i NOS induces vascular endothelial cell migration and apoptosis via autophagy in ischemia/reperfusion injury

Cellular Physiology and Biochemistry

Volumn 38, Issue 4, 2016, Pages 1575-1588

  Zhu, Tiebing ^a,b   Yao, Qi ^a   Wang, Wei ^a   Yao, Honghong ^b,c   Chao, Jie ^b,c  

^a NANJING MEDICAL UNIVERSITY   (China)

^b MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^c SOUTHEAST UNIVERSITY   (China)

Author keywords

Angiogenesis; Apoptosis; Autophagy; HUVEC; iNOS; Migration

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LC3B PROTEIN; N(G) NITROARGININE METHYL ESTER; UBIQUITIN; UNCLASSIFIED DRUG; AUTOPHAGY RELATED PROTEIN 5; BECN1 PROTEIN, HUMAN; CASPASE 3; CASPASE 9; ENZYME INHIBITOR; MAP1LC3B PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ADENOVIRIDAE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; HEART MUSCLE ISCHEMIA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LYSOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL MOTION; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOBLOTTING; METABOLISM; PATHOLOGY;

APOPTOSIS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 5; BCL-2-ASSOCIATED X PROTEIN; BECLIN-1; CASPASE 3; CASPASE 9; CELL MOVEMENT; ENZYME INHIBITORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE II; PROTO-ONCOGENE PROTEINS C-BCL-2; REPERFUSION INJURY; UP-REGULATION;

EID: 84963614503     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000443098     Document Type: Article

References (61)

1. Liu Y, Yang H, Song L, Li N, Han QY, Tian C, Gao E, Du J, Xia YL, Li HH. Aggf1 protects from myocardial ischemia/reperfusion injury by regulating myocardial apoptosis and angiogenesis. Apoptosis 2014; 19: 1254-1268
2. Altamirano F, Wang ZV, Hill JA. Cardioprotection in ischemia/reperfusion injury: Novel mechanisms and clinical translation. J Physiol 2015; 593: 3773-3788
3. Song MA, Paradis AN, Gay MS, Shin J, Zhang L. Differential expression of micrornas in ischemic heart disease. Drug Discov Today 2015; 20: 223-235
4. Yu D, Li M, Tian Y, Liu J, Shang J. Luteolin inhibits ros-Activated mapk pathway in myocardial ischemia/ reperfusion injury. Life Sci 2015; 122: 15-25
5. Zhu T, Yao Q, Hu X, Chen C, Yao H, Chao J. The role of mcpip1 in ischemia/reperfusion injury-induced huvec migration and apoptosis. Cell Physiol Biochem 2015; 37: 577-591
6. Luo T, Chen B, Zhao Z, He N, Zeng Z, Wu B, Fukushima Y, Dai M, Huang Q, Xu D, Bin J, Kitakaze M, Liao Y. Histamine h2 receptor activation exacerbates myocardial ischemia/reperfusion injury by disturbing mitochondrial and endothelial function. Basic Res Cardiol 2013; 108: 342
7. Niu J, Azfer A, Zhelyabovska O, Fatma S, Kolattukudy PE. Monocyte chemotactic protein (mcp)-1 promotes angiogenesis via a novel transcription factor, mcp-1-induced protein (mcpip). J Biol Chem 2008; 283: 14542-14551
8. Zhang X, Liang X, Lin X, Zhang S, Huang Z, Chen C, Guo Y, Xuan F, Xu X, Huang R. Mechanism of the protective effect of yulangsan flavonoid on myocardial ischemia/reperfusion injury in rats. Cell Physiol Biochem 2014; 34: 1050-1062
9. Calvillo L, Vanoli E, Andreoli E, Besana A, Omodeo E, Gnecchi M, Zerbi P, Vago G, Busca G, Schwartz PJ. Vagal stimulation, through its nicotinic action, limits infarct size and the inflammatory response to myocardial ischemia and reperfusion. J Cardiovasc Pharmacol 2011; 58: 500-507
10. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res 2004; 95: 858-866
11. Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res 1997; 80: 829-837
12. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005; 438: 932-936
13. Wang X, Zhang Y, Zhang W, Liu H, Zhou Z, Dai X, Cheng Y, Fang S, Yao H, Chao J. Mcpip1 regulates alveolar macrophage apoptosis and pulmonary fibroblast activation after in vitro exposure to silica. Toxicol Sci 2016; DOI: 10.1093/toxsci/kfw029
14. Peters K, Troyer D, Kummer S, Kirkpatrick CJ, Rauterberg J. Apoptosis causes lumen formation during angiogenesis in vitro. Microvasc Res 2002; 64: 334-338
15. Tertemiz F, Kayisli UA, Arici A, Demir R. Apoptosis contributes to vascular lumen formation and vascular branching in human placental vasculogenesis. Biol Reprod 2005; 72: 727-735
16. Duval H, Harris M, Li J, Johnson N, Print C. New insights into the function and regulation of endothelial cell apoptosis. Angiogenesis 2003; 6: 171-183
17. Cho SO, Lim JW, Kim H. Red ginseng extract inhibits the expression of mcp-1 and inos in helicobacter pylori-infected gastric epithelial cells by suppressing the activation of nadph oxidase and jak2/stat3. J Ethnopharmacol 2013; 150: 761-764
18. Su Z, Ye J, Qin Z, Ding X. Protective effects of madecassoside against doxorubicin induced nephrotoxicity in vivo and in vitro. Sci Rep 2015; 5: 18314
19. Chen H, Xu Y, Wang J, Zhao W, Ruan H. Baicalin ameliorates isoproterenol-induced acute myocardial infarction through inos, inflammation and oxidative stress in rat. Int J Clin Exp Pathol 2015; 8: 10139-10147
20. Martinez-Gonzalez J, Alfon J, Berrozpe M, Badimon L. Hmg-coa reductase inhibitors reduce vascular monocyte chemotactic protein-1 expression in early lesions from hypercholesterolemic swine independently of their effect on plasma cholesterol levels. Atherosclerosis 2001; 159: 27-33
21. Khanna A, Guo M, Mehra M, Royal W, 3rd: Inflammation and oxidative stress induced by cigarette smoke in lewis rat brains. J Neuroimmunol 2013; 254: 69-75
22. Zhang Y, Guo W, Wen Y, Xiong Q, Liu H, Wu J, Zou Y, Zhu Y. Scm-198 attenuates early atherosclerotic lesions in hypercholesterolemic rabbits via modulation of the inflammatory and oxidative stress pathways. Atherosclerosis 2012; 224: 43-50
23. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010; 330: 1344-1348
24. Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E. Excess peroxisomes are degraded by autophagic machinery in mammals. J Biol Chem 2006; 281: 4035-4041
25. Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 2008; 105: 20567-20574
26. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ, Gibson SB. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving bnip3. Autophagy 2008; 4: 195-204
27. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU. Calpain-mediated cleavage of atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-1132
28. Green DR, Galluzzi L, Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011; 333: 1109-1112
29. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469: 323-335
30. Surico D, Farruggio S, Marotta P, Raina G, Mary D, Surico N, Vacca G, Grossini E. Human chorionic gonadotropin protects vascular endothelial cells from oxidative stress by apoptosis inhibition, cell survival signalling activation and mitochondrial function protection. Cell Physiol Biochem 2015; 36: 2108-2120
31. Hsieh MJ, Lin CW, Chiou HL, Yang SF, Chen MK. Dehydroandrographolide, an inos inhibitor, extracted from andrographis paniculata (burm.F.) nees, induces autophagy in human oral cancer cells. Oncotarget 2015; 6: 30831-30849
32. Kandemir FM, Ozkaraca M, Yildirim BA, Hanedan B, Kirbas A, Kilic K, Aktas E, Benzer F. Rutin attenuates gentamicin-induced renal damage by reducing oxidative stress, inflammation, apoptosis, and autophagy in rats. Ren Fail 2015; 37: 518-525
33. Han L, Xu C, Jiang C, Li H, Zhang W, Zhao Y, Zhang L, Zhang Y, Zhao W, Yang B. Effects of polyamines on apoptosis induced by simulated ischemia/reperfusion injury in cultured neonatal rat cardiomyocytes. Cell Biol Int 2007; 31: 1345-1352
34. Yan L, Zhu TB, Wang LS, Pan SY, Tao ZX, Yang Z, Cao K, Huang J. Inhibitory effect of hepatocyte growth factor on cardiomyocytes apoptosis is partly related to reduced calcium sensing receptor expression during a model of simulated ischemia/reperfusion. Mol Biol Rep 2011; 38: 2695-2701
35. Van Horn K, Toth C. Evaluation of the anaeropack campylo system for growth of microaerophilic bacteria. J Clin Microbiol 1999; 37: 2376-2377
36. Lo LW, Koch CJ, Wilson DF. Calibration of oxygen-dependent quenching of the phosphorescence of pd-meso-Tetra (4-carboxyphenyl) porphine: A phosphor with general application for measuring oxygen concentration in biological systems. Anal Biochem 1996; 236: 153-160
37. Chao J, Wood JG, Blanco VG, Gonzalez NC. The systemic inflammation of alveolar hypoxia is initiated by alveolar macrophage-borne mediator(s). Am J Respir Cell Mol Biol 2009; 41: 573-582
38. Liu X, Fang S, Liu H, Wang X, Dai X, Yin Q, Yun T, Wang W, Zhang Y, Liao H, Zhang W, Yao H, Chao J. Role of human pulmonary fibroblast-derived mcp-1 in cell activation and migration in experimental silicosis. Toxicol Appl Pharmacol 2015; 288: 152-160
39. Chao J, Pena T, Heimann DG, Hansen C, Doyle DA, Yanala UR, Guenther TM, Carlson MA. Expression of green fluorescent protein in human foreskin fibroblasts for use in 2d and 3d culture models. Wound Repair Regen 2014; 22: 134-140
40. Wang W, Liu H, Dai X, Fang S, Wang X, Zhang Y, Yao H, Zhang X, Chao J. P53/puma expression in human pulmonary fibroblasts mediates cell activation and migration in silicosis. Sci Rep 2015; 5: 16900
41. Liu H, Dai X, Cheng Y, Fang S, Zhang Y, Wang X, Zhang W, Liao H, Yao H, Chao J. Mcpip1 mediates silica-induced cell migration in human pulmonary fibroblasts. Am J Physiol Lung Cell Mol Physiol 2015; 310: L121-132
42. Carlson MA, Longaker MT, Thompson JS. Modulation of fak, akt, and p53 by stress release of the fibroblast-populated collagen matrix. J Surg Res 2004; 120: 171-177
43. Hariharan N, Zhai P, Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011; 14: 2179-2190
44. Li HY, Cui XY, Wu W, Yu FY, Yao HR, Liu Q, Song EW, Chen JQ. Pyk2 and src mediate signaling to ccl18-induced breast cancer metastasis. J Cell Biochem 2014; 115: 596-603
45. Talero E, Garcia-Maurino S, Motilva V. Melatonin, autophagy and intestinal bowel disease. Curr Pharm Des 2014; 20: 4816-4827
46. Sarkar S, Korolchuk VI, Renna M, Imarisio S, Fleming A, Williams A, Garcia-Arencibia M, Rose C, Luo S, Underwood BR, Kroemer G, OKane CJ, Rubinsztein DC. Complex inhibitory effects of nitric oxide on autophagy. Mol Cell 2011; 43: 19-32
47. Keeley EC, Boura JA, Grines CL. Primary angioplasty versus intravenous thrombolytic therapy for acute myocardial infarction: A quantitative review of 23 randomised trials. Lancet 2003; 361: 13-20
48. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med 2007; 357: 1121-1135
49. Schafer C, Ladilov Y, Inserte J, Schafer M, Haffner S, Garcia-Dorado D, Piper HM. Role of the reverse mode of the na+/ca2+ exchanger in reoxygenation-induced cardiomyocyte injury. Cardiovasc Res 2001; 51: 241-250
50. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 2006; 70: 181-190
51. Shimizu T, Okamoto H, Chiba S, Matsui Y, Sugawara T, Akino M, Nan J, Kumamoto H, Onozuka H, Mikami T, Kitabatake A. Vegf-mediated angiogenesis is impaired by angiotensin type 1 receptor blockade in cardiomyopathic hamster hearts. Cardiovasc Res 2003; 58: 203-212
52. Ibanez B, Heusch G, Ovize M, Van de Werf F. Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol 2015; 65: 1454-1471
53. Yang B, Yang J, Bai J, Pu P, Liu J, Wang F, Ruan B. Suv39h1 protects from myocardial ischemia-reperfusion injury in diabetic rats. Cell Physiol Biochem 2014; 33: 1176-1185
54. Li Q, Wang F, Zhang YM, Zhou JJ, Zhang Y. Activation of cannabinoid type 2 receptor by jwh133 protects heart against ischemia/reperfusion-induced apoptosis. Cell Physiol Biochem 2013; 31: 693-702
55. Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res 2002; 53: 31-47
56. Panaro MA, Brandonisio O, Acquafredda A, Sisto M, Mitolo V. Evidences for inos expression and nitric oxide production in the human macrophages. Curr Drug Targets Immune Endocr Metabol Disord 2003; 3: 210-221
57. Wildhirt SM, Weismueller S, Schulze C, Conrad N, Kornberg A, Reichart B. Inducible nitric oxide synthase activation after ischemia/reperfusion contributes to myocardial dysfunction and extent of infarct size in rabbits: Evidence for a late phase of nitric oxide-mediated reperfusion injury. Cardiovasc Res 1999; 43: 698-711
58. Younce CW, Kolattukudy PE. Mcp-1 causes cardiomyoblast death via autophagy resulting from er stress caused by oxidative stress generated by inducing a novel zinc-finger protein, mcpip. Biochem J 2010; 426: 43-53
59. Roy A, Kolattukudy PE. Monocyte chemotactic protein-induced protein (mcpip) promotes inflammatory angiogenesis via sequential induction of oxidative stress, endoplasmic reticulum stress and autophagy. Cell Signal 2012; 24: 2123-2131
60. Xie M, Morales CR, Lavandero S, Hill JA. Tuning flux: Autophagy as a target of heart disease therapy. Curr Opin Cardiol 2011; 26: 216-222
61. Valentim L, Laurence KM, Townsend PA, Carroll CJ, Soond S, Scarabelli TM, Knight RA, Latchman DS, Stephanou A. Urocortin inhibits beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury. J Mol Cell Cardiol 2006; 40: 846-852