Simvastatin augments the efficacy of therapeutic angiogenesis induced by bone marrow-derived mesenchymal stem cells in a murine model of hindlimb ischemia

Molecular Biology Reports

Volumn 39, Issue 1, 2012, Pages 285-293

  Zhang, Yuqing ^a   Zhang, Rusheng ^b   Li, Yong ^c   He, Guoping ^c   Zhang, Dingguo ^d   Zhang, Fumin ^e  

^a THE AFFILIATED JIANGNING HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b AFFILIATED HOSPITAL OF NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

^c Wujin Hospital Affiliated with Jiangsu University   (China)

^d NANJING MEDICAL UNIVERSITY   (China)

^e THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Bone marrow stem cell; Hindlimb ischemia; Statin

Indexed keywords

SIMVASTATIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAPILLARY DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; FEMALE; HINDLIMB; IN VITRO STUDY; IN VIVO STUDY; LASER DOPPLER FLOWMETRY; LIMB ISCHEMIA; LOW DRUG DOSE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; REVASCULARIZATION;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; GREEN FLUORESCENT PROTEINS; HINDLIMB; HYDROGEN PEROXIDE; ISCHEMIA; LASER-DOPPLER FLOWMETRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; SIMVASTATIN;

MURINAE; MUS; MUS MUSCULUS;

EID: 84855205756     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-011-0737-y     Document Type: Article

References (39)

1. C Diehm JR Allenberg D Pittrow M Mahn G Tepohl RL Haberl H Darius I Burghaus HJ Trampisch 2009 Mortality and vascular morbidity in older adults with asymptomatic versus symptomatic peripheral artery disease Circulation 120 2053 2061 19901192 10.1161/CIRCULATIONAHA.109.865600
2. JW Olin DE Allie M Belkin RO Bonow DE Casey Jr MA Creager TC Gerber AT Hirsch MR Jaff JA Kaufman CA Lewis ET Martin LG Martin P Sheehan KJ Stewart D Treat-Jacobson CJ White ZJ Zheng FA Masoudi 2010 Accf/aha/acr/scai/sir/svm/svn/ svs 2010 performance measures for adults with peripheral artery disease: a report of the American college of cardiology foundation/American heart association task force on performance measures, the American college of radiology, the society for cardiac angiography and interventions, the society for interventional radiology, the society for vascular medicine, the society for vascular nursing, and the society for vascular surgery (writing committee to develop clinical performance measures for peripheral artery disease) Circulation 122 2583 2618 21126978 10.1161/CIR.0b013e3182031a3c
3. KC Wollert H Drexler 2010 Cell therapy for the treatment of coronary heart disease: a critical appraisal Nat Rev Cardiol 7 204 215 20177405 10.1038/nrcardio.2010.1
4. S Grajek M Popiel L Gil P Breborowicz M Lesiak R Czepczynski K Sawinski E Straburzynska-Migaj A Araszkiewicz A Czyz M Kozlowska-Skrzypczak M Komarnicki 2010 Influence of bone marrow stem cells on left ventricle perfusion and ejection fraction in patients with acute myocardial infarction of anterior wall: randomized clinical trial: impact of bone marrow stem cell intracoronary infusion on improvement of microcirculation Eur Heart J 31 691 702 20022872
5. H Lawall P Bramlage B Amann 2010 Stem cell and progenitor cell therapy in peripheral artery disease: a critical appraisal Thromb Haemost 103 696 709 20174766 10.1160/TH09-10-0688 1:CAS:528:DC%2BC3cXls1agu78%3D
6. M Dezawa H Ishikawa Y Itokazu T Yoshihara M Hoshino S Takeda C Ide Y Nabeshima 2005 Bone marrow stromal cells generate muscle cells and repair muscle degeneration Science 309 314 317 16002622 10.1126/science.1110364 1:CAS:528:DC%2BD2MXlsl2jtLs%3D (Pubitemid 40967871)
7. MF Pittenger AM Mackay SC Beck RK Jaiswal R Douglas JD Mosca MA Moorman DW Simonetti S Craig DR Marshak 1999 Multi-lineage potential of adult human mesenchymal stem cells Science 284 143 147 10102814 10.1126/science.284.5411.143 1:CAS:528:DyaK1MXitlCnu7o%3D (Pubitemid 29282067)
8. L Chen EE Tredget PY Wu Y Wu 2008 Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing PLoS One 3 e1886 18382669 10.1371/journal.pone.0001886 (Pubitemid 351943822)
9. D Zhang F Zhang Y Zhang X Gao C Li N Yang K Cao 2007 Combining erythropoietin infusion with intramyocardial delivery of bone marrow cells is more effective for cardiac repair Transpl Int 20 174 183 17239026 10.1111/j.1432-2277.2006.00407.x (Pubitemid 46121995)
10. JM Hare JH Traverse TD Henry N Dib RK Strumpf SP Schulman G Gerstenblith AN DeMaria AE Denktas RS Gammon JB Hermiller Jr MA Reisman GL Schaer W Sherman 2009 A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction J Am Coll Cardiol 54 2277 2286 19958962 10.1016/j.jacc.2009.06.055 1:CAS:528:DC%2BC3cXmsl2guw%3D%3D
11. PJ Psaltis AC Zannettino SG Worthley S Gronthos 2008 Concise review: mesenchymal stromal cells: potential for cardiovascular repair Stem Cells 26 2201 2210 18599808 10.1634/stemcells.2008-0428
12. SE Nissen EM Tuzcu P Schoenhagen T Crowe WJ Sasiela J Tsai J Orazem RD Magorien C O'Shaughnessy P Ganz 2005 Statin therapy, LDL cholesterol, c-reactive protein, and coronary artery disease N Engl J Med 352 29 38 15635110 10.1056/NEJMoa042000 1:CAS:528:DC%2BD2MXis12msQ%3D%3D (Pubitemid 40075678)
13. JJ Kastelein ML Bots 2009 Statin therapy with ezetimibe or niacin in high-risk patients N Engl J Med 361 2180 2183 19915218 10.1056/NEJMe0908841 1:CAS:528:DC%2BD1MXhsFWgs7rI
14. M Sata H Nishimatsu E Suzuki S Sugiura M Yoshizumi Y Ouchi Y Hirata R Nagai 2001 Endothelial nitric oxide synthase is essential for the hmg-coa reductase inhibitor cerivastatin to promote collateral growth in response to ischemia FASEB J 15 2530 2532 11641268 1:CAS:528:DC%2BD3MXoslSjtLY%3D
15. I Pourati C Kimmelstiel W Rand RH Karas 2003 Statin use is associated with enhanced collateralization of severely diseased coronary arteries Am Heart J 146 876 881 14597938 10.1016/S0002-8703(03)00413-7 1:CAS:528: DC%2BD3sXovVWnsr4%3D (Pubitemid 37378578)
16. H Shao Y Tan D Eton Z Yang MG Uberti S Li A Schulick H Yu 2008 Statin and stromal cell-derived factor-1 additively promote angiogenesis by enhancement of progenitor cells incorporation into new vessels Stem Cells 26 1376 1384 18308946 10.1634/stemcells.2007-0785 1:CAS:528:DC%2BD1cXnsFCgurg%3D
17. M Weis C Heeschen AJ Glassford JP Cooke 2002 Statins have biphasic effects on angiogenesis Circulation 105 739 745 11839631 10.1161/hc0602.103393 1:CAS:528:DC%2BD38XitFais7c%3D (Pubitemid 34157379)
18. Y Li D Zhang Y Zhang G He F Zhang 2010 Augmentation of neovascularization in murine hindlimb ischemia by combined therapy with simvastatin and bone marrow-derived mesenchymal stem cells transplantation J Biomed Sci 17 75 20846454 10.1186/1423-0127-17-75
19. M Sata H Nishimatsu J Osuga K Tanaka N Ishizaka S Ishibashi Y Hirata R Nagai 2004 Statins augment collateral growth in response to ischemia but they do not promote cancer and atherosclerosis Hypertension 43 1214 1220 15166180 10.1161/01.HYP.0000126186.29571.41 1:CAS:528:DC%2BD2cXktFSksrY%3D (Pubitemid 38691742)
20. RJ Jaumdally PK Goon C Varma AD Blann GY Lip 2010 Effects of atorvastatin on circulating cd34+/cd133+/cd45- progenitor cells and indices of angiogenesis (vascular endothelial growth factor and the angiopoietins 1 and 2) in atherosclerotic vascular disease and diabetes mellitus J Intern Med 267 385 393 19754853 10.1111/j.1365-2796.2009.02151.x 1:CAS:528:DC%2BC3cXltlWlt7o%3D
21. A Kawamoto T Murayama K Kusano M Ii T Tkebuchava S Shintani A Iwakura I Johnson P von Samson A Hanley M Gavin C Curry M Silver H Ma M Kearney DW Losordo 2004 Synergistic effect of bone marrow mobilization and vascular endothelial growth factor-2 gene therapy in myocardial ischemia Circulation 110 1398 1405 15337699 10.1161/01.CIR.0000141563.71410.64 1:CAS:528:DC%2BD2cXnt12ju78%3D (Pubitemid 39238017)
22. T Iwase N Nagaya T Fujii T Itoh H Ishibashi-Ueda M Yamagishi K Miyatake T Matsumoto S Kitamura K Kangawa 2005 Adrenomedullin enhances angiogenic potency of bone marrow transplantation in a rat model of hindlimb ischemia Circulation 111 356 362 15655128 10.1161/01.CIR.0000153352.29335.B9 1:CAS:528: DC%2BD2MXmtFersA%3D%3D (Pubitemid 40165344)
23. BG Jaganathan B Ruester L Dressel S Stein M Grez E Seifried R Henschler 2007 Rho inhibition induces migration of mesenchymal stromal cells Stem Cells 25 1966 1974 17510214 10.1634/stemcells.2007-0167 1:CAS:528:DC%2BD2sXhtVSqsbbK (Pubitemid 47258174)
24. G Kasper N Dankert J Tuischer M Hoeft T Gaber JD Glaeser D Zander M Tschirschmann M Thompson G Matziolis GN Duda 2007 Mesenchymal stem cells regulate angiogenesis according to their mechanical environment Stem Cells 25 903 910 17218399 10.1634/stemcells.2006-0432 1:CAS:528:DC%2BD2sXls1Kmtrw%3D (Pubitemid 46572587)
25. D Zhang Y Li T Zhu F Zhang Z Yang D Miao 2011 Zinc supplementation results in improved therapeutic potential of bone marrow-derived mesenchymal stromal cells in a mouse ischemic limb model Cytotherapy 13 156 164 20839997 10.3109/14653249.2010.512633 1:CAS:528:DC%2BC3MXmtVCmtA%3D%3D
26. GC Hughes BH Annex 2005 Angiogenic therapy for coronary artery and peripheral arterial disease Expert Rev Cardiovasc Ther 3 521 535 15889979 10.1586/14779072.3.3.521 1:CAS:528:DC%2BD2MXlt1equ74%3D (Pubitemid 40691921)
27. Perin EC, Silva GV (2010) Cell-based therapy for chronic ischemic heart disease-a clinical perspective. Cardiovasc Ther. doi: 10.1111/j.1755-5922.2010. 00214.x
28. S Ohnishi H Sumiyoshi S Kitamura N Nagaya 2007 Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions FEBS Lett 581 3961 3966 17662720 10.1016/j.febslet.2007.07.028 1:CAS:528:DC%2BD2sXovFylu7g%3D (Pubitemid 47212103)
29. T Kinnaird E Stabile MS Burnett M Shou CW Lee S Barr S Fuchs SE Epstein 2004 Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms Circulation 109 1543 1549 15023891 10.1161/01.CIR.0000124062.31102.57 1:STN:280:DC%2BD2c7lslWnsw%3D%3D (Pubitemid 38420184)
30. M Gnecchi H He OD Liang LG Melo F Morello H Mu N Noiseux L Zhang RE Pratt JS Ingwall VJ Dzau 2005 Paracrine action accounts for marked protection of ischemic heart by akt-modified mesenchymal stem cells Nat Med 11 367 368 15812508 10.1038/nm0405-367 1:CAS:528:DC%2BD2MXivFChurc%3D (Pubitemid 40562318)
31. T Iwase N Nagaya T Fujii T Itoh S Murakami T Matsumoto K Kangawa S Kitamura 2005 Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia Cardiovasc Res 66 543 551 15914119 10.1016/j.cardiores.2005.02.006 1:CAS:528:DC%2BD2MXks1anu74%3D (Pubitemid 40725766)
32. AH Amin ZY Abd Elmageed D Nair MI Partyka PJ Kadowitz S Belmadani K Matrougui 2010 Modified multipotent stromal cells with epidermal growth factor restore vasculogenesis and blood flow in ischemic hind-limb of type ii diabetic mice Lab Invest 90 985 996 20440273 10.1038/labinvest.2010.86 1:CAS:528:DC%2BC3cXotFeisbg%3D
33. MR Ward DJ Stewart 2008 Erythropoietin and mesenchymal stromal cells in angiogenesis and myocardial regeneration: one plus one equals three? Cardiovasc Res 79 357 359 18550635 10.1093/cvr/cvn153 1:CAS:528:DC%2BD1cXptlyktLw%3D
34. T Deuse C Peter PW Fedak T Doyle H Reichenspurner WH Zimmermann T Eschenhagen W Stein JC Wu RC Robbins S Schrepfer 2009 Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction Circulation 120 S247 S254 19752375 10.1161/CIRCULATIONAHA.108.843680 1:CAS:528: DC%2BD1MXhtFWhurrL
35. J Tang J Wang L Guo X Kong J Yang F Zheng L Zhang Y Huang 2010 Mesenchymal stem cells modified with stromal cell-derived factor 1 alpha improve cardiac remodeling via paracrine activation of hepatocyte growth factor in a rat model of myocardial infarction Mol Cells 29 9 19 20016947 10.1007/s10059-010-0001-7
36. U Laufs 2003 Beyond lipid-lowering: effects of statins on endothelial nitric oxide Eur J Clin Pharmacol 58 719 731 12634978 1:CAS:528: DC%2BD3sXitFaisLs%3D (Pubitemid 36399228)
37. JP Halcox JE Deanfield 2004 Beyond the laboratory: clinical implications for statin pleiotropy Circulation 109 II42 II48 15173062 10.1161/01.CIR. 0000129500.29229.92
38. M Massaro A Zampolli E Scoditti MA Carluccio C Storelli A Distante R De Caterina 2010 Statins inhibit cyclooxygenase-2 and matrix metalloproteinase-9 in human endothelial cells: anti-angiogenic actions possibly contributing to plaque stability Cardiovasc Res 86 311 320 19946014 10.1093/cvr/cvp375 1:CAS:528:DC%2BC3cXlt1GltL8%3D
39. M Katsumoto T Shingu R Kuwashima A Nakata S Nomura K Chayama 2005 Biphasic effect of hmg-coa reductase inhibitor, pitavastatin, on vascular endothelial cells and angiogenesis Circ J 69 1547 1555 16308507 10.1253/circj.69.1547 1:CAS:528:DC%2BD2MXhtlamsLjF (Pubitemid 41743974)