Mesenchymal stem cell transplantation for the infarcted heart: Therapeutic potential for insulin resistance beyond the heart

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Hughey, Curtis C ^a   Ma, Lianli ^b   James, Freyja D ^b   Bracy, Deanna P ^b   Wang, Zhizhang ^b   Wasserman, David H ^b   Rottman, Jeffrey N ^b,c   Hittel, Dustin S ^a   Shearer, Jane ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Diabetes; Glucose uptake; Isotopic tracer; Mitochondria; Myocardial infarction

Indexed keywords

FATTY ACID; GLUCOSE TRANSPORTER 4; INSULIN;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; CATHETERIZATION; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HEART EJECTION FRACTION; HEART INFARCTION; HEART PERFORMANCE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LIPID DIET; M MODE ECHOCARDIOGRAPHY; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RESPIROMETRY; SKELETAL MUSCLE;

ADIPOSE TISSUE; ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FATTY ACIDS; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MUSCLE, SKELETAL; MYOCARDIAL INFARCTION; MYOCARDIUM; OXIDATIVE PHOSPHORYLATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECOVERY OF FUNCTION; STROKE VOLUME; SYSTOLE; TIME FACTORS;

EID: 84883299742     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-128     Document Type: Article

References (70)

1. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev 1999, 79(1):215-262.
2. Minicucci MF, Azevedo PS, Polegato BF, Paiva SA, Zornoff LA. Heart failure after myocardial infarction: clinical implications and treatment. Clin Cardiol 2011, 34(7):410-414. 10.1002/clc.20922, 21688276.
3. Henning RJ. Stem cells in cardiac repair. Future Cardiol 2011, 7(1):99-117. 10.2217/fca.10.109, 21174514.
4. Keats EC, Khan ZA. Vascular stem cells in diabetic complications: evidence for a role in the pathogenesis and the therapeutic promise. Cardiovasc Diabetol 2012, 11:37. 10.1186/1475-2840-11-37, 3476432, 22524626.
5. Ranganath SH, Levy O, Inamdar MS, Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012, 10(3):244-258. 10.1016/j.stem.2012.02.005, 3294273, 22385653.
6. Janssens S. Stem cells in the treatment of heart disease. Annu Rev Med 2010, 61:287-300. 10.1146/annurev.med.051508.215152, 20059339.
7. Penn MS, Ellis S, Gandhi S, Greenbaum A, Hodes Z, Mendelsohn FO, Strasser D, Ting AE, Sherman W. Adventitial delivery of an allogeneic bone marrow-derived adherent stem cell in acute myocardial infarction: phase I clinical study. Circ Res 2012, 110(2):304-311. 10.1161/CIRCRESAHA.111.253427, 22052917.
8. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, et al. 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 2009, 54(24):2277-2286. 10.1016/j.jacc.2009.06.055, 3580848, 19958962.
9. Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, et al. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006, 367(9505):113-121. 10.1016/S0140-6736(05)67861-0, 16413875.
10. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008, 103(11):1204-1219. 10.1161/CIRCRESAHA.108.176826, 2667788, 19028920.
11. Robey TE, Saiget MK, Reinecke H, Murry CE. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 2008, 45(4):567-581. 10.1016/j.yjmcc.2008.03.009, 2587485, 18466917.
12. Haider H, Ashraf M. Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation. J Mol Cell Cardiol 2008, 45(4):554-566. 10.1016/j.yjmcc.2008.05.004, 2670565, 18561945.
13. Wollert KC, Drexler H. Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol 2010, 7(4):204-215. 10.1038/nrcardio.2010.1, 20177405.
14. Feygin J, Mansoor A, Eckman P, Swingen C, Zhang J. Functional and bioenergetic modulations in the infarct border zone following autologous mesenchymal stem cell transplantation. Am J Physiol Heart Circ Physiol 2007, 293(3):H1772-1780. 10.1152/ajpheart.00242.2007, 17573463.
15. Gnecchi M, He H, Melo LG, Noiseaux N, Morello F, De Boer RA, Zhang L, Pratt RE, Dzau VJ, Ingwall JS. Early beneficial effects of bone marrow-derived mesenchymal stem cells overexpressing Akt on cardiac metabolism after myocardial infarction. Stem Cells 2009, 27(4):971-979. 10.1002/stem.12, 2873075, 19353525.
16. Zeng L, Hu Q, Wang X, Mansoor A, Lee J, Feygin J, Zhang G, Suntharalingam P, Boozer S, Mhashilkar A, et al. Bioenergetic and functional consequences of bone marrow-derived multipotent progenitor cell transplantation in hearts with postinfarction left ventricular remodeling. Circulation 2007, 115(14):1866-1875. 10.1161/CIRCULATIONAHA.106.659730, 17389266.
17. Mazo M, Planat-Benard V, Abizanda G, Pelacho B, Leobon B, Gavira JJ, Penuelas I, Cemborain A, Penicaud L, Laharrague P, et al. Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur J Heart Fail 2008, 10(5):454-462. 10.1016/j.ejheart.2008.03.017, 18436478.
18. Hughey CC, Johnsen VL, Ma L, James FD, Young PP, Wasserman DH, Rottman JN, Hittel DS, Shearer J. Mesenchymal stem cell transplantation for the infarcted heart: a role in minimizing abnormalities in cardiac-specific energy metabolism. Am J Physiol Endocrinol Metab 2012, 302(2):E163-172. 10.1152/ajpendo.00443.2011, 3340898, 21971524.
19. Howard BV, Rodriguez BL, Bennett PH, Harris MI, Hamman R, Kuller LH, Pearson TA, Wylie-Rosett J. Prevention Conference VI: Diabetes and Cardiovascular disease: Writing Group I: epidemiology. Circulation 2002, 105(18):e132-137. 10.1161/01.CIR.0000013953.41667.09, 11994263.
20. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA: 1979, 241(19):2035-2038.
21. Sethi SS, Akl EG, Farkouh ME. Diabetes mellitus and acute coronary syndrome: lessons from randomized clinical trials. Curr Diab Rep 2012, 12(3):294-304. 10.1007/s11892-012-0272-9, 22528594.
22. Von Bibra H, St John Sutton M. Impact of diabetes on postinfarction heart failure and left ventricular remodeling. Curr Heart Fail Rep 2011, 8(4):242-251. 10.1007/s11897-011-0070-8, 3208100, 21842146.
23. Ingelsson E, Sundstrom J, Arnlov J, Zethelius B, Lind L. Insulin resistance and risk of congestive heart failure. JAMA: 2005, 294(3):334-341.
24. Lomuscio A, Castagnone M, Vergani D, Verzoni A, Beltrami A, Ravaglia R, Pozzoni L. Clinical correlation between diabetic and non diabetic patients with myocardial infarction. Acta cardiologica 1991, 46(5):543-554.
25. Glass CE, Singal PK, Singla DK. Stem cells in the diabetic infarcted heart. Heart Fail Rev 2010, 15(6):581-588. 10.1007/s10741-010-9172-8, 3072799, 20559720.
26. Abozguia K, Clarke K, Lee L, Frenneaux M. Modification of myocardial substrate use as a therapy for heart failure. Nat Clin Pract Cardiovasc Med 2006, 3(9):490-498. 10.1038/ncpcardio0583, 16932766.
27. Ingwall JS, Weiss RG. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 2004, 95(2):135-145. 10.1161/01.RES.0000137170.41939.d9, 15271865.
28. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 2007, 356(11):1140-1151. 10.1056/NEJMra063052, 17360992.
29. Taha M, Lopaschuk GD. Alterations in energy metabolism in cardiomyopathies. Ann Med 2007, 39(8):594-607. 10.1080/07853890701618305, 17934906.
30. Van Bilsen M, Van Nieuwenhoven FA, van der Vusse GJ. Metabolic remodelling of the failing heart: beneficial or detrimental?. Cardiovasc Res 2009, 81(3):420-428.
31. Jaswal JS, Keung W, Wang W, Ussher JR, Lopaschuk GD. Targeting fatty acid and carbohydrate oxidation-a novel therapeutic intervention in the ischemic and failing heart. Biochim Biophys Acta 2011, 1813(7):1333-1350. 10.1016/j.bbamcr.2011.01.015, 21256164.
32. Razeghi P, Young ME, Ying J, Depre C, Uray IP, Kolesar J, Shipley GL, Moravec CS, Davies PJ, Frazier OH, et al. Downregulation of metabolic gene expression in failing human heart before and after mechanical unloading. Cardiology 2002, 97(4):203-209. 10.1159/000063122, 12145475.
33. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD. Mitochondrial proton and electron leaks. Essays Biochem 2010, 47:53-67. 10.1042/bse0470053, 3122475, 20533900.
34. Witteles RM, Fowler MB. Insulin-resistant cardiomyopathy clinical evidence, mechanisms, and treatment options. J Am Coll Cardiol 2008, 51(2):93-102. 10.1016/j.jacc.2007.10.021, 18191731.
35. Wende AR, Symons JD, Abel ED. Mechanisms of lipotoxicity in the cardiovascular system. Curr Hypertens Rep 2012, 14(6):517-531. 10.1007/s11906-012-0307-2, 23054891.
36. Issad T, Masson E, Pagesy P. O-GlcNAc modification, insulin signaling and diabetic complications. Diabetes Metab 2010, 36(6 Pt 1):423-435.
37. Murray AJ, Anderson RE, Watson GC, Radda GK, Clarke K. Uncoupling proteins in human heart. Lancet 2004, 364(9447):1786-1788. 10.1016/S0140-6736(04)17402-3, 15541452.
38. Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 2011, 109(8):923-940. 10.1161/CIRCRESAHA.111.243147, 3604746, 21960725.
39. Gnecchi M, Danieli P, Cervio E. Mesenchymal stem cell therapy for heart disease. Vasc Pharmacol 2012, 57(1):48-55.
40. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004, 95(1):9-20. 10.1161/01.RES.0000135902.99383.6f, 15242981.
41. Oh JY, Lee RH, Yu JM, Ko JH, Lee HJ, Ko AY, Roddy GW, Prockop DJ. Intravenous mesenchymal stem cells prevented rejection of allogeneic corneal transplants by aborting the early inflammatory response. Mol Ther 2012, 20(11):2143-2152. 10.1038/mt.2012.165, 22929658.
42. Rottman JN, Ni G, Khoo M, Wang Z, Zhang W, Anderson ME, Madu EC. Temporal changes in ventricular function assessed echocardiographically in conscious and anesthetized mice. J Am Soc Echocardiogr 2003, 16(11):1150-1157. 10.1067/S0894-7317(03)00471-1, 14608286.
43. Exil VJ, Roberts RL, Sims H, McLaughlin JE, Malkin RA, Gardner CD, Ni G, Rottman JN, Strauss AW. Very-long-chain acyl-coenzyme a dehydrogenase deficiency in mice. Circ Res 2003, 93(5):448-455. 10.1161/01.RES.0000088786.19197.E4, 12893739.
44. Fueger PT, Lee-Young RS, Shearer J, Bracy DP, Heikkinen S, Laakso M, Rottman JN, Wasserman DH. Phosphorylation barriers to skeletal and cardiac muscle glucose uptakes in high-fat fed mice: studies in mice with a 50% reduction of hexokinase II. Diabetes 2007, 56(10):2476-2484. 10.2337/db07-0532, 17639019.
45. Shearer J, Fueger PT, Bracy DP, Wasserman DH, Rottman JN. Partial gene deletion of heart-type fatty acid-binding protein limits the severity of dietary-induced insulin resistance. Diabetes 2005, 54(11):3133-3139. 10.2337/diabetes.54.11.3133, 16249436.
46. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 2006, 55(2):390-397. 10.2337/diabetes.55.02.06.db05-0686, 16443772.
47. Morgan CR, Lazarow A. Immunoassay of pancreatic and plasma insulin following alloxan injection of rats. Diabetes 1965, 14(10):669-671.
48. Shearer J, Fueger PT, Wang Z, Bracy DP, Wasserman DH, Rottman JN. Metabolic implications of reduced heart-type fatty acid binding protein in insulin-resistant cardiac muscle. Biochim Biophys Acta 2008, 1782(10):586-592. 10.1016/j.bbadis.2008.07.003, 18692568.
49. Rottman JN, Bracy D, Malabanan C, Yue Z, Clanton J, Wasserman DH. Contrasting effects of exercise and NOS inhibition on tissue-specific fatty acid and glucose uptake in mice. Am J Physiol Endocrinol Metab 2002, 283(1):E116-123.
50. Hughey CC, Hittel DS, Johnsen VL, Shearer J. Respirometric oxidative phosphorylation assessment in saponin-permeabilized cardiac fibers. J Vis Exp: JoVE 2011, 48:1-7.
51. Yan B, Abdelli LS, Singla DK. Transplanted induced pluripotent stem cells improve cardiac function and induce neovascularization in the infarcted hearts of db/db mice. Mol Pharm 2011, 8(5):1602-1610. 10.1021/mp2003576, 21851072.
52. Hamman BL, Bittl JA, Jacobus WE, Allen PD, Spencer RS, Tian R, Ingwall JS. Inhibition of the creatine kinase reaction decreases the contractile reserve of isolated rat hearts. Am J Physiol 1995, 269(3 Pt 2):H1030-1036.
53. Neubauer S, Horn M, Cramer M, Harre K, Newell JB, Peters W, Pabst T, Ertl G, Hahn D, Ingwall JS, et al. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 1997, 96(7):2190-2196. 10.1161/01.CIR.96.7.2190, 9337189.
54. Zhang J, McDonald KM. Bioenergetic consequences of left ventricular remodeling. Circulation 1995, 92(4):1011-1019. 10.1161/01.CIR.92.4.1011, 7641336.
55. Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat rev Endocrinol 2012, 8(2):92-103.
56. Jameel MN, Li Q, Mansoor A, Qiang X, Sarver A, Wang X, Swingen C, Zhang J. Long-term functional improvement and gene expression changes after bone marrow-derived multipotent progenitor cell transplantation in myocardial infarction. Am J Physiol Heart Circ Physiol 2010, 298(5):H1348-1356. 10.1152/ajpheart.01100.2009, 20173039.
57. Costford SR, Seifert EL, Bezaire V, M FG, Bevilacqua L, Gowing A, Harper ME. The energetic implications of uncoupling protein-3 in skeletal muscle. Appl Physiol Nutr Metab 2007, 32(5):884-894. 10.1139/H07-063, 18059613.
58. Azzu V, Jastroch M, Divakaruni AS, Brand MD. The regulation and turnover of mitochondrial uncoupling proteins. Biochim Biophys Acta 2010, 1797(6-7):785-791. 2891119, 20211596.
59. Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yanez AJ, Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant 2008, 14(6):631-640. 10.1016/j.bbmt.2008.01.006, 18489988.
60. Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci U S A 2006, 103(46):17438-17443. 10.1073/pnas.0608249103, 1634835, 17088535.
61. Si Y, Zhao Y, Hao H, Liu J, Guo Y, Mu Y, Shen J, Cheng Y, Fu X, Han W. Infusion of mesenchymal stem cells ameliorates hyperglycemia in type 2 diabetic rats: identification of a novel role in improving insulin sensitivity. Diabetes 2012, 61(6):1616-1625. 10.2337/db11-1141, 3357293, 22618776.
62. Jiang R, Han Z, Zhuo G, Qu X, Li X, Wang X, Shao Y, Yang S, Han ZC. Transplantation of placenta-derived mesenchymal stem cells in type 2 diabetes: a pilot study. Front Med 2011, 5(1):94-100. 10.1007/s11684-011-0116-z, 21681681.
63. Couri CE, De Oliveira MC, Simoes BP. Risks, benefits, and therapeutic potential of hematopoietic stem cell transplantation for autoimmune diabetes. Current diab Rep 2012, 12(5):604-611.
64. Hou D, Youssef EA, Brinton TJ, Zhang P, Rogers P, Price ET, Yeung AC, Johnstone BH, Yock PG, March KL. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 2005, 112(9 Suppl):I150-156.
65. Campbell NG, Suzuki K. Cell delivery routes for stem cell therapy to the heart: current and future approaches. J Cardiovasc Transl Res 2012, 5(5):713-726. 10.1007/s12265-012-9378-3, 22648235.
66. Kobayasi R, Akamine EH, Davel AP, Rodrigues MA, Carvalho CR, Rossoni LV. Oxidative stress and inflammatory mediators contribute to endothelial dysfunction in high-fat diet-induced obesity in mice. J Hypertens 2010, 28(10):2111-2119. 10.1097/HJH.0b013e32833ca68c, 20616756.
67. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, Lee MK, Dey A, Rothermel B, Kim YB, Kalinowski A, et al. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 2005, 54(12):3530-3540. 10.2337/diabetes.54.12.3530, 16306372.
68. Ayala JE, Samuel VT, Morton GJ, Obici S, Croniger CM, Shulman GI, Wasserman DH, McGuinness OP. Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis Model Mech 2010, 3(9-10):525-534. 2938392, 20713647.
69. Hearse DJ. Models and problems in the study of myocardial ischemia and tissue protection. Eur Heart J 1983, 4 Suppl C:43-48.
70. Miura T, Miki T. Limitation of myocardial infarct size in the clinical setting: current status and challenges in translating animal experiments into clinical therapy. Basic Res Cardiol 2008, 103(6):501-513. 10.1007/s00395-008-0743-y, 18716709.