Epithelial cell mitochondrial dysfunction and PINK1 are induced by transforming growth factor- beta1 in pulmonary fibrosis

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Patel, Avignat S ^a   Song, Jin Woo ^b   Chu, Sarah G ^a   Mizumura, Kenji ^f   Osorio, Juan C ^a   Shi, Ying ^a   El Chemaly, Souheil ^a   Lee, Chun Geun ^c   Rosas, Ivan O ^a,d   Elias, Jack A ^e   Choi, Augustine M K ^f   Morse, Danielle ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Asan Medical Center   (South Korea)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^e BROWN UNIVERSITY   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; PINK1 PROTEIN; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; BLEOMYCIN; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG FIBROSIS; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UPREGULATION; ANIMAL; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYMOLOGY; LUNG ALVEOLUS; METABOLISM; MITOCHONDRION; PATHOLOGY;

MURINAE; MUS;

ANIMALS; BLEOMYCIN; CELL DEATH; CELL LINE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; PROTEIN KINASES; PULMONARY ALVEOLI; PULMONARY FIBROSIS; REACTIVE OXYGEN SPECIES; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84925433501     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121246     Document Type: Article

References (40)

1. Saraste M. Oxidative phosphorylation at the fin de siecle. Science. 1999; 283: 1488-1493. PMID: 10066163
2. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005; 39: 359-407. PMID: 16285865
3. Parsons MJ, Green DR. Mitochondria in cell death. Essays Biochem. 2010; 47: 99-114. doi: 10.1042/bse0470099 PMID: 20533903
4. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 2004; 304: 1158-1160. PMID: 15087508
5. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998; 392: 605-608. PMID: 9560156
6. Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011; 12: 9-14. doi: 10.1038/nrm3028 PMID: 21179058
7. Meissner C, Lorenz H, Weihofen A, Selkoe DJ, Lemberg MK. The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem. 2011; 117: 856-867. doi: 10.1111/j.1471-4159.2011.07253.x PMID: 21426348
8. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010; 8: e1000298. doi: 10.1371/journal.pbio.1000298 PMID: 20126261
9. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, et al. Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep. 2012; 13: 378-385. doi: 10.1038/embor.2012.14 PMID: 22354088
10. Lazarou M, Jin SM, Kane LA, Youle RJ. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell. 2012; 22: 320-333. doi: 10.1016/j.devcel.2011.12.014 PMID: 22280891
11. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008; 183: 795-803. doi: 10.1083/jcb.200809125 PMID: 19029340
12. Osborn-Heaford HL, Ryan AJ, Murthy S, Racila AM, He C, Sieren JC, et al. Mitochondrial Rac1 GTPase import and electron transfer from cytochrome c are required for pulmonary fibrosis. J Biol Chem. 2012; 287: 3301-3312. doi: 10.1074/jbc.M111.308387 PMID: 22157762
13. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, et al. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal. 2011; 15: 607-619. doi: 10.1089/ars.2010.3829 PMID: 21391892
14. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 2008; 320: 674-677. doi: 10.1126/science.1156995 PMID: 18403674
15. Xu JF, Washko GR, Nakahira K, Hatabu H, Patel AS, Fernandez IE, et al. Statins and pulmonary fibrosis: the potential role of NLRP3 inflammasome activation. Am J Respir Crit Care Med. 2012; 185: 547-556. doi: 10.1164/rccm.201108-1574OC PMID: 22246178
16. Jain M, Rivera S, Monclus EA, Synenki L, Zirk A, Eisenbart J, et al. Mitochondrial reactive oxygen species regulate transforming growth factor-beta signaling. J Biol Chem. 2013; 288: 770-777. doi: 10.1074/jbc.M112.431973 PMID: 23204521
17. Pociask DA, Sime PJ, Brody AR. Asbestos-derived reactive oxygen species activate TGF-beta1. Lab Invest. 2004; 84: 1013-1023. PMID: 15122306
18. Liu RM, Gaston Pravia KA. Oxidative stress and glutathione in TGF-beta-mediated fibrogenesis. Free Radic Biol Med. 2010; 48: 1-15. doi: 10.1016/j.freeradbiomed.2009.09.026 PMID: 19800967
19. Yoon YS, Lee JH, Hwang SC, Choi KS, Yoon G. TGF beta1 induces prolonged mitochondrial ROS generation through decreased complex IV activity with senescent arrest in Mv1Lu cells. Oncogene. 2005; 24: 1895-1903. PMID: 15688038
20. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, Martella G, et al. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A. 2007; 104: 11441-11446. PMID: 17563363
21. Patel AS, Lin L, Geyer A, Haspel JA, An CH, Cao J, et al. Autophagy in idiopathic pulmonary fibrosis. PLoS One. 2012; 7: e41394. doi: 10.1371/journal.pone.0041394 PMID: 22815997
22. Cai Q, Zakaria HM, Simone A, Sheng ZH. Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol. 2012; 22: 545-552. doi: 10.1016/j.cub.2012.02.005 PMID: 22342752
23. Chen H, Chan DC. Mitochondrial dynamics - fusion, fission, movement, and mitophagy - in neurodegenerative diseases. Hum Mol Genet. 2009; 18: R169-176. doi: 10.1093/hmg/ddp326 PMID: 19808793
24. Twig G, Shirihai OS. The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal. 2011; 14: 1939-1951. doi: 10.1089/ars.2010.3779 PMID: 21128700
25. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gauiter CA, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol. 2010; 189: 211-221. doi: 10.1083/jcb.200910140 PMID: 20404107
26. Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy. 2012; 8: 1462-1476. doi: 10.4161/auto.21211 PMID: 22889933
27. Thannickal VJ, Horowitz JC. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc. 2012; 3: 350-356.
28. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer. 2003; 3: 807-821. PMID: 14557817
29. Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys. 2007; 462: 245-253. PMID: 17475204
30. Bueno M, Lai YC, Romero Y, Brands J, St Croix CM, Kamga C, et al. PINK1 deficiency impairs mitochondrial homeostasis and promotes lung fibrosis. J Clin Inves. 2015; 125 (2): 521-538. doi: 10.1172/JCI74942 PMID: 25562319
31. Mi S, Li Z, Yang HZ, Liu H, Wang JP, Ma YG, et al. Blocking IL-17A promotes the resolution of pulmonary inflammation and fibrosis via TGF-beta1-dependent and-independent mechanisms. J Immunol. 2011; 187: 3003-3014. doi: 10.4049/jimmunol.1004081 PMID: 21841134
32. Araya J, Kojima J, Takasaka N, Ito S, Fujii S, Hara H, et al. Insufficient autophagy in idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol. 2013; 304: L56-69. doi: 10.1152/ajplung.00213.2012 PMID: 23087019
33. Wood-Kaczmar A, Gandhi S, Yao Z, Abramov AY, Miljan EA, Keen G, et al. PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS One. 2008; 3: e2455. doi: 10.1371/journal.pone.0002455 PMID: 18560593
34. Baloyannis SJ. Mitochondrial alterations in Alzheimer's disease. J Alzheimers Dis. 2006; 9: 119-126. PMID: 16873959
35. Hoshino A, Matoba S, Iwai-Kanai E, Nakamura H, Kimata M, Nakaoka M, et al. p53-TIGAR axis attenuates mitophagy to exacerbate cardiac damage after ischemia. J Mol Cell Cardiol. 2012; 52: 175-184. doi: 10.1016/j.yjmcc.2011.10.008 PMID: 22044588
36. Muqit MM, Abou-Sleiman PM, Saurin AT, Harvey K, Gandhi S, Deas E, et al. Altered cleavage and localization of PINK1 to aggresomes in the presence of proteasomal stress. J Neurochem. 2006; 98: 156-169. PMID: 16805805
37. Baker TA, Bach HHt, Gamelli RL, Love RB, Majetschak M. Proteasomes in lungs from organ donors and patients with end-stage pulmonary diseases. Physiol Res. 2014; 63: 311-319. PMID: 24564596
38. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 2006; 441: 1157-1161. PMID: 16672980
39. Dagda RK, Cherra SJ 3rd, Kulich SM, Tandon A, Park D, Chu CT. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem. 2009; 284: 13843-13855. doi: 10.1074/jbc.M808515200 PMID: 19279012
40. Gispert S, Ricciardi F, Kurz A, Azizov M, Hoepken HH, Becker D, et al. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One. 2009; 4: e5777. doi: 10.1371/journal.pone.0005777 PMID: 19492057