Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediated mitochondrial transfer

Microvascular Research

Volumn 92, Issue , 2014, Pages 10-18

  Liu, Kaiming ^a,b   Ji, Kunqian ^a,b   Guo, Liang ^a   Wu, Wei ^a   Lu, Huixia ^a   Shan, Peiyan ^a   Yan, Chuanzhu ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; LENTIVIRUS VECTOR; MITOCHONDRIAL DNA; NANOTUBE; PHOSPHATIDYLSERINE;

APOPTOSIS; ARTICLE; CELL ACTIVITY; CELL DAMAGE; CELL DIFFERENTIATION; CELL PROTECTION; CELL REGENERATION; CELL TRANSFER; CELL VIABILITY; DNA POLYMORPHISM; ENDOTHELIUM CELL; GENE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STEM CELL; MITOCHONDRION; OXYGEN CONSUMPTION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; REOXYGENATION; REPERFUSION INJURY; SCA1 GENE; SCA3 GENE; SHORT TANDEM REPEAT; STEM CELL TRANSPLANTATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; BIOLOGICAL MODEL; CELL COMMUNICATION; COCULTURE; CONFOCAL MICROSCOPY; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

APOPTOSIS; CELL COMMUNICATION; COCULTURE TECHNIQUES; DNA, MITOCHONDRIAL; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MODELS, BIOLOGICAL; NANOTUBES; OXYGEN CONSUMPTION; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; REPERFUSION INJURY;

EID: 84895930290     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2014.01.008     Document Type: Article

References (44)

1. Andres A.M., et al. Comparative genetics of functional trinucleotide tandem repeats in humans and apes. J. Mol. Evol. 2004, 59:329-339.
2. Chan P.H. Mitochondrial dysfunction and oxidative stress as determinants of cell death/survival in stroke. Ann. N. Y. Acad. Sci. 2005, 1042:203-209.
3. Chauveau A., et al. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5545-5550.
4. Cselenyak A., et al. Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biol. 2010, 11:29.
5. Cui X., et al. Grape seed proanthocyanidin extracts enhance endothelial nitric oxide synthase expression through 5'-AMP activated protein kinase/Surtuin 1-Krupple like factor 2 pathway and modulate blood pressure in ouabain induced hypertensive rats. Biol. Pharm. Bull. 2012, 35:2192-2197.
6. Dar A., et al. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 2012, 125:87-99.
7. Depraetere V. "Eat me" signals of apoptotic bodies. Nat. Cell Biol. 2000, 2:E104.
8. Dyall S.D., et al. Ancient invasions: from endosymbionts to organelles. Science 2004, 304:253-257.
9. Galluzzi L., et al. Mitochondrial control of cellular life, stress, and death. Circ. Res. 2012, 111:1198-1207.
10. Hase K., et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 2009, 11:1427-1432.
11. He K., et al. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc. Res. 2011, 92:39-47.
12. Hughes A.L., Gottschling D.E. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 2012, 492:261-265.
13. Invernizzi F., et al. Microscale oxygraphy reveals OXPHOS impairment in MRC mutant cells. Mitochondrion 2012, 12:328-335.
14. Kinnaird T., et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 2004, 94:678-685.
15. Kluge M.A., et al. Mitochondria and endothelial function. Circ. Res. 2013, 112:1171-1188.
16. Konishi H., et al. Latrunculin a has a strong anticancer effect in a peritoneal dissemination model of human gastric cancer in mice. Anticancer Res. 2009, 29:2091-2097.
17. Lee J., et al. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 2012, 441:523-540.
18. Li J., et al. Reperfusion promotes mitochondrial dysfunction following focal cerebral ischemia in rats. PLoS One 2012, 7:e46498.
19. Lidell M.E., et al. The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes 2011, 60:427-435.
20. Lin Y.C., et al. Human umbilical mesenchymal stem cells promote recovery after ischemic stroke. Stroke 2011, 42:2045-2053.
21. Liu K., et al. The interactions between brain microvascular endothelial cells and mesenchymal stem cells under hypoxic conditions. Microvasc. Res. 2008, 75:59-67.
22. Lou E., et al. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One 2012, 7:e33093.
23. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
24. Nakano-Doi A., et al. Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells 2010, 28:1292-1302.
25. Onfelt B., et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J. Immunol. 2006, 177:8476-8483.
26. Pasquier J., et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J. Transl. Med. 2013, 11:94.
27. Ravichandran K.S. Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J. Exp. Med. 2010, 207:1807-1817.
28. Ravichandran K.S. Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 2011, 35:445-455.
29. Rizzuto R., et al. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr. Biol. 1995, 5:635-642.
30. Rogers G.W., et al. High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS One 2011, 6:e21746.
31. Rustom A., et al. Nanotubular highways for intercellular organelle transport. Science 2004, 303:1007-1010.
32. Soleimani M., Nadri S. A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat. Protoc. 2009, 4:102-106.
33. Spees J.L., et al. Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2397-2402.
34. Spees J.L., et al. Mitochondrial transfer between cells can rescue aerobic respiration. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1283-1288.
35. Vallabhaneni K.C., et al. Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes. Stem Cells Dev. 2012, 21:3104-3113.
36. Wang X., Gerdes H.H. Long-distance electrical coupling via tunneling nanotubes. Biochim. Biophys. Acta 2012, 1818:2082-2086.
37. Wang X., et al. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17194-17199.
38. Wang Y., et al. Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ. 2011, 18:732-742.
39. Wen Y.D., et al. Hydrogen sulfide protects HUVECs against hydrogen peroxide induced mitochondrial dysfunction and oxidative stress. PLoS One 2013, 8:e53147.
40. Yasuda K., et al. Adriamycin nephropathy: a failure of endothelial progenitor cell-induced repair. Am. J. Pathol. 2010, 176:1685-1695.
41. Yasuda K., et al. Tunneling nanotubes mediate rescue of prematurely senescent endothelial cells by endothelial progenitors: exchange of lysosomal pool. Aging (Albany NY) 2011, 3:597-608.
42. Zhang W.H., et al. Nortriptyline protects mitochondria and reduces cerebral ischemia/hypoxia injury. Stroke 2008, 39:455-462.
43. Zhou X., et al. Trimetazidine protects against smoking-induced left ventricular remodeling via attenuating oxidative stress, apoptosis, and inflammation. PLoS One 2012, 7:e40424.
44. Zou Y., et al. Characterization of nuclear localization signal in the N terminus of CUL4B and its essential role in cyclin E degradation and cell cycle progression. J. Biol. Chem. 2009, 284:33320-33332.