Oxygen cycling in conjunction with stem cell transplantation induces NOS3 expression leading to attenuation of fibrosis and improved cardiac function

Cardiovascular Research

Volumn 93, Issue 1, 2012, Pages 89-99

  Khan, Mahmood ^a   Meduru, Sarath ^a   Gogna, Rajan ^a   Madan, Esha ^a   Citro, Lucas ^a   Kuppusamy, Muthulakshmi L ^a   Sayyid, Muzzammil ^a   Mostafa, Mahmoud ^a   Hamlin, Robert L ^b   Kuppusamy, Periannan ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Endothelial nitric oxide synthase; Hyperbaric oxygen; Mesenchymal stem cell; Myocardial infarction; Stem cell therapy

Indexed keywords

CONNEXIN 43; ENDOTHELIAL NITRIC OXIDE SYNTHASE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENGRAFTMENT; FIBROSIS; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; HEART VENTRICLE REMODELING; HYPERBARIC OXYGEN; MALE; MESENCHYMAL STEM CELL; MOLECULAR DYNAMICS; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEM CELL TRANSPLANTATION;

ANIMALS; BASE SEQUENCE; COMBINED MODALITY THERAPY; CONNEXIN 43; DNA PRIMERS; FIBROSIS; GENE EXPRESSION; HYPERBARIC OXYGENATION; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, INBRED F344;

EID: 84555186803     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr277     Document Type: Article

References (46)

1. van Laake LW, Passier R, Monshouwer-Kloots J, Nederhoff MG, Ward-van Oostwaard D, Field LJ et al. Monitoring of cell therapy and assessment of cardiac function using magnetic resonance imaging in a mouse model of myocardial infarction. Nat Protoc 2007;2:2551-2567.
2. Afzal MR, Haider H, Idris NM, Jiang S, Ahmed RP, Ashraf M. Preconditioning promotes survival and angiomyogenic potential of mesenchymal stem cells in the infarcted heart via NF-kappaB signaling. Antioxid Redox Signal 2010;12:693-702.
3. Ahmed RP, Haider KH, Shujia J, Afzal MR, Ashraf M. Sonic Hedgehog gene delivery to the rodent heart promotes angiogenesis via iNOS/netrin-1/PKC pathway. PLoS One 2011;5:e8576.
4. Iso Y, Spees JL, Serrano C, Bakondi B, Pochampally R, Song YH et al. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochem Biophys Res Commun 2007;354:700-706. (Pubitemid 46186241)
5. 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. (Pubitemid 37173705)
6. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-705. (Pubitemid 32290358)
7. Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H et al. Autologous bone-marrow stem cell transplantation for myocardial regeneration. Lancet 2003;361: 45-46. (Pubitemid 36050962)
8. Kudo M, Wang Y, Wani MA, Xu M, Ayub A, Ashraf M. Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart. J Mol Cell Cardiol 2003;35:1113-1119. (Pubitemid 37083255)
9. Strauer BE, Brehm M, Zeus T, Bartsch T, Schannwell C, Antke C et al. Regeneration of human infarcted heart muscle by intracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: the IACT Study. J Am Coll Cardiol 2005; 46:1651-1658. (Pubitemid 41531618)
10. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004;364:141-148. (Pubitemid 38891685)
11. Rosenzweig A. Cardiac cell therapy-mixed results from mixed cells. N Engl J Med 2006;355:1274-1277. (Pubitemid 44427452)
12. Gussoni E, Blau HM, Kunkel LM. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 1997;3:970-977.
13. Rando TA, Blau HM. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 1994;125:1275-1287. (Pubitemid 24189532)
14. Vincent KA, Shyu KG, Luo Y, Magner M, Tio RA, Jiang C et al. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an HIF-1alpha/VP16 hybrid transcription factor. Circulation 2000;102:2255-2261.
15. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol 2001;33:1897-1918. (Pubitemid 33097270)
16. Kubes P, Granger DN. Nitric oxide modulates microvascular permeability. Am J Physiol 1992;262:H611-H615.
17. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 1991;88:4651-4655. (Pubitemid 21914599)
18. Radomski MW, Palmer RM, Moncada S. Comparative pharmacology of endotheliumderived relaxing factor, nitric oxide and prostacyclin in platelets. Br J Pharm 1987;92: 181-187. (Pubitemid 17134934)
19. Mangialardi G, Monopoli A, Ongini E, Spinetti G, Fortunato O, Emanueli C et al. Nitric oxide-donating statin improves multiple functions of circulating angiogenic cells. Br J Pharm 2011;164:570-583.
20. Buras JA, Stahl GL, Svoboda KK, Reenstra WR. Hyperbaric oxygen downregulates ICAM-1 expression induced by hypoxia and hypoglycemia: the role of NOS. Am J Physiol Cell Physiol 2000;278:C292-C302. (Pubitemid 30131146)
21. Cabigas BP, Su J, Hutchins W, Shi Y, Schaefer RB, Recinos RF et al. Hyperoxic and hyperbaric-induced cardioprotection: role of nitric oxide synthase 3. Cardiovasc Res 2006;72:143-151. (Pubitemid 44310642)
22. Khan M, Meduru S, Mohan IK, Kuppusamy ML, Wisel S, Kulkarni A et al. Hyperbaric oxygenation enhances transplanted cell graft and functional recovery in the infarct heart. J Mol Cell Cardiol 2009;47:275-287.
23. Khan M, Meduru S, Mostafa M, Khan S, Hideg K, Kuppusamy P. Trimetazidine, administered at the onset of reperfusion, ameliorates myocardial dysfunction and injury by activation of p38 mitogen-activated protein kinase and Akt signaling. J Pharmacol Exp Ther 2010;333:421-429.
24. Khan M, Mohan IK, Kutala VK, Kotha SR, Parinandi NL, Hamlin RL et al. Sulfaphenazole protects heart against ischemia-reperfusion injury and cardiac dysfunction by overexpression of iNOS, leading to enhancement of nitric oxide bioavailability and tissue oxygenation. Antioxid Redox Signal 2009;11:725-738.
25. Wisel S, Khan M, Kuppusamy ML, Mohan IK, Chacko SM, Rivera BK et al. Pharmacological preconditioning of mesenchymal stem cells with trimetazidine (1-[2,3,4-trimethoxybenzyl]piperazine) protects hypoxic cells against oxidative stress and enhances recovery of myocardial function in infarcted heart through Bcl-2 expression. J Pharmacol Exp Ther 2009;329:543-550.
26. Cai H, Li Z, Davis ME, Kanner W, Harrison DG, Dudley SC Jr. Akt-dependent phosphorylation of serine 1179 and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase 1/2 cooperatively mediate activation of the endothelial nitricoxide synthase by hydrogen peroxide. Mol Pharmacol 2003;63:325-331. (Pubitemid 36158367)
27. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 2007;42:271-279. (Pubitemid 46135596)
28. Tanaka T, Nakamura H, Yodoi J, Bloom ET. Redox regulation of the signaling pathways leading to eNOS phosphorylation. Free Radic Biol Med 2005;38:1231-1242. (Pubitemid 40445540)
29. Thomas SR, Chen K, Keaney JF Jr. Hydrogen peroxide activates endothelial nitricoxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 2002;277: 6017-6024. (Pubitemid 34968385)
30. Mazure NM, Brahimi-Horn MC, Berta MA, Benizri E, Bilton RL, Dayan F et al. HIF-1: master and commander of the hypoxic world. A pharmacological approach to its regulation by siRNAs. Biochem Pharmacol 2004;68:971-980. (Pubitemid 39094259)
31. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995;92:5510-5514.
32. Wang GL, Semenza GL. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem 1993;268:21513-21518. (Pubitemid 23320639)
33. Jurgensen JS, Rosenberger C, Wiesener MS, Warnecke C, Horstrup JH, Grafe M et al. Persistent induction of HIF-1alpha and-2alpha in cardiomyocytes and stromal cells of ischemic myocardium. Faseb J 2004;18:1415-1417. (Pubitemid 39561599)
34. Kido M, Du L, Sullivan CC, Li X, Deutsch R, Jamieson SW et al. Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol 2005;46:2116-2124. (Pubitemid 41713601)
35. Yogaratnam JZ, Laden G, Guvendik L, Cowen M, Cale A, Griffin S. Pharmacological preconditioning with hyperbaric oxygen: can this therapy attenuate myocardial ischemic reperfusion injury and induce myocardial protection via nitric oxide? J Surg Res 2008;149:155-164.
36. Rakhit RD, Marber MS. Nitric oxide: an emerging role in cardioprotection? Heart (British Cardiac Society) 2001;86:368-372. (Pubitemid 32889367)
37. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
38. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999;399:597-601.
39. Dudzinski DM, Michel T. Life history of eNOS: partners and pathways. Cardiovasc Res 2007;75:247-260. (Pubitemid 46961923)
40. Shi Y, Baker JE, Zhang C, Tweddell JS, Su J, Pritchard KA Jr. Chronic hypoxia increases endothelial nitric oxide synthase generation of nitric oxide by increasing heat shock protein 90 association and serine phosphorylation. Circ Res 2002;91:300-306. (Pubitemid 34976995)
41. Drummond GR, Cai H, Davis ME, Ramasamy S, Harrison DG. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ Res 2000;86:347-354. (Pubitemid 30108830)
42. Mathy-Hartert M, Deby-Dupont GP, Reginster JY, Ayache N, Pujol JP, Henrotin YE. Regulation by reactive oxygen species of interleukin-1beta, nitric oxide and prostaglandin E(2) production by human chondrocytes. Osteoarthr Cartil 2002;10:547-555. (Pubitemid 34919070)
43. Benedetti S, Lamorgese A, Piersantelli M, Pagliarani S, Benvenuti F, Canestrari F. Oxidative stress and antioxidant status in patients undergoing prolonged exposure to hyperbaric oxygen. Clin Biochem 2004;37:312-317. (Pubitemid 38314886)
44. Elayan IM, Axley MJ, Prasad PV, Ahlers ST, Auker CR. Effect of hyperbaric oxygen treatment on nitric oxide and oxygen free radicals in rat brain. J Neurophysiol 2000; 83:2022-2029. (Pubitemid 30198657)
45. Vigneron A, Vousden KH. p53, ROS and senescence in the control of aging. Aging (Albany NY) 2010;2:471-474.
46. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B et al. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 2005;115:1221-1231. (Pubitemid 40629040)