Cardiac stem cells with electrical stimulation improve ischaemic heart function through regulation of connective tissue growth factor and miR-378

Cardiovascular Research

Volumn 100, Issue 2, 2013, Pages 241-251

  Kim, Sun Wook ^a   Kim, Ha Won ^a   Huang, Wei ^a   Okada, Motoi ^a   Welge, Jeffrey A ^b   Wang, Yigang ^a   Ashraf, Muhammad ^a  

^a Department of Molecular and Cellular Physiology ^*  (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

CTGF; Electrical stimulation; Ischaemic heart; miR 378; Survival

Indexed keywords

CASPASE 3; CONNECTIVE TISSUE GROWTH FACTOR; FOCAL ADHESION KINASE; GLYCOGEN SYNTHASE KINASE 3BETA; MICRORNA; MICRORNA 378; MYOCYTE ENHANCER FACTOR 2; PROTEIN KINASE B; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIAC STEM CELL; CELL ADHESION; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVATION; ENZYME INHIBITION; HEART FUNCTION; HEART INFARCTION; IN VITRO STUDY; ISCHEMIC PRECONDITIONING; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; STEM CELL;

CTGF; ELECTRICAL STIMULATION; ISCHAEMIC HEART; MIR-378; SURVIVAL;

ANIMALS; ANTIGENS, LY; CELL ADHESION; CELL SURVIVAL; CONNECTIVE TISSUE GROWTH FACTOR; CYTOPROTECTION; ELECTRIC STIMULATION THERAPY; FOCAL ADHESION PROTEIN-TYROSINE KINASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICRORNAS; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84886042742     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt192     Document Type: Article

References (44)

1. Niagara MI, Haider HK, Jiang S, Ashraf M. Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circ Res 2007;100:545-555.
2. Hoke NN, Salloum FN, Kass DA, Das A, Kukreja RC. Preconditioning by phosphodiesterase-5 inhibition improves therapeutic efficacy of adipose-derived stem cells following myocardial infarction in mice. Stem Cells 2012;30:326-335.
3. Kim HW, Haider HK, Jiang S, Ashraf M. Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 2009;284:33161-33168.
4. Rajapakse N, Kis B, Horiguchi T, Snipes J, Busija D. Diazoxide pretreatment induces delayed preconditioning in astrocytes against oxygen glucose deprivation and hydrogen peroxide-induced toxicity. J Neurosci Res 2003;73:206-214.
5. Yau TM, Kim C, Ng D, Li G, Zhang Y, Weisel RD et al. Increasing transplanted cell survival with cell-based angiogenic gene therapy. Ann Thorac Surg 2005;80:1779-1786.
6. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;9:1195-1201.
7. Hutter JJ, Mestril R, Tam EK, Sievers RE, Dillmann WH, Wolfe CL. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 1996;94:1408-1411.
8. Wang X, Zhao T, Huang W, Wang T, Qian J, Xu M et al. Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors. Stem Cells 2009;27:3021-3031.
9. Dubey AK, Gupta SD, Basu B. Optimization of electrical stimulation parameters for enhanced cell proliferation on biomaterial surfaces. J Biomed Mater Res B Appl Biomater 2011;98:18-29.
10. Chang KA, Kim JW, Kim JA, Lee SE, Kim S, Suh WH et al. Biphasic electrical currents stimulation promotes both proliferation and differentiation of fetal neural stem cells. PLoS One 2011;6:e18738.
11. McCaig CD, Rajnicek AM, Song B, Zhao M. Controlling cell behavior electrically: current views and future potential. Physiol Rev 2005;85:943-978.
12. Genovese JA, Spadaccio C, Chachques E, Schussler O, Carpentier A, Chachques JC et al. Cardiac pre-differentiation of human mesenchymal stem cells by electrostimulation. Front Biosci 2009;14:2996-3002.
13. Sauer H, Rahimi G, Hescheler J, Wartenberg M. Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem 1999;75:710-723.
14. Chen MQ, Xie X, Hollis Whittington R, Kovacs GT, Wu JC, Giovangrandi L. Cardiac differentiation of embryonic stem cells with point-source electrical stimulation. Conf Proc IEEE Eng Med Biol Soc 2008;2008:1729-1732.
15. Serena E, Figallo E, Tandon N, Cannizzaro C, Gerecht S, Elvassore N et al. Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Exp Cell Res 2009;315:3611-3619.
16. Baba T, Kameda M, Yasuhara T, Morimoto T, Kondo A, Shingo T et al. Electrical stimulation of the cerebral cortex exerts antiapoptotic, angiogenic, and anti-inflammatory effects in ischemic stroke rats through phosphoinositide 3-kinase/Akt signaling pathway. Stroke 2009;40:e598-e605.
17. Zhao M, Bai H, Wang E, Forrester JV, McCaig CD. Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J Cell Sci 2004;117:397-405.
18. + cardiac progenitor cells for myocardial regeneration. PLoS One 2011;6:e25265.
19. Tarnavski O, McMullen JR, Schinke M, Nie Q, Kong S, Izumo S. Mouse cardiac surgery: comprehensive techniques for the generation of mouse models of human diseases and their application for genomic studies. Physiol Genomics 2004;16:349-360.
20. Skoumal R, Tóth M, Serpi R, Rysä J, Leskinen H, Ulvila J et al. Parthenolide inhibits STAT3 signaling and attenuates angiotensin II-induced left ventricular hypertrophy via modulation of fibroblast activity. J Mol Cell Cardiol 2011;50:634-641.
21. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001;7:1028-1034.
22. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003;114: 763-776.
23. Zhou X, Zhai X, Ashraf M. Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocytes. Circulation 1996;93:1177-1184.
24. Hausenloy DJ, Yellon DM. The second window of preconditioning (SWOP) where are we now? Cardiovasc Drugs Ther 2010;24:235-254.
25. Frame MC, Patel H, Serrels B, Lietha D, Eck MJ. The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 2010;11:802-814.
26. Shi-wen X, Stanton LA, Kennedy L, Pala D, Chen Y, Howat SL et al. CCN2Is necessary for adhesive responses to transforming growth factor-beta1 in embryonic fibroblasts. J Biol Chem 2006;281:10715-10726.
27. Ono M, Kubota S, Fujisawa T, Sonoyama W, Kawaki H, Akiyama K et al. Promotion of hydroxyapatite-associated, stem cell-based bone regeneration by CCN2. Cell Transplant 2008;17:231-240.
28. Mestdagh P, Fredlund E, Pattyn F, Rihani A, Van Maerken T, Vermeulen J et al. An integrative genomics screen uncovers ncRNA T-UCR functions in neuroblastoma tumours. Oncogene 2010;29:3583-3592.
29. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008;36:D149-D153.
30. Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 2006;126:1203-1217.
31. Khwaja A, Rodriguez-Viciana P, Wennström S, Warne PH, Downward J. Matrix adhesion and Ras transformation both activate a phosphoinositide3- OHkinase and protein kinase B/Akt cellular survival pathway. EMBO J 1997;16:2783-2793.
32. Lu Q, Rounds S. Focal adhesion kinase and endothelial cell apoptosis. Microvasc Res 2012; 83:56-63.
33. Bellas RE, Harrington EO, Sheahan KL, Newton J, Marcus C, Rounds S. FAK blunts adenosine-homocysteine-induced endothelial cell apoptosis: requirement for PI3-kinase. Am J Physiol Lung Cell Mol Physiol 2002;282:L1135-L1142.
34. Lim ST, Chen XL, Lim Y, Hanson DA, Vo TT, Howerton K et al. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol Cell 2008; 29:9-22.
35. Ammoun S, Schmid MC, Zhou L, Ristic N, Ercolano E, Hilton DA et al. Insulin-like growth factor-binding protein-1 (IGFBP-1) regulates human Schwannoma proliferation, adhesion and survival. Oncogene 2011;31:1710-1722.
36. Shi-Wen X, Leask A, Abraham D. Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fibrosis. Cytokine Growth Factor Rev 2008;19: 133-144.
37. Ahmed MS, 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 2010;300:H1291-H1302.
38. Babic AM, Chen CC, Lau LF. Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin alphavbeta3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 1999;19:2958-2966.
39. Chen CC, Lau LF. Functions and mechanisms of action of CCNmatricellular proteins. Int J Biochem Cell Biol. 2009;41:771-783.
40. Guo F, Carter DE, Leask A. Mechanical tension increases CCN2/CTGF expression and proliferation in gingival fibroblasts via a TGFb-dependent mechanism. PLoS One 2011;6: e19756.
41. Tan TW, Lai CH, Huang CY, Yang WH, Chen HT, Hsu HC et al. CTGF enhances migration and MMP-13 up-regulation via alphavbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J Cell Biochem 2009; 107:345-356.
42. van Almen GC, Verhesen W, van Leeuwen RE, van de Vrie M, Eurlings C, Schellings MW et al. MicroRNA-18 and microRNA-19 regulate CTGF and TSP-1 expression in age-related heart failure. Aging Cell 2011;10:769-779.
43. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, van der Made I et al. miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res 2009;104:170-178.
44. Knezevic I, Patel A, Sundaresan NR, Gupta MP, Solaro RJ, Nagalingam RS et al. A novel cardiomyocyte-enriched microRNA, miR-378, targets insulin-like growth factor 1 receptor: implications in postnatal cardiac remodeling and cell survival. J Biol Chem 2012; 287:12913-12926.