Long-term functional improvement and gene expression changes after bone marrow-derived multipotent progenitor cell transplantation in myocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 298, Issue 5, 2010, Pages

  Jameel, Mohammad Nurulqadr ^a   Li, Qinglu ^a   Mansoor, Abdul ^a   Qiang, Xiong ^a   Sarver, Aaron ^a   Wang, Xiaohong ^a   Swingen, Cory ^a   Zhang, Jianyi ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Energetics; Heart failure; Metabolism; Scar size

Indexed keywords

MITOCHONDRIAL ENZYME; MYOCYTE ENHANCER BINDING FACTOR 2A; MYOCYTE ENHANCER FACTOR 2; OXIDOREDUCTASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN 91;

ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CONTROLLED STUDY; CORONARY ARTERY LIGATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; HEART INFARCTION; HEART VENTRICLE REMODELING; HEART WORK; HISTOLOGY; MULTIPOTENT STEM CELL; MUSCLE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SCAR; STEM CELL TRANSPLANTATION; SWINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOTIN; BONE MARROW TRANSPLANTATION; DNA, COMPLEMENTARY; ENERGY METABOLISM; GENE EXPRESSION; HEMODYNAMICS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MULTIPOTENT STEM CELLS; MYOCARDIAL INFARCTION; MYOCARDIUM; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOCREATINE; RNA; STROKE VOLUME; SWINE; TREATMENT OUTCOME; VENTRICULAR REMODELING;

EID: 77951834574     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01100.2009     Document Type: Article

References (40)

1. Amado LC, Saliaris AP, Schuleri KH, St John M, Xie JS, Cattaneo S, Durand DJ, Fitton T, Kuang JQ, Stewart G, Lehrke S, Baumgartner WW, Martin BJ, Heldman AW, Hare JM. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci USA 102: 11474-11479, 2005. (Pubitemid 41153844)
2. Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 355: 1222-1232, 2006. (Pubitemid 44427446)
3. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 106: 3009-3017, 2002. (Pubitemid 35440281)
4. Black BL, Olson EN. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14: 167-196, 1998.
5. Chen W, Cho Y, Merkle H, Ye Y, Zhang Y, Gong G, Zhang J, Ugurbil K. In vitro and in vivo studies of 1H NMR visibility to detect deoxyhemoglobin and deoxymyoglobin signals in myocardium. Magn Reson Med 42: 1-5, 1999. (Pubitemid 29325605)
6. Dai W, Hale SL, Martin BJ, Kuang JQ, Dow JS, Wold LE, Kloner RA. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation 112: 214-223, 2005. (Pubitemid 40982304)
7. 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 293: H1772-H1780, 2007. (Pubitemid 47367227)
8. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, Dzau VJ. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11: 367-368, 2005. (Pubitemid 40562318)
9. Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 20: 661-669, 2006. (Pubitemid 44933310)
10. Hu Q, Wang X, Lee J, Mansoor A, Liu J, Zeng L, Swingen C, Zhang G, Feygin J, Ochiai K, Bransford TL, From AH, Bache RJ, Zhang J. Profound bioenergetic abnormalities in peri-infarct myocardial regions. Am J Physiol Heart Circ Physiol 291: H648-H657, 2006. (Pubitemid 44175070)
11. Iso Y, Spees JL, Serrano C, Bakondi B, Pochampally R, Song YH, Sobel BE, Delafontaine P, Prockop DJ. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochem Biophys Res Commun 354: 700-706, 2007. (Pubitemid 46186241)
12. Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, Maertens J, Rademakers F, Dymarkowski S, Gheysens O, Van Cleemput J, Bormans G, Nuyts J, Belmans A, Mortelmans L, Boogaerts M, Van de Werf F. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 367: 113-121, 2006. (Pubitemid 43077127)
13. Linke A, Muller P, Nurzynska D, Casarsa C, Torella D, Nascimbene A, Castaldo C, Cascapera S, Bohm M, Quaini F, Urbanek K, Leri A, Hintze TH, Kajstura J, Anversa P. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci USA 102: 8966-8971, 2005. (Pubitemid 40881062)
14. Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, Endresen K, Ilebekk A, Mangschau A, Fjeld JG, Smith HJ, Taraldsrud E, Grogaard HK, Bjornerheim R, Brekke M, Muller C, Hopp E, Ragnarsson A, Brinchmann JE, Forfang K. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 355: 1199-1209, 2006. (Pubitemid 44427444)
15. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, Dzau VJ. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 9: 1195-1201, 2003. (Pubitemid 37173705)
16. Meyer GP, Wollert KC, Lotz J, Steffens J, Lippolt P, Fichtner S, Hecker H, Schaefer A, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation 113: 1287-1294, 2006. (Pubitemid 43739450)
17. Murakami Y, Zhang J, Eijgelshoven MH, Chen W, Carlyle WC, Zhang Y, Gong G, Bache RJ. Myocardial creatine kinase kinetics in hearts with postinfarction left ventricular remodeling. Am J Physiol Heart Circ Physiol 276: H892-H900, 1999. (Pubitemid 29157461)
18. Murakami Y, Zhang Y, Cho YK, Mansoor AM, Chung JK, Chu C, Francis G, Ugurbil K, Bache RJ, From AH, Jerosch-Herold M, Wilke N, Zhang J. Myocardial oxygenation during high work states in hearts with postinfarction remodeling. Circulation 99: 942-948, 1999. (Pubitemid 29094310)
19. Naya FJ, Black BL, Wu H, Bassel-Duby R, Richardson JA, Hill JA, Olson EN. Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor. Nat Med 8: 1303-1309, 2002. (Pubitemid 35373564)
20. Noiseux N, Gnecchi M, Lopez-Ilasaca M, Zhang L, Solomon SD, Deb A, Dzau VJ, Pratt RE. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 14: 840-850, 2006. (Pubitemid 44752717)
21. Raju SV, Zheng M, Schuleri KH, Phan AC, Bedja D, Saraiva RM, Yiginer O, Vandegaer K, Gabrielson KL, O'Donnell CP, Berkowitz DE, Barouch LA, Hare JM. Activation of the cardiac ciliary neurotrophic factor receptor reverses left ventricular hypertrophy in leptin-deficient and leptin-resistant obesity. Proc Natl Acad Sci USA 103: 4222-4227, 2006.
22. Rezende LF, Stoppiglia LF, Souza KL, Negro A, Langone F, Boschero AC. Ciliary neurotrophic factor promotes survival of neonatal rat islets via the BCL-2 anti-apoptotic pathway. J Endocrinol 195: 157-165, 2007. (Pubitemid 350056009)
23. Rota M, Kajstura J, Hosoda T, Bearzi C, Vitale S, Esposito G, Iaffaldano G, Padin-Iruegas ME, Gonzalez A, Rizzi R, Small N, Muraski J, Alvarez R, Chen X, Urbanek K, Bolli R, Houser SR, Leri A, Sussman MA, Anversa P. Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc Natl Acad Sci USA 104: 17783-17788, 2007. (Pubitemid 350210912)
24. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Assmus B, Tonn T, Dimmeler S, Zeiher AM. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355: 1210-1221, 2006. (Pubitemid 44427445)
25. Ten Hove M, Chan S, Lygate C, Monfared M, Boehm E, Hulbert K, Watkins H, Clarke K, Neubauer S. Mechanisms of creatine depletion in chronically failing rat heart. J Mol Cell Cardiol 38: 309-313, 2005. (Pubitemid 40215200)
26. Trachtenberg BH, Hare JM. Biomarkers of oxidative stress in heart failure. Heart Fail Clin 5: 561-577, 2009.
27. Tsai S, Cassady JP, Freking BA, Nonneman DJ, Rohrer GA, Piedrahita JA. Annotation of the Affymetrix porcine genome microarray. Anim Genet 37: 423-424, 2006. (Pubitemid 44091679)
28. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121, 2001. (Pubitemid 32397092)
29. Wallis J, Lygate CA, Fischer A, ten Hove M, Schneider JE, Sebag-Montefiore L, Dawson D, Hulbert K, Zhang W, Zhang MH, Watkins H, Clarke K, Neubauer S. Supranormal myocardial creatine and phosphocreatine concentrations lead to cardiac hypertrophy and heart failure: insights from creatine transporter-overexpressing transgenic mice. Circulation 112: 3131-3139, 2005.
30. Wang X, Jameel MN, Li Q, Mansoor A, Qiang X, Swingen C, Panetta C, Zhang J. Stem cells for myocardial repair with use of a transarterial catheter. Circulation 120: S238-S246, 2009.
31. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364: 141-148, 2004. (Pubitemid 38891685)
32. Ye Y, Gong G, Ochiai K, Liu J, Zhang J. High-energy phosphate metabolism and creatine kinase in failing hearts: a new porcine model. Circulation 103: 1570-1576, 2001. (Pubitemid 32226267)
33. Zeng L, Hu Q, Wang X, Mansoor A, Lee J, Feygin J, Zhang G, Suntharalingam P, Boozer S, Mhashilkar A, Panetta CJ, Swingen C, Deans R, From AH, Bache RJ, Verfaillie CM, Zhang J. Bioenergetic and functional consequences of bone marrow-derived multipotent progenitor cell transplantation in hearts with postinfarction left ventricular remodeling. Circulation 115: 1866-1875, 2007.
34. Zeng L, Rahrmann E, Hu Q, Lund T, Sandquist L, Felten M, O'Brien TD, Zhang J, Verfaillie C. Multipotent adult progenitor cells from swine bone marrow. Stem Cells 24: 2355-2366, 2006. (Pubitemid 44674294)
35. Zhang J, Duncker DJ, Ya X, Zhang Y, Pavek T, Wei H, Merkle H, Ugurbil K, From AH, Bache RJ. Effect of left ventricular hypertrophy secondary to chronic pressure overload on transmural myocardial 2-deoxyglucose uptake. A 31P NMR spectroscopic study. Circulation 92: 1274-1283, 1995.
36. Zhang J, McDonald KM. Bioenergetic consequences of left ventricular remodeling. Circulation 92: 1011-1019, 1995.
37. Zhang J, Merkle H, Hendrich K, Garwood M, From AH, Ugurbil K, Bache RJ. Bioenergetic abnormalities associated with severe left ventricular hypertrophy. J Clin Invest 92: 993-1003, 1993. (Pubitemid 23262424)
38. Zhang J, Murakami Y, Zhang Y, Cho YK, Ye Y, Gong G, Bache RJ, Ugurbil K, From AH. Oxygen delivery does not limit cardiac performance during high work states. Am J Physiol Heart Circ Physiol 277: H50-H57, 1999. (Pubitemid 29354677)
39. Zhang J, Toher C, Erhard M, Zhang Y, Ugurbil K, Bache RJ, Lange T, Homans DC. Relationships between myocardial bioenergetic and left ventricular function in hearts with volume-overload hypertrophy. Circulation 96: 334-343, 1997. (Pubitemid 27298441)
40. Zhang J, Wilke N, Wang Y, Zhang Y, Wang C, Eijgelshoven MH, Cho YK, Murakami Y, Ugurbil K, Bache RJ, From AH. Functional and bioenergetic consequences of postinfarction left ventricular remodeling in a new porcine model. MRI and 31 P-MRS study. Circulation 94: 1089-1100, 1996. (Pubitemid 26292866)