Constitutive HIF-1α expression blunts the beneficial effects of cardiosphere-derived cell therapy in the heart by altering paracrine factor balance

Journal of Cardiovascular Translational Research

Volumn 4, Issue 3, 2011, Pages 363-372

  Bonios, Michael ^a   Chang, Connie Yachan ^a   Terrovitis, John ^a   Pinheiro, Aurelio ^a   Barth, Andreas ^a   Dong, Peihong ^a   Santaularia, Miguel ^a   Brian Foster, D ^a   Raman, Venu ^a   Abraham, Theodore P ^a   Abraham, Maria Roselle ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Animal models of human disease; Cardiac regeneration; Cardiosphere derived cells; Constitutively active HIF 1 ; Echocardiography; Myocardial infarction; Paracrine factor balance

Indexed keywords

ENDOTHELIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LENTIVIRUS VECTOR; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIOSPHERE DERIVED CELL; CELL THERAPY; CIRCUMFERENTIAL STRAIN; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENGRAFTMENT; FEMALE; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; MALE; MUSCLE STRAIN; NONHUMAN; PARACRINE SIGNALING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; RATS; RATS, INBRED WKY; SPHEROIDS, CELLULAR; STROKE VOLUME; TIME FACTORS; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR FUNCTION, LEFT;

ANIMALIA; LENTIVIRUS; RATTUS;

EID: 79960563927     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-011-9265-3     Document Type: Article

References (42)

1. Orlic, D., Kajstura, J., Chimenti, S., Jakoniuk, I., Anderson, S. M., Li, B., et al. (2001). Bone marrow cells regenerate infarcted myocardium. Nature, 410(6829), 701-705. (Pubitemid 32290358)
2. Terrovitis, J., Lautamaki, R., Bonios, M., Fox, J., Engles, J. M., Yu, J., et al. (2009). Noninvasive quantification and optimization of acute cell retention by in vivo positron emission tomography after intramyocardial cardiac-derived stem cell delivery. Journal of the American College of Cardiology, 54(17), 1619-1626. doi:10.1016/j.jacc.2009.04.097.
3. Bartunek, J., Wijns, W., Heyndrickx, G. R., & Vanderheyden, M. (2006). Timing of intracoronary bone-marrow-derived stem cell transplantation after ST-elevation myocardial infarction. Nature Clinical Practice. Cardiovascular Medicine, 3(Suppl 1), S52-56.
4. Jiang, B. H., Rue, E., Wang, G. L., Roe, R., & Semenza, G. L. (1996). Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. The Journal of Biological Chemistry, 271(30), 17771-17778. (Pubitemid 26250751)
5. Sarkar, K., Fox-Talbot, K., Steenbergen, C., Bosch-Marce, M., & Semenza, G. L. (2009). Adenoviral transfer of HIF-1alpha enhances vascular responses to critical limb ischemia in diabetic mice. Proceedings of the National Academy of Sciences of the United States of America, 106(44), 18769-18774.
6. Rey, S., Lee, K., Wang, C. J., Gupta, K., Chen, S., McMillan, A., et al. (2009). Synergistic effect of HIF-1alpha gene therapy and HIF-1-activated bone marrow-derived angiogenic cells in a mouse model of limb ischemia. Proceedings of the National Academy of Sciences of the United States of America, 106(48), 20399-20404.
7. Semenza, G. L. (2010). Vascular responses to hypoxia and ischemia. Arteriosclerosis, Thrombosis, and Vascular Biology, 30(4), 648-652.
8. Semenza, G. L. (2009). Regulation of vascularization by hypoxiainducible factor 1. Annals of the New York Academy of Sciences, 1177, 2-8.
9. Rey, S., & Semenza, G. L. (2010). Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovascular Research, 86(2), 236-242.
10. Wang, G. L., & Semenza, G. L. (1993). Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. The Journal of Biological Chemistry, 268(29), 21513-21518. (Pubitemid 23320639)
11. Semenza, G. L., Shimoda, L. A., & Prabhakar, N. R. (2006). Regulation of gene expression by HIF-1. Novartis Foundation Symposium, 272, 2-8. discussion 8-14, 33-16.
12. Kim, C. H., Cho, Y. S., Chun, Y. S., Park, J. W., & Kim, M. S. (2002). Early expression of myocardial HIF-1alpha in response to mechanical stresses: regulation by stretch-activated channels and the phosphatidylinositol 3-kinase signaling pathway. Circulation Research, 90(2), E25-33.
13. Lee, S. H., Wolf, P. L., Escudero, R., Deutsch, R., Jamieson, S. W., & Thistlethwaite, P. A. (2000). Early expression of angiogenesis factors in acute myocardial ischemia and infarction. The New England Journal of Medicine, 342(9), 626-633. (Pubitemid 30118415)
14. Kelly, B. D., Hackett, S. F., Hirota, K., Oshima, Y., Cai, Z., Berg-Dixon, S., et al. (2003). Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxiainducible factor 1. Circulation Research, 93(11), 1074-1081. (Pubitemid 37485038)
15. Patel, T. H., Kimura, H., Weiss, C. R., Semenza, G. L., & Hofmann, L. V. (2005). Constitutively active HIF-1alpha improves perfusion and arterial remodeling in an endovascular model of limb ischemia. Cardiovascular Research, 68(1), 144-154. (Pubitemid 41253565)
16. Sutter, C. H., Laughner, E., & Semenza, G. L. (2000). Hypoxiainducible factor 1alpha protein expression is controlled by oxygen-regulated ubiquitination that is disrupted by deletions and missense mutations. Proceedings of the National Academy of Sciences of the United States of America, 97(9), 4748-4753. (Pubitemid 30238629)
17. Yamakawa, M., Liu, L. X., Date, T., Belanger, A. J., Vincent, K. A., Akita, G. Y., et al. (2003). Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circulation Research, 93(7), 664-673. (Pubitemid 37222163)
18. Kizana, E., Chang, C. Y., Cingolani, E., Ramirez-Correa, G. A., Sekar, R. B., Abraham, M. R., et al. (2007). Gene transfer of connexin43 mutants attenuates coupling in cardiomyocytes: novel basis for modulation of cardiac conduction by gene therapy. Circulation Research, 100(11), 1597-1604. (Pubitemid 46897263)
19. Yingzhong, Y., Fan, W., Zhu, L., Zhao, T., Ma, L., Wu, Y., et al. (2008). Effects of hypoxia on mRNA expression of housekeeping genes in rat brain tissue and primary cultured neural cells. Fronteirs of Medicine in China, 2, 239-243.
20. Chen, J., He, L., Dinger, B., Stensaas, L., & Fidone, S. (2002). Role of endothelin and endothelin A-type receptor in adaptation of the carotid body to chronic hypoxia. American Journal of Physiology. Lung Cellular and Molecular Physiology, 282(6), L1314-1323. (Pubitemid 34654588)
21. Fukushima, S., Varela-Carver, A., Coppen, S. R., Yamahara, K., Felkin, L. E., Lee, J., et al. (2007). Direct intramyocardial but not intracoronary injection of bone marrow cells induces ventricular arrhythmias in a rat chronic ischemic heart failure model. Circulation, 115(17), 2254-2261. (Pubitemid 46685893)
22. Berridge, M. V., Herst, P. M., & Tan, A. S. (2005). Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnology Annual Review, 11, 127-152. (Pubitemid 41510276)
23. Abraham, T. P., Laskowski, C, Zhan, W. Z., Belohlavek, M., Martin, E. A., Greenleaf, J. F., et al. (2003). Myocardial contractility by strain echocardiography: comparison with physiological measurements in an in vitro model. American Journal of Physiology. Heart and Circulatory Physiology, 285(6), H2599-2604. doi:10.1152/ajpheart.00994.2002. (Pubitemid 37443079)
24. Urheim, S., Cauduro, S., Frantz, R, McGoon, M., Belohlavek, M., Green, T., et al. (2005). Relation of tissue displacement and strain to invasively determined right ventricular stroke volume. The American Journal of Cardiology, 96(8), 1173-1178. doi:10.1016/j.amjcard.2005.06.049. (Pubitemid 41416616)
25. Helm, R. H., Leclercq, C., Faris, O. P., Ozturk, C, McVeigh, E., Lardo, A. C., et al. (2005). Cardiac dyssynchrony analysis using circumferential versus longitudinal strain: implications for assessing cardiac resynchronization. Circulation, 111(21), 2760-2767. doi: 10.1161/CIRCULATIONAHA.104.508457. (Pubitemid 40791547)
26. Langeland, S., D'Hooge, J., Wouters, P. F., Leather, H. A., Claus, P., Bijnens, B., et al. (2005). Experimental validation of a new ultrasound method for the simultaneous assessment of radial and longitudinal myocardial deformation independent of insonation angle. Circulation, 112(14), 2157-2162. doi:10.1161/CIRCULATIONAHA. 105.554006. (Pubitemid 41475810)
27. Koopman, L. P., Slorach, C, Hui, W., Manlhiot, C, McCrindle, B. W., Friedberg, M. K., et al. (2010). Comparison between different speckle tracking and color tissue Doppler techniques to measure global and regional myocardial deformation in children. Journal of the American Society of Echocardiography, 23(9), 919-928. doi: 10.1016/j.echo.2010.06.014.
28. Stastna, M., Chimenti, I., Marban, E., & Van Eyk, J. E. (2010). Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics, 10(2), 245-253.
29. Belaidi, E., Joyeux-Faure, M., Ribuot, C, Launois, S. H., Levy, P., & Godin-Ribuot, D. (2009). Major role for hypoxia inducible factor-1 and the endothelin system in promoting myocardial infarction and hypertension in an animal model of obstructive sleep apnea. Journal of the American College of Cardiology, 53(15), 1309-1317.
30. Watson, J. A., Watson, C. J., McCrohan, A. M., Woodfine, K., Tosetto, M., McDaid, J., et al. (2009). Generation of an epigenetic signature by chronic hypoxia in prostate cells. Human Molecular Genetics, 18(19), 3594-3604.
31. Dandel, M., Lehmkuhl, H., Knosalla, C, Suramelashvili, N., & Hetzer, R (2009). Strain and strain rate imaging by echocardiography-basic concepts and clinical applicability. Current Cardiology Review, 5(2), 133-148.
32. Bosch-Marce, M., Okuyama, H., Wesley, J. B., Sarkar, K., Kimura, H., Liu, Y. V, et al. (2007). Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circulation Research, 101(12), 1310-1318. (Pubitemid 350294648)
33. 2+ exchanger report cardiogenic differentiation in stem cells. Molecular Therapy, 16(5), 957-964. (Pubitemid 351587107)
34. Lei, L., Mason, S., Liu, D., Huang, Y., Marks, C, Hickey, R, et al. (2008). Hypoxia-inducible factor-dependent degeneration, failure, and malignant transformation of the heart in the absence of the von Hippel-Lindau protein. Molecular and Cellular Biology, 28(11), 3790-3803. (Pubitemid 351732913)
35. Ke, Q., & Costa, M. (2006). Hypoxia-inducible factor-1 (HIF-1). Molecular Pharmacology, 70(5), 1469-1480.
36. Yanagisawa, M., Kurihara, H, Kimura, S., Tomobe, Y, Kobayashi, M., Mitsui, Y, et al. (1988). A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature, 332(6163), 411-415. (Pubitemid 18090241)
37. Hocher, B., George, I., Rebstock, J., Bauch, A., Schwarz, A., Neumayer, H. H., et al. (1999). Endothelin system-dependent cardiac remodeling in renovascular hypertension. Hypertension, 33(3), 816-822. (Pubitemid 29140440)
38. Rebsamen, M. C., Church, D. J., Morabito, D., Vallotton, M. B., & Lang, U. (1997). Role of cAMP and calcium influx in endothelin-1-induced ANP release in rat cardiomyocytes. The American Journal of Physiology, 273(5 Pt 1), E922-931.
39. Chimenti, I., Smith, R. R., Li, T. S., Gerstenblith, G., Messina, E., Giacomello, A., et al. (2010). Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circulation Research, 106(5), 971-980.
40. Gnecchi, M., Zhang, Z., Ni, A., & Dzau, V. J. (2008). Paracrine mechanisms in adult stem cell signaling and therapy. Circulation Research, 103(11), 1204-1219.
41. Semenza, G. L. (2004). Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda), 19, 176-182. (Pubitemid 39481932)
42. Popovic, Z. B., Benejam, C., Bian, J., Mal, N., Drinko, J., Lee, K., et al. (2007). Speckle-tracking echocardiography correctly identifies segmental left ventricular dysfunction induced by scarring in a rat model of myocardial infarction. The American Journal of Physiology, 292(6), H2809-2816. (Pubitemid 47084530)