Carbon monoxide activates autophagy via mitochondrial reactive oxygen species formation

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 4, 2011, Pages 867-873

  Lee, Seon Jin ^a   Ryter, Stefan W ^a   Xu, Jin Fu ^a,c   Nakahira, Kiichi ^a   Kim, Hong Pyo ^a,d   Choi, Augustine M K ^a   Kim, Young Sam ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Yonsei University College of Medicine   (South Korea)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d University of Ulsan   (South Korea)

Author keywords

Apoptosis; Autophagy; Carbon monoxide; Epithelial cells; Hyperoxia

Indexed keywords

ACETYLCYSTEINE; AUTOPHAGY PROTEIN 5; CARBON MONOXIDE; MICROTUBULE ASSOCIATED PROTEIN 1; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRONCHUS MUCOSA; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; HYPEROXIA; LIGHT CHAIN; LUNG ALVEOLUS EPITHELIUM; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

ADMINISTRATION, INHALATION; ANIMALS; ANTIOXIDANTS; AUTOPHAGY; CARBON MONOXIDE; CELL LINE, TUMOR; CYTOPROTECTION; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GASES; HUMANS; HYPEROXIA; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

ANIMALIA; VASCONCELLEA CANDICANS;

EID: 80053638297     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0352OC     Document Type: Article

References (44)

1. Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology 2003;187:25-38. (Pubitemid 36385053)
2. Von Burg R. Toxicology update: carbon monoxide. J Appl Toxicol 1999;19:379-386.
3. Stewart RD. The effect of carbon monoxide on humans. Annu Rev Pharmacol 1975;15:409-423.
4. Piantadosi CA. Biological chemistry of carbon monoxide. Antioxid Redox Signal 2002;4:259-270. (Pubitemid 34517177)
5. Ryter S, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays 2004;26:270.
6. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000;6:422-428. (Pubitemid 30208159)
7. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 2003;9:183-190. (Pubitemid 36227720)
8. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999;276:L688-L694. (Pubitemid 29211371)
9. Dolinay T, Szilasi M, Liu M, Choi AM. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury. Am J Respir Crit Care Med 2004;170:613-620. (Pubitemid 39202202)
10. Hoetzel A, Dolinay T, Vallbracht S, Zhang Y, Kim HP, Ifedigbo E, Alber S, Kaynar AM, Schmidt R, Ryter SW, et al. Carbon monoxide protects against ventilator-induced lung injury via PPAR-γ and inhibition of Egr-1. Am J Respir Crit Care Med 2008;177:1223-1232. (Pubitemid 351860931)
11. Hoetzel A, Schmidt R, Vallbracht S, Goebel U, Dolinay T, Kim HP, Ifedigbo E, Ryter SW, Choi AM. Carbon monoxide prevents ventilator-induced lung injury via caveolin-1. Crit Care Med 2009;37:1708-1715.
12. Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, Davis RJ, Choi AM, Lee PJ. Carbon monoxide inhibition of apoptosis during ischemia reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem 2003;278:1248-1258. (Pubitemid 36790808)
13. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
14. Kim HP, Ryter SW, Choi AM. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 2006;46:411-449. (Pubitemid 43271196)
15. Kim HP, Wang X, Nakao A, Kim SI, Murase N, Choi ME, Ryter SW, Choi AM. Caveolin-1 expression by means of p38beta mitogen-activated protein kinase mediates the antiproliferative effect of carbon monoxide. Proc Natl Acad Sci USA 2005;102:11319-11324. (Pubitemid 41153818)
16. Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM, Soares MP. Carbon monoxide generated by heme oxygenase-1 suppresses endothelial cell apoptosis. J Exp Med 2000;192:1015-1026.
17. Zhang X, Shan P, Alam J, Davis RJ, Flavell RA, Lee PJ. Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen-activated protein kinase pathway during ischemia reperfusion lung injury. J Biol Chem 2003;278:22061-22070. (Pubitemid 36792616)
18. Wang X, Wang Y, Kim HP, Nakahira K, Ryter SW, Choi AM. Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J Biol Chem 2007;282:1718-1726. (Pubitemid 47076716)
19. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, et al.; Nomenclature Committee on Cell Death 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009;16:3-11.
20. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010;140:313-326.
21. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010;90:1383-1435.
22. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-1075. (Pubitemid 351317450)
23. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ 2005;12:1542-1552. (Pubitemid 41553991)
24. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 2006;1:23-36.
25. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005;1:84-91.
26. Kim PK, Park SY, Koty PP, Hua Y, Luketich JD, Billiar TR. Fas-associating death domain protein overexpression induces apoptosis in lung cancer cells. J Thorac Cardiovasc Surg 2003;125:1336-1342. (Pubitemid 36759234)
27. Chen ZH, Kim HP, Sciurba FC, Lee SJ, Feghali-Bostwick C, Stolz DB, Dhir R, Landreneau RJ, Schuchert MJ, Yousem SA, et al. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS ONE 2008;3:e3316.
28. Nakahira K, Kim HP, Geng XH, Nakao A, Wang X, Murase N, Drain PF, Wang X, Sasidhar M, Nabel EG, et al. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med 2006;203:2377-2389. (Pubitemid 44498371)
29. Taillé C, El-Benna J, Lanone S, Boczkowski J, Motterlini R. Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J Biol Chem 2005;280:25350-25360. (Pubitemid 40962237)
30. Bilban M, Bach FH, Otterbein SL, Ifedigbo E, d'Avila JC, Esterbauer H, Chin BY, Usheva A, Robson SC, Wagner O, et al. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 2006;24:601-610. (Pubitemid 43728155)
31. Mukhopadhyay P, Rajesh M, Yoshihiro K, Haskó G, Pacher P. Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem Biophys Res Commun 2007;358:203-208. (Pubitemid 46719103)
32. Mukhopadhyay P, Rajesh M, Haskó G, Hawkins BJ, Madesh M, Pacher P. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2007;2:2295-2301. (Pubitemid 351565867)
33. Xu Y, Eissa NT. Autophagy in innate and adaptive immunity. Proc Am Thorac Soc 2010;7:22-28.
34. Zhou B, Boudreau N, Coulber C, Hammarback J, Rabinovitch M. Microtubule-associated protein 1 light chain 3 is a fibronectin mRNA-binding protein linked to mRNA translation in lamb vascular smooth muscle cells. J Clin Invest 1997;100:3070-3082. (Pubitemid 28022845)
35. Ying L, Lau A, Alvira CM, West R, Cann GM, Zhou B, Kinnear C, Jan E, Sarnow P, Van de Rijn M, et al. LC3-mediated fibronectin mRNA translation induces fibrosarcoma growth by increasing connective tissue growth factor. J Cell Sci 2009;122:1441-1451.
36. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007;26:1749-1760. (Pubitemid 46624042)
37. Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010;49:835-842.
38. Jiang J, Stoyanovsky DA, Belikova NA, Tyurina YY, Zhao Q, Tungekar MA, Kapralova V, Huang Z, Mintz AH, Greenberger JS, et al. A mitochondria-targeted triphenylphosphonium-conjugated nitroxide functions as a radioprotector/ mitigator. Radiat Res 2009;172:706-717.
39. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010;107:106-116.
40. Suliman HB, Carraway MS, Tatro LG, Piantadosi CA. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci 2007;120:299-308.
41. Rhodes MA, Carraway MS, Piantadosi CA, Reynolds CM, Cherry AD, Wester TE, Natoli MJ, Massey EW, Moon RE, Suliman HB. Carbon monoxide, skeletal muscle oxidative stress, and mitochondrial biogenesis in humans. Am J Physiol Heart Circ Physiol 2009;297:H392-H399.
42. Mayr FB, Spiel A, Leitner J, Marsik C, Germann P, Ullrich R, Wagner O, Jilma B. Effects of carbon monoxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 2006;171:354-360.
43. Mitchell LA, Channell MM, Royer CM, Ryter SW, Choi AM, McDonald JD. Evaluation of inhaled carbon monoxide as an anti-inflammatory therapy in a non-human primate model of lung inflammation. Am J Physiol Lung Cell Mol Physiol 2010;299:L891-L897.
44. Bathoorn E, Slebos DJ, Postma DS, Koeter GH, van Oosterhout AJ, van der Toorn M, Boezen HM, Kerstjens HA. Anti-inflammatory effects of inhaled carbon monoxide in patients with COPD: a pilot study. Eur Respir J 2007;30:1131-1137. (Pubitemid 351194760)