Ex vivo Akt/HO-1 gene therapy to human endothelial progenitor cells enhances myocardial infarction recovery

Cell Transplantation

Volumn 21, Issue 7, 2012, Pages 1443-1461

  Brunt, Keith R ^a,b   Wu, Jun ^b   Chen, Zhilin ^a   Poeckel, Daniel ^a   Dercho, Ryan A ^a   Melo, Luis G ^a   Funk, Colin D ^a   Ward, Christopher A ^a   Li, Ren Ke ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Cardiac function; Cytokine; Extracellular matrix; Growth factor; Heart; Monocyte; Regeneration; Secretome; Stem cell; Vasculogenesis

Indexed keywords

HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ARTICLE; CARDIAC PATIENT; CELL ADHESION; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; CONVALESCENCE; ENDOTHELIAL PROGENITOR CELL; EX VIVO STUDY; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GENE THERAPY; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; NEOVASCULARIZATION (PATHOLOGY); OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CORONARY VESSELS; ENDOTHELIAL CELLS; GENETIC THERAPY; HEME OXYGENASE-1; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; PHAGOCYTOSIS; PROTEIN ARRAY ANALYSIS; PROTEOME; PROTO-ONCOGENE PROTEINS C-AKT; STEM CELL TRANSPLANTATION; STEM CELLS; VENTRICULAR REMODELING;

MUS MUSCULUS;

EID: 84863396121     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X653002     Document Type: Article

References (46)

1. Ackah, E.; Yu, J.; Zoellner, S.; Iwakiri, Y.; Skurk, C.; Shibata, R.; Ouchi, N.; Easton, R. M.; Galasso, G.; Birnbaum, M. J.; Walsh, K.; Sessa, W. C. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115:2119-2127; 2005.
2. Alev, C.; Ii, M.; Asahara, T. Endothelial progenitor cells: A 'novel' tool for the therapy of ischemic diseases. Antioxid. Redox Signal. 15:949-965; 2011.
3. Allen, J. B.; Khan, S.; Lapidos, K. A.; Ameer, G. A. Toward engineering a human neoendothelium with circulating progenitor cells. Stem Cells 28:318-328; 2010.
4. Asahara, T.; Murohara, T.; Sullivan, A.; Silver, M.; van der Zee, R.; Li, T.; Witzenbichler, B.; Schatteman, G.; Isner, J. M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967; 1997.
5. Belosjorow, S.; Bolle, I.; Duschin, A.; Heusch, G.; Schulz, R. TNF-alpha antibodies are as effective as ischemic preconditioning in reducing infarct size in rabbits. Am. J. Physiol. Heart Circ. Physiol. 284:H927-H930; 2003.
6. Brunt, K. R.; Fenrich, K. K.; Kiani, G.; Tse, M. Y.; Pang, S. C.; Ward, C. A.; Melo, L. G. Protection of human vascular smooth muscle cells from H2O2-induced apoptosis through functional codependence between HO-1 and AKT. Arterioscler. Thromb. Vasc. Biol. 26:2027-2034; 2006.
7. Brunt, K. R.; Hall, S. R.; Ward, C. A.; Melo, L. G. Endothelial progenitor cell and mesenchymal stem cell isolation, characterization, viral transduction. Methods Mol. Med. 139:197-210; 2007.
8. Chang, E. I.; Loh, S. A.; Ceradini, D. J.; Chang, E. I.; Lin, S. E.; Bastidas, N.; Aarabi, S.; Chan, D. A.; Freedman, M. L.; Giaccia, A. J.; Gurtner, G. C. Age decreases endothelial progenitor cell recruitment through decreases in hypoxia-inducible factor 1alpha stabilization during ischemia. Circulation 116:2818-2829; 2007.
9. Chavakis, E.; Koyanagi, M.; Dimmeler, S. Enhancing the outcome of cell therapy for cardiac repair: Progress from bench to bedside and back. Circulation 121:325-335; 2010.
10. Cho, H. J.; Lee, N.; Lee, J. Y.; Choi, Y. J.; Ii, M.; Wecker, A.; Jeong, J. O.; Curry, C.; Qin, G.; Yoon, Y. S. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J. Exp. Med. 204:3257-3269; 2007.
11. Deshane, J.; Chen, S.; Caballero, S.; Grochot-Przeczek, A.; Was, H.; Li Causi, S.; Lach, R.; Hock, T. D.; Chen, B.; Hill-Kapturczak, N.; Siegal, G. P.; Dulak, J.; Jozkowicz, A.; Grant, M. B.; Agarwal, A. Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J. Exp. Med. 204:605-618; 2007.
12. Dulak, J.; Deshane, J.; Jozkowicz, A.; Agarwal, A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: Focus on angiogenesis. Circulation 117:231-241; 2008.
13. Erzurum, S. C.; Lemarchand, P.; Rosenfeld, M. A.; Yoo, J. H.; Crystal, R. G. Protection of human endothelial cells from oxidant injury by adenovirus-mediated transfer of the human catalase cDNA. Nucleic Acids Res. 21:1607-1612; 1993.
14. Frangogiannis, N. G. The mechanistic basis of infarct healing. Antioxid. Redox Signal. 8:1907-1939; 2006.
15. Gnecchi, M.; He, H.; Liang, O. D.; Melo, L. G.; Morello, F.; Mu, H.; Noiseux, N.; Zhang, L.; Pratt, R. E.; Ingwall, J. S.; Dzau, V. J. Paracrine action by Akt-modified mesenchymal stem cells. Nat. Med. 11:367-368; 2005.
16. Hamid, T.; Gu, Y.; Ortines, R. V.; Bhattacharya, C.; Wang, G.; Xuan, Y. T.; Prabhu, S. D. Divergent tumor necrosis factor receptor-related remodeling responses in heart failure: role of nuclear factor-kappaB and inflammatory activation. Circulation 119:1386-1397; 2009.
17. Hori, M.; Nishida, K. Oxidative stress and left ventricular remodeling after myocardial infarction. Cardiovasc. Res. 81:457-464; 2009.
18. Hu, Z.; Chen, J.; Wei, Q.; Xia, Y. Bidirectional actions of hydrogen peroxide on endothelial nitric-oxide synthase phosphorylation and function: Co-commitment and interplay of Akt and AMPK. J. Biol. Chem. 283:25256-25263; 2008.
19. Jujo, K.; Ii, M.; Losordo, D. W. Endothelial progenitor cells in neovascularization of infarcted myocardium. J. Mol. Cell. Cardiol. 45:530-544; 2008.
20. Jung, Y.; Isaacs, J. S.; Lee, S.; Trepel, J.; Liu, Z. G.; Neckers, L. Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem. J. 370(Pt. 3):1011-1017; 2003.
21. Kevil, C. G.; Okayama, N.; Alexander, J. S. H(2)O(2)-mediated permeability II: Importance of tyrosine phosphatase and kinase activity. Am. J. Physiol. Cell Physiol. 281: C1940-C1947; 2001.
22. Kim, J. Y.; Song, S. H.; Kim, K. L.; Ko, J. J.; Im, J. E.; Yie, S. W.; Ahn, Y. K.; Kim, D. K.; Suh, W. Human cord blood-derived endothelial progenitor cells and their conditioned media exhibit therapeutic equivalence for diabetic wound healing. Cell Transplant. 19:1635-1644; 2010.
23. Kocher, A. A.; Schuster, M. D.; Szabolcs, M. J.; Takuma, S.; Burkhoff, D.; Wang, J.; Homma, S.; Edwards, N. M.; Itescu, S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardio-myocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7:430-436; 2001.
24. Kroon, M. E.; Koolwijk, P.; van der Vecht, B.; van Hinsbergh, V. W. Urokinase receptor expression on human microvas-cular endothelial cells is increased by hypoxia: Implications for capillary-like tube formation in a fibrin matrix. Blood 96:2775-2783; 2000.
25. Lin, H. H.; Chen, Y. H.; Chang, P. F.; Lee, Y. T.; Yet, S. F.; Chau, L. Y. Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1. J. Mol. Cell. Cardiol. 45:44-55; 2008.
26. Madeddu, P.; Kraenkel, N.; Barcelos, L. S. Phosphoinositide 3-kinase gamma gene knockout impairs postischemic neovascularization and endothelial progenitor cell functions. Arterioscler. Thromb. Vasc. Biol. 28:68-76; 2008.
27. Manalo, D. J.; Rowan, A.; Lavoie, T.; Natarajan, L.; Kelly, B. D.; Ye, S. Q.; Garcia, J. G.; Semenza, G. L. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669; 2005.
28. Mangi, A. A.; Noiseux, N.; Kong, D.; He, H.; Rezvani, M.; Ingwall, J. S.; Dzau, V. J. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9:1195-1201; 2003.
29. Mann, D. L.; McMurray, J. J.; Packer, M.; Swedberg, K.; Borer, J. S.; Colucci, W. S.; Djian, J.; Drexler, H.; Feldman, A.; Kober, L.; Krum, H.; Liu, P.; Nieminen, M.; Tavazzi, L.; van Veldhuisen, D. J.; Waldenstrom, A.; Warren, M.; Westheim, A.; Zannad, F.; Felming, T. Targeted anticytokine therapy in patients with chronic heart failure: Results of the Randomized Etanercept Worldwide Evaluation (RENEWAL). Circulation 109:1594-1602; 2004.
30. Oh, I. Y.; Yoon, C. H.; Hur, J.; Kim, J. H.; Kim, T. Y.; Lee, C. S.; Park, K. W.; Chae, I. H.; Oh, B. H.; Park, Y. B.; Kim, H. S. Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle. Blood 110:3891-3899; 2007.
31. Overton, W. R. Modified histogram subtraction technique for analysis of flow cytometry data. Cytometry 9:619-626; 1988. Erratum in: Cytometry 10:492-494; 1989.
32. Petrache, I.; Verin, A. D.; Crow, M. T.; Birukova, A.; Liu, F.; Garcia, J. G. Differential effect of MLC kinase in TNF-alpha-induced endothelial cell apoptosis and barrier dysfunction. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L1168-L1178; 2001.
33. Pozzobon, M.; Bollini, S.; Iop, L.; De Gaspari, P.; Chiavegato, A.; Rossi, C. A.; Giuliani, S.; Fascetti Leon, F.; Elvassore, N.; Sartore, S.; De Coppi, P. Human bone marrow-derived CD133(+) cells delivered to a collagen patch on cryoinjured rat heart promote angiogenesis and arteriogenesis. Cell Transplant. 19:1247-1260; 2010.
34. Richardson, M. R.; Yoder, M. C. Endothelial progenitor cells: Quo vadis? J. Mol. Cell. Cardiol. 50:266-272; 2011.
35. Rius, J.; Guma, M.; Schachtrup, C.; Akassoglou, K.; Zinkernagel, A. S.; Nizet, V.; Johnson, R. S.; Haddad, G. G.; Karin, M. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453:807-811; 2008.
36. Skyschally, A.; Gres, P.; Hoffmann, S.; Haude, M.; Erbel, R.; Schulz, R.; Heusch, G. Bidirectional role of tumor necrosis factor-alpha in coronary microembolization: progressive contractile dysfunction versus delayed protection against infarction. Circ. Res. 100:140-146; 2007.
37. Sun, Z.; Wu, J.; Fujii, H.; Wu, J.; Li, S. H.; Porozov, S.; Belleli, A.; Fulga, V.; Porat, Y.; Li, R. K. Human angiogenic cell precursors restore function in the infarcted rat heart: A comparison of cell delivery routes. Eur. J. Heart Fail. 10:525-533; 2008.
38. Suuronen, E. J.; Price, J.; Veinot, J. P.; Ascah, K.; Kapila, V.; Guo, X. W.; Wong, S.; Mesana, T. G.; Ruel, M. Comparative effects of mesenchymal progenitor cells, endothelial progenitor cells, or their combination on myocardial infarct regeneration and cardiac function. J. Thorac. Cardiovasc. Surg. 134:1249-1258; 2007.
39. Swynghedauw, B. Molecular mechanisms of myocardial remodeling. Physiol. Rev. 79(1):215-262; 1999.
40. Terada, L. S.; Guidot, D. M.; Leff, J. A.; Willingham, I. R.; Hanley, M. E.; Piermattei, D.; Repine, J. E. Hypoxia injures endothelial cells by increasing endogenous xanthine oxidase activity. Proc. Natl. Acad. Sci. USA 89: 3362-3366; 1992.
41. Tongers, J.; Knapp, J. M.; Korf, M.; Kempf, T.; Limbourg, A.; Limbourg, F. P.; Li, Z.; Bauersachs, J.; Han, X.; Drexler, H.; Fiedler, B.; Wollert, K. C. Haeme oxygenase promotes progenitor cell mobilization, neovascularization, and functional recovery after critical hindlimb ischaemia in mice. Cardiovasc. Res. 78:294-300; 2008.
42. Tsubokawa, T.; Yagi, K.; Nakanishi, C.; Zuka, M.; Nohara, A.; Ino, H.; Fujino, N.; Konno, T.; Kawashiri, M. A.; Ishibashi-Ueda, H.; Nagaya, N.; Yamagishi, M. Impact of anti-apoptotic and anti-oxidative effects of bone marrow mesenchymal stem cells with transient overexpression of heme oxygenase-1 on myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol. 298:H1320-H1329; 2010.
43. Wagener, F. A.; Feldman, E.; de Witte, T.; Abraham, N. G. Heme induces the expression of adhesion molecules ICAM-1, VCAM-1, and E selectin in vascular endothelial cells. Proc. Soc. Exp. Biol. Med. 216:456-463; 1997.
44. Yang, Z.; von Ballmoos, M. W.; Faessler, D.; Voelzmann, J.; Ortmann, J.; Diehm, N.; Kalka-Moll, W.; Baumgartner, I.; Di Santo, S.; Kalka, C. Paracrine factors secreted by endothelial progenitor cells prevent oxidative stress-induced apoptosis of mature endothelial cells. Atherosclerosis 211:103-109; 2010.
45. Zhang, Y.; Ingram, D. A.; Murphy, M. P.; Saadatzadeh, M. R.; Mead, L. E.; Prater, D. N.; Rehman, J. Release of proinflammatory mediators and expression of proinflam-matory adhesion molecules by endothelial progenitor cells. Am. J. Physiol. Heart Circ. Physiol. 296:H1675-H1682; 2009.
46. Zhou, J.; Schmid, T.; Brüne, B. Tumor necrosis factor-alpha causes accumulation of a ubiquitinated form of hypoxia inducible factor-1alpha through a nuclear factor-kappaB-dependent pathway. Mol. Biol. Cell 14:2216-2225; 2003.