Trichostatin a promotes cardiomyocyte differentiation of rat mesenchymal stem cells after 5-azacytidine induction or during coculture with neonatal cardiomyocytes via a mechanism independent of histone deacetylase inhibition

Cell Transplantation

Volumn 21, Issue 5, 2012, Pages 985-996

  Yang, Ge ^a   Tian, Jie ^b   Feng, Chuan ^a   Zhao, Li li ^a   Liu, Zhenguo ^c   Zhu, Jing ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b CHILDREN S HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

5 azacytidine; Cardiac differentiation; Coculture; Histone deacetylase; Mesenchymal stem cells; Trichostatin a

Indexed keywords

AZACITIDINE; HISTONE DEACETYLASE; MYOCYTE ENHANCER FACTOR 2C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRICHOSTATIN A; TROPONIN T; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEART MUSCLE CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; AZACITIDINE; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; GATA4 TRANSCRIPTION FACTOR; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HOMEODOMAIN PROTEINS; HYDROXAMIC ACIDS; MESENCHYMAL STEM CELLS; MYOCYTES, CARDIAC; MYOGENIC REGULATORY FACTORS; RATS; RATS, WISTAR; TIME FACTORS; TRANSCRIPTION FACTORS; TROPONIN T;

EID: 84862579693     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X593145     Document Type: Article

References (50)

1. Arikawa, E.; Sun, Y.; Wang, J.; Zhou, Q.; Ning, B.; Dial, S. L.; Guo, L.; Yang, J. Cross-platform comparison of SYBR Green real-time PCR with TaqMan PCR, microarrays and other gene expression measurement technologies evaluated in the MicroArray Quality Control (MAQC) study. BMC Genomics 9:328; 2008.
2. Armiñán, A.; Gandía, C.; Bartual, M.; García-Verdugo, J. M.; Lledó, E.; Mirabet, V.; Llop, M.; Barea, J.; Montero, J. A.; Sepúlveda, P. Cardiac differentiation is driven by NKX2.5 and GATA4 nuclear translocation in tissue-specific mesenchymal stem cells. Stem Cells Dev. 18(6):90-918; 2009.
3. Balana, B.; Nicoletti, C.; Zahanich, I.; Graf, E. M.; Christ, T.; Boxberger, S.; Ravens, U. 5-Azacytidine induces changes in electrophysiological properties of human mesenchymal stem cells. Cell Res. 16(12):949-960; 2006.
4. Bascle, A.; Lees, E. Chromatin acetylation and remodeling at the cis promoter during STAT5-induced transcription. Nucleic Acid Res. 31(23):6882-6890; 2003.
5. Battiwalla, M.; Hematti, P. Mesenchymal stem cells in hematopoietic stem cell transplantation. Cytotherapy 11(5): 503-515; 2009.
6. Burlacu, A. Can 5-Azacytidine convert the adult stem cells into cardiomyocytes? A brief overview. Arch. Physiol. Biochem. 112(4-5):260-264; 2006.
7. Chedrawy, E. G.; Wang, J. S.; Nguyen, D. M.; Shum-Tim, D.; Chiu, R. C. Incorporation and integration of implanted myogenic and stem cells into native myocardial fibers: Anatomic basis for functional improvements. J. Thorac. Cardiovasc. Surg. 124(3):584-590; 2002.
8. Chen, J.; Baydoun, A. R.; Xu, R.; Deng, L.; Liu, X.; Zhu, W.; Shi, L.; Cong, X.; Hu, S.; Chen, X. Lysophosphatidic acid protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis. Stem Cells 26(1): 135-145; 2008.
9. Collins, J. M.; Russell, B. Stem cell therapy for cardiac repair. J. Cardiovasc. Nurs. 24(2):93-97; 2009.
10. Cress, W. D.; Seto, E. Histone deacetylases, transcriptional control, and cancer. J. Cell. Physiol. 184(1):1-16; 2000.
11. De Boer, J.; Licht, R.; Bongers, M.; van der Klundert, T.; Arends, R.; van Blitterswijk, C. Inhibition of histone acetylation as a tool in bone tissue engineering. Tissue Eng. 12(10):2927-2937; 2006.
12. Drummond, D. C.; Noble, C. O.; Kirpotin, D. B.; Guo, Z.; Scott, G. K.; Benz, C. C. Clinical development of histone deacetylase inhibitors as anticancer agents. Annu. Rev. Pharmacol. Toxicol. 45:495-528; 2005.
13. Fandy, T. E.; Shankar, S.; Ross, D. D.; Sausville, E.; Srivastava, R. K. Interactive effects of HDAC inhibitors and TRAIL on apoptosis are associated with changes in mitochondrial functions and expressions of cell cycle regulatory genes in multiple myeloma. Neoplasia 7(7):646-657; 2005.
14. Feng, C.; Zhu, J.; Zhao, L.; Lu, T.; Zhang, W.; Liu, Z.; Tian, J. Suberoylanilide hydroxamic acid promotes cardiomyocyte differentiation of rat mesenchymal stem cells. Exp. Cell Res. 315(17):3044-3051; 2009.
15. Furlani, D.; Li, W.; Pittermann, E.; Klopsch, C.; Wang, L.; Knopp, A.; Jungebluth, P.; Thedinga, E.; Havenstein, C.; Westien, I.; Ugurlucan, M.; Li, R. K.; Ma, N.; Steinhoff, G. A transformed cell population derived from cultured mesenchymal stem cells has no functional effect after transplantation into the injured heart. Cell Transplant. 18(3):319-331; 2009.
16. Gallo, M. P.; Ramella, R.; Alloatti, G.; Penna, C.; Pagliaro, P.; Marcantoni, A.; Bonafé, F.; Losano, G.; Levi, R. Limited plasticity of mesenchymal stem cells cocultured with adult cardiomyocytes. J. Cell. Biochem. 100(1):86-99; 2007.
17. Gilchrist, S.; Gilbert, N.; Perry, P.; Bickmore, W. A. Nuclear organization of centromeric domains is not perturbed by inhibition of histone deacetylases. Chromosome Res. 12(5):505-516; 2004.
18. Granger, A.; Abdullah, I.; Huebner, F.; Stout, A.; Wang, T.; Huebner, T.; Epstein, J. A.; Gruber, P. J. Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J. 22(10):3549-3560; 2008.
19. Gregory, C. A.; Ylostalo, J.; Prockop, D. J. Adult bone marrow stem/progenitor cells (MSCs) are preconditioned by microenvironmental "niches" in culture: A two-stage hypothesis for regulation of MSC fate. Sci. STKE 2005(294):pe37; 2005.
20. Karamboulas, C.; Swedani, A.; Ward, C.; Al-Madhoun, A. S.; Wilton, S.; Boisvenue, S.; Ridgeway, A. G.; Skerjanc, I. S. HDAC activity regulates entry of mesoderm cells into the cardiac muscle lineage. J. Cell Sci. 119(20):4305-4314; 2006.
21. Kawamura, T.; Ono, K.; Morimoto, T.; Wada, H.; Hirai, M.; Hidaka, K.; Morisaki, T.; Heike, T.; Nakahata, T.; Kita, T.; Hasegawa, K. Acetylation of GATA-4 is involved in the differentiation of embryonic stem cells into cardiac myocytes. J. Biol. Chem. 280(20):19682-19688; 2005.
22. Koninckx, R.; Hensen, K.; Daniëls, A.; Moreels, M.; Lambrichts, I.; Jongen, H.; Clijsters, C.; Mees, U.; Steels, P.; Hendrikx, M.; Rummens, J. L. Human bone marrow stem cells cocultured with neonatal rat cardiomyocytes display limited cardiomyogenic plasticity. Cytotherapy 11(6):778-792; 2009.
23. Lee, J. H.; Hart, S. R.; Skalnik, D. G. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 38(1):32-38; 2004.
24. Li, H.; Yu, B.; Zhang, Y.; Pan, Z.; Xu, W.; Li, H. Jagged1 protein enhances the differentiation of mesenchymal stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 341(2):320-325; 2006.
25. Li, X.; Yu, X.; Lin, Q.; Deng, C.; Shan, Z.; Yang, M.; Lin, S. Bone marrow mesenchymal stem cells differentiate into functional cardiac phenotypes by cardiac microenvironment. J. Mol. Cell. Cardiol. 42(2):295-303; 2007.
26. Liu, Y.; Song, J.; Liu, W.; Wan, Y.; Chen, X.; Hu, C. Growth and differentiation of rat bone marrow stromal cells: Does 5-azacytidine trigger their cardiomyogenic differentiation? Cardiovasc. Res. 58(2):460-468; 2003.
27. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C (T)] method. Methods 25(4):402-408; 2001.
28. Martin-Rendon, E.; Brunskill, S.; Dorée, C.; Hyde, C.; Watt, S.; Mathur, A.; Stanworth, S. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst. Rev. 4:CD006536; 2008.
29. Mei, S.; Ho, A. D.; Mahlknecht, U. Role of histone deacetylase inhibitors in the treatment of cancer (Review). Int. J. Oncol. 25(6):1509-1519; 2004.
30. Miskon, A.; Mahara, A.; Uyama, H.; Yamaoka, T. A suspension induction for myocardial differentiation of rat mesenchymal stem cells on various extracellular matrix proteins. Tissue Eng. Part C Methods 16(5):979-987; 2010.
31. Muscari, C.; Bonafé, F.; Carboni, M.; Govoni, M.; Stanic, I.; Gamberini, C.; Ricci, F.; Tazzari, P. L.; Caldarera, C. M.; uarnieri, C. Difluoromethylornithine stimulates early cardiac commitment of mesenchymal stem cells in a model of mixed culture with cardiomyocytes. J. Cell. Biochem. 103(4):1046-1052; 2008.
32. Nassiri, S. M.; Khaki, Z.; Soleimani, M.; Ahmadi, S. H.; Jahanzad, I.; Rabbani, S.; Sahebjam, M.; Ardalan, F. A.; Fathollahi, M. S. The similar effect of transplantation of marrow-derived mesenchymal stem cells with or without prior differentiation induction in experimental myocardial infarction. J. Biomed. Sci. 14(6):745-755; 2007.
33. Peixoto, P.; Lansiaux, A. Histone-deacetylases inhibitors: From TSA to SAHA. Bull. Cancer 93(1):27-36; 2006.
34. Psaltis, P. J.; Zannettino, A. C.; Worthley, S. G.; Gronthos, S. Concise review: Mesenchymal stromal cells: Potential for cardiovascular repair. Stem Cells 26(9): 2201-2210; 2008.
35. Reilly, G. C.; Engler, A. J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43(1):55-62; 2010.
36. Seidel, M. Borczyńska, A.; Rozwadowska, N.; Kurpisz, M. Cell-based therapy for heart failure: Skeletal myoblasts. Cell Transplant. 18(7):695-707; 2009.
37. Serakinci, N.; Hoare, S. F.; Kassem, M.; Atkinson, S. P.; Keith, W. N. Telomerase promoter reprogramming and interaction with general transcription factors in the human mesenchymal stem cell. Regen. Med. 1(1):125-131; 2006.
38. Snykers, S.; Vanhaecke, T.; De Becker, A.; Papeleu, P.; Vinken, M.; Van Riet, I.; Rogiers, V. Chromatin remodeling agent trichostatin A: A key-factor in the hepatic differentiation of human mesenchymal stem cells derived of adult bone marrow. BMC Dev. Biol. 7:24; 2007.
39. Taddei, A.; Roche, D.; Bickmore, W. A.; Almouzni, G. The effect of histone deacetvlase inhibitors on heterochromatin: Implications for anticancer therapy? EMBO Rep. 6(6):520-524; 2005.
40. Tokcaer-Keskin, Z.; Akar, A. R.; Ayaloglu-Butun, F.; Terzioglu-Kara, E.; Durdu, S.; Ozyurda, U.; Ugur, M.; Akcali, K. C. Timing of induction of cardiomyocyte differentiation for in vitro cultured mesenchymal stem cells: A perspective for emergencies. Can. J. Physiol. Pharmacol. 87(2):143-150; 2009.
41. Tsai, C. C.; Chen, C. L.; Liu, H. C.; Lee, Y. T.; Wang, H. W.; Hou, L. T.; Hung, S. C. Overexpression of hTERT increases stem-like properties and decreases spontaneous differentiation in human mesenchymal stem cell lines. J. Biomed. Sci. 17(1):64-77; 2010.
42. Wang, M.; Yang, Y.; Yang, D.; Luo, F.; Liang, W.; Guo, S.; Xu, J. The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology 126(2):220-232; 2009.
43. Wang, T.; Xu, Z.; Jiang, W.; Ma, A. Cell-to-cell contact induces mesenchymal stem cell to differentiate into cardiomyocyte and smooth muscle cell. Int. J. Cardiol. 109(1): 74-81; 2006.
44. Wang, Y.; Feng, C.; Xue, J.; Sun, A.; Li, J.; Wu, J. Adenovirus-mediated hypoxia-inducible factor 1alpha doublemutant promotes differentiation of bone marrow stem cells to cardiomyocytes. J. Physiol. Sci. 59(6):413-420; 2009.
45. Xu, J.; Liu, X.; Chen, J.; Zacharek, A.; Cui, X.; SavantBhonsale, S.; Chopp, M.; Liu, Z. Cell-cell interaction promotes rat marrow stromal cell differentiation into endothelial cell via activation of TACE/TNF-alpha signaling. Cell Transplant. 19(1):43-53; 2009.
46. Xu, W.; Zhang, X.; Qian, H.; Zhu, W.; Sun, X.; Hu, J.; Zhou, H.; Chen, Y. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp. Biol. Med. 229(7):623-631; 2004.
47. Yang, C.; Przyborski, S.; Cooke, M. J.; Zhang, X.; Stewart, R.; Anyfantis, G.; Atkinson, S. P.; Saretzki, G.; Armstrong, L.; Lako, M. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 26(4):850-863; 2008.
48. Ye, N. S.; Chen, J.; Luo, G. A.; Zhang, R. L.; Zhao, Y. F.; Wang, Y. M. Proteomic profiling of rat bone marrow mesenchymal stem cells induced by 5-azacytidine. Stem Cells Dev. 15(5):665-676; 2006.
49. Yoon, J.; Shim, W. J.; Ro, Y. M.; Lim, D. S. Transdifferentiation of mesenchymal stem cells into cardiomyocytes by direct cell-to-cell contact with neonatal cardiomyocyte but not adult cardiomyocytes. Ann. Hematol. 84(11):715-721; 2005.
50. Zhang, S.; Jia, Z.; Ge, J.; Gong, L.; Ma, Y.; Li, T.; Guo, J.; Chen, P.; Hu, Q.; Zhang, P.; Liu, Y.; Li, Z.; Ma, K.; Li, L.; Zhou, C. Purified human bone marrow multipotent mesenchymal stem cells regenerate infarcted myocardium in experimental rats. Cell Transplant. 14(10):787-798; 2005.