Transplantation of mesenchymal stem cells overexpressing IL10 attenuates cardiac impairments in rats with myocardial infarction

Journal of Cellular Physiology

Volumn 233, Issue 1, 2018, Pages 587-595

  Meng, Xin ^a   Li, Jianping ^a   Yu, Ming ^a   Yang, Jian ^a   Zheng, Minjuan ^a   Zhang, Jinzhou ^a   Sun, Chao ^a   Liang, Hongliang ^a   Liu, Liwen ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

cardiac injury; inflammation; interleukin 10; mesenchymal stem cell; myocardial infarction

Indexed keywords

ADENOVIRUS VECTOR; INTERLEUKIN 10; GLUCOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HEART FUNCTION; HEART INFARCTION; HEART INJURY; HEMODYNAMIC PARAMETERS; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; VIRAL GENE DELIVERY SYSTEM; ADENOVIRIDAE; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE; CELL CULTURE; CELL HYPOXIA; CELL SURVIVAL; DEFICIENCY; DISEASE MODEL; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; GENETICS; HEART CONTRACTION; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE PRESSURE; MESENCHYMAL STROMA CELL; METABOLISM; MYOCARDIAL INFARCTION; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TIME FACTOR; UPREGULATION;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENETIC THERAPY; GENETIC VECTORS; GLUCOSE; INTERLEUKIN-10; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIUM; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TRANSDUCTION, GENETIC; TRANSFECTION; UP-REGULATION; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE;

EID: 85019376081     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25919     Document Type: Article

References (40)

1. Abbate, A., Kontos, M. C., Grizzard, J. D., Biondi-Zoccai, G. G., Van Tassell, B. W., Robati, R., … Vetrovec, G. W. (2010). Interleukin-1 blockade with anakinra to prevent adverse cardiac remodeling after acute myocardial infarction (Virginia Commonwealth University Anakinra Remodeling Trial [VCU-ART] Pilot study). American Journal of Cardiology, 105, 1371–1377. e1371.
2. Aggarwal, S., & Pittenger, M. F. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105, 1815–1822.
3. Arslan, F., Lai, R. C., Smeets, M. B., Akeroyd, L., Choo, A., Aguor, E. N., … de Kleijn, D. P. (2013). Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Research, 10, 301–312.
4. Bartholomew, A., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K., Patil, S., … Hoffman, R. (2002). Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Experimental Hematology, 30, 42–48.
5. Bernstein, H. S., & Srivastava, D. (2012). Stem cell therapy for cardiac disease. Pediatric Research, 71, 491–499.
6. Bujak, M., Dobaczewski, M., Chatila, K., Mendoza, L. H., Li, N., Reddy, A., & Frangogiannis, N. G. (2008). Interleukin-1 receptor type I signaling critically regulates infarct healing and cardiac remodeling. The American Journal of Pathology, 173, 57–67.
7. Burchfield, J. S., Iwasaki, M., Koyanagi, M., Urbich, C., Rosenthal, N., Zeiher, A. M., & Dimmeler, S. (2008). Interleukin-10 from transplanted bone marrow mononuclear cells contributes to cardiac protection after myocardial infarction. Circulation Research, 103, 203–211.
8. Chen, S. L., Fang, W. W., Ye, F., Liu, Y. H., Qian, J., Shan, S. J., … Sun, J. P. (2004). Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. American Journal of Cardiology, 94, 92–95.
9. Choi, J. J., Yoo, S. A., Park, S. J., Kang, Y. J., Kim, W. U., Oh, I. H., & Cho, C. S. (2008). Mesenchymal stem cells overexpressing interleukin-10 attenuate collagen-induced arthritis in mice. Clinical and Experimental Immunology, 153, 269–276.
10. Christia, P., & Frangogiannis, N. G. (2013). Targeting inflammatory pathways in myocardial infarction. European Journal of Clinical Investigation, 43, 986–995.
11. Dewald, O., Zymek, P., Winkelmann, K., Koerting, A., Ren, G., Abou-Khamis, T., … Frangogiannis, N. G. (2005). CCL2/Monocyte Chemoattractant Protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circulation Research, 96, 881–889.
12. Fan, H., Zhao, G., Liu, L., Liu, F., Gong, W., Liu, X., … Hou, Y. (2012). Pre-treatment with IL-1beta enhances the efficacy of MSC transplantation in DSS-induced colitis. Cellular and Molecular Immunology, 9, 473–481.
13. Frangogiannis, N. G., Smith, C. W., & Entman, M. L. (2002). The inflammatory response in myocardial infarction. Cardiovascular Research, 53, 31–47.
14. Ghannam, S., Pene, J., Moquet-Torcy, G., Jorgensen, C., & Yssel, H. (2010). Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. The Journal of Immunology, 185, 302–312.
15. Gnecchi, M., He, H., Liang, O. D., Melo, L. G., Morello, F., Mu, H., … Dzau, V. J. (2005). Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nature Medicine, 11, 367–368.
16. Guo, J., Duckles, S. P., Weiss, J. H., Li, X., & Krause, D. N. (2012). 17beta-Estradiol prevents cell death and mitochondrial dysfunction by an estrogen receptor-dependent mechanism in astrocytes after oxygen-glucose deprivation/reperfusion. Free Radical Biology & Med, 52, 2151–2160.
17. Guo, J., Lin, G. S., Bao, C. Y., Hu, Z. M., & Hu, M. Y. (2007). Anti-inflammation role for mesenchymal stem cells transplantation in myocardial infarction. Inflammation, 30, 97–104.
18. Hahn, J. Y., Cho, H. J., Kang, H. J., Kim, T. S., Kim, M. H., Chung, J. H., … Kim, H. S. (2008). Pre-treatment of mesenchymal stem cells with a combination of growth factors enhances gap junction formation, cytoprotective effect on cardiomyocytes, and therapeutic efficacy for myocardial infarction. Journal of the American College of Cardiology, 51, 933–943.
19. Hare, J. M., Traverse, J. H., Henry, T. D., Dib, N., Strumpf, R. K., Schulman, S. P., … Sherman, W. (2009). A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. Journal of the American College of Cardiology, 54, 2277–2286.
20. Holladay, C. A., Duffy, A. M., Chen, X., Sefton, M. V., O'Brien, T. D., & Pandit, A. S. (2012). Recovery of cardiac function mediated by MSC and interleukin-10 plasmid functionalised scaffold. Biomaterials, 33, 1303–1314.
21. Janssens, S., Dubois, C., Bogaert, J., Theunissen, K., Deroose, C., Desmet, W., … Van de Werf, F. (2006). Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: Double-blind, randomised controlled trial. The Lancet, 367, 113–121.
22. Kaur, K., Sharma, A. K., & Singal, P. K. (2006). Significance of changes in TNF-alpha and IL-10 levels in the progression of heart failure subsequent to myocardial infarction. American Journal of Physiology—Heart and Circulatory Physiology, 291, H106–H113.
23. Krampera, M., Cosmi, L., Angeli, R., Pasini, A., Liotta, F., Andreini, A., … Annunziato, F. (2006). Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells, 24, 386–398.
24. Krampera, M., Glennie, S., Dyson, J., Scott, D., Laylor, R., Simpson, E., & Dazzi, F. (2003). Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood, 101, 3722–3729.
25. Krishnamurthy, P., Rajasingh, J., Lambers, E., Qin, G., Losordo, D. W., & Kishore, R. (2009). IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR. Circulation Research, 104, e9–e18.
26. Lim, S. Y., Kim, Y. S., Ahn, Y., Jeong, M. H., Hong, M. H., Joo, S. Y., … Park, J. C. (2006). The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model. Cardiovascular Research, 70, 530–542.
27. Liu, X., Qu, X., Chen, Y., Liao, L., Cheng, K., Shao, C., … Zhao, R. C. (2012). Mesenchymal stem/stromal cells induce the generation of novel IL-10-dependent regulatory dendritic cells by SOCS3 activation. The Journal of Immunology, 189, 1182–1192.
28. Mangi, A. A., Noiseux, N., Kong, D., He, H., Rezvani, M., Ingwall, J. S., & Dzau, V. J. (2003). Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nature Medicine, 9, 1195–1201.
29. Manning, E., Pham, S., Li, S., Vazquez-Padron, R. I., Mathew, J., Ruiz, P., & Salgar, S. K. (2010). Interleukin-10 delivery via mesenchymal stem cells: A novel gene therapy approach to prevent lung ischemia-reperfusion injury. Human Gene Therapy, 21, 713–727.
30. Min, C. K., Kim, B. G., Park, G., Cho, B., & Oh, I. H. (2007). IL-10-transduced bone marrow mesenchymal stem cells can attenuate the severity of acute graft-versus-host disease after experimental allogeneic stem cell transplantation. Bone Marrow Transplantation, 39, 637–645.
31. Oyama, J., Blais, C., Jr., Liu, X., Pu, M., Kobzik, L., Kelly, R. A., & Bourcier, T. (2004). Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation, 109, 784–789.
32. Peng, H. H., Wu, S., Davis, J. J., Wang, L., Roth, J. A., Marini, F. C. III., & Fang, B. (2006). A rapid and efficient method for purification of recombinant adenovirus with arginine-glycine-aspartic acid-modified fibers. Analytical Biochemistry, 354, 140–147.
33. Segers, V. F., & Lee, R. T. (2008). Stem-cell therapy for cardiac disease. Nature, 451, 937–942.
34. Seropian, I. M., Toldo, S., Van Tassell, B. W., & Abbate, A. (2014). Anti-inflammatory strategies for ventricular remodeling following ST-segment elevation acute myocardial infarction. Journal of the American College of Cardiology, 63, 1593–1603.
35. Shi, C. Z., Zhang, X. P., Lv, Z. W., Zhang, H. L., Xu, J. Z., Yin, Z. F., … Wang, C. Q. (2012). Adipose tissue-derived stem cells embedded with eNOS restore cardiac function in acute myocardial infarction model. International Journal of Cardiology, 154, 2–8.
36. Stamm, C., Westphal, B., Kleine, H. D., Petzsch, M., Kittner, C., Klinge, H., … Steinhoff, G. (2003). Autologous bone-marrow stem-cell transplantation for myocardial regeneration. The Lancet, 361, 45–46.
37. Tang, J., Xie, Q., Pan, G., Wang, J., & Wang, M. (2006). Mesenchymal stem cells participate in angiogenesis and improve heart function in rat model of myocardial ischemia with reperfusion. European Journal of Cardio-Thoracic Surgery, 30, 353–361.
38. Tang, Y. L., Zhao, Q., Qin, X., Shen, L., Cheng, L., Ge, J., & Phillips, M. I. (2005). Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Annals of Thoracic Surgery, 80, 229–236.
39. Wang, Y., Chen, X., Cao, W., & Shi, Y. (2014). Plasticity of mesenchymal stem cells in immunomodulation: Pathological and therapeutic implications. Nature Immunology, 15, 1009–1016.
40. Yang, S. H., Park, M. J., Yoon, I. H., Kim, S. Y., Hong, S. H., Shin, J. Y., … Park, C. G. (2009). Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Experimental and Molecular Medicine, 41, 315–324.