Therapeutic efficacy of apelin on transplanted mesenchymal stem cells in hindlimb ischemic mice via regulation of autophagy

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Liang, Dong ^a,c   Han, Dong ^a,b   Fan, Weiwei ^a,d   Zhang, Ran ^a   Qiao, Hongyu ^b   Fan, Miaomiao ^b   Su, Tao ^b   Ma, Sai ^b   Li, Xiujuan ^b   Chen, Jiangwei ^b   Wang, Yabin ^a   Ren, Jun ^e   Cao, Feng ^a,b  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c Shaanxi People's Armed Police Corps Hospital   (China)

^d XIAMEN UNIVERSITY   (China)

^e UNIVERSITY OF WYOMING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; APLN PROTEIN, MOUSE; BECLIN 1; GREEN FLUORESCENT PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MTOR PROTEIN, MOUSE; PROTEIN KINASE B; SIGNAL PEPTIDE; TARGET OF RAPAMYCIN KINASE;

ANIMAL; APOPTOSIS; AUTOPHAGY; CYTOLOGY; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HINDLIMB; INTRAMUSCULAR DRUG ADMINISTRATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; PATHOLOGY; PRIMARY CELL CULTURE; REPERFUSION INJURY; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULARIZATION;

ADIPOKINES; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; AUTOPHAGY; BECLIN-1; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HINDLIMB; INJECTIONS, INTRAMUSCULAR; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, TRANSGENIC; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-AKT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84959085585     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21914     Document Type: Article

References (54)

1. Rooke, T. W. et al. 2011 ACCF/AHA focused update of the guideline for the management of patients with peripheral artery disease (updating the 2005 guideline): a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol(JACC) 58, 2020-2045 (2011).
2. Lawall, H., Bramlage, P. & Amann, B. Stem cell and progenitor cell therapy in peripheral artery disease. Thromb Haemost 103, 696-709 (2010).
3. van der Bogt, K. E. et al. Molecular imaging of bone marrow mononuclear cell survival and homing in murine peripheral artery disease. JACC: Cardiovasc Imag 5, 46-55 (2012).
4. Fan, W. et al. Adipose stromal cell and sarpogrelate orchestrate the recovery of inflammation-induced angiogenesis in aged hindlimb ischemic mice. Aging cell 12, 32-41 (2013).
5. Pan, H., Cai, N., Li, M., Liu, G. H. & Izpisua Belmonte, J. C. Autophagic control of cell 'stemness'. EMBO Mol Med 5, 327-331(2013).
6. Guan, J.-L. et al. Autophagy in stem cells. Autophagy 9, 830-849 (2013).
7. Zhang, Q. et al. Autophagy activation: a novel mechanism of atorvastatin to protect mesenchymal stem cells from hypoxia and serum deprivation via AMP-activated protein kinase/mammalian target of rapamycin pathway. Stem Cells Dev 21, 1321-1332 (2012).
8. Shin, J. Y. et al. Mesenchymal stem cells enhance autophagy and increase β -amyloid clearance in Alzheimer disease models. Autophagy 10, 32-44 (2014).
9. Chen, J. et al. Melatonin attenuates inflammatory response-induced brain edema in early brain injury following a subarachnoid hemorrhage: a possible role for the regulation of pro-inflammatory cytokines. J Pineal Res 57, 340-347 (2014).
10. Haider, H. K. & Ashraf, M. Preconditioning and stem cell survival. J Cardiovasc Transl 3, 89-102 (2010).
11. Ravikumar, B. et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90, 1383-1435 (2010).
12. Marino, G. & Lopez-Otin, C. Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. CMLS-Cell Mol Life S 61, 1439-1454 (2004).
13. Przyklenk, K., Dong, Y., Undyala, V. V. & Whittaker, P. Autophagy as a therapeutic target for ischaemia/reperfusion injury? Concepts, controversies, and challenges. Cardiovasc Res 94, 197-205 (2012).
14. Ma, S., Wang, Y., Chen, Y. & Cao, F. The role of the autophagy in myocardial ischemia/reperfusion injury. BBA-Mol Basis Dis 1852, 271-276 (2015).
15. Zhang, Q., Yao, F., Raizada, M. K., O'Rourke, S. T. & Sun, C. Apelin gene transfer into the rostral ventrolateral medulla induces chronic blood pressure elevation in normotensive rats. Circ Res 104, 1421-1428 (2009).
16. Japp, A. G. & Newby, D. E. The apelin-APJ system in heart failure: pathophysiologic relevance and therapeutic potential. Biochem Pharmacol 75, 1882-1892 (2008).
17. Lee, D. K. et al. Characterization of apelin, the ligand for the APJ receptor. J Neurochem 74, 34-41 (2000).
18. Kleinz, M. J. & Davenport, A. P. Emerging roles of apelin in biology and medicine. Pharmacol Therapeut 107, 198-211 (2005).
19. Simpkin, J. C. et al. Apelin-13 and apelin-36 exhibit direct cardioprotective activity against ischemiareperfusion injury. Basic Res Cardiol 102, 518-528 (2007).
20. Khaksari, M., Aboutaleb, N., Nasirinezhad, F., Vakili, A. & Madjd, Z. Apelin-13 protects the brain against ischemic reperfusion injury and cerebral edema in a transient model of focal cerebral ischemia. J Mol neurosci 48, 201-208 (2012).
21. Wang, W. et al. Loss of Apelin exacerbates myocardial infarction adverse remodeling and ischemia-reperfusion injury: therapeutic potential of synthetic Apelin analogues. J Am Heart Assoc 2, e000249 (2013).
22. Zeng, X., Yu, S. P., Taylor, T., Ogle, M. & Wei, L. Protective effect of apelin on cultured rat bone marrow mesenchymal stem cells against apoptosis. Stem Cell Res 8, 357-367 (2012).
23. Jiao, H., Zhang, Z., Ma, Q., Fu, W. & Liu, Z. Mechanism underlying the inhibitory effect of Apelin-13 on glucose deprivation-induced autophagy in rat cardiomyocytes. Exp Ther Med 5, 797-802 (2013).
24. Yang, L. et al. ERK1/2 mediates lung adenocarcinoma cell proliferation and autophagy induced by apelin-13. Acta Bioch bioph Sin 46, 100-111 (2013).
25. Vrtovec, B. et al. Comparison of transendocardial and intracoronary CD34+ cell transplantation in patients with nonischemic dilated cardiomyopathy. Circulation 128, S42-S49 (2013).
26. Silva, S. A. et al. Autologous bone-marrow mononuclear cell transplantation after acute myocardial infarction: comparison of two delivery techniques. Cell Transplant 18, 343-352 (2009).
27. Aranguren, X. L., Verfaillie, C. M. & Luttun, A. Emerging hurdles in stem cell therapy for peripheral vascular disease. J Mol Med-JMM 87, 3-16 (2009).
28. Robey, T. E., Saiget, M. K., Reinecke, H. & Murry, C. E. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 45, 567-581 (2008).
29. Zeng, X. J. et al. Apelin protects heart against ischemia/reperfusion injury in rat. Peptides 30, 1144-1152 (2009).
30. Tempel, D. et al. Apelin enhances cardiac neovascularization after myocardial infarction by recruiting aplnr + circulating cells. Circ Res 111, 585-598 (2012).
31. Lachmann, N. & Nikol, S. Therapeutic angiogenesis for peripheral artery disease: stem cell therapy. Vasa 36, 241-251 (2007).
32. Fan, W. et al. Adipose stromal cells amplify angiogenic signaling via the VEGF/mTOR/Akt pathway in a murine hindlimb ischemia model: a 3D multimodality imaging study. PloS one 7, e45621 (2012).
33. Li, L., Li, L., Zhang, Z. & Jiang, Z. Hypoxia promotes bone marrow-derived mesenchymal stem cell proliferation through apelin/APJ/autophagy pathway. Acta Bioch Bioph Sin 47, 362-367 (2015).
34. Li, L. et al. Effects of apelin-13 on rat bone marrow-derived mesenchymal stem cell proliferation through the AKT/GSK3β/cyclin D1 pathway. Int J Pept Res Ther 20, 421-425 (2014).
35. Zhang, J. et al. Apelin/APJ signaling promotes hypoxia-induced proliferation of endothelial progenitor cells via phosphoinositide-3 kinase/Akt signaling. Mol Med Rep 12, 3829-3834, (2015).
36. Li, L., Zeng, H. & Chen, J. X. Apelin-13 increases myocardial progenitor cells and improves repair postmyocardial infarction. Am J Physiol Heart Circ Physiol 303, H605-618 (2012).
37. Masri, B., Morin, N., Cornu, M., Knibiehler, B. & Audigier, Y. Apelin (65-77) activates p70 S6 kinase and is mitogenic for umbilical endothelial cells. Faseb J 18, 1909-1911 (2004).
38. Cui, R.-R. et al. Apelin suppresses apoptosis of human vascular smooth muscle cells via APJ/PI3-K/Akt signaling pathways. Amino acids 39, 1193-1200 (2010).
39. Codogno, P. & Meijer, A. J. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12, 1509-1518 (2005).
40. Sekiguchi, A., Kanno, H., Ozawa, H., Yamaya, S. & Itoi, E. Rapamycin promotes autophagy and reduces neural tissue damage and locomotor impairment after spinal cord injury in mice. J Neurotraum 29, 946-956 (2012).
41. Noh, H. S. et al. Propofol protects the autophagic cell death induced by the ischemia/reperfusion injury in rats. Mol Cells 30, 455-460 (2010).
42. Meley, D. et al. AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem 281, 34870-34879 (2006).
43. Sengupta, S., Peterson, T. R. & Sabatini, D. M. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40, 310-322 (2010).
44. Wullschleger, S., Loewith, R. & Hall, M. N. TOR signaling in growth and metabolism. Cell 124, 471-484 (2006).
45. Alers, S., Löffler, A. S., Wesselborg, S. & Stork, B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 32, 2-11 (2012).
46. Meric-Bernstam, F. & Gonzalez-Angulo, A. M. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 27, 2278-2287 (2009).
47. Asnaghi, L. et al. Bcl-2 phosphorylation and apoptosis activated by damaged microtubules require mTOR and are regulated by Akt. Oncogene 23, 5781-5791 (2004).
48. Pattingre, S. et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939 (2005).
49. Matsui, Y. et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100, 914-922 (2007).
50. Nguyen, P. K., Riegler, J. & Wu, J. C. Stem cell imaging: from bench to bedside. Cell stem cell 14, 431-444 (2014).
51. Fan, W. et al. mTORC1 and mTORC2 play different roles in the functional survival of transplanted adipose-derived stromal cells in hind limb ischemic mice via regulating inflammation in vivo. Stem cells 31, 203-214(2013).
52. Huang, X. P. et al. Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122, 2419-2429 (2010).
53. Han, D. et al. Ghrelin Improves Functional Survival of Engrafted Adipose-Derived Mesenchymal Stem Cells in Ischemic Heart through PI3K/Akt Signaling Pathway. Biomed Res Int 2015, e858349 (2015).
54. Stabile, E. et al. Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation 108, 205-210 (2003).