Cancer phototherapy via selective photoinactivation of respiratory chain oxidase to trigger a fatal superoxide anion burst

Antioxidants and Redox Signaling

Volumn 20, Issue 5, 2014, Pages 733-746

  Wu, Shengnan ^a   Zhou, Feifan ^a   Wei, Yanchun ^a   Chen, Wei R ^a   Chen, Qun ^a   Xing, Da ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER THERAPY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIGHT ABSORPTION; LOW LEVEL LASER THERAPY; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RED LIGHT; RESPIRATORY CHAIN; TUMOR VOLUME;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; FEMALE; HUMANS; LASER THERAPY, LOW-LEVEL; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOCHONDRIA; NEOPLASM TRANSPLANTATION; SUPEROXIDES;

EID: 84893515484     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5229     Document Type: Article

References (48)

1. Anthony G, Reimann A, and Kadenbach B. Tissue-specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa. Proc Natl Acad Sci USA 90: 1652-1656, 1993. (Pubitemid 23069914)
2. Bini L, Magi B, Marzocchi B, Arcuri F, Tripodi S, Cintorino M, Sanchez JC, Frutiger S, Hughes G, Pallini V, Hochstrasser DF, and Tosi P. Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 18: 2832-2841, 1997. (Pubitemid 28059956)
3. Chen ZX and Pervaiz S. Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ 14: 1617-1627, 2007. (Pubitemid 47278847)
4. Chen ZX and Pervaiz S. Involvement of cytochrome c oxidase subunits Va and Vb in the regulation of cancer cell metabolism by Bcl-2. Cell Death Differ 17: 408-420, 2010.
5. Chu J, Wu S, and Xing D. Survivin mediates self-protection through ROS/cdc25c/CDK1 signaling pathway during tumor cell apoptosis induced by high fluence low-power laser irradiation. Cancer Lett 297: 207-219, 2010.
6. Dawson TL, Gores GJ, Nieminen AL, Herman B, and Lemasters JJ. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol 264: C961-C967, 1993. (Pubitemid 23118118)
7. Eells JT, Wong-Riley MTT, VerHoeve J, Henry M, Buchman EV, Kane MP, Gould LJ, Das R, Jett M, Hodqolis B, Marqolis D, and Whelan HT. Mitochondrial signal transduction in accelerated wound and retinal healing by near-infrared light therapy. Mitochondrion 4: 559-567, 2004. (Pubitemid 39646806)
8. Franco R and Cidlowski JA. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 16: 1303-1314, 2009.
9. Frigo L, Fávero GM, Lima HJ, Maria DA, Bjordal JM, Joensen J, Iversen VV, Marcos RL, Parizzoto NA, and Lopes-Martins RA. Low-level laser irradiation (InGaAlP-660 nm) increases fibroblast cell proliferation and reduces cell death in a dose-dependent manner. Photomed Laser Surg 28: S151-S156, 2010.
10. Gao X and Xing D. Molecular mechanisms of cell proliferation induced by low power laser irradiation. J Biomed Sci 16: 4, 2009.
11. Giovambattista P, Renata C, Barbara B, Salvatore F, Daniela F, Silvia B, and Tommaso G. Mitochondrial superoxide dismutase: a promising target for new anticancer therapies. Curr Med Chem 11: 1299-1308, 2004.
12. Gogvadze V, Orrenius S, and Zhivotovsky B. Mitochondria in cancer cells: what is so special about them? Trends Cell Biol 18: 165-173, 2008.
13. Halliwell B. Oxidative stress and cancer: have we moved forward? Biochem J 401: 1-11, 2007. (Pubitemid 46115897)
14. Hamanaka RB and Chandel NS. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35: 505-513, 2010.
15. Herrmann PC, Gillespie JW, Charboneau L, Bichsel VE, Paweletz CP, Calvert VS, Kohn EC, Emmert-Buck MR, Liotta LA, and Petricoin EF 3rd. Mitochondrial proteome: altered cytochrome c oxidase subunit levels in prostate cancer. Proteomics 3: 1801-1810, 2003. (Pubitemid 37129826)
16. Huang L, Wu S, and Xing D. High fluence low-power laser irradiation induces apoptosis via inactivation of Akt/GSK3b signaling pathway. J Cell Physiol 226: 588-601, 2011.
17. Jia L, Kelsey SM, Grahn MF, Jiang XR, and Newland AC. Increased activity and sensitivity of mitochondrial respiratory enzymes to tumor necrosis factor alpha-mediated inhibition is associated with increased cytotoxicity in drug-resistant leukemic cell lines. Blood 87: 2401-2410, 1996.
18. Karu TI. Primary and secondary mechanisms of action of visible-to-near IR radiation on cells. J Photochem Photobiol B Biol 49: 1-17, 1999.
19. Karu TI. Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62: 607-610, 2010.
20. Karu TI and Kolyakov SF. Exact action spectra for cellular responses relevant to phototherapy. Photomed Laser Surg 23: 355-361, 2005. (Pubitemid 41362243)
21. Karu TI, Pyatibrat L, Kolyakov S, and Afanasyeva N. Absorption measurements of a cell monolayer relevant to phototherapy: reduction of cytochrome c oxidase under near IR radiation. J Photochem Photobiol B Biol 81: 98-106, 2005. (Pubitemid 41574466)
22. Kroemer G, Galluzzi L, and Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163, 2007. (Pubitemid 46209992)
23. Luciakova K and Kuzela S. Increased steady-state levels of several mitochondrial and nuclear gene transcripts in rat hepatoma with a low content of mitochondria. Eur J Biochem 205: 1187-1193, 1992.
24. Marcus RA and Sutin N. Electron transfer in chemistry and biology. Biochem Biophys Acta 811: 265-322, 1985.
25. Murayama H, Sadakane K, Yamanoha B, and Kogure S. Low-power 808-nm laser irradiation inhibits cell proliferation of a human-derived glioblastoma cell line in vitro. Lasers Med Sci 27: 87-93, 2012.
26. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H, and Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 95: 14681-14686, 1998. (Pubitemid 29003690)
27. Orrenius S, Gogvadze V, and Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47: 143-183, 2007.
28. Pastore D, Greco M, and Passarella S. Specific helium-neon laser sensitivity of the purified cytochrome c oxidase. Int J Rad Biol 76: 863-870, 2000. (Pubitemid 30352770)
29. Penta JS, Johnson FM, Wachsmanb JT, and Copeland WC. Mitochondrial DNA in human malignancy. Mutat Res 488: 119-133, 2001. (Pubitemid 32436427)
30. Regan JJ, Ramirez BE, Winkler JR, Gray HB, and Malmstrom BG. Pathways for electron tunneling in cytochrome c oxidase. J Bioenerg Biomembr 30: 35-39, 1998. (Pubitemid 28262405)
31. Schroeder P, Pohl C, Marks C, Calles C, Wild S, and Krutmann J. Cellular response to infrared radiation involves retrograde mitochondrial signaling. Free Radic Biol Med 43: 128-135, 2007. (Pubitemid 46874843)
32. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, and Korsmeyer SJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67, 2002. (Pubitemid 34065906)
33. Tata DB and Waynant RW. Laser therapy: a review of its mechanism of action and potential medical applications. Laser Photonics Rev 5: 1-12, 2011.
34. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344, 2003. (Pubitemid 37321833)
35. Wang F, Chen T, Xing D, Wang J, and Wu Y. Measuring dynamics of caspase-3 activity in living cells using FRET technique during apoptosis induced by high fluence lowpower laser irradiation. Lasers Surg Med 36: 2-7, 2005. (Pubitemid 40224024)
36. Weishaupt A and Kadenbach B. Selective removal of subunit VIb increases the activity of cytochrome c oxidase. Biochemistry 31: 11477-11481, 1992.
37. Whitaker-Menezes D, Martinez-Outschoorn UE, Flomenberg N, Birbe RC, Witkiewicz AK, Howell A, Pavlides S, Tsirigos A, Ertel A, Pestell RG, Broda P, Minetti C, Lisanti MP, and Sotgia F. Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ. Cell Cycle 10: 4047-4064, 2011.
38. Wu H, Rao GN, Dai B, and Singh P. Autocrine gastrins in colon cancer cells up-regulate cytochrome c oxidase Vb and down-regulate efflux of cytochrome c and activation of caspase-3. J Biol Chem 275: 32491-32498, 2000.
39. Wu S and Xing D. Intracellular signaling cascades following light irradiation. Laser Photonics Rev [Epub ahead of print]; DOI: 10.1002/lpor.201300015.
40. Wu S, Xing D, Gao X, and Chen WR. High fluence lowpower laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species. J Cell Physiol 218: 603-611, 2008.
41. Wu S, Xing D, Wang F, and Chen WR. Mechanistic study of apoptosis induced by high fluence low-power laser irradiation using fluorescence imaging techniques. J Biomed Opt 2: 064015, 2007.
42. Wu S, Zhou F, Zhang Z, and Xing D. Bax is essential for Drp1-mediated mitochondrial fission but not for mitochondrial outer membrane permeabilization caused by photodynamic therapy. J Cell Physiol 226: 530-541, 2011.
43. Wu S, Zhou F, Zhang Z, and Xing D. Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission/fusion protein. FEBS J 278: 941-954, 2011.
44. Xing D and Wu S. Chapter 47. LLLT signaling pathways. In: Handbook of Photomedicine, edited by Hamblin MR and Huang Y. London, United Kingdom: Taylor & Francis, 2013, pp. 535-556.
45. Yoshikawa S. X-ray structure and reaction mechanism of bovine heart cytochrome c oxidase. Biochem Soc T 27: 351-362, 1999.
46. Zhang J, Xing D, and Gao X. Low-power laser irradiation activates Src tyrosine kinase through reactive oxygen species-mediated signaling pathway. J Cell Physiol 217: 518-528, 2008.
47. Zhao H, Xing D, and Chen Q. New insights of mitochondria reactive oxygen species generation and cell apoptosis induced by low dose photodynamic therapy. Eur J Cancer 47: 2750-2761, 2011.
48. Zhou F, Xing D, and Chen WR. Regulation of HSP70 on activating macrophages using PDT-induced apoptotic cells. Cancer Lett 264: 135-144, 2008.