Effects of sildenafil and/or muscle derived stem cells on myocardial infarction

Journal of Translational Medicine

Volumn 10, Issue 1, 2012, Pages

  Wang, Judy S C ^a   Kovanecz, Istvan ^a,c   Vernet, Dolores ^a,b   Nolazco, Gaby ^a,b   Kopchok, George E ^a   Chow, Sheryl L ^d   White, Rodney A ^a   Gonzalez Cadavid, Nestor F ^a,b,c  

^a LOS ANGELES BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b CHARLES R DREW UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

Fibrosis; Heart failure; Myocardial infarction; PDE5 inhibitors; Stem cells

Indexed keywords

COLLAGEN; GELATINASE A; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; PHOSPHODIESTERASE V; SILDENAFIL; TROPONIN T;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE CELL; IMAGE ANALYSIS; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LOW DRUG DOSE; MALE; MUSCLE DERIVED STEM CELL; MYOFIBROBLAST; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; STEM CELL; TACHYPHYLAXIS; UPREGULATION; WESTERN BLOTTING; ZYMOGRAPHY;

ANIMALS; MALE; MYOCARDIAL INFARCTION; MYOCARDIUM; PHOSPHODIESTERASE INHIBITORS; PIPERAZINES; PURINES; RATS; RATS, INBRED F344; STEM CELLS; SULFONES;

EID: 84864753099     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-10-159     Document Type: Article

References (58)

1. Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther 2009, 123:255-278. 10.1016/j.pharmthera.2009.05.002, 19460403.
2. Forte A, Della Corte A, De Feo M, Cerasuolo F, Cipollaro M. Role of myofibroblasts in vascular remodeling: focus on restenosis and aneurysm. Cardiovasc Res 2010, 88:395-405. 10.1093/cvr/cvq224, 20621923.
3. Kovanecz I, Nolazco G, Ferrini MG, Toblli JE, Heydarkhan S, Vernet D, Rajfer J, Gonzalez-Cadavid NF. Early onset of fibrosis within the arterial media in a rat model of type 2 diabetes mellitus with erectile dysfunction. BJU Int 2009, 103:1396-1404. 10.1111/j.1464-410X.2008.08251.x, 19154511.
4. Toblli JE, Ferrini MG, Cao G, Vernet D, Angerosa M, Gonzalez-Cadavid NF. Antifibrotic effects of pioglitazone on the kidney in a rat model of type 2 diabetes mellitus. Nephrol Dial Transplant 2009, 24:2384-2391. 10.1093/ndt/gfp103, 2727296, 19297362.
5. Serrano AL, Muñoz-Cánoves P. Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 2010, 316:3050-3058. 10.1016/j.yexcr.2010.05.035, 20570674.
6. Gonzalez-Cadavid NF. Mechanisms of penile fibrosis. J Sex Med 2009, 3:353-362.
7. Gajarsa JJ, Kloner RA. Left ventricular remodeling in the post-infarction heart: a review of cellular, molecular mechanisms, and therapeutic modalities. Heart Fail Rev 2011, 16:13-21. 10.1007/s10741-010-9181-7, 20623185.
8. Kukreja RC, Salloum FN, Das A, Koka S, Ockaili RA, Xi L. Emerging new uses of phosphodiesterase-5 inhibitors in cardiovascular diseases. Exp Clin Cardiol 2011, 16:e30-e35. 3206106, 22131856.
9. Kukreja RC. Cardiovascular protection with sildenafil following chronic inhibition of nitric oxide synthase. Br J Pharmacol 2007, 150:538-540. 2189762, 17245364.
10. Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ, Heusch G, Vinten-Johansen J, Yellon DM, Schulz R. Working Group of Cellular Biology of Heart of European Society of Cardiology. Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 2010, 87:406-423. 10.1093/cvr/cvq129, 20448097.
11. Kumar P, Francis GS, Tang WH. Phosphodiesterase 5 inhibition in heart failure: mechanisms and clinical implications. Nat Rev Cardiol 2009, 6:349-355. 10.1038/nrcardio.2009.32, 19377497.
12. Salloum FN, Abbate A, Das A, Houser JE, Mudrick CA, Qureshi IZ, Hoke NN, Roy SK, Brown WR, Prabhakar S, Kukreja RC. Sildenafil (Viagra) attenuates ischemic cardiomyopathy and improves left ventricular function in mice. Am J Physiol Heart Circ Physiol 2008, 294:H1398-H1406.
13. Das A, Salloum FN, Xi L, Rao YJ, Kukreja RC. ERK phosphorylation mediates sildenafil-induced myocardial protection against ischemia-reperfusion injury in mice. Am J Physiol Heart Circ Physiol 2009, 296:H1236-H1243. 10.1152/ajpheart.00100.2009, 2685342, 19286961.
14. Pérez NG, Piaggio MR, Ennis IL, Garciarena CD, Morales C, Escudero EM, Cingolani OH, Chiappe de Cingolani G, Yang XP, Cingolani HE. Phosphodiesterase 5A inhibition induces Na+/H + exchanger blockade and protection against myocardial infarction. Hypertension 2007, 49:1095-1103. 10.1161/HYPERTENSIONAHA.107.087759, 17339532.
15. Salloum FN, Takenoshita Y, Ockaili RA, Daoud VP, Chou E, Yoshida K, Kukreja RC. Sildenafil and vardenafil but not nitroglycerin limit myocardial infarction through opening of mitochondrial K(ATP) channels when administered at reperfusion following ischemia in rabbits. J Mol Cell Cardiol 2007, 42:453-458. 10.1016/j.yjmcc.2006.10.015, 3031787, 17157308.
16. Koka S, Kukreja RC. Attenuation of Doxorubicin-induced Cardiotoxicity by Tadalafil: A Long Acting Phosphodiesterase-5 Inhibitor. Mol Cell Pharmacol 2010, 2:173-178. 3076676, 21499570.
17. Koneru S, Varma Penumathsa S, Thirunavukkarasu M, Vidavalur R, Zhan L, Singal PK, Engelman RM, Das DK, Maulik N. Sildenafil-mediated neovascularization and protection against myocardial ischaemia reperfusion injury in rats: role of VEGF/angiopoietin-1. J Cell Mol Med 2008, 12:2651-2664. 10.1111/j.1582-4934.2008.00319.x, 18373738.
18. Sesti C, Florio V, Johnson EG, Kloner RA. The phosphodiesterase-5 inhibitor tadalafil reduces myocardial infarct size. Int J Impot Res 2007, 19:55-61. 10.1038/sj.ijir.3901497, 16858368.
19. Salloum FN, Chau VQ, Hoke NN, Abbate A, Varma A, Ockaili RA, Toldo S, Kukreja RC. Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase g-dependent generation of hydrogen sulfide.Circulation 2009, 120:S31-36. Erratum in. Circulation 2009, 120:e139.
20. Shan X, Quaile MP, Monk JK, French B, Cappola TP, Margulies KB. Differential Expression of PDE5 in Failing and Non-Failing Human Myocardium. Circ Heart Fail 2012, 5:79-86. 10.1161/CIRCHEARTFAILURE.111.961706, 22135403.
21. Kovanecz I, Rambhatla A, Ferrini M, Vernet D, Sanchez S, Rajfer J, Gonzalez-Cadavid N. Long-term continuous sildenafil treatment ameliorates corporal veno-occlusive dysfunction (CVOD) induced by cavernosal nerve resection in rats. Int J Impot Res 2008, 20:202-212. 10.1038/sj.ijir.3901612, 17882231.
22. Kovanecz I, Rambhatla A, Ferrini MG, Vernet D, Sanchez S, Rajfer J, Gonzalez-Cadavid N. Chronic daily tadalafil prevents the corporal fibrosis and veno-occlusive dysfunction that occurs after cavernosal nerve resection. BJU Int 2008, 101:203-210.
23. Ferrini MG, Kovanecz I, Sanchez S, Vernet D, Davila HH, Rajfer J, Gonzalez-Cadavid NF. Long-term continuous treatment with sildenafil ameliorates aging related erectile dysfunction and the underlying corporal fibrosis in the rat. Biol Reprod 2007, 76:915-923. 10.1095/biolreprod.106.059642, 17287493.
24. Magheli A, Burnett AL. Medscape. Erectile dysfunction following prostatectomy: prevention and treatment. Nat Rev Urol 2009, 6:415-427. 10.1038/nrurol.2009.126, 19657376.
25. Hemnes AR, Zaiman A, Champion HC. PDE 5A inhibition attenuates bleomycin-induced pulmonary fibrosis and pulmonary hypertension through inhibition of ROS generation and RhoA/Rho kinase activation. Am J Physiol Lung Cell Mol Physiol 2008, 294:L24-L33.
26. Jeong KH, Lee TW, Ihm CG, Lee SH, Moon JY, Lim SJ. Effects of sildenafil on oxidative and inflammatory injuries of the kidney in streptozotocin-induced diabetic rats. Am J Nephrol 2009, 29:274-282. 10.1159/000158635, 18812693.
27. Gonzalez-Cadavid NF, Rajfer J. Treatment of Peyronie's disease with PDE 5 inhibitors: an antifibrotic strategy. Nat Rev Urol 2010, 7:215-221. 10.1038/nrurol.2010.24, 20212516.
28. Mazo M, Pelacho B, Prósper F. Stem cell therapy for chronic myocardial infarction. J Cardiovasc Transl Res 2010, 3:79-88. 10.1007/s12265-009-9159-9, 20560022.
29. Lin YC, Leu S, Sun CK, Yen CH, Kao YH, Chang LT, Tsai TH, Chua S, Fu M, Ko SF, Wu CJ, Lee FY, Yip HK. Early combined treatment with sildenafil and adipose-derived mesenchymal stem cells preserves heart function in rat dilated cardiomyopathy. J Transl Med 2010, 8:88. 10.1186/1479-5876-8-88, 2956711, 20868517.
30. 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. 10.1002/stem.789, 22102597.
31. Mujoo K, Sharin VG, Bryan NS, Krumenacker JS, Sloan C, Parveen S, Nikonoff LE, Kots AY, Murad F. Role of nitric oxide signaling components in differentiation of embryonic stem cells into myocardial cells. Proc Natl Acad Sci USA 2008, 105:18924-18929. 10.1073/pnas.0810230105, 2596213, 19020077.
32. Ybarra N, del Castillo JR, Troncy E. Involvement of the nitric oxide-soluble guanylyl cyclase pathway in the oxytocin-mediated differentiation of porcine bone marrow stem cells into cardiomyocytes. Nitric Oxide 2011, 24:25-33. 10.1016/j.niox.2010.09.008, 20934529.
33. Oshima H, Payne TR, Urish KL, Sakai T, Ling Y, Gharaibeh B, Tobita K, Keller BB, Cummins JH, Huard J. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther 2005, 12:1130-1141. 10.1016/j.ymthe.2005.07.686, 16125468.
34. Payne TR, Oshima H, Okada M, Momoi N, Tobita K, Keller BB, Peng H, Huard J. A relationship between vascular endothelial growth factor, angiogenesis, and cardiac repair after muscle stem cell transplantation into ischemic hearts. J Am Coll Cardiol 2007, 50:1677-1684. 10.1016/j.jacc.2007.04.100, 17950150.
35. Okada M, Payne TR, Zheng B, Oshima H, Momoi N, Tobita K, Keller BB, Phillippi JA, Péault B, Huard J. Myogenic endothelial cells purified from human skeletal muscle improve cardiac function after transplantation into infarcted myocardium. J Am Coll Cardiol 2008, 52:1869-1880. 10.1016/j.jacc.2008.07.064, 2719893, 19038685.
36. Tamaki T, Akatsuka A, Okada Y, Uchiyama Y, Tono K, Wada M, Hoshi A, Iwaguro H, Iwasaki H, Oyamada A, Asahara T. Cardiomyocyte formation by skeletal muscle-derived multi-myogenic stem cells after transplantation into infarcted myocardium. PLoS One 2008, 3:e1789. 10.1371/journal.pone.0001789, 2262151, 18335059.
37. Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, Péault B, Cummins J, Huard J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc 2008, 3:1501-1509. 10.1038/nprot.2008.142, 18772878.
38. Nolazco G, Kovanecz I, Vernet D, et al. Effect of muscle-derived stem cells on the restoration of corpora cavernosa smooth muscle and erectile function in the aged rat. BJU Int 2008, 101:1156-1164. 10.1111/j.1464-410X.2008.07507.x, 18294308.
39. Ho MH, Heydarkhan S, Vernet D, Kovanecz I, Ferrini MG, Bhatia NN, Gonzalez-Cadavid NF. Stimulating vaginal repair in rats through skeletal muscle-derived stem cells seeded on small intestinal submucosal scaffolds. Obstet Gynecol 2009, 114:300-309. 10.1097/AOG.0b013e3181af6abd, 3217318, 19622991.
40. Tsao J, Vernet D, Gelfand R, Kovanecz I, Nolazco G, Gonzalez-Cadavid NF. Myostatin inactivation affects myogenesis by muscle derived stem cells in vitro and in the mdx mouse 2009, Kansas City, Missouri, USA: Military Health Research Forum.
41. Brown RD, Jones GM, Laird RE, Hudson P, Long S. Cytokines regulate matrix metalloproteinases and migration in cardiac fibroblasts. Biochem Biophys Re Commun 2007, 362:200-235.
42. Gómez-Pinedo U, Rodrigo R, Cauli O, Herraiz S, Garcia-Verdugo JM, Pellicer B, Pellicer A, Felipo V. cGMP modulates stem cells differentiation to neurons in brain in vivo. Neuroscience 2010, 165:1275-1283. 10.1016/j.neuroscience.2009.11.046, 19958812.
43. Kovanecz I, Rivera S, Nolazco G, Vernet D, Rajfer J, Gonzalez-Cadavid NF. Long term daily molsidomine and low dose sildenafil, and corporal implantation of muscle derived stem cells (MDSC), alone or in combination, prevent corporal venooclusive dysfunction (CVOD) in a rat model of cavernosal nerve damage. J Urol 2011, 185:e452.
44. Muirhead GJ, Rance DJ, Walker DK, Wastall P. Comparative human pharmacokinetics and metabolism of single-dose oral and intravenous sildenafil. Br J Clin Pharmacol 2002, 53:13S-20S. 1874255, 11879255.
45. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 1966, 50:219-244.
46. Chau VQ, Salloum FN, Hoke NN, Abbate A, Kukreja RC. Mitigation of the progression of heart failure with sildenafil involves inhibition of RhoA/Rho-kinase pathway. Am J Physiol Heart Circ Physiol 2011, 300:H2272-H2279. 10.1152/ajpheart.00654.2010, 3119085, 21398594.
47. Ferrini MG, Rivera S, Moon J, Vernet D, Rajfer J, Gonzalez-Cadavid NF. The Genetic Inactivation of Inducible Nitric Oxide Synthase (iNOS) Intensifies Fibrosis and Oxidative Stress in the Penile Corpora Cavernosa in Type 1 Diabetes. J Sex Med 2010, 7:3033-3044. 10.1111/j.1743-6109.2010.01884.x, 20626593.
48. Zhang M, Takimoto E, Hsu S, Lee DI, Nagayama T, Danner T, Koitabashi N, Barth AS, Bedja D, Gabrielson KL, Wang Y, Kass DA. Myocardial remodeling is controlled by myocyte-targeted gene regulation of phosphodiesterase type 5. J Am Coll Cardiol 2010, 56:2021-2030. 10.1016/j.jacc.2010.08.612, 3036840, 20970280.
49. Lin G, Xin ZC, Lue TF, Lin CS. Up and down-regulation of phosphodiesterase-5 as related to tachyphylaxis and priapism. J Urol 2003, 170:S15-S18. 10.1097/01.ju.0000075500.11519.e8, 12853767.
50. Musicki B, Champion HC, Becker RE, Kramer MF, Liu T, Sezen SF, Burnett AL. In vivo analysis of chronic phosphodiesterase-5 inhibition with sildenafil in penile erectile tissues: no tachyphylaxis effect. J Urol 2005, 174:1493-1496. 10.1097/01.ju.0000173006.47623.2c, 16145478.
51. Li Y, Huard J. Differentiation of muscle-derived cells into myofibroblasts in injured skeletal muscle. Am J Pathol 2002, 161:895-907. 10.1016/S0002-9440(10)64250-2, 1867256, 12213718.
52. Ono Y, Sensui H, Okutsu S, Nagatomi R. Notch2 negatively regulates myofibroblastic differentiation of myoblasts. J Cell Physiol 2007, 210:358-369. 10.1002/jcp.20838, 17044085.
53. Carlson S, Trial J, Soeller C, Entman ML. Cardiac mesenchymal stem cells contribute to scar formation after myocardial infarction. Cardiovasc Res 2011, 91:99-107. 10.1093/cvr/cvr061, 3112022, 21357194.
54. Vernet D, Magee T, Qian A, Nolazco G, Rajfer J, Gonzalez-Cadavid N. Phosphodiesterase type 5 is not upregulated by tadalafil in cultures of human penile cells. J Sex Med 2006, 3:84-94. discussion 94-95, 10.1111/j.1743-6109.2005.00197.x, 16409221.
55. Dorn GW. Novel pharmacotherapies to abrogate postinfarction ventricular remodeling. Nat Rev Cardiol 2009, 6:283-291. 10.1038/nrcardio.2009.12, 19352332.
56. Ludwig M, Steinhoff G, Li J. The regenerative potential of angiotensin AT(2) receptor in cardiac repair. Can J Physiol Pharmacol 2012, 90:287-293. 10.1139/y11-108, 22364522.
57. Qian C, Schoemaker RG, van Gilst WH, Roks AJ. The role of the rennin angiotensin-aldosterone system in cardiovascular progenitor cell function. Clin Sci (Lond) 2009, 116:301-314.
58. Ma TK, Kam KK, Yan BP, Lam YY. Renin-angiotensin-aldosterone system blockade for cardiovascular diseases: current status. Br J Pharmacol 2010, 160:1273-1292. 10.1111/j.1476-5381.2010.00750.x, 2938800, 20590619.