Double-stranded RNA-dependent protein kinase deficiency protects the heart from systolic overload-induced congestive heart failure

Circulation

Volumn 129, Issue 13, 2014, Pages 1397-1406

  Wang, Huan ^a   Xu, Xin ^a   Fassett, John ^a   Kwak, Dongmin ^a   Liu, Xiaoyu ^a,b   Hu, Xinli ^a,c   Falls, Therasa J ^d   Bell, John C ^d   Li, Hongliang ^e   Bitterman, Peter ^a   Bache, Robert J ^a   Chen, Yingjie ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b TONGJI UNIVERSITY   (China)

^c PEKING UNIVERSITY   (China)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

Author keywords

apoptosis; heart failure; inflammation; innate immunity; protein kinases R; translation initiation; translation regulation

Indexed keywords

CASPASE; LIPOPOLYSACCHARIDE; PROTEIN KINASE R; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; BONE MARROW CELL; CONGESTIVE HEART FAILURE; CONTROLLED STUDY; ENZYME DEFICIENCY; HEART LEFT VENTRICLE CONTRACTILITY; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART SIZE; HEART VENTRICLE OVERLOAD; HUMAN; HUMAN TISSUE; LEUKOCYTE; LUNG CONGESTION; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

APOPTOSIS; HEART FAILURE; INFLAMMATION; INNATE IMMUNITY; PROTEIN KINASES R; TRANSLATION INITIATION; TRANSLATION REGULATION;

ADULT; AGED; ANIMALS; AORTA; APOPTOSIS; BLOOD PRESSURE; CYTOKINES; DISEASE MODELS, ANIMAL; EIF-2 KINASE; FEMALE; HEART FAILURE; HEMODYNAMICS; HUMANS; HYPERTROPHY; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MYOCYTES, CARDIAC; UP-REGULATION; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84898059190     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.002209     Document Type: Article

References (39)

1. Williams BR. PKR: a sentinel kinase for cellular stress. Oncogene. 1999;18:6112-6120.
2. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-264.
3. Li G, Scull C, Ozcan L, Tabas I. NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis. J Cell Biol. 2010;191:1113-1125.
4. Nakamura T, Furuhashi M, Li P, Cao H, Tuncman G, Sonenberg N, Gorgun CZ, Hotamisligil GS. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell. 2010;140:338-348.
5. Wang J, Laschinger C, Zhao XH, Mak B, Seth A, McCulloch CA. Mechanical force activates eIF-2alpha phospho-kinases in fibroblast. Biochem Biophys Res Commun. 2005;330:123-130.
6. Asakura Y, Fujiwara Y, Kato N, Sato Y, Komatsu T. Serine/threonine kinase PKR: a sentinel kinase that discriminates a signaling pathway mediated by TLR4 from those mediated by TLR3 and TLR9. Am J Hematol. 2007;82:640-642.
7. Romano PR, Garcia-Barrio MT, Zhang X, Wang Q, Taylor DR, Zhang F, Herring C, Mathews MB, Qin J, Hinnebusch AG. Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2alpha kinases PKR and GCN2. Mol Cell Biol. 1998;18:2282-2297.
8. Kumar A, Haque J, Lacoste J, Hiscott J, Williams BR. Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc Natl Acad Sci USA. 1994;91:6288-6292.
9. Couturier J, Morel M, Pontcharraud R, Gontier V, Fauconneau B, Paccalin M, Page G. Interaction of double-stranded RNA-dependent protein kinase (PKR) with the death receptor signaling pathway in amyloid beta (Abeta)-treated cells and in APPSLPS1 knock-in mice. J Biol Chem. 2010;285:1272-1282.
10. von Roretz C, Gallouzi IE. Protein kinase RNA/FADD/caspase-8 pathway mediates the proapoptotic activity of the RNA-binding protein human antigen R (HuR). J Biol Chem. 2010;285:16806-16813.
11. Balachandran S, Kim CN, Yeh WC, Mak TW, Bhalla K, Barber GN. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 1998;17:6888-6902.
12. Lu Z, Xu X, Hu X, Lee S, Traverse JH, Zhu G, Fassett J, Tao Y, Zhang P, dos Remedios C, Pritzker M, Hall JL, Garry DJ, Chen Y. Oxidative stress regulates left ventricular PDE5 expression in the failing heart. Circulation. 2010;121:1474-1483.
13. Kadokami T, Frye C, Lemster B, Wagner CL, Feldman AM, McTiernan CF. Anti-tumor necrosis factor-alpha antibody limits heart failure in a transgenic model. Circulation. 2001;104:1094-1097.
14. Stewart MJ, Blum MA, Sherry B. PKR's protective role in viral myocarditis. Virology. 2003;314:92-100.
15. Abraham N, Stojdl DF, Duncan PI, Méthot N, Ishii T, Dubé M, Vanderhyden BC, Atkins HL, Gray DA, McBurney MW, Koromilas AE, Brown EG, Sonenberg N, Bell JC. Characterization of transgenic mice with targeted disruption of the catalytic domain of the double-stranded RNA-dependent protein kinase, PKR. J Biol Chem. 1999;274:5953-5962.
16. Blalock WL, Bavelloni A, Piazzi M, Tagliavini F, Faenza I, Martelli AM, Follo MY, Cocco L. Multiple forms of PKR present in the nuclei of acute leukemia cells represent an active kinase that is responsive to stress. Leukemia. 2011;25:236-245.
17. Lu B, Nakamura T, Inouye K, Li J, Tang Y, Lundbäck P, Valdes-Ferrer SI, Olofsson PS, Kalb T, Roth J, Zou Y, Erlandsson-Harris H, Yang H, Ting JP, Wang H, Andersson U, Antoine DJ, Chavan SS, Hotamisligil GS, Tracey KJ. Novel role of PKR in inflammasome activation and HMGB1 release. Nature. 2012;488:670-674.
18. Wencker D, Chandra M, Nguyen K, Miao W, Garantziotis S, Factor SM, Shirani J, Armstrong RC, Kitsis RN. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest. 2003;111:1497-1504.
19. Condorelli G, Morisco C, Stassi G, Notte A, Farina F, Sgaramella G, de Rienzo A, Roncarati R, Trimarco B, Lembo G. Increased cardiomyocyte apoptosis and changes in proapoptotic and antiapoptotic genes bax and bcl-2 during left ventricular adaptations to chronic pressure overload in the rat. Circulation. 1999;99:3071-3078.
20. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA, Quaini E, Di Loreto C, Beltrami CA, Krajewski S, Reed JC, Anversa P. Apoptosis in the failing human heart. N Engl J Med. 1997;336:1131-1141.
21. Yeung MC, Liu J, Lau AS. An essential role for the interferon-inducible, double-stranded RNA-activated protein kinase PKR in the tumor necrosis factor-induced apoptosis in U937 cells. Proc Natl Acad Sci USA. 1996;93:12451-12455.
22. Der SD, Yang YL, Weissmann C, Williams BR. A double-stranded RNA-activated protein kinase-dependent pathway mediating stress-induced apoptosis. Proc Natl Acad Sci USA. 1997;94:3279-3283.
23. Timmers L, Sluijter JP, van Keulen JK, Hoefer IE, Nederhoff MG, Goumans MJ, Doevendans PA, van Echteld CJ, Joles JA, Quax PH, Piek JJ, Pasterkamp G, de Kleijn DP. Toll-like receptor 4 mediates maladaptive left ventricular remodeling and impairs cardiac function after myocardial infarction. Circ Res. 2008;102:257-264.
24. Eissler R, Schmaderer C, Rusai K, Kühne L, Sollinger D, Lahmer T, Witzke O, Lutz J, Heemann U, Baumann M. Hypertension augments cardiac Tolllike receptor 4 expression and activity. Hypertens Res. 2011;34:551-558.
25. Goh KC, deVeer MJ, Williams BR. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 2000;19:4292-4297.
26. Cabanski M, Steinmüller M, Marsh LM, Surdziel E, Seeger W, Lohmeyer J. PKR regulates TLR2/TLR4-dependent signaling in murine alveolar macrophages. Am J Respir Cell Mol Biol. 2008;38:26-31.
27. Sullivan DE, Ferris BM, Nguyen H, Abboud E, Brody AR. TNF-α induces TGFβ1-expression in lung fibroblasts at the transcriptional level via AP-1 activation. J Cell Mol Med. 2009;13:1866-1876.
28. Srivastava SP, Kumar KU, Kaufman RJ. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J Biol Chem. 1998;273:2416-2423.
29. Gullestad L, Ueland T, Vinge LE, Finsen A, Yndestad A, Aukrust P. Inflammatory cytokines in heart failure: mediators and markers. Cardiology. 2012;122:23-35.
30. Haudek SB, Taffet GE, Schneider MD, Mann DL. TNF provokes cardiomyocyte apoptosis and cardiac remodeling through activation of multiple cell death pathways. J Clin Invest. 2007;117:2692-2701.
31. Dhingra S, Bagchi AK, Ludke AL, Sharma AK, Singal PK. Akt regulates IL-10 mediated suppression of TNFalpha-induced cardiomyocyte apoptosis by upregulating Stat3 phosphorylation. PLoS One. 2011;6:e25009.
32. Wang X, Fan Z, Wang B, Luo J, Ke ZJ. Activation of double-stranded RNA-activated protein kinase by mild impairment of oxidative metabolism in neurons. J Neurochem. 2007;103:2380-2390.
33. Sharma B, Altman JK, Goussetis DJ, Verma AK, Platanias LC. Protein kinase R as mediator of the effects of interferon (IFN) gamma and tumor necrosis factor (TNF) alpha on normal and dysplastic hematopoiesis. J Biol Chem. 2011;286:27506-27514.
34. Goh KC, deVeer MJ, Williams BR. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 2000;19:4292-4297.
35. Williams BR. Signal integration via PKR. Sci STKE. 2001;2001:re2.
36. Cabanski M, Steinmüller M, Marsh LM, Surdziel E, Seeger W, Lohmeyer J. PKR regulates TLR2/TLR4-dependent signaling in murine alveolar macrophages. Am J Respir Cell Mol Biol. 2008;38:26-31.
37. Sun M, Chen M, Dawood F, Zurawska U, Li JY, Parker T, Kassiri Z, Kirshenbaum LA, Arnold M, Khokha R, Liu PP. Tumor necrosis factor-alpha mediates cardiac remodeling and ventricular dysfunction after pressure overload state. Circulation. 2007;115:1398-1407.
38. Bracey NA, Beck PL, Muruve DA, Hirota SA, Guo J, Jabagi H, Wright JR Jr, Macdonald JA, Lees-Miller JP, Roach D, Semeniuk LM, Duff HJ. The Nlrp3 Inflammasome promotes myocardial dysfunction in structural cardiomyopathy through IL-1β. Exp Physiol. 2013;98:462-472.
39. Scheuner D, Patel R, Wang F, Lee K, Kumar K, Wu J, Nilsson A, Karin M, Kaufman RJ. Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem. 2006;281:21458-21468.