuclear factor kappaB in promoting double positive thymocyte apoptosis. J Exp Med. 1999;189:145-158.
27. Bian X, McAllister-Lucas LM, Shao F, Schumacher KR, Feng Z, Porter AG, Castle VP, Opipari AW Jr. NF-kappa B activation mediates doxorubicin-induced cell death in N-type neuroblastoma cells. J Biol Chem. 2001;276:48921-48929.
28. Mustapha S, Kirshner A, De Moissac D, Kirshenbaum LA. A direct requirement of nuclear factor-kappa B for suppression of apoptosis in ventricular myocytes. Am J Physiol Heart Circ Physiol. 2000;279: H939-H945.
29. Baetz D, Regula KM, Ens K, Shaw J, Kothari S, Yurkova N, Kirshenbaum LA. Nuclear factor-kappaB-mediated cell survival involves transcriptional silencing of the mitochondrial death gene BNIP3 in ventricular myocytes. Circulation. 2005;112:3777-3785. (Pubitemid 43739519)
30. Werner SL, Barken D, Hoffmann A. Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science. 2005;309:1857-1861. (Pubitemid 41325096)
31. Ashida N, Senbanerjee S, Kodama S, Foo SY, Coggins M, Spencer JA, Zamiri P, Shen D, Li L, Sciuto T, Dvorak A, Gerszten RE, Lin CP, Karin M, Rosenzweig A. IKKbeta regulates essential functions of the vascular endothelium through kinase-dependent and-independent pathways. Nat Commun. 2011;2:318.
32. Feldman AM, Combes A, Wagner D, Kadakomi T, Kubota T, You Li YY, McTiernan C. The role of tumor necrosis factor in the pathophysiology of heart failure. J Am Coll Cardiol. 2000;35:537-544. (Pubitemid 30167009)
33. Hall G, Singh IS, Hester L, Hasday JD, Rogers TB. Inhibitor-kappaB kinase-beta regulates LPS-induced TNF-alpha production in cardiac myocytes through modulation of NF-kappaB p65 subunit phosphorylation. Am J Physiol Heart Circ Physiol. 2005;289:H2103-H2111. (Pubitemid 41509428)
34. Levy DE, Marie IJ. RIGging an antiviral defense-it's in the CARDs. Nat Immunol. 2004;5:699-701.
35. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol. 2004;5:730-737. (Pubitemid 39023305)
36. Sun L, Liu S, Chen ZJ. SnapShot: pathways of antiviral innate immunity. Cell. 2010;140:436-436, e432.
37. Ye J, Chen S, Maniatis T. Cardiac glycosides are potent inhibitors of interferon-beta gene expression. Nat Chem Biol. 2011;7:25-33.
38. Prabhu SD. Cytokine-induced modulation of cardiac function. Circ Res. 2004;95:1140-1153. (Pubitemid 39648205)
39. Dawn B, Guo Y, Rezazadeh A, Huang Y, Stein AB, Hunt G, Tiwari S, Varma J, Gu Y, Prabhu SD, Kajstura J, Anversa P, Ildstad ST, Bolli R. Postinfarct cytokine therapy regenerates cardiac tissue and improves left ventricular function. Circ Res. 2006;98:1098-1105.
40. Venkatesan B, Valente AJ, Prabhu SD, Shanmugam P, Delafontaine P, Chandrasekar B. EMMPRIN activates multiple transcription factors in cardiomyocytes, and induces interleukin-18 expression via Rac1-dependent PI3K/Akt/IKK/NF-kappaB andMKK7/JNK/AP-1 signaling. J Mol Cell Cardiol. 2010;49:655-663.
41. Mallat Z, Henry P, Fressonnet R, Alouani S, Scoazec A, Beaufils P, Chvatchko Y, Tedgui A. Increased plasma concentrations of interleukin-18 in acute coronary syndromes. Heart. 2002;88:467-469. (Pubitemid 35221955)
42. Mallat Z, Heymes C, Corbaz A, Logeart D, Alouani S, Cohen-Solal A, Seidler T, Hasenfuss G, Chvatchko Y, Shah AM, Tedgui A. Evidence for altered interleukin 18 (IL)-18 pathway in human heart failure. FASEB J. 2004;18:1752-1754. (Pubitemid 39561673)
43. Reddy VS, Prabhu SD, Mummidi S, Valente AJ, Venkatesan B, Shanmugam P, Delafontaine P, Chandrasekar B. Interleukin-18 induces EMMPRIN expression in primary cardiomyocytes via JNK/Sp1 signaling and MMP-9 in part via EMMPRIN and through AP-1 and NF-kappaB activation. Am J Physiol Heart Circ Physiol. 2010;299:H1242-H1254.
44. Tang YL, Zhu W, Cheng M, Chen L, Zhang J, Sun T, Kishore R, Phillips MI, Losordo DW, Qin G. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res. 2009; 104:1209-1216.
45. Pyo RT, Sui J, Dhume A, Palomeque J, Blaxall BC, Diaz G, Tunstead J, Logothetis DE, Hajjar RJ, Schecter AD. CXCR4 modulates contractility in adult cardiac myocytes. J Mol Cell Cardiol. 2006;41:834-844. (Pubitemid 44635574)
46. Chen J, Chemaly E, Liang L, Kho C, Lee A, Park J, Altman P, Schecter AD, Hajjar RJ, Tarzami ST. Effects of CXCR4 gene transfer on cardiac function after ischemia-reperfusion injury. Am J Pathol. 2010;176: 1705-1715.
47. Agarwal U, Ghalayini W, Dong F, Weber K, Zou YR, Rabbany SY, Rafii S, Penn MS. Role of cardiac myocyte CXCR4 expression in development and left ventricular remodeling after acute myocardial infarction. Circ Res. 2010;107:667-676.
48. Gerszten RE, Garcia-Zepeda EA, Lim YC, Yoshida M, Ding HA, Gimbrone MA Jr, Luster AD, Luscinskas FW, Rosenzweig A. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature. 1999;398:718-723.
49. Gottlieb R. ICE-ing the heart. Circ Res. 2005;96:1036-1038. (Pubitemid 40791374)
50. Frantz S, Ducharme A, Sawyer D, Rohde LE, Kobzik L, Fukazawa R, Tracey D, Allen H, Lee RT, Kelly RA. Targeted deletion of caspase-1 reduces early mortality and left ventricular dilatation following myocardial infarction. J Mol Cell Cardiol. 2003;35:685-694. (Pubitemid 36677452)
51. Syed FM, Hahn HS, Odley A, Guo Y, Vallejo JG, Lynch RA, Mann DL, Bolli R, Dorn GW II. Proapoptotic effects of caspase-1/interleukinconverting enzyme dominate in myocardial ischemia. Circ Res. 2005;96: 1103-1109. (Pubitemid 40791383)
52. Schroder K, Tschopp J. The inflammasomes. Cell. 2010;140:821-832.
53. Tschopp J, Schroder K. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat Rev Immunol. 2010;10:210-215.
54. Ting JP, Duncan JA, Lei Y. How the noninflammasome NLRs function in the innate immune system. Science. 2010;327:286-290.
55. Kawaguchi M, Takahashi M, Hata T, Kashima Y, Usui F, Morimoto H, Izawa A, Takahashi Y, Masumoto J, Koyama J, Hongo M, Noda T, Nakayama J, Sagara J, Taniguchi S, Ikeda U. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation. 2011;123:594-604.
56. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116:3015-3025. (Pubitemid 44684486)
57. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu P-H, Rybkin II, Shelton JM, Manieri M, Cinti S, Schoen FJ, Bassel-Duby R, Rosenzweig A, Ingwall JS, Spiegelman BM. Transcriptional coactivator PGC-1-alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005;1:259.
58. Arany Z, Novikov M, Chin S, Ma Y, Rosenzweig A, Spiegelman BM. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1-alpha. Proc Natl Acad Sci. 2006; 103:10086-10091. (Pubitemid 43993627)
59. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, Flanagan DP, Medeiros DM, Kovacs A, Kelly DP. Transcriptional coactivators PGC-1 alpha and PGC-l beta control overlapping programs required for perinatal maturation of the heart. Gene Devel. 2008;22:1948-1961. (Pubitemid 352008642)
60. Handschin C, Choi CS, Chin S, Kim S, Kawamori D, Kurpad AJ, Neubauer N, Hu J, Mootha VK, Kim YB, Kulkarni RN, Shulman GI, Spiegelman BM. Abnormal glucose homeostasis in skeletal muscle specific PGC-1alpha knockout mice reveals skeletal muscle pancreatic beta cell crosstalk. J Clin Invest. 2007;117:3463-3474. (Pubitemid 350097002)
61. Schilling J, Lai L, Sambandam N, Dey CE, Leone TC, Kelly DP. Toll-like receptor-mediated inflammatory signaling reprograms cardiac energy metabolism by repressing peroxisome proliferator-activated receptor-gamma coactivator-1 signaling. Circ Heart Fail. 2011;4: 474-482.
62. Xue B, Kahn BB. AMPK integrates nutrient and hormonal signals to regulate food intake and energy balance through effects in the hypothalamus and peripheral tissues. J Physiol. 2006;574(Pt 1):73-83. (Pubitemid 43905798)
63. Young LH. AM. P-activated protein kinase conducts the ischemic stress response orchestra. Circulation. 2008;117:832-840. (Pubitemid 351640685)
64. Arad M, Seidman CE, Seidman JG. AMP-activated protein kinase in the heart: role during health and disease. Circ Res. 2007;100: 474-488. (Pubitemid 46673257)
65. Leick L, Fentz J, Bienso RS, Knudsen JG, Jeppesen J, Kiens B, Wojtaszewski JF, Pilegaard H. PGC-1 alpha is required for AICAR-induced expression of GLUT4 and mitochondrial proteins in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2010;299:E456-E465.
66. Miller RA, Birnbaum MJ. An energetic tale of AMPK-independent effects of metformin. J Clin Invest. 2010;120:2267-2270.
67. Fryer LG, Parbu-Patel A, Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J Biol Chem. 2002;277:25226-25232. (Pubitemid 34951829)
68. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, DePinho RA, Montminy M, Cantley LC. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science. 2005;310: 1642-1646. (Pubitemid 41780780)
69. Yang Z, Kahn BB, Shi H, Xue BZ. Macrophage alpha-1 AMP-activated protein kinase (alpha1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J Biol Chem. 2010;285:19051-19059.
70. Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ, Cross JR, Jung E, Thompson CB, Jones RG, Pearce EJ. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood. 2010;115:4742-4749.
71. Roger T, David J, Glauser MP, Calandra T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature. 2001;414: 920-924. (Pubitemid 34024744)
72. Yu CM, Lai KW, Chen YX, Huang XR, Lan HY. Expression of macrophage migration inhibitory factor in acute ischemic myocardial injury. J Histochem Cytochem. 2003;51:625-631. (Pubitemid 36520618)
73. Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R. MIF as a glucocorticoid-induced modulator of cytokine production. Nature. 1995;377:68-71.
74. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature. 2008;451:578-582. (Pubitemid 351186266)
75. Qi D, Hu X, Wu X, Merk M, Leng L, Bucala R, Young LH. Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischemia/reperfusion. J Clin Invest. 2009;119: 3807-3816.
76. Baran KW, Nguyen M, McKendall GR, Lambrew CT, Dykstra G, Palmeri ST, Gibbons RJ, Borzak S, Sobel BE, Gourlay SG, Rundle AC, Gibson CM, Barron HV, Limitation of Myocardial Infarction Following Thrombolysis in Acute Myocardial Infarction (LIMIT AMI) Study Group. Double-blind, randomized trial of an anti-CD18 antibody in conjunction with recombinant tissue plasminogen activator for acute myocardial infarction: limitation of myocardial infarction following thrombolysis in acute myocardial infarction (LIMIT AMI) study. Circulation. 2001;104: 2778-2783. (Pubitemid 33126650)
77. Faxon DP, Gibbons RJ, Chronos NAF, Gurbel PA, Sheehan F, HALT-MI Investigators. The effect of blockade of the CD11/CD18 integrin receptor on infarct size in patients with acute myocardial infarction treated with direct angioplasty: the results of the HALT-MI study. J Am Coll Cardiol. 2002;40:1199-1204.
78. Kwon HJ, Cote TR, Cuffe MS, Kramer JM, Braun MM. Case reports of heart failure after therapy with a tumor necrosis factor antagonist. Ann Intern Med. 2003;138:807-811.
79. Mann DL, McMurray JJ, Packer M, Swedberg K, Borer JS, Colucci WS, Djian J, Drexler H, Feldman A, Kober L, Krum H, Liu P, Nieminen M, Tavazzi L, van Veldhuisen DJ, Waldenstrom A, Warren M, Westheim A, Zannad F, Fleming T. Targeted anticytokine therapy in patients with chronic heart failure: results of the Randomized Etanercept Worldwide Evaluation (RENEWAL). Circulation. 2004; 109:1594-1602. (Pubitemid 38451714)
80. Chung ES, Packer M, Lo KH, Fasanmade AA, Willerson JT, Anti-TNF Therapy Against Congestive Heart Failure Investigators. Randomized, double-blind, placebo-controlled, pilot trial of infliximab, a chimeric monoclonal antibody to tumor necrosis factor-alpha, in patients with moderate-to-severe heart failure: results of the anti-TNF Therapy Against Congestive Heart Failure (ATTACH) trial. Circulation. 2003;107: 3133-3140. (Pubitemid 36793081)
81. Wojnicz R, Nowalany-Kozielska E, Wojciechowska C, Glanowska G, Wilczewski P, Niklewski T, Zembala M, Polonski L, Rozek MM, Wodniecki J. Randomized, placebo-controlled study for immunosuppressive treatment of inflammatory dilated cardiomyopathy: two-year follow-up results. Circulation. 2001;104:39-45. (Pubitemid 32623287)
82. Cooper LT Jr, Hare JM, Tazelaar HD, Edwards WD, Starling RC, Deng MC, Menon S, Mullen GM, Jaski B, Bailey KR, Cunningham MW, Dec GW, Giant Cell Myocarditis Treatment Trial Investigators. Usefulness of immunosuppression for giant cell myocarditis. Am J Cardiol. 2008;102: 1535-1539.
83. Frustaci A, Russo MA, Chimenti C. Randomized study on the efficacy of immunosuppressive therapy in patients with virus-negative inflam-matory cardiomyopathy: the TIMIC study. Eur Heart J. 2009;30: 1995-2002.
84. Schroder K, Muruve DA, Tschopp J. Innate immunity: cytoplasmic DNA sensing by the AIM2 inflammasome. Curr Biol. 2009;19: R262-R265.
85. Frantz S, Kelly RA, Bourcier T. Role of TLR-2 in the activation of nuclear factor kappaB by oxidative stress in cardiac myocytes. J Biol Chem. 2001;276:5197-5203.
86. Blyszczuk P, Kania G, Dieterle T, Marty RR, Valaperti A, Berthonneche C, Pedrazzini T, Berger CT, Dirnhofer S, Matter CM, Penninger JM, Luscher TF, Eriksson U. Myeloid differentiation factor-88/interleukin-1 signaling controls cardiac fibrosis and heart failure progression in inflammatory dilated cardiomyopathy. Circ Res. 2009;105:912-920.
87. Cook SA, Novikov MS, Ahn Y, Matsui T, Rosenzweig A. A20 is dynamically regulated in the heart and inhibits the hypertrophic response. Circulation. 2003;108:664-667. (Pubitemid 36999248)
88. Shaw J, Yurkova N, Zhang T, Gang H, Aguilar F, Weidman D, Scramstad C, Weisman H, Kirshenbaum LA. Antagonism of E2F-1 regulated Bnip3 transcription by NF-kappaB is essential for basal cell survival. Proc Natl Acad Sci USA. 2008;105:20734-20739.
89. Kubota T, McTiernan CF, Frye CS, Slawson SE, Lemster BH, Koretsky AP, Demetris AJ, Feldman AM. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circ Res. 1997;81:627-635. (Pubitemid 27432751)
90. Bryant D, Becker L, Richardson J, Shelton J, Franco F, Peshock R, Thompson M, Giroir B. Cardiac failure in transgenic mice with myocardial expression of tumor necrosis factor-alpha. Circulation. 1998;97: 1375-1381. (Pubitemid 28182676)
91. Kawano S, Kubota T, Monden Y, Tsutsumi T, Inoue T, Kawamura N, Tsutsui H, Sunagawa K. Blockade of NF-kappaB improves cardiac function and survival after myocardial infarction. Am J Physiol Heart Circ Physiol. 2006;291:H1337-H1344. (Pubitemid 44343679)
92. Hamid T, Guo SZ, Kingery JR, Xiang X, Dawn B, Prabhu SD. Cardiomyocyte NF-kappaB p65 promotes adverse remodelling, apoptosis, and endoplasmic reticulum stress in heart failure. Cardiovasc Res. 2011;89:129-138.