The Role of Mitochondria-Derived Reactive Oxygen Species in Hyperthermia-Induced Platelet Apoptosis

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Wang, Zhicheng ^a,b   Cai, Feng ^b   Chen, Xiaoyu ^c   Luo, Meihong ^b   Hu, Lingling ^b   Lu, Yuan ^a  

^a FUDAN UNIVERSITY   (China)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; LIPOXYGENASE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPERTHERMIA; LIPID PEROXIDATION; MITOCHONDRION; OXIDATIVE STRESS; THROMBOCYTE; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION;

APOPTOSIS; BLOOD PLATELETS; CARDIOLIPINS; HUMANS; HYPERTHERMIA, INDUCED; LIPID PEROXIDATION; MALONDIALDEHYDE; MITOCHONDRIA; ORGANOPHOSPHORUS COMPOUNDS; PIPERIDINES; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 84883418353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075044     Document Type: Article

References (54)

1. Souslova T, Averill-Bates DA, (2004) Multidrug-resistant hela cells overexpressing MRP1 exhibit sensitivity to cell killing by hyperthermia: interactions with etoposide. Int J Radiat Oncol Biol Phys 60: 1538-1551. doi:10.1016/j.ijrobp.2004.07.686. PubMed: 15590186.
2. Luchetti F, Canonico B, Della Felice M, Burattini S, Battistelli M, et al. (2003) Hyperthermia triggers apoptosis and affects cell adhesiveness in human neuroblastoma cells. Histol Histopathol 18: 1041-1052. PubMed: 12973673.
3. Pajonk F, van Ophoven A, McBride WH, (2005) Hyperthermia-induced proteasome inhibition and loss of androgen receptor expression in human prostate cancer cells. Cancer Res 65: 4836-4843. doi:10.1158/0008-5472.CAN-03-2749. PubMed: 15930304.
4. Atmaca A, Al-Batran SE, Neumann A, Kolassa Y, Jäger D, et al. (2009) Whole-body hyperthermia (WBH) in combination with carboplatin in patients with recurrent ovarian cancer- a phase II study. Gynecol Oncol 112: 384-388. doi:10.1016/j.ygyno.2008.11.001. PubMed: 19059635.
5. Fotopoulou C, Cho CH, Kraetschell R, Gellermann J, Wust P, et al. (2010) Regional abdominal hyperthermia combined with systemic chemotherapy for the treatment of patients with ovarian cancer relapse: Results of a pilot study. Int J Hyperthermia 26: 118-126. doi:10.3109/02656730903369200. PubMed: 20146566.
6. Wang Z, Shi Q, Li S, Du J, Liu J, et al. (2010) Hyperthermia induces platelet apoptosis and glycoprotein Ibalpha ectodomain shedding. Platelets 21: 229-237. doi:10.3109/09537100903443949. PubMed: 20158380.
7. Zhao QL, Fujiwara Y, Kondo T, (2006) Mechanism of cell death induction by nitroxide and hyperthermia. Free Radic Biol Med 40: 1131-1143. doi:10.1016/j.freeradbiomed.2005.10.064. PubMed: 16545680.
8. Katschinski DM, Boos K, Schindler SG, Fandrey J, (2000) Pivotal role of reactive oxygen species as intracellular mediators of hyperthermia-induced apoptosis. J Biol Chem 275: 21094-21098. doi:10.1074/jbc.M001629200. PubMed: 10781588.
9. Luo H, Yang A, Schulte BA, Wargovich MJ, Wang GY, (2013) Resveratrol induces premature senescence in lung cancer cells via ROS-mediated DNA damage. PLOS ONE 8: e60065. doi:10.1371/journal.pone.0060065. PubMed: 23533664.
10. Sciancalepore M, Luin E, Parato G, Ren E, Giniatullin R, et al. (2012) Reactive oxygen species contribute to the promotion of the ATP-mediated proliferation of mouse skeletal myoblasts. Free Radic Biol Med 53: 1392-1398. doi:10.1016/j.freeradbiomed.2012.08.002. PubMed: 22917975.
11. Balaban RS, Nemoto S, Finkel T, (2005) Mitochondria, oxidants, and aging. Cell 120: 483-495. doi:10.1016/j.cell.2005.02.001. PubMed: 15734681.
12. Celotto AM, Liu Z, Vandemark AP, Palladino MJ, (2012) A novel Drosophila SOD2 mutant demonstrates a role for mitochondrial ROS in neurodevelopment and disease. Brain Behav 2: 424-434. doi:10.1002/brb3.73. PubMed: 22950046.
13. Zhou M, Xu A, Tam PK, Lam KS, Huang B, et al. (2012) Upregulation of UCP2 by adiponectin: the involvement of mitochondrial superoxide and hnRNP K. PLOS ONE 7: e32349. doi:10.1371/journal.pone.0032349. PubMed: 22359684.
14. Bolisetty S, Jaimes EA, (2013) Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 14: 6306-6344. doi:10.3390/ijms14036306. PubMed: 23528859.
15. Schulz E, Wenzel P, Münzel T, Daiber A, (2012) Mitochondrial redox signaling: interaction of mitochondrial reactive oxygen species with other sources of oxidative stress. Antioxid Redox Signal (. (2012)) [Epub ahead of print] PubMed: 22657349.
16. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, et al. (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287: 27255-27264. doi:10.1074/jbc.M112.374629. PubMed: 22689576.
17. Bryan N, Ahswin H, Smart N, Bayon Y, Wohlert S, et al. (2012) Reactive oxygen species (ROS) -a family of fate deciding molecules pivotal in constructive inflammation and wound healing. Eur Cells Mater 24: 249-265.
18. Klaunig JE, Wang Z, Pu X, Zhou S, (2011) Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol Appl Pharmacol 254: 86-99. doi:10.1016/j.taap.2009.11.028. PubMed: 21296097.
19. Moon EJ, Sonveaux P, Porporato PE, Danhier P, Gallez B, et al. (2010) NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci U S A 107: 20477-20482. doi:10.1073/pnas.1006646107. PubMed: 21059928.
20. Wartenberg M, Gronczynska S, Bekhite MM, Saric T, Niedermeier W, et al. (2005) Regulation of the multidrug resistance transporter P-glycoprotein in multicellular prostate tumor spheroids by hyperthermia and reactive oxygen species. Int J Cancer 113: 229-240. doi:10.1002/ijc.20596. PubMed: 15389514.
21. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, et al. (2010) Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107: 106-116. doi:10.1161/CIRCRESAHA.109.214601. PubMed: 20448215.
22. Lim S, Rashid MA, Jang M, Kim Y, Won H, et al. (2011) Mitochondria-targeted antioxidants protect pancreatic β-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell Physiol Biochem 28: 873-886. doi:10.1159/000335802. PubMed: 22178940.
23. Vela L, Contel M, Palomera L, Azaceta G, Marzo I, (2011) Iminophosphorane-organogold(III) complexes induces cell death through mitochondrial ROS production. J Inorg Biochem 105: 1306-1313. doi:10.1016/j.jinorgbio.2011.06.004. PubMed: 21864808.
24. Loor G, Kondapalli J, Iwase H, Chandel NS, Waypa GB, et al. (2011) Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim Biophys Acta 1813: 1382-1394. doi:10.1016/j.bbamcr.2010.12.008. PubMed: 21185334.
25. Venkataraman S, Wagner BA, Jiang X, Wang HP, Schafer FQ, et al. (2004) Overexpression of manganse superoxide dismutase promotes the survival of prostate cancer cells exposed to hyperthermia. Free Radic Res 38: 1119-1132. doi:10.1080/10715760400010470. PubMed: 15512801.
26. Wang Z, Shi Q, Yan R, Liu G, Zhang W, et al. (2010) The role of calpain in the regulation of ADAM17-dependent GPIbalpha ectodomain shedding. Arch Biochem Biophys 495: 136-143. doi:10.1016/j.abb.2010.01.003. PubMed: 20060803.
27. Ferlini C, Scambia G, (2007) Assay for apoptosis using the mitochondrial probes, Rhodamine 123 and 10-N-nonyl acridine orange. Nat Protoc 2: 3111-3114. doi:10.1038/nprot.2007.397. PubMed: 18079710.
28. Pandey KB, Rizvi SI, (2010) Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxid Med Cell Longev 3: 2-12. doi:10.4161/oxim.3.1.10476. PubMed: 20716923.
29. Wang Z, Li S, Shi Q, Yan R, Liu G, et al. (2010) Calmodulin antagonists induce platelet apoptosis. Thromb Res 125: 340-350. doi:10.1016/j.thromres.2010.02.001. PubMed: 20172594.
30. Zhang W, Zhao L, Liu J, Du J, Wang Z, et al. (2012) Cisplatin induces platelet apoptosis through the ERK signaling pathway. Thromb Res 130: 81-91. doi:10.1016/j.thromres.2012.02.013. PubMed: 22445428.
31. Dai K, Yan R, Li S, Fan Y, Zhuang F, et al. (2009) Prolonged inhibition of protein kinase A results in metalloproteinase-dependent platelet GPIbalpha shedding. Thromb Res 124: 101-109. doi:10.1016/j.thromres.2008.12.044. PubMed: 19181367.
32. Begonja AJ, Gambaryan S, Geiger J, Aktas B, Pozgajova M, et al. (2005) Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbeta3-integrin activation independent of the NO/cGMP pathway. Blood 106: 2757-2760. doi:10.1182/blood-2005-03-1047. PubMed: 15976180.
33. Krötz F, Sohn HY, Pohl U, (2004) Reactive oxygen species: players in the platelet game. Arterioscler Thromb Vasc Biol 24: 1988-1996. doi:10.1161/01.ATV.0000145574.90840.7d. PubMed: 15374851.
34. Kälvegren H, Bylin H, Leanderson P, Richter A, Grenegård M, et al. (2005) Chlamydia pneumoniae induces nitric oxide synthase and lipoxygenase-dependent production of reactive oxygen species in platelets. Effects on oxidation of low density lipoproteins. Thromb Haemost 94: 327-335. PubMed: 16113822.
35. Dröse S, Brandt U, (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 283: 21649-21654. doi:10.1074/jbc.M803236200. PubMed: 18522938.
36. Kanter M, Aktas C, Erboga M, (2013) Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term: an immunohistochemical and ultrastructural study. Toxicol Ind Health 29: 99-113. doi:10.1177/0748233711425082. PubMed: 22082826.
37. Yuki H, Kondo T, Zhao QL, Fujiwara Y, Tanabe K, et al. (2003) A free radical initiator, 2,2'-azobis (2-aminopropane) dihydrochloride enhances hyperthermia-induced apoptosis in human uterine cervical cancer cell lines. Free Radic Res 37: 631-643. doi:10.1080/1071576031000088292. PubMed: 12868490.
38. Petrosillo G, Ruggiero FM, Paradies G, (2003) Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J 17: 2202-2208. doi:10.1096/fj.03-0012com. PubMed: 14656982.
39. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, et al. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1: 223-232. doi:10.1038/nchembio727. PubMed: 16408039.
40. Renault TT, Manon S, (2011) Bax: Addressed to kill. Biochimie 93: 1379-1391. doi:10.1016/j.biochi.2011.05.013. PubMed: 21641962.
41. Willems SH, Tape CJ, Stanley PL, Taylor NA, Mills IG, et al. (2010) Thiol isomerases negatively regulate the cellular shedding activity of ADAM17. Biochem J 428: 439-450. doi:10.1042/BJ20100179. PubMed: 20345372.
42. Marjanovic JA, Stojanovic A, Brovkovych VM, Skidgel RA, Du X, (2008) Signaling-mediated functional activation of inducible nitric-oxide synthase and its role in stimulating platelet activation. J Biol Chem 283: 28827-28834. doi:10.1074/jbc.M801646200. PubMed: 18753139.
43. Lambert AJ, Buckingham JA, Boysen HM, Brand MD, (2008) Diphenyleneiodonium acutely inhibits reactive oxygen species production by mitochondrial complex I during reverse, but not forward electron transport. Biochim Biophys Acta 1777: 397-403. doi:10.1016/j.bbabio.2008.03.005. PubMed: 18395512.
44. Tissier R, Chenoune M, Pons S, Zini R, Darbera L, et al. (2013) Mild hypothermia reduces per-ischemic reactive oxygen species production and preserves mitochondrial respiratory complexes. Resuscitation, 84: 249-255. doi:10.1016/j.resuscitation.2012.06.030. PubMed: 22796545.
45. Brand MD, Nicholls DG, (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312. doi:10.1042/BJ20110162. PubMed: 21726199.
46. Shen GX, (2012) Mitochondrial dysfunction, oxidative stress and diabetic cardiovascular disorders. Cardiovasc Hematol Disord Drug Targets 12: 106-112. doi:10.2174/1871529X11202020106. PubMed: 23030449.
47. Swerdlow RH, (2007) Treating neurodegeneration by modifying mitochondria: potential solutions to a "complex" problem. Antioxid Redox Signal 9: 1591-1603. doi:10.1089/ars.2007.1676. PubMed: 17663643.
48. White MG, Saleh O, Nonner D, Barrett EF, Moraes CT, et al. (2012) Mitochondrial dysfunction induced by heat stress in cultured rat CNS neurons. J Neurophysiol 108: 2203-2214. doi:10.1152/jn.00638.2011. PubMed: 22832569.
49. Stankiewicz AR, Livingstone AM, Mohseni N, Mosser DD, (2009) Regulation of heat-induced apoptosis by Mcl-1 degradation and its inhibition by Hsp70. Cell Death Differ 16: 638-647. doi:10.1038/cdd.2008.189. PubMed: 19148187.
50. Luanpitpong S, Chanvorachote P, Nimmannit U, Leonard SS, Stehlik C, et al. (2012) Mitochondrial superoxide mediates doxorubicin-induced keratinocyte apoptosis through oxidative modification of ERK and Bcl-2 ubiquitination. Biochem Pharmacol 83: 1643-1654. doi:10.1016/j.bcp.2012.03.010. PubMed: 22469513.
51. Luanpitpong S, Chanvorachote P, Stehlik C, Tse W, Callery PS, et al. (2013) Regulation of apoptosis by Bcl-2 cysteine oxidation in human lung epithelial cells. Mol Biol Cell 24: 858-869. doi:10.1091/mbc.E12-10-0747. PubMed: 23363601.
52. Kagan VE, Bayir A, Bayir H, Stoyanovsky D, Borisenko GG, et al. (2009) Mitochondria-targeted disruptors and inhibitors of cytochrome c/cardiolipin peroxidase complexes: a new strategy in anti-apoptotic drug discovery. Mol Nutr Food Res 53: 104-114. doi:10.1002/mnfr.200700402. PubMed: 18979502.
53. Tyurina YY, Tyurin VA, Kaynar AM, Kapralova VI, Wasserloos K, et al. (2010) Oxidative lipidomics of hyperoxic acute lung injury: mass spectrometric characterization of cardiolipin and phosphatidylserine peroxidation. Am J Physiol Lung Cell Mol Physiol 299: L73-L85. doi:10.1152/ajplung.00035.2010. PubMed: 20418384.
54. Zhang S, Ye J, Zhang Y, Xu X, Liu J, et al. (2013) P2Y12 protects platelets from apoptosis via PI3K-dependent Bak/Bax inactivation. J Thromb Haemost 11: 149-160. doi:10.1111/jth.12063. PubMed: 23140172.