Bone marrow-derived mesenchymal stem cells rescue injured H9c2 cells via transferring intact mitochondria through tunneling nanotubes in an in vitro simulated ischemia/reperfusion model

Molecular Medicine Reports

Volumn 13, Issue 2, 2016, Pages 1517-1524

  Han, Hui ^a   Hu, Jinquan ^b   Yan, Qiang ^c   Zhu, Jinzhou ^a   Zhu, Zhengbin ^a   Chen, Yanjia ^a   Sun, Jiateng ^a   Zhang, Ruiyan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

Apoptosis; Co culture system; Ischemia reperfusion injury; Mesenchymal stem cells; Mitochondrial dysfunction; Tunneling nanotubes

Indexed keywords

CASPASE 3; LATRUNCULIN A; NANOTUBE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL COMMUNICATION; CELL INTERACTION; CELL SURVIVAL; CELL TRANSPORT; COCULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; HEART MUSCLE CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL TRANSFER; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; RAT; REPERFUSION INJURY; ANIMAL; BONE MARROW CELL; CARDIAC MUSCLE CELL; CELL LINE; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PROCEDURES; TRANSPLANTATION;

ANIMALS; APOPTOSIS; BONE MARROW CELLS; CELL LINE; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MITOCHONDRIA; MYOCYTES, CARDIAC; NANOTUBES; RATS; REPERFUSION INJURY;

EID: 84956935498     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2015.4726     Document Type: Article

References (35)

1. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, et al: Heart disease and stroke statistics-2011 update: A report from the American heart association. Circulation 123: e18-e209, 2011.
2. Forouzanfar MH, Moran AE, Flaxman AD, Roth G, Mensah GA, Ezzati M, Naghavi M and Murray CJ: Assessing the global burden of ischemic heart disease, part 2: analytic methods and estimates of the global epidemiology of ischemic heart disease in 2010. Glob Heart 7: 331-342, 2012.
3. Yu D, Li M, Tian Y, Liu J and Shang J: Luteolin inhibits ROS-activated MAPK pathway in myocardial ischemia/reperfusion injury. Life Sci 122: 15-25, 2015.
4. Chen C, Feng Y, Zou L, Wang L, Chen HH, Cai JY, Xu JM, Sosnovik DE and Chao W: Role of extracellular RNA and TLR3-Trif signaling in myocardial ischemia-reperfusion injury. J Am Heart Assoc 3: e000683, 2014.
5. Tanaka-Esposito C, Chen Q and Lesnefsky EJ: Blockade of electron transport before ischemia protects mitochondria and decreases myocardial injury during reperfusion in aged rat hearts. Transl Res 160: 207-216, 2012.
6. Gustafsson AB and Gottlieb RA: Bcl-2 family members and apoptosis, taken to heart. Am J Physiol Cell Physiol 292: C45-C51, 2007.
7. Pfeffer MA and Braunwald E: Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications. Circulation 81: 1161-1172, 1990.
8. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj and Horwitz E: Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8: 315-317, 2006.
9. Al-Nbaheen M, Vishnubalaji R, Ali D, Bouslimi A, Al-Jassir F, Megges M, Prigione A, Adjaye J, Kassem M and Aldahmash A: Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev 9: 32-43, 2013.
10. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S and Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147, 1999.
11. Jameel MN and Zhang J: Stem cell therapy for ischemic heart disease. Antioxid Redox Signal 13: 1879-1897, 2010.
12. Karpov AA, Uspenskaya YK, Minasian SM, Puzanov MV, Dmitrieva RI, Bilibina AA, Anisimov SV and Galagudza MM: The effect of bone marrow-and adipose tissue-derived mesenchymal stem cell transplantation on myocardial remodelling in the rat model of ischaemic heart failure. Int J Exp Pathol 94: 169-177, 2013.
13. Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, et al: Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: Double-blind, randomised controlled trial. Lancet 367: 113-121, 2006.
14. Lunde K, Fjeld JG, Smith HJ, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, Endresen K, Ilebekk A, et al: Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 355: 1199-1209, 2006.
15. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, et al: Bone marrow cells regenerate infarcted myocardium. Nature 410: 701-705, 2001.
16. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, et al: Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664-668, 2004.
17. Kawada H, Fujita J, Kinjo K, Matsuzaki Y, Tsuma M, Miyatake H, Muguruma Y, Tsuboi K, Itabashi Y, Ikeda Y, et al: Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood 104: 3581-3587, 2004.
18. Spees JL, Olson SD, Whitney MJ and Prockop DJ: Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA 103: 1283-1288, 2006.
19. Crevensten G, Walsh AJ, Ananthakrishnan D, Page P, Wahba GM, Lotz JC and Berven S: Intervertebral disc cell therapy for regeneration: Mesenchymal stem cell implantation in rat intervertebral discs. Ann Biomed Eng 32: 430-434, 2004.
20. Li B, Li R, Zhang C, Bian HJ, Wang F, Xiao J, Liu SW, Yi W, Zhang MX, Wang SX, et al: MicroRNA-7a/b protects against cardiac myocyte injury in ischemia/reperfusion by targeting poly(ADP-ribose) polymerase. PLoS One 9: e90096, 2014.
21. Ekhterae D, Lin Z, Lundberg MS, Crow MT, Brosius FC III and Núñez G: ARC inhibits cytochrome c release from mitochondria and protects against hypoxia-induced apoptosis in heart-derived H9c2 cells. Circ Res 85: e70-e77, 1999.
22. Yang Z, Liu Y, Deng W, Dai J, Li F, Yuan Y, Wu Q, Zhou H, Bian Z and Tang Q: Hesperetin attenuates mitochondria-dependent apoptosis in lipopolysaccharide-induced H9C2 cardiomyocytes. Mol Med Rep 9: 1941-1946, 2014.
23. Han H, Zhu J, Zhu Z, Ni J, Du R, Dai Y, Chen Y, Wu Z, Lu L and Zhang R: p-Cresyl sulfate aggravates cardiac dysfunction associated with chronic kidney disease by enhancing apoptosis of cardiomyocytes. J Am Heart Assoc 4: e001852, 2015.
24. Gao X, Zhang H, Zhuang W, Yuan G, Sun T, Jiang X, Zhou Z, Yuan H, Zhang Z and Dong H: PEDF and PEDF-derived peptide 44mer protect cardiomyocytes against hypoxia-induced apoptosis and necroptosis via anti-oxidative effect. Sci Rep 4: 5637, 2014.
25. Loor G, Kondapalli J, Iwase H, Chandel NS, Waypa GB, Guzy RD, Vanden Hoek TL and Schumacker PT: Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim Biophys Acta 1813: 1382-1394, 2011.
26. Galluzzi L, Kepp O, Trojel-Hansen C and Kroemer G: Mitochondrial control of cellular life, stress and death. Circ Res 111: 1198-1207, 2012.
27. Plotnikov EY, Khryapenkova TG, Galkina SI, Sukhikh GT and Zorov DB: Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp Cell Res 316: 2447-2455, 2010.
28. Liu K, Ji K, Guo L, Wu W, Lu H, Shan P and Yan C: Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediated mitochondrial transfer. Microvasc Res 92: 10-18, 2014.
29. Wang Y, Cui J, Sun X and Zhang Y: Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ 18: 732-742, 2011.
30. Pasquier J, Guerrouahen BS, Al Thawadi H, Ghiabi P, Maleki M, Abu-Kaoud N, Jacob A, Mirshahi M, Galas L, Rafii S, et al: Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 11: 94, 2013.
31. Cselenyák A, Benko Z, Szepes M, Kiss L and Lacza Z: Stem cell transplantation in an in vitro simulated ischemia/reperfusion model. J Vis Exp 57: e3575, 2011.
32. Rustom A, Saffrich R, Markovic I, Walther P and Gerdes HH: Nanotubular highways for intercellular organelle transport. Science 303: 1007-1010, 2004.
33. Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, Gholami S, Moreira AL, Manova-Todorova K and Moore MA: Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One 7: e33093, 2012.
34. Plotnikov EY, Khryapenkova TG, Vasileva AK, Marey MV, Galkina SI, Isaev NK, Sheval EV, Polyakov VY, Sukhikh GT and Zorov DB: Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture. J Cell Mol Med 12: 1622-1631, 2008.
35. Coué M, Brenner SL, Spector I and Korn ED: Inhibition of actin polymerization by latrunculin A. FEBS Lett 213: 316-318, 1987.