Delta-opioid receptor activation promotes mesenchymal stem cell survival via PKC/STAT3 signaling pathway

Circulation Journal

Volumn 76, Issue 1, 2012, Pages 204-212

  Higuchi, Sayaka ^a   Ii, Masaaki ^b   Zhu, Ping ^c   Ashraf, Muhammad ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

Author keywords

Apoptosis; Delta opioid receptor; Mcl 1; Mesenchymal stem cells; Protein kinase C; STAT3

Indexed keywords

DELTA OPIATE RECEPTOR; PROTEIN KINASE C; PROTEIN MCL 1; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL PROTECTION; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MCL 1 GENE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RAT; RECEPTOR BLOCKING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BENZAMIDES; CELL SURVIVAL; CELLS, CULTURED; DACTINOMYCIN; MALE; MESENCHYMAL STEM CELLS; MODELS, ANIMAL; NALTREXONE; PIPERAZINES; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, INBRED F344; RECEPTORS, OPIOID, DELTA; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84455203109     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-11-0309     Document Type: Article

References (46)

1. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002; 105: 93-98.
2. Bel A, Messas E, Agbulut O, Richard P, Samuel JL, Bruneval P, et al. Transplantation of autologous fresh bone marrow into infarcted myocardium: A word of caution. Circulation 2003; 108: II-247-II-252.
3. Price MJ, Chou CC, Frantzen M, Miyamoto T, Kar S, Lee S, et al. Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties. Int J Cardiol 2006; 111: 231-239.
4. Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V, et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 2006; 290: H2196-H2203.
5. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 2006; 98: 1414-1421.
6. Valina C, Pinkernell K, Song YH, Bai X, Sadat S, Campeau RJ, et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 2007; 28: 2667-2677.
7. Quevedo HC, Hatzistergos KE, Oskouei BN, Feigenbaum GS, Rodriguez JE, Valdes D, et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009; 106: 14022-14027.
8. Hosoda T, Kajstura J, Leri A, Anversa P. Mechanisms of myocardial regeneration. Circ J 2010; 74: 13-17.
9. Chen Y, Wang G, Zeng L. Adipose tissue or bone marrow, store for purchasing mesenchymal stem cells? Circ J 2011; 75: 2060-2061.
10. Müller-Ehmsen J, Krausgrill B, Burst V, Schenk K, Neisen UC, Fries JW, et al. Effective engraftment but poor mid-term persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. Mol Cell Cardiol 2006; 41: 876-884.
11. Haider HKH, Ashraf M. Strategies to promote donor cell survival: Combining preconditioning approach with stem cell transplantation. J Mol Cell Cardiol 2008; 45: 554-566.
12. Nakanishi C, Nagaya N, Ohnishi S, Yamahara K, Takabatake S, Konno T, et al. Gene and protein expression analysis of mesenchymal stem cells derived from rat adipose tissue and bone marrow. Circ J 2011; 75: 2260-2268.
13. Fryer RM, Auchampach JA, Gross GJ. Therapeutic receptor targets of ischemic preconditioning (Review). Cardiovasc Res 2002; 55: 520-525.
14. Pugsley MK. The diverse molecular mechanisms responsible for the actions of opioids on the cardiovascular system. Pharmacol Ther 2002; 93: 51-75.
15. Gross GJ. Role of opioids in acute and delayed preconditioning. J Mol Cell Cardiol 2003; 35: 709-718.
16. Peart JN, Gross ER, Gross GJ. Opioid-induced preconditioning: Recent advances and future perspectives. Vascul Pharmacol 2005; 42: 211-218.
17. Schultz JE, Hsu AK, Gross GJ. Ischemic preconditioning in the intact rat heart is mediated by δ1- but not μ- or κ-opioid receptors. Circulation 1998; 97: 1282-1289.
18. Fryer RM, Wang Y, Hsu AK, Gross GJ. Essential activation of PKCdelta in opioid-initiated cardioprotection. Am J Physiol Heart Circ Physiol 2001; 280: H1346-H1353.
19. Fryer RM, Hsu AK, Gross GJ. ERK and p38 MAP kinase activation are components of opioid-induced delayed cardioprotection. Basic Res Cardiol 2001; 96: 136-142.
20. Sigg DC, Coles JA Jr, Oeltgen PR, Iaizzo PA. Role of δ-opioid receptor agonists on infarct size reduction in swine. Am J Physiol Heart Circ Physiol 2002; 282: H1953-H1960.
21. Peart JN, Gross GJ. Exogenous activation of δ- and κ-opioid receptors affords cardioprotection in isolated murine heart. Basic Res Cardiol 2004; 99: 29-37.
22. Romano MA, Seymour EM, Berry JA, McNish RA, Bolling SF. Relative contribution of endogenous opioids to myocardial ischemic tolerance. J Surg Res 2004; 118: 32-37.
23. Peart JN, Gross ER, Reichelt ME, Hsu A, Headrick JP, Gross GJ. Activation of kappa-opioid receptors at reperfusion affords cardioprotection in both rat and mouse hearts. Basic Res Cardiol 2008; 103: 454-463.
24. Shujia J, Haider HK, Idris NM, Lu G, Ashraf M. Stable therapeutic effects of mesenchymal stem cell-based multiple gene delivery for cardiac repair. Cardiovasc Res 2008; 77: 525-533.
25. Takemura G, Kato S, Aoyama T, Hayakawa Y, Kanoh M, Maruyama R, et al. Characterization of ultrastructure and its relation with DNA fragmentation in Fas-induced apoptosis of cultured cardiac myocytes. J Pathol 2001; 193: 546-556.
26. Jongkamonwiwat N, Phansuwan-Pujito P, Sarapoke P, Chetsawang B, Casalotti SO, Forge A, et al. The presence of opioid receptors in rat inner ear. Heart Res 2003; 181: 85-93.
27. 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.
28. Otani H, Matsuhisa S, Akita Y, Kyoi S, Enoki C, Tatsumi K, et al. Role of mechanical stress in the form of cardiomyocyte death during the early phase of reperfusion. Circ J 2006; 10: 1344-1355.
29. Persson AI, Thorlin T, Bull C, Zarnegar P, Ekman R, Terenius L, et al. Mu- and delta-opioid receptor antagonists decrease proliferation and increase neurogenesis in cultures of rat adult hippocampal progenitors. Eur J Neurosci 2003; 17: 1159-1172.
30. Zhang J, Haddad GG, Xia Y. δ-, but not μ- and κ-, opioid receptor activation protects neocortical neurons from glutamate-induced excitotoxic injury. Brain Res 2000; 885: 143-153.
31. Agirregoitia E, Valdivia A, Carracedo A, Casis L, Gil J, Subiran N, et al. Expression and localization of δ-, κ-, and μ-opioid receptors in human spermatozoa and implications for sperm motility. J Clin Endocr Metab 2006; 91: 4969-4975.
32. Narita M, Kuzumaki N, Miyatake M, Sato F, Wachi H, Seyama Y, et al. Role of delta-opioid receptor function in neurogenesis and neuroprotection. J Neurochem 2006; 97: 1494-1505.
33. Heiss A, Ammer H, Eisinger DA. delta-Opioid receptor-stimulated Akt signaling in neuroblastoma · glioma (NG108-15) hybrid cells involves receptor tyrosine kinase-mediated PI3K activation. Exp Cell Res 2009; 315: 2115-2125.
34. Xu H, Yang YJ, Qian HY, Tang YD, Wang H, Zhang Q. Rosuvastatin treatment activates JAK-STAT pathway and increases efficacy of allogeneic mesenchymal stem cell transplantation in infarcted hearts. Circ J 2011; 75: 1476-1485.
35. Cohen MV, Yang XM, Liu GS, Heusch G, Downey JM. Acetyline, bradykinin, opioids and phenylephrine, but not adenosine trigger preconditioning by generating oxygen radicals and opening mitochondrial KATP channels. Circ Res 2001; 89: 273-278.
36. Gross ER, Hsu AK, Gross GJ. The JAK/STAT pathway is essential for opioid-induced cardioprotection: JAK2 as a mediator of STAT3, Akt, and GSK-3β. Am J Physiol Heart Circ Physiol 2006; 291: H827-H834.
37. Lo RK, Wong YH. Signal transducer and activator of transcription 3 activation by the delta-opioid receptor via Galpha14 involves multiple intermediates. Mol Pharmacol 2004; 65: 1427-1439.
38. Bell SP, Sack MN, Patel A, Opie LH, Yellon DM. Delta opioid receptor stimulation mimics ischemic preconditioning in human heart muscle. J Am Coll Cardiol 2000; 36: 2296-2302.
39. Miura T, Takayuki M. GSK-3β, a therapeutic target for cardiomyocyte protection. Circ J 2009; 73: 1184-1192.
40. Huang MH, Nguyen V, Wu Y, Rastogi S, Lui CY, Birnbaum Y, et al. Reducing ischaemia/reperfusion injury through δ-opioid-regulated intrinsic cardiac adrenergic cells: Adrenopeptidergic co-signalling. Cardiovasc Res 2009; 84: 452-460.
41. Dauer DJ, Ferraro B, Song L, Yu B, Mora L, Buettner R, et al. Stat3 regulates genes common to both wound healing and cancer. Oncogene 2005; 24: 3397-3408.
42. Bhattacharya S, Ray RM, Johnson LR. STAT3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyaminedepleted cells. Biochem J 2005; 392: 335-344.
43. Ardehali H, O'Rourke B. Mitochondrial KATP channels in cell survival and death. J Mol Cell Cardiol 2005; 39: 7-16.
44. Xu M, Wang Y, Ayub A, Ashraf M. Mitochondrial KATP channel activation reduces anoxic injury by restoring mitochondrial membrane potential. Am J Physiol Heart Circ Physiol 2001; 281: H1295-H1303.
45. Szabó I, Bock J, Grassmé H, Soddemann M, Wilker B, Lang F, et al. Mitochondrial potassium channel Kv1.3 mediates Bax-induced apoptosis in lymphocytes. Proc Natl Acad Sci USA 2008; 105: 14861-14866.
46. Schultz JE, Gross GJ. Opioids and cardioprotection. Pharmacol Ther 2001; 89: 123-137.