Autophagy through 4EBP1 and AMPK regulates oxidative stress-induced premature senescence in auditory cells

Oncotarget

Volumn 6, Issue 6, 2015, Pages 3644-3655

  Tsuchihashi, Nana Akagi ^a,b   Hayashi, Ken ^a,c   Dan, Katsuaki ^a   Goto, Fumiyuki ^a   Nomura, Yasuyuki ^d   Fujioka, Masato ^a   Kanzaki, Sho ^a   Komune, Shizuo ^b   Ogawa, Kaoru ^a  

^a KEIO UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c Kamio Memorial Hospital   (Japan)

^d NIHON UNIVERSITY   (Japan)

Author keywords

AMPK; Auditory cell; Autophagy; Oxidative stress; Premature senescence

Indexed keywords

BETA GALACTOSIDASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 4E BINDING PROTEIN 1; LIPOFUSCIN; CARRIER PROTEIN; EIF4EBP1 PROTEIN, MOUSE; HYDROGEN PEROXIDE; PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; AUDITORY CELL; AUTOLYSOSOME; AUTOPHAGY; CELL AGING; CELL CULTURE; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CORTI ORGAN; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL LINE; COCHLEAR HAIR CELL; CYTOLOGY; DRUG EFFECTS; GENE SILENCING; GENETIC TRANSFECTION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CARRIER PROTEINS; CELL AGING; CELL LINE; GENE KNOCKDOWN TECHNIQUES; HAIR CELLS, AUDITORY; HYDROGEN PEROXIDE; MICE; OXIDATIVE STRESS; PHOSPHOPROTEINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84924248799     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2874     Document Type: Article

References (55)

1. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, Sluis B, Kirkland JL, Deursen JM. Clearance of p16Ink4a-positive cells delays ageing-associated disorders. Nature. 2012; 479:232-236.
2. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961; 25:585-621.
3. Yu G, Bradley JD, Attardi LD, Blackburn EH. In vivo alteration of telomere sequences and senescence caused by mutated Tetrahymena telomerase RNAs. Nature. 1990; 344:126-132.
4. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell. 2007; 130:223-33.
5. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007; 8:729-40.
6. Gates G, Mills JH. Presbycusis. Lancet. 2005; 366:1111-20.
7. Yamasoba T, Someya S, Yamada C, Weindruch R, Prolla TA, Tanokura M. Role of mitochondrial dysfunction and mitochondrial DNA mutations in age-related hearing loss. Hear Res. 2007; 226:185-93.
8. Someya S, Xu J, Kondo K, Ding D, Salvi RJ, Yamasoba T, Rabinovitch PS, Weindruch R, Leeuwenburgh C, Tanokura M, Prolla TA. Age-related hearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis. Proc Natl Acad Sci U S A. 2009; 106:19432-7.
9. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2009; 451:1069-1075.
10. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001; 2:211-61.
11. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature. 2004; 432:1032-6.
12. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, Saito T, Yang Y, Kouno T, Fukutomi T, Hoshii T, Hirao A, Takagi K, et al. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell. 2013; 51:618-31.
13. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback J, Urano F, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 2006; 26:9220-31.
14. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, Wolfe DM, Martinez-Vicente M, Massey AC, Sovak G, Uchiyama Y, Westaway D, Cuervo AM, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell. 2010; 141:1146-58.
15. Taneike M, Yamaguchi O, Nakai A, Hikoso S, Takeda T, Mizote I, Oka T, Tamai T, Oyabu J, Murakawa T, Nishida K, Shimizu T, Hori M, et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy. 2010; 6:600-6.
16. Stranicro S, Cavallini G, Donati A, Pallottini V, Martini C, Trentalance A, Bergamini E. Stimulation of autophagy by antilipolytic drugs may rescue rodents from age-associated hypercholesterolemia. Rejuvenation Res. 2009; 12:77-84.
17. Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 2009; 11:1305-14.
18. Morselli E, Maiuri MC, Markaki M, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis. 2010; 1:e10.
19. Kang HT, Lee KB, Kim SY, Choi HR, Park SC. Autophagy impairment induces premature senescence in primary human fibroblasts. PLoS One. 2011; 6:e23367.
20. Han C, Someya S. Maintaining good hearing: calorie restriction, Sirt3, and glutathione. Exp Gerontol. 2013; 8:1091-5.
21. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C, Tanokura M, Denu JM, Prolla TA. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell. 2010; 43:802-12.
22. Wang W, Yang X, López de Silanes I, Carling D, Gorospe M. Increased AMP:ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J Biol Chem. 2003; 278:27016-23.
23. 2-induced premature senescence in primary human keratinocytes. PLoS One. 2012; 7:e35092.
24. Roach PJ. AMPK → ULK1 → autophagy. Mol Cell Biol. 2011; 31:3082-4.
25. Jung CH, Ro S-H, Cao J, Otto NM, Kim D-H. mTOR regulation of autophagy. FEBS Lett. 2010; 584:1287-95.
26. Kalinec GM, Webster P, Lim DJ, Kalinec F. A cochlear cell line as an in vitro system for drug ototoxicity screening. Audiol Neuro-Otology. 2003; 8:177-89.
27. 2-induced cell death via modulation of p53 and JNK in cultured skin keratinocytes. J Cell Mol Med. 2009; 13:3632-43.
28. Young JJ, Patel A, Rai P. Suppression of thioredoxin-1 induces premature senescence in normal human fibroblasts. B Biochem. Biophys. Res. Commun. 2010; 392:363-8.
29. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol. 2011; 192:547-556.
30. Campisi J, Andersen JK, Kapahi P, Melov S. Cellular senescence: a link between cancer and age-related degenerative disease? Semin Cancer Biol. 2011; 21:354-359.
31. De Cecco M, Jeyapalan J, Zhao X, Tamamori-Adachi M, Sedivy JM. Nuclear protein accumulation in cellular senescence and organismal aging revealed with a novel single-cell resolution fluorescence microscopy assay. Aging (Albany NY). 2011; 3:955-967.
32. Tchkonia T, Zhu Y, van Deursen J, Campisi J, Kirkland JL. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J Clin Invest. 2013; 123:966-72.
33. Chen F-Q, Hill K, Guan Y-J, Schacht J, Sha S-H. Activation of apoptotic pathways in the absence of cell death in an inner-ear immortomouse cell line. Hear Res. 2012; 284:33-41.
34. El Mouedden M, Laurent G, Mingeot-Leclercq MP, Tulkens PM. Gentamicin-induced apoptosis in renal cell lines and embryonic rat fibroblasts. Toxicol Sci. 2000; 56:229-39.
35. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW. Rb-Mediated Heterochromatin Formation and Silencing of E2F Target Genes during Cellular Senescence. Cell. 2003; 113:703-716.
36. Singh K, Matsuyama S, Drazba JA, Almasan A. Autophagy-dependent senescence in response to DNA damage and chronic apoptotic stress. Autophagy. 2012; 8:236-251.
37. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science. 2004; 306:990-995.
38. Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol. 2010; 12:836-41.
39. 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; 26:1749-60.
40. Hands SL, Proud CG, Wyttenbach A. mTOR's role in ageing: protein synthesis or autophagy? Aging (Albany NY). 2009; 1:586-597.
41. Nowotny K, Jung T, Grune T, Höhn A. Accumulation of modified proteins and aggregate formation in aging. Exp Gerontol. 2014; 57C:122-131.
42. Luo Y, Zou P, Zou J, Wang J, Zhou D, Liu L. Autophagy regulates ROS-induced cellular senescence via p21 in a p38 MAPKα dependent manner. Exp Gerontol. 2012; 46:860-867.
43. Pattison JS, Osinska H, Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res. 2011; 109:151-60.
44. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005; 169:425-34.
45. Eskelinen E, Illert A. Role of LAMP-2 in lysosome biogenesis and autophagy. Mol Biol. 2002; 13:3355-3368.
46. Courtois-Cox S, Genther Williams SM, Reczek EE, Johnson BW, McGillicuddy L, Johannessen CM, Hollstein PE, MacCollin M, Cichowski K. A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell. 2006; 10:459-72.
47. Chao SK, Lin J, Brouwer-Visser J, Smith AB, Horwitz SB, McDaid HM. Resistance to discodermolide, a microtubule-stabilizing agent and senescence inducer, is 4E-BP1-dependent. Proc Natl Acad Sci U S A. 2011; 108:391-6.
48. Jia K, Levine B. Autophagy is Required for Dietary Restriction-Mediated Life Span Extension in C. elegans. Autophagy. 2007; 3:6:597-599.
49. Kang HT, Lee KB, Kim SY, Choi HR, Park SC. Autophagy impairment induces premature senescence in primary human fibroblasts. PLoS One. 2011; 6:e23367.
50. Colombo SL, Moncada S. AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J. 2009; 421:163-9.
51. Gauthier M-S, O'Brien EL, Bigornia S, Mott M, Cacicedo JM, Xu XJ, Gokce N, Apovian C, Ruderman N. Decreased AMP-activated protein kinase activity is associated with increased inflammation in visceral adipose tissue and with whole-body insulin resistance in morbidly obese humans. Biochem Biophys Res Commun. 2011; 404:382-7.
52. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem. 2009; 284:28319-31.
53. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007; 6:472-83.
54. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011; 13:132-41.
55. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011; 331:456-61.