Differentiation of embryonic stem cells into cardiomyocytes used to investigate the cardioprotective effect of salvianolic acid B through BNIP3 involved pathway

Cell Transplantation

Volumn 24, Issue 3, 2015, Pages 561-571

  Huang, Chih Yang ^a,b,c   Chen, Shao Yu ^a   Fu, Ru Huei ^a,d   Huang, Yu Chuen ^c,d   Chen, Shih Yin ^c,d   Shyu, Woei Cherng ^a,d   Lin, Shinn Zong ^a,d,e,f   Liu, Shih Ping ^a,b,d  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b ASIA UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^f Cardiology Section   (Taiwan)

Author keywords

B cell CLL lymphoma 2 (Bcl 2) adenovirus E1B 19 kDa interacting protein 3 (BNIP3); Cardiomyocytes; Embryonic stem cells; Hypoxia; Salvianolic acid B (Sal B)

Indexed keywords

ACTININ; CARDIOVASCULAR AGENT; CASPASE 3; DESMIN; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; POLY DEXTRO LYSINE; PROTEIN BNIP3; SALVIA MILTIORRHIZA EXTRACT; SALVIANOLIC ACID B; TROPONIN; BENZOFURAN DERIVATIVE; BNIP3 PROTEIN, RAT; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; POLYLYSINE; PROTECTIVE AGENT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROTECTION; CELL SURVIVAL; CONCENTRATION (PARAMETERS); DIABETES MELLITUS; DOWN REGULATION; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ENZYME INHIBITION; GENE OVEREXPRESSION; HEART PROTECTION; MOUSE; MTT ASSAY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL CULTURE; SURVIVAL RATE; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; HEART MUSCLE CELL; METABOLISM; RAT; SIGNAL TRANSDUCTION;

ADENOVIRIDAE;

ANIMALS; APOPTOSIS; BENZOFURANS; CASPASE 3; CELL DIFFERENTIATION; CELL HYPOXIA; CELLS, CULTURED; DOWN-REGULATION; EMBRYONIC STEM CELLS; GLUCOSE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; MYOCYTES, CARDIAC; POLYLYSINE; PROTECTIVE AGENTS; RATS; SIGNAL TRANSDUCTION;

EID: 84927168893     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368915X686995     Document Type: Article

References (41)

1. Bialik, S.; Geenen, D. L.; Sasson, I. E.; Cheng, R.; Horner, J. W.; Evans, S. M.; Lord, E. M.; Koch, C. J.; Kitsis, R. N. Myocyte apoptosis during acute myocardial infarction in the mouse localizes to hypoxic regions but occurs independently of p53. J. Clin. Invest. 100(6):1363–1372; 1997.
2. Burton, T. R.; Gibson, S. B. The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ. 16(4):515–523; 2009.
3. Centers for Disease Control and Prevention (CDC). Self-reported heart disease and stroke among adults with and without diabetes–United States, 1999–2001. MMWR. Morb. Mortal. Wkly. Rep. 52(44):1065–1070; 2003.
4. Chen, G.; Cizeau, J.; VandeVelde, C.; Park, J. H.; Bozek, G.; Bolton, J.; Shi, L.; Dubik, D.; Greenberg, A. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J. Biol. Chem. 274(1):7–10; 1999.
5. Cheng, W.; Kajstura, J.; Nitahara, J. A.; Li, B.; Reiss, K.; Liu, Y.; Clark, W. A.; Krajewski, S.; Reed, J. C.; Olivetti, G.; Anversa, P. Programmed myocyte cell death affects the viable myocardium after infarction in rats. Exp. Cell Res. 226(2):316–327; 1996.
6. Chinnadurai, G.; Vijayalingam, S.; Gibson, S. B. BNIP3 subfamily BH3-only proteins: Mitochondrial stress sensors in normal and pathological functions. Oncogene 27(Suppl 1):S114–S127; 2008.
7. Cizeau, J.; Ray, R.; Chen, G.; Gietz, R. D.; Greenberg, A. H. The C. elegans orthologue ceBNIP3 interacts with CED-9 and CED-3 but kills through a BH3- and caspaseindependent mechanism. Oncogene 19(48):5453–5463; 2000.
8. Crow, M. T. Hypoxia, BNip3 proteins, and the mitochondrial death pathway in cardiomyocytes. Circ. Res. 91(3): 183–185; 2002.
9. Daido, S.; Kanzawa, T.; Yamamoto, A.; Takeuchi, H.; Kondo, Y.; Kondo, S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64(12):4286–4293; 2004.
10. Diwan, A.; Matkovich, S. J.; Yuan, Q.; Zhao, W.; Yatani, A.; Brown, J. H.; Molkentin, J. D.; Kranias, E. G.; Dorn, G. W. 2nd Endoplasmic reticulum-mitochondria crosstalk in NIX-mediated murine cell death. J. Clin. Invest. 119(1): 203–212; 2009.
11. Dorn, G. W.2nd; Kirshenbaum, L. A. Cardiac reanimation: Targeting cardiomyocyte death by BNIP3 and NIX/BNIP3L. Oncogene 27(Suppl 1):S158–S167; 2008.
12. Graham, R. M.; Frazier, D. P.; Thompson, J. W.; Haliko, S.; Li, H.; Wasserlauf, B. J.; Spiga, M. G.; Bishopric, N. H.; Webster, K. A. A unique pathway of cardiac myocyte death caused by hypoxia-acidosis. J. Exp. Biol. 207(Pt 18):3189– 3200; 2004.
13. Gu, K.; Cowie, C. C.; Harris, M. I. Diabetes and decline in heart disease mortality in US adults. JAMA 281(14): 1291–1297; 1999.
14. Halterman, M. W.; Federoff, H. J. HIF-1alpha and p53 promote hypoxia-induced delayed neuronal death in models of CNS ischemia. Exp. Neurol. 159(1):65–72; 1999.
15. Harris, A. L. Hypoxia–A key regulatory factor in tumour growth. Nat. Rev. Cancer 2(1):38–47; 2002.
16. Ho, J. H.; Hong, C. Y. Salvianolic acids: Small compounds with multiple mechanisms for cardiovascular protection. J. Biomed.Sci. 18:30; 2011.
17. Hwang, J. M.; Weng, Y. J.; Lin, J. A.; Bau, D. T.; Ko, F. Y.; Tsai, F. J.; Tsai, C. H.; Wu, C. H.; Lin, P. C.; Huang, C. Y.; Kuo, W. W. Hypoxia-induced compensatory effect as related to Shh and HIF-1alpha in ischemia embryo rat heart. Mol. Cell. Biochem. 311(1–2):179–187; 2008.
18. Itoh, G.; Tamura, J.; Suzuki, M.; Suzuki, Y.; Ikeda, H.; Koike, M.; Nomura, M.; Jie, T.; Ito, K. DNA fragmentation of human infarcted myocardial cells demonstrated by the nick end labeling method and DNA agarose gel electrophoresis. Am. J. Pathol. 146(6):1325–1331; 1995.
19. Kanzawa, T.; Zhang, L.; Xiao, L.; Germano, I. M.; Kondo, Y.; Kondo, S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 24(6):980– 991; 2005.
20. Kim, J. Y.; Ahn, H. J.; Ryu, J. H.; Suk, K.; Park, J. H. BH3-only protein Noxa is a mediator of hypoxic cell death induced by hypoxia-inducible factor 1alpha. J. Exp. Med. 199(1):113–124; 2004.
21. Kobayashi, Y.; Hattori, M.; Wada, S.; Iwase, H.; Kadono, M.; Tatsumi, H.; Kuwahata, M.; Fukui, M.; Hasegawa, G.; Nakamura, N.; Kido, Y. Assessment of daily food and nutrient intake in Japanese type 2 diabetes mellitus patients using dietary reference intakes. Nutrients 5(7):2276–2288; 2013.
22. Lee, C. M.; Chen, S. Y.; Lee, Y. C.; Huang, C. Y.; Chen, Y. M. Benzo[a]pyrene and glycine N-methyltransferse interactions: Gene expression profiles of the liver detoxification pathway. Toxicol. Appl. Pharmacol. 214:126–135.
23. Lee, S. H.; Wolf, P. L.; Escudero, R.; Deutsch, R.; Jamieson, S. W.; Thistlethwaite, P. A. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N. Engl. J. Med. 342(9):626–633; 2000.
24. Li, W.; Ding, S. Converting mouse epiblast stem cells into mouse embryonic stem cells by using small molecules. Methods Mol. Biol. 1074:31–37; 2013.
25. Liu, S. P.; Fu, R. H.; Huang, Y. C.; Chen, S. Y.; Chien, Y. J.; Hsu, C. Y.; Tsai, C. H.; Shyu, W. C.; Lin, S. Z. Induced pluripotent stem (iPS) cell research overview. Cell Transplant. 20(1):15–19; 2011.
26. Liu, S. P.; Fu, R. H.; Wu, D. C.; Hsu, C. Y.; Chang, C. H.; Lee, W.; Lee, Y. D.; Liu, C. H.; Chien, Y. J.; Lin, S. Z.; Shyu, W. C. Mouse-induced pluripotent stem cells generated under hypoxic conditions in the absence of viral infection and oncogenic factors and used for ischemic stroke therapy. Stem Cells Dev. 23(4):421–433; 2014.
27. Nakayama, H.; Chen, X.; Baines, C. P.; Klevitsky, R.; Zhang, X.; Zhang, H.; Jaleel, N.; Chua, B. H.; Hewett, T. E.; Robbins, J.; Houser, S. R.; Molkentin, J. D. Ca2+- and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J. Clin. Invest. 117(9): 2431–2444; 2007.
28. Narula, J.; Kolodgie, F. D.; Virmani, R. Apoptosis and cardiomyopathy. Curr. Opin. Cardiol. 15(3):183–188; 2000.
29. Palojoki, E.; Saraste, A.; Eriksson, A.; Pulkki, K.; Kallajoki, M.; Voipio-Pulkki, L. M.; Tikkanen, I. Cardiomyocyte apoptosis and ventricular remodeling after myocardial infarction in rats. Am. J. Physiol. Heart Circ. Physiol. 280(6):H2726–H2731; 2001.
30. Pitts, K. R.; Derry, J. M.; Kerkof, K.; Lawrence, W. A.; Toombs, C. F. Differentially regulated functional gene clusters identified during ischemia and reperfusion in isolated cardiac myocytes using coverslip hypoxia. J. Pharmacol. Toxicol. Methods 57(1):42–51; 2008.
31. Ray, R.; Chen, G.; VandeVelde, C.; Cizeau, J.; Park, J. H.; Reed, J. C.; Gietz, R. D.; Greenberg, A. H. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J. Biol. Chem. 275(2):1439–1448; 2000.
32. Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676; 2006.
33. Tanaka, M.; Ito, H.; Adachi, S.; Akimoto, H.; Nishikawa, T.; Kasajima, T.; Marumo, F.; Hiroe, M. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ. Res. 75(3):426–433; 1994.
34. Thomas, R. J.; Palumbo, P. J.; Melton, L. J.3rd; Roger, V. L.; Ransom, J.; O’Brien, P. C.; Leibson, C. L. Trends in the mortality burden associated with diabetes mellitus: A population-based study in Rochester, Minn, 1970-1994. Arch. Intern. Med. 163(4):445–451; 2003.
35. Wang, M.; Sun, G. B.; Sun, X.; Wang, H. W.; Meng, X. B.; Qin, M.; Sun, J.; Luo, Y.; Sun, X. B. Cardioprotective effect of salvianolic acid B against arsenic trioxide-induced injury in cardiac H9c2 cells via the PI3K/Akt signal pathway. Toxicol. Lett. 216(2–3):100–107; 2013.
36. Wang, Y.; Qian, D. J.; Zhong, W. Y.; Lu, J. H.; Guo, X. K.; Cao, Y. L.; Liu, J. TGF-beta1 induces the formation of vascular-like structures in embryoid bodies derived from human embryonic stem cells. Exp. Ther. Med. 8(1): 52–58; 2014.
37. Xu, L.; Deng, Y.; Feng, L.; Li, D.; Chen, X.; Ma, C.; Liu, X.; Yin, J.; Yang, M.; Teng, F.; Wu, W.; Guan, S.; Jiang, B.; Guo, D. Cardio-protection of salvianolic acid B through inhibition of apoptosis network. PloS One 6(9):e24036; 2011.
38. Yasuda, M.; Theodorakis, P.; Subramanian, T.; Chinnadurai, G. Adenovirus E1B-19K/BCL-2 interacting protein BNIP3 contains a BH3 domain and a mitochondrial targeting sequence. J. Biol. Chem. 273(20):12415–12421; 1998.
39. Ying, Q. L.; Nichols, J.; Chambers, I.; Smith, A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115(3):281–292; 2003.
40. Zheng, K.; Sheng, Z.; Li, Y.; Lu, H. Salidroside inhibits oxygen glucose deprivation (OGD)/re-oxygenation-induced H9c2 cell necrosis through activating of Akt-Nrf2 signaling. Biochem. Biophys. Res. Commun. 451(1):79–85; 2014.
41. Zhou, Y. F.; Zheng, X. W.; Zhang, G. H.; Zong, Z. H.; Qi, G. X. The effect of hypoxia-inducible factor 1-alpha on hypoxia-induced apoptosis in primary neonatal rat ventricular myocytes. Cardiovasc. J. Afr. 21(1):37–41; 2010.