Ca2+/calmodulin-dependent kinase II triggers cell membrane injury by inducing complement factor B gene expression in the mouse heart

Journal of Clinical Investigation

Volumn 119, Issue 4, 2009, Pages 986-996

  Singh, Madhu V ^a   Kapoun, Ann ^b   Higgins, Linda ^c   Kutschke, William ^a   Thurman, Joshua M ^d   Zhang, Rong ^e   Singh, Minati ^f   Yang, Jinying ^a   Guan, Xiaoqun ^a   Lowe, John S ^a   Weiss, Robert M ^a   Zimmermann, Kathy ^g   Yull, Fiona E ^h   Blackwell, Timothy S ^h   Mohler, Peter J ^a   Anderson, Mark E ^a  

^a UNIVERSITY OF IOWA   (United States)

^b OncoMed Pharmaceuticals Inc   (United States)

^c InteKrin Therapeutics Inc   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^f E11 SSH   (United States)

^g VETERANS AFFAIRS MEDICAL CENTER   (United States)

^h VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; ENDOTOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTATE DEHYDROGENASE; MESSENGER RNA; AC3 I PEPTIDE; AC3-I PEPTIDE; LIPOPOLYSACCHARIDE; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL MEMBRANE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEART; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HEART MUSCLE; METABOLISM; MOUSE MUTANT; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL MEMBRANE; COMPLEMENT FACTOR B; GENE EXPRESSION; GENE EXPRESSION PROFILING; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES; RNA, MESSENGER;

EID: 65249154058     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI35814     Document Type: Article

References (64)

1. Schulman, H., and Greengard, P. 1978. Ca2+-dependent protein phosphorylation system in membranes from various tissues, and its activation by "calcium-dependent regulator". Proc. Natl. Acad. Sci. U. S. A. 75:5432-5436.
2. Erickson, J.R., et al. 2008. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell. 133:462-474.
3. Zhang, R., et al. 2005. Calmodulin kinase II inhibition protects against structural heart disease. Nat. Med. 11:409-417.
4. Yang, Y., et al. 2006. Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am. J. Physiol. Heart Circ. Physiol. 291:H3065-H3075.
5. Grueter, C.E., Abiria, S.A., Wu, Y., Anderson, M.E., and Colbran, R.J. 2008. Differential regulated interactions of calcium/calmodulin-dependent protein kinase II with isoforms of voltage-gated calcium channel beta subunits. Biochemistry. 47:1760-1767.
6. Wagner, S., et al. 2006. Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J. Clin. Invest. 116:3127-3138.
7. Wu, X., et al. 2006. Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitationtranscription coupling. J. Clin. Invest. 116:675-682.
8. Braunwald, E. 2008. Biomarkers in heart failure. N. Engl. J. Med. 358:2148-2159.
9. Knuefermann, P., Vallejo, J., and Mann, D.L. 2004. The role of innate immune responses in the heart in health and disease. Trends Cardiovasc. Med. 14:1-7.
10. Ridker, P.M. 2007. Inflammatory biomarkers and risks of myocardial infarction, stroke, diabetes, and total mortality: implications for longevity. Nutr. Rev. 65:S253-S259.
11. Mann, D.L. 2003. Stress-activated cytokines and the heart: from adaptation to maladaptation. Annu. Rev. Physiol. 65:81-101.
12. Malave, H.A., Taylor, A.A., Nattama, J., Deswal, A., and Mann, D.L. 2003. Circulating levels of tumor necrosis factor correlate with indexes of depressed heart rate variability: a study in patients with mildto-moderate heart failure. Chest. 123:716-724.
13. Feldman, A.M., et al. 2000. The role of tumor necrosis factor in the pathophysiology of heart failure. J. Am. Coll. Cardiol. 35:537-544.
14. Yasojima, K., Schwab, C., McGeer, E.G., and McGeer, P.L. 1998. Human heart generates complement proteins that are upregulated and activated after myocardial infarction. Circ. Res. 83:860-869.
15. Yasojima, K., Kilgore, K.S., Washington, R.A., Lucchesi, B.R., and McGeer, P.L. 1998. Complement gene expression by rabbit heart: upregulation by ischemia and reperfusion. Circ. Res. 82:1224-1230.
16. Vakeva, A.P., et al. 1998. Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: role of the terminal complement components and inhibition by anti-C5 therapy. Circulation. 97:2259-2267.
17. Rossen, R.D., et al. 1985. Selective accumulation of the first component of complement and leukocytes in ischemic canine heart muscle. A possible initiator of an extra myocardial mechanism of ischemic injury. Circ. Res. 57:119-130.
18. Pinckard, R.N., et al. 1975. Consumption of classical complement components by heart subcellular membranes in vitro and in patients after acute myocardial infarction. J. Clin. Invest. 56:740-750.
19. Gros, P., Milder, F.J., and Janssen, B.J. 2008. Complement driven by conformational changes. Nat. Rev. Immunol. 8:48-58.
20. Afanasyeva, M., and Rose, N.R. 2002. Cardiomyopathy is linked to complement activation. Am. J. Pathol. 161:351-357.
21. Yang, I., et al. 2002. Within the fold: assessing differential expression measures and reproducibility in microarray assays. Genome Biol. 3:research0062.01-research0062.12.
22. Gulick, J., Subramaniam, A., Neumann, J., and Robbins, J. 1991. Isolation and characterization of the mouse cardiac myosin heavy chain genes. J. Biol. Chem. 266:9180-9185.
23. Homeister, J.W., Satoh, P., and Lucchesi, B.R. 1992. Effects of complement activation in the isolated heart. Role of the terminal complement components. Circ. Res. 71:303-319.
24. Matsumoto, M., et al. 1997. Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc. Natl. Acad. Sci. U. S. A. 94:8720-8725.
25. Parra, V., et al. 2008. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc. Res. 77:387-397.
26. Takeda, K., Kaisho, T., and Akira, S. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335-376.
27. Moynagh, P.N. 2005. The NF-kappaB pathway. J. Cell Sci. 118:4589-4592.
28. Schreiber, J., et al. 2006. Coordinated binding of NF-kappaB family members in the response of human cells to lipopolysaccharide. Proc. Natl. Acad. Sci. U. S. A. 103:5899-5904.
29. Blackwell, T.S., et al. 2000. Multiorgan nuclear factor kappa B activation in a transgenic mouse model of systemic inflammation. Am. J. Respir. Crit. Care Med. 162:1095-1101.
30. Chang, B.H., Mukherji, S., and Soderling, T.R. 1998. Characterization of a calmodulin kinase II inhibitor protein in brain. Proc. Natl. Acad. Sci. U. S. A. 95:10890-10895.
31. Huang, Y., Krein, P.M., Muruve, D.A., and Winston, B.W. 2002. Complement factor B gene regulation: synergistic effects of TNF-alpha and IFN-gamma in macrophages. J. Immunol. 169:2627-2635.
32. Irwin, M.W., et al. 1999. Tissue expression and immunolocalization of tumor necrosis factoralpha in postinfarction dysfunctional myocardium. Circulation. 99:1492-1498.
33. Bryant, D., et al. 1998. Cardiac failure in transgenic mice with myocardial expression of tumor necrosis factor-{alpha}. Circulation. 97:1375-1381.
34. Nathan, C. 2002. Points of control in inflammation. Nature. 420:846-852.
35. Frangogiannis, N.G., Smith, C.W., and Entman, M.L. 2002. The inflammatory response in myocardial infarction. Cardiovasc. Res. 53:31-47.
36. Entman, M.L., and Smith, C.W. 1994. Postreperfusion inflammation: a model for reaction to injury in cardiovascular disease. Cardiovasc. Res. 28:1301-1311.
37. Entman, M.L., et al. 1991. Inflammation in the course of early myocardial ischemia. FASEB J. 5:2529-2537.
38. Vallance, P., Collier, J., and Bhagat, K. 1997. Infection, inflammation, and infarction: does acute endothelial dysfunction provide a link? Lancet. 349:1391-1392.
39. Taqueti, V.R., Mitchell, R.N., and Lichtman, A.H. 2006. Protecting the pump: controlling myocardial inflammatory responses. Annu. Rev. Physiol. 68:67-95.
40. Riedemann, N.C., and Ward, P.A. 2003. Complement in ischemia reperfusion injury. Am. J. Pathol. 162:363-367.
41. Maier, L.S., and Bers, D.M. 2007. Role of Ca2+/ calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc. Res. 73:631-640.
42. Backs, J., Song, K., Bezprozvannaya, S., Chang, S., and Olson, E.N. 2006. CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J. Clin. Invest. 116:1853-1864.
43. Meffert, M.K., Chang, J.M., Wiltgen, B.J., Fanselow, M.S., and Baltimore, D. 2003. NF-kappa B functions in synaptic signaling and behavior. Nat. Neurosci. 6:1072-1078.
44. Jang, M.K., et al. 2001. Ca2+/calmodulin-dependent protein kinase IV stimulates nuclear factorkappa B transactivation via phosphorylation of the p65 subunit. J. Biol. Chem. 276:20005-20010.
45. Ishiguro, K., et al. 2006. Ca2+/calmodulin-dependent protein kinase II is a modulator of CARMA1-mediated NF-kappaB activation. Mol. Cell. Biol. 26:5497-5508.
46. Hughes, K., Edin, S., Antonsson, A., and Grundstrom, T. 2001. Calmodulin-dependent kinase II mediates T cell receptor/CD3- and phorbol esterinduced activation of IkappaB kinase. J. Biol. Chem. 276:36008-36013.
47. Zwaka, T.P., et al. 2002. Complement and dilated cardiomyopathy: a role of sublytic terminal complement complex-induced tumor necrosis factoralpha synthesis in cardiac myocytes. Am. J. Pathol. 161:449-457.
48. Kilgore, K.S., et al. 1997. Sublytic concentrations of the membrane attack complex of complement induce endothelial interleukin-8 and monocyte chemoattractant protein-1 through nuclear factorkappa B activation. Am. J. Pathol. 150:2019-2031.
49. Reiter, Y., Ciobotariu, A., and Fishelson, Z. 1992. Sublytic complement attack protects tumor cells from lytic doses of antibody and complement. Eur. J. Immunol. 22:1207-1213.
50. Oyama, J., et al. 2004. Reduced myocardial isch emia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation. 109:784-789.
51. Hua, F., et al. 2005. Blocking the MyD88-dependent pathway protects the myocardium from ischemia/reperfusion injury in rat hearts. Biochem. Biophys. Res. Commun. 338:1118-1125.
52. Gupta, S., Purcell, N.H., Lin, A., and Sen, S. 2002. Activation of nuclear factor-kappaB is necessary for myotrophin-induced cardiac hypertrophy. J. Cell Biol. 159:1019-1028.
53. Li, H.-L., et al. 2007. Targeted cardiac overexpression of A20 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction. Circulation. 115:1885-1894.
54. Misra, A., et al. 2003. Nuclear factor-{kappa}B protects the adult cardiac myocyte against ischemiainduced apoptosis in a murine model of acute myocardial infarction. Circulation. 108:3075-3078.
55. Moss, N.C., Stansfield, W.E., Willis, M.S., Tang, R.-H., and Selzman, C.H. 2007. IKKbeta inhibition attenuates myocardial injury and dysfunction following acute ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 293:H2248-H2253.
56. Zhang, T., et al. 2002. The cardiac-specific nuclear delta B isoform of Ca2+/calmodulin-dependent protein kinase II induces hypertrophy and dilated cardiomyopathy associated with increased protein phosphatase 2A activity. J. Biol. Chem. 277:1261-1267.
57. Zhang, T., and Brown, J.H. 2004. Role of Ca2+/ calmodulin-dependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc. Res. 63:476-486.
58. Li, J., et al. 2006. Calmodulin kinase II inhibition shortens action potential duration by upregulation of K+ currents. Circ. Res. 99:1092-1099.
59. Khoo, M.S.C., et al. 2006. Death, cardiac dysfunction, and arrhythmias are increased by calmodulin kinase II in calcineurin cardiomyopathy. Circulation. 114:1352-1359.
60. Maier, L.S., and Bers, D.M. 2002. Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J. Mol. Cell. Cardiol. 34:919-939.
61. Arni, S., Keilbaugh, S.A., Ostermeyer, A.G., and Brown, D.A. 1998. Association of GAP-43 with detergent-resistant membranes requires two palmitoylated cysteine residues. J. Biol. Chem. 273:28478-28485.
62. Kapoun, A.M., et al. 2004. B-type natriuretic peptide exerts broad functional opposition to transforming growth factor-beta in primary human cardiac fibroblasts: fibrosis, myofibroblast conversion, proliferation, and inflammation. Circ. Res. 94:453-461.
63. Weiss, R.M., Ohashi, M., Miller, J.D., Young, S.G., and Heistad, D.D. 2006. Calcific aortic valve stenosis in old hypercholesterolemic mice. Circulation. 114:2065-2069.
64. Dignam, J.D., Lebovitz, R.M., and Roeder, R.G. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.