Induction of the matricellular protein CCN1 through RhoA and MRTF-A contributes to ischemic cardioprotection

Journal of Molecular and Cellular Cardiology

Volumn 75, Issue , 2014, Pages 152-161

  Zhao, Xia ^a   Ding, Eric Y ^a   Yu, Olivia M ^a   Xiang, Sunny Y ^a   Tan Sah, Valerie P ^a   Yung, Bryan S ^a   Hedgpeth, Joe ^a   Neubig, Richard R ^b   Lau, Lester F ^c   Brown, Joan Heller ^a   Miyamoto, Shigeki ^a  

^a San Diego   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Cardioprotection; CCN1; GPCRs; MRTF A; RhoA

Indexed keywords

CARBACHOL; CELL PROTEIN; CYSTEINE RICH PROTEIN 61; ENDOTHELIN 1; ISOPRENALINE; LYSOPHOSPHATIDIC ACID; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; PHENYLEPHRINE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK PROTEIN; SPHINGOSINE 1 PHOSPHATE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; G PROTEIN COUPLED RECEPTOR; LYSOPHOSPHOLIPID; MYOCARDIN-RELATED TRANSCRIPTION FACTOR-A, RAT; PROTEIN BINDING; SMALL INTERFERING RNA; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME BINDING; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; CELL NUCLEUS; CYTOLOGY; DRUG EFFECTS; HEART VENTRICLE; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

MUS; RATTUS;

ANIMALS; ANIMALS, NEWBORN; CARDIOTONIC AGENTS; CELL MEMBRANE; CELL NUCLEUS; CYSTEINE-RICH PROTEIN 61; HEART VENTRICLES; IN VITRO TECHNIQUES; LYSOPHOSPHOLIPIDS; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; REPERFUSION INJURY; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SPHINGOSINE; TRANSCRIPTION FACTORS;

EID: 84922804601     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.07.017     Document Type: Article

References (66)

1. O'Brien T.P., Yang G.P., Sanders L., Lau L.F. Expression of Cyr61, a growth factor-inducible immediate-early gene. Mol Cell Biol Jul 1990, 10(7):3569-3577.
2. Lau L.F. CCN1/Cyr61: the very model of a modern matricellular protein. Cell Mol Life Sci Oct 2011, 68(19):3149-3163.
3. Jun J.I., Lau L.F. Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov Dec 2011, 10(12):945-963.
4. Chen C.C., Young J.L., Monzon R.I., Chen N., Todorovic V., Lau L.F. Cytotoxicity of TNFalpha is regulated by integrin-mediated matrix signaling. EMBO J Mar 7 2007, 26(5):1257-1267.
5. Hsu P.L., Su B.C., Kuok Q.Y., Mo F.E. Extracellular matrix protein CCN1 regulates cardiomyocyte apoptosis in mice with stress-induced cardiac injury. Cardiovasc Res Apr 1 2013, 98(1):64-72.
6. Walsh C.T., Radeff-Huang J., Matteo R., Hsiao A., Subramaniam S., Stupack D., et al. Thrombin receptor and RhoA mediate cell proliferation through integrins and cysteine-rich protein 61. FASEB J Nov 2008, 22(11):4011-4021.
7. Yoshida Y., Togi K., Matsumae H., Nakashima Y., Kojima Y., Yamamoto H., et al. CCN1 protects cardiac myocytes from oxidative stress via beta1 integrin-Akt pathway. Biochem Biophys Res Commun Apr 13 2007, 355(3):611-618.
8. Walsh C.T., Stupack D., Brown J.H. G protein-coupled receptors go extracellular: RhoA integrates the integrins. Mol Interv Aug 2008, 8(4):165-173.
9. Young N., Pearl D.K., Van Brocklyn J.R. Sphingosine-1-phosphate regulates glioblastoma cell invasiveness through the urokinase plasminogen activator system and CCN1/Cyr61. Mol Cancer Res Jan 2009, 7(1):23-32.
10. Young N., Van Brocklyn J.R. Roles of sphingosine-1-phosphate (S1P) receptors in malignant behavior of glioma cells. Differential effects of S1P2 on cell migration and invasiveness. Exp Cell Res May 1 2007, 313(8):1615-1627.
11. Hanna M., Liu H., Amir J., Sun Y., Morris S.W., Siddiqui M.A., et al. Mechanical regulation of the proangiogenic factor CCN1/CYR61 gene requires the combined activities of MRTF-A and CREB-binding protein histone acetyltransferase. J Biol Chem Aug 21 2009, 284(34):23125-23136.
12. Tamura I., Rosenbloom J., Macarak E., Chaqour B. Regulation of Cyr61 gene expression by mechanical stretch through multiple signaling pathways. Am J Physiol Cell Physiol Nov 2001, 281(5):C1524-C1532.
13. Hill C.S., Wynne J., Treisman R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell Jun 30 1995, 81(7):1159-1170.
14. Gauthier-Rouviere C., Cavadore J.C., Blanchard J.M., Lamb N.J., Fernandez A. p67SRF is a constitutive nuclear protein implicated in the modulation of genes required throughout the G1 period. Cell Regul Jul 1991, 2(7):575-588.
15. Hill C.S., Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell Jan 27 1995, 80(2):199-211.
16. Vartiainen M.K., Guettler S., Larijani B., Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science Jun 22 2007, 316(5832):1749-1752.
17. Shore P., Sharrocks A.D. The MADS-box family of transcription factors. Eur J Biochem Apr 1 1995, 229(1):1-13.
18. Wang D.Z., Li S., Hockemeyer D., Sutherland L., Wang Z., Schratt G., et al. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A Nov 12 2002, 99(23):14855-14860.
19. Lockman K., Hinson J.S., Medlin M.D., Morris D., Taylor J.M., Mack C.P. Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J Biol Chem Oct 8 2004, 279(41):42422-42430.
20. Miralles F., Posern G., Zaromytidou A.I., Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell May 2 2003, 113(3):329-342.
21. Kuwahara K., Kinoshita H., Kuwabara Y., Nakagawa Y., Usami S., Minami T., et al. Myocardin-related transcription factor A is a common mediator of mechanical stress- and neurohumoral stimulation-induced cardiac hypertrophic signaling leading to activation of brain natriuretic peptide gene expression. Mol Cell Biol Sep 2010, 30(17):4134-4148.
22. Morissette M.R., Sah V.P., Glembotski C.C., Brown J.H. The Rho effector, PKN, regulates ANF gene transcription in cardiomyocytes through a serum response element. Am J Physiol Heart Circ Physiol Jun 2000, 278(6):H1769-H1774.
23. Sah V.P., Hoshijima M., Chien K.R., Brown J.H. Rho is required for Galphaq and alpha1-adrenergic receptor signaling in cardiomyocytes. Dissociation of Ras and Rho pathways. J Biol Chem Dec 6 1996, 271(49):31185-31190.
24. Mo F.E., Lau L.F. The matricellular protein CCN1 is essential for cardiac development. Circ Res Oct 27 2006, 99(9):961-969.
25. Hilfiker-Kleiner D., Kaminski K., Kaminska A., Fuchs M., Klein G., Podewski E., et al. Regulation of proangiogenic factor CCN1 in cardiac muscle: impact of ischemia, pressure overload, and neurohumoral activation. Circulation May 11 2004, 109(18):2227-2233.
26. Todorovic V., Chen C.C., Hay N., Lau L.F. The matrix protein CCN1 (Cyr61) induces apoptosis in fibroblasts. J Cell Biol Nov 7 2005, 171(3):559-568.
27. Del Re D.P., Miyamoto S., Brown J.H. Focal adhesion kinase as a RhoA-activable signaling scaffold mediating Akt activation and cardiomyocyte protection. J Biol Chem Dec 19 2008, 283(51):35622-35629.
28. Means C.K., Xiao C.Y., Li Z., Zhang T., Omens J.H., Ishii I., et al. Sphingosine 1-phosphate S1P2 and S1P3 receptor-mediated Akt activation protects against in vivo myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol Jun 2007, 292(6):H2944-H2951.
29. Xiang S.Y., Vanhoutte D., Del Re D.P., Purcell N.H., Ling H., Banerjee I., et al. RhoA protects the mouse heart against ischemia/reperfusion injury. J Clin Invest Aug 2011, 121(8):3269-3276.
30. Xiang S.Y., Ouyang K., Yung B.S., Miyamoto S., Smrcka A.V., Chen J., et al. PLCepsilon, PKD1, and SSH1L transduce RhoA signaling to protect mitochondria from oxidative stress in the heart. Sci Signal Dec 17 2013, 6(306):ra108.
31. Miyamoto S., Purcell N.H., Smith J.M., Gao T., Whittaker R., Huang K., et al. PHLPP-1 negatively regulates Akt activity and survival in the heart. Circ Res Aug 20 2010, 107(4):476-484.
32. Thomas R.L., Roberts D.J., Kubli D.A., Lee Y., Quinsay M.N., Owens J.B., et al. Loss of MCL-1 leads to impaired autophagy and rapid development of heart failure. Genes Dev Jun 15 2013, 27(12):1365-1377.
33. Sagi S.A., Seasholtz T.M., Kobiashvili M., Wilson B.A., Toksoz D., Brown J.H. Physical and functional interactions of Galphaq with Rho and its exchange factors. J Biol Chem May 4 2001, 276(18):15445-15452.
34. Howes A.L., Miyamoto S., Adams J.W., Woodcock E.A., Brown J.H. Galphaq expression activates EGFR and induces Akt mediated cardiomyocyte survival: dissociation from Galphaq mediated hypertrophy. J Mol Cell Cardiol May 2006, 40(5):597-604.
35. Kim K.H., Chen C.C., Monzon R.I., Lau L.F. Matricellular protein CCN1 promotes regression of liver fibrosis through induction of cellular senescence in hepatic myofibroblasts. Mol Cell Biol May 2013, 33(10):2078-2090.
36. Aktories K., Just I. In vitro ADP-ribosylation of Rho by bacterial ADP-ribosyltransferases. Methods Enzymol 1995, 256:184-195.
37. Carles M., Lafargue M., Goolaerts A., Roux J., Song Y., Howard M., et al. Critical role of the small GTPase RhoA in the development of pulmonary edema induced by Pseudomonas aeruginosa in mice. Anesthesiology Nov 2010, 113(5):1134-1143.
38. Han J.S., Macarak E., Rosenbloom J., Chung K.C., Chaqour B. Regulation of Cyr61/CCN1 gene expression through RhoA GTPase and p38MAPK signaling pathways. Eur J Biochem Aug 2003, 270(16):3408-3421.
39. Evelyn C.R., Wade S.M., Wang Q., Wu M., Iniguez-Lluhi J.A., Merajver S.D., et al. CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol Cancer Ther Aug 2007, 6(8):2249-2260.
40. Evelyn C.R., Bell J.L., Ryu J.G., Wade S.M., Kocab A., Harzdorf N.L., et al. Design, synthesis and prostate cancer cell-based studies of analogs of the Rho/MKL1 transcriptional pathway inhibitor, CCG-1423. Bioorg Med Chem Lett Jan 15 2010, 20(2):665-672.
41. Johnson L.A., Rodansky E.S., Haak A.J., Larsen S.D., Neubig R.R., Higgins P.D. Novel Rho/MRTF/SRF inhibitors block matrix-stiffness and TGF-beta-induced fibrogenesis in human colonic myofibroblasts. Inflamm Bowel Dis Jan 2014, 20(1):154-165.
42. Lundquist M.R., Storaska A.J., Liu T.C., Larsen S.D., Evans T., Neubig R.R., et al. Redox modification of nuclear actin by MICAL-2 regulates SRF signaling. Cell Jan 30 2014, 156(3):563-576.
43. Yang G.P., Lau L.F. Cyr61, product of a growth factor-inducible immediate early gene, is associated with the extracellular matrix and the cell surface. Cell Growth Differ Jul 1991, 2(7):351-357.
44. Murphy E., Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev Apr 2008, 88(2):581-609.
45. Davidson S.M., Hausenloy D., Duchen M.R., Yellon D.M. Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int J Biochem Cell Biol Mar 2006, 38(3):414-419.
46. Hausenloy D.J., Yellon D.M. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res Feb 15 2004, 61(3):448-460.
47. Kozasa T., Jiang X., Hart M.J., Sternweis P.M., Singer W.D., Gilman A.G., et al. p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science Jun 26 1998, 280(5372):2109-2111.
48. Windh R.T., Lee M.J., Hla T., An S., Barr A.J., Manning D.R. Differential coupling of the sphingosine 1-phosphate receptors Edg-1, Edg-3, and H218/Edg-5 to the G(i), G(q), and G(12) families of heterotrimeric G proteins. J Biol Chem Sep 24 1999, 274(39):27351-27358.
49. Takuwa Y., Takuwa N., Sugimoto N. The Edg family G protein-coupled receptors for lysophospholipids: their signaling properties and biological activities. J Biochem Jun 2002, 131(6):767-771.
50. Rieken S., Herroeder S., Sassmann A., Wallenwein B., Moers A., Offermanns S., et al. Lysophospholipids control integrin-dependent adhesion in splenic B cells through G(i) and G(12)/G(13) family G-proteins but not through G(q)/G(11). J Biol Chem Dec 1 2006, 281(48):36985-36992.
51. Kawanabe Y., Okamoto Y., Nozaki K., Hashimoto N., Miwa S., Masaki T. Molecular mechanism for endothelin-1-induced stress-fiber formation: analysis of G proteins using a mutant endothelin(A) receptor. Mol Pharmacol Feb 2002, 61(2):277-284.
52. Arai K., Maruyama Y., Nishida M., Tanabe S., Takagahara S., Kozasa T., et al. Differential requirement of G alpha12, G alpha13, G alphaq, and G beta gamma for endothelin-1-induced c-Jun NH2-terminal kinase and extracellular signal-regulated kinase activation. Mol Pharmacol Mar 2003, 63(3):478-488.
53. Del Re D.P., Miyamoto S., Brown J.H. RhoA/Rho kinase up-regulate Bax to activate a mitochondrial death pathway and induce cardiomyocyte apoptosis. J Biol Chem Mar 16 2007, 282(11):8069-8078.
54. Hilal-Dandan R., Means C.K., Gustafsson A.B., Morissette M.R., Adams J.W., Brunton L.L., et al. Lysophosphatidic acid induces hypertrophy of neonatal cardiac myocytes via activation of Gi and Rho. J Mol Cell Cardiol Apr 2004, 36(4):481-493.
55. Cen B., Selvaraj A., Prywes R. Myocardin/MKL family of SRF coactivators: key regulators of immediate early and muscle specific gene expression. J Cell Biochem Sep 1 2004, 93(1):74-82.
56. Kireeva M.L., Mo F.E., Yang G.P., Lau L.F. Cyr61, a product of a growth factor-inducible immediate-early gene, promotes cell proliferation, migration, and adhesion. Mol Cell Biol Apr 1996, 16(4):1326-1334.
57. Krishnamurthy P., Subramanian V., Singh M., Singh K. Deficiency of beta1 integrins results in increased myocardial dysfunction after myocardial infarction. Heart Sep 2006, 92(9):1309-1315.
58. Shai S.Y., Harpf A.E., Babbitt C.J., Jordan M.C., Fishbein M.C., Chen J., et al. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res Mar 8 2002, 90(4):458-464.
59. Okada H., Lai N.C., Kawaraguchi Y., Liao P., Copps J., Sugano Y., et al. Integrins protect cardiomyocytes from ischemia/reperfusion injury. J Clin Invest Oct 1 2013, 123(10):4294-4308.
60. Vessey D.A., Li L., Honbo N., Karliner J.S. Sphingosine 1-phosphate is an important endogenous cardioprotectant released by ischemic pre- and postconditioning. Am J Physiol Heart Circ Physiol Oct 2009, 297(4):H1429-H1435.
61. Matsui Y., Sadoshima J. Rapid upregulation of CTGF in cardiac myocytes by hypertrophic stimuli: implication for cardiac fibrosis and hypertrophy. J Mol Cell Cardiol Aug 2004, 37(2):477-481.
62. Ohnishi H., Oka T., Kusachi S., Nakanishi T., Takeda K., Nakahama M., et al. Increased expression of connective tissue growth factor in the infarct zone of experimentally induced myocardial infarction in rats. J Mol Cell Cardiol Nov 1998, 30(11):2411-2422.
63. Ahmed M.S., Gravning J, Martinov VN, von Lueder TG, Edvardsen T, Czibik G, et al. Mechanisms of novel cardioprotective functions of CCN2/CTGF in myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. Apr 2011, 300(4):H1291-302.
64. Spiegel S., Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol May 2003, 4(5):397-407.
65. Cordis G.A., Yoshida T., Das D.K. HPTLC analysis of sphingomylein, ceramide and sphingosine in ischemic/reperfused rat heart. J Pharm Biomed Anal Mar 1998, 16(7):1189-1193.
66. Hernandez O.M., Discher D.J., Bishopric N.H., Webster K.A. Rapid activation of neutral sphingomyelinase by hypoxia-reoxygenation of cardiac myocytes. Circ Res Feb 4 2000, 86(2):198-204.