Insulin receptor substrate-1 prevents autophagy-dependent cell death caused by oxidative stress in mouse NIH/3T3 cells

Journal of Biomedical Science

Volumn 19, Issue 1, 2012, Pages

  Chan, Shih Hung ^a,b   Kikkawa, Ushio ^c   Matsuzaki, Hidenori ^c,d   Chen, Jyh Hong ^b   Chang, Wen Chang ^a,e  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^c KOBE UNIVERSITY   (Japan)

^d KAWASAKI MEDICAL SCHOOL   (Japan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Autophagy; Cancer; Cell death; Glucose oxidase; Insulin receptor substrate; Mammalian target of rapamycin; Oxidative stress; p70 ribosomal protein S6 kinase; Reactive oxygen species

Indexed keywords

AUTOPHAGY PROTEIN 5; GLUCOSE OXIDASE; GREEN FLUORESCENT PROTEIN; INSULIN RECEPTOR SUBSTRATE 1; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; INSULIN RECEPTOR SUBSTRATE;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CELL PROLIFERATION; CELL STRAIN 3T3; CELL SURVIVAL; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; CORONARY ARTERY ATHEROSCLEROSIS; MOUSE; NEOPLASM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; AUTOPHAGY; CELL DEATH; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICE; NEOPLASMS; NIH 3T3 CELLS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84863644541     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-19-64     Document Type: Article

References (65)

1. Insulin rapidly stimulates tyrosine phosphorylation of a Mr-185,000 protein in intact cells. White MF, Maron R, Kahn CR, Nature 1985 318 183 186 10.1038/318183a0 2414672
2. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Sun XJ, Rothenberg P, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, White MF, Nature 1991 352 73 77 10.1038/352073a0 1648180
3. Pleiotropic insulin signals are engaged by multisite phosphorylation of IRS-1. Sun XJ, Crimmins DL, Myers MG, Miralpeix M, White MF, Mol Cell Biol 1993 13 7418 7428 7504175
4. Expression and function of the insulin receptor substrate proteins in cancer. Mardilovich K, Pankratz S, Shaw L, Cell Commun Signal 2009 7 14 10.1186/1478-811X-7-14 19534786
5. Increased expression of insulin receptor substrate-1 in human pancreatic cancer. Bergmann U, Funatomi H, Kornmann M, Beger HG, Korc M, Biochem Biophys Res Commun 1996 220 886 890 10.1006/bbrc.1996.0500 8607861
6. Enhanced expression of the insulin receptor substrate-2 docking protein in human pancreatic cancer. Kornmann M, Maruyama H, Bergmann U, Tangvoranuntakul P, Beger HG, White MF, Korc M, Cancer Res 1998 58 4250 4254 9766646
7. Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Hellawell GO, Turner GDH, Davies DR, Poulsom R, Brewster SF, Macaulay VM, Cancer Res 2002 62 2942 2950 12019176
8. Insulin-like growth factor binding protein-3 and insulin receptor substrate-1 in breast cancer: correlation with clinical parameters and disease-free survival. Rocha RL, Hilsenbeck SG, Jackson JG, VanDenBerg CL, Weng CN, Lee AV, Yee D, Clin Cancer Res 1997 3 103 109 9815544
9. Expression of insulin receptor substrate 1 in primary breast cancer and lymph node metastases. Koda M, Sulkowska M, Kanczuga-Koda L, Sulkowski S, J Clin Pathol 2005 58 645 649 10.1136/jcp.2004.022590 15917419
10. Insulin receptor substrate-1 is an important mediator of ovarian cancer cell growth suppression by all-trans retinoic acid. Ravikumar S, Perez-Liz G, Del Vale L, Soprano DR, Soprano KJ, Cancer Res 2007 67 9266 9275 10.1158/0008-5472.CAN-07-2088 17909034
11. Insulin receptor substrate-1 is the predominant signaling molecule activated by insulin-like growth factor-I, insulin, and interleukin-4 in estrogen receptor-positive human breast cancer cells. Jackson JG, White MF, Yee D, J Biol Chem 1998 273 9994 10003 10.1074/jbc.273.16.9994 9545345
12. Free radical biology and medicine: it's a gas, man! Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, Davies KJA, Am J Physiol Regul Integr Comp Physiol 2006 291 491 R511 10.1152/ajpregu.00614.2005 16627692
13. Cellular response to oxidative stress: Signaling for suicide and survival. Martindale JL, Holbrook NJ, J Cell Physiol 2002 192 1 15 10.1002/jcp.10119 12115731
14. Production of large amounts of hydrogen peroxide by human tumor cells. Szatrowski TP, Nathan CF, Cancer Res 1991 51 794 798 1846317
15. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by -phenylethyl isothiocyanate. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, Huang P, Cancer Cell 2006 10 241 252 10.1016/j.ccr.2006.08.009 16959615
16. Reactive oxygen species in cancer cells: Live by the sword, die by the sword. Paul TS, Cancer Cell 2006 10 175 176 10.1016/j.ccr.2006.08.015 16959608
17. Reactive oxygen species: role in the development of cancer and various chronic conditions. Waris G, Ahsan H, J Carcinog 2006 5 14 10.1186/1477-3163-5- 14 16689993
18. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, Zhivotovsky B, Blagosklonny MV, Malorni W, Knight RA, Piacentini M, Nagata S, Melino G, Cell Death Differ 2005 12 1463 1467 16247491
19. Mechanisms of cell death in oxidative stress. Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, Choi AM, Antioxid Redox Signal 2007 9 49 89 10.1089/ars.2007.9.49 17115887
20. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD, Nature 2005 434 658 662 10.1038/nature03434 15800627
21. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y, Nature 2005 434 652 658 10.1038/nature03317 15800626
22. Oxidative stress-induced necrotic cell death via mitochondira-dependent burst of reactive oxygen species. Kyungsun C, Jinho K, Kim GW, Chulhee C, Curr Neurovasc Res 2009 6 213 222 10.2174/156720209789630375 19807658
23. Superoxide is the major reactive oxygen species regulating autophagy. Chen Y, Azad MB, Gibson SB, Cell Death Differ 2009 16 1040 1052 10.1038/cdd.2009.49 19407826
24. Activation of antibacterial autophagy by NADPH oxidases. Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, Magalhaes MAO, Glogauer M, Grinstein S, Brumell JH, Proc Natl Acad Sci USA 2009 106 6226 6231 10.1073/pnas.0811045106 19339495
25. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z, EMBO J 2007 26 1749 1760 10.1038/sj.emboj.7601623 17347651
26. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Lee JS, Giordano S, Zhang JH, Biochem J 2012 441 523 540 10.1042/BJ20111451 22187934
27. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB, Cell Death Differ 2007 15 171 182 17917680
28. Reactive oxygen species stabilize hypoxia-inducible factor-1 alpha protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells. Jung SN, Yang WK, Kim J, Kim HS, Kim EJ, Yun H, Park H, Kim SS, Choe W, Kang I, Ha J, Carcinogenesis 2008 29 713 721 18258605
29. Autophagy and signaling: their role in cell survival and cell death. Codogno P, Meijer AJ, Cell Death Differ 2005 12 1509 1518 16247498
30. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ, Mol Cell 2008 30 214 226 10.1016/j.molcel.2008.03.003 18439900
31. Mammalian autophagy: core molecular machinery and signaling regulation. Yang Z, Klionsky DJ, Curr Opin Cell Biol 2010 22 124 131 10.1016/j.ceb.2009.11. 014 20034776
32. TSC2 mediates cellular energy response to control cell growth and survival. Inoki K, Zhu T, Guan K-L, Cell 2003 115 577 590 10.1016/S0092-8674(03) 00929-2 14651849
33. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Alexander A, Cai S-L, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan K-L, Shen J, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL, Proc Natl Acad Sci USA 2010 107 4153 4158 10.1073/pnas.0913860107 20160076
34. Energy depletion inhibits phosphatidylinositol 3-Kinase/Akt signaling and induces apoptosis via AMP-activated protein kinase-dependent phosphorylation of IRS-1 at Ser-794. Tzatsos A, Tsichlis PN, J Biol Chem 2007 282 18069 18082 10.1074/jbc.M610101200 17459875
35. IRS1 degradation and increased serine phosphorylation cannot predict the degree of metabolic insulin resistance induced by oxidative stress. Potashnik R, Bloch-Damti A, Bashan N, Rudich A, Diabetologia 2003 46 639 648 12750770
36. Sridharan S, Jain K, Basu A, Regulation of autophagy by kinases. Cancers 2011 3 2630 2654
37. Insulin antagonizes ischemia-induced Thr172 phosphorylation of AMP-activated protein kinase -subunits in heart via hierarchical phosphorylation of Ser485/491. Horman S, Vertommen D, Heath R, Neumann D, Mouton V, Woods A, Schlattner U, Wallimann T, Carling D, Hue L, Rider MH, J Biol Chem 2006 281 5335 5340 16340011
38. Preferential mitochondrial DNA injury caused by glucose oxidase as a steady generator of hydrogen peroxide in human fibroblasts. Salazar JJ, Van Houten B, Mut Res 1997 385 139 149 10.1016/S0921-8777(97)00047-5
39. In search of an autophagomometer Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk VI, Kaushik S, Klionsky DJ, Autophagy 2009 5 585 589 10.4161/auto.5.5.8823 19411822
40. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T, EMBO J 2000 19 5720 5728 10.1093/emboj/19.21.5720 11060023
41. How to interpret LC3 immunoblotting. Mizushima N, Yoshimori T, Autophagy 2007 3 542 545 17611390
42. Mizushima N, Yoshimori T, Levine B, Methods in mammalian autophagy research. Cell 2010 140 313 326
43. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Levine B, Klionsky DJ, Dev Cell 2004 6 463 477 10.1016/S1534-5807(04)00099-1 15068787
44. A ubiquitin-like system mediates protein lipidation. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y, Nature 2000 408 488 492 10.1038/35044114 11100732
45. Potential therapeutic applications of autophagy. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ, Nat Rev Drug Discov 2007 6 304 312 10.1038/nrd2272 17396135
46. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC, Nat Genet 2004 36 585 595 10.1038/ng1362 15146184
47. Autophagic cell death: the story of a misnomer. Kroemer G, Levine B, Nat Rev Mol Cell Biol 2008 9 1004 1010 10.1038/nrm2529 18971948
48. TSC-22D1 isoforms have opposing roles in mammary epithelial cell survival. Huser CA, Pringle MA, Heath VJ, Bell AK, Kendrick H, Smalley MJ, Crighton D, Ryan KM, Gusterson BA, Stein T, Cell Death Differ 2009 17 304 315 19745830
49. Methods for detecting autophagy and determining autophagy-induced cell death. Chen Y, Azad MB, Gibson SB, Can J Physiol Pharmacol 2010 88 285 295 10.1139/Y10-010 20393593
50. The end of autophagic cell death? Shen S, Kepp O, Kroemer G, Autophagy 2012 8 1 3 10.4161/auto.8.1.16618 22082964
51. Martin Seamus J: Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Elgendy M, Sheridan C, Brumatti G, Mol Cell 2011 42 23 35 10.1016/j.molcel.2011.02.009 21353614
52. The Pan-Bcl-2 Inhibitor ()-Gossypol triggers autophagic cell death in malignant glioma. Voss V, Senft C, Lang V, Ronellenfitsch MW, Steinbach JP, Seifert V, Kögel D, Mol Cancer Res 2010 8 1002 1016 10.1158/1541-7786.MCR- 09-0562 20587533
53. Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Puissant A, Robert G, Fenouille N, Luciano F, Cassuto J-P, Raynaud S, Auberger P, Cancer Res 2010 70 1042 1052 10.1158/0008-5472.CAN-09-3537 20103647
54. Inhibition of macroautophagy triggers apoptosis. Boya P, González-Polo R-A, Casares N, Perfettini J-L, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G, Mol Cell Biol 2005 25 1025 1040 10.1128/MCB.25.3.1025-1040.2005 15657430
55. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB, Cell 2005 120 237 248 10.1016/j.cell.2004.11.046 15680329
56. Association and dissociation of autophagy, apoptosis and necrosis by systematic chemical study. Shen S, Kepp O, Michaud M, Martins I, Minoux H, Metivier D, Maiuri MC, Kroemer RT, Kroemer G, Oncogene 2011 30 4544 4556 10.1038/onc.2011.168 21577201
57. Insulin receptor substrates (IRS) are critical regulators of autophagy and cardiomyocyte survival [abstract]. Riehle C, Bugger H, Sena S, Pires KM, Theobald HA, Perry-Garza CN, Frank D, Dong X, Moon A, Gottlieb R, White MF, Abel D, Circulation 2009 120 901
58. ERK and cell death: Mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence. Cagnol S, Chambard J-C, FEBS J 2010 277 2 21 10.1111/j.1742-4658.2009.07366.x 19843174
59. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Scott RC, Schuldiner O, Neufeld TP, Dev Cell 2004 7 167 178 10.1016/j.devcel.2004.07.009 15296714
60. Mammalian target of rapamycin and S6 Kinase 1 positively regulate 6-thioguanine-induced autophagy. Zeng X, Kinsella TJ, Cancer Res 2008 68 2384 2390 10.1158/0008-5472.CAN-07-6163 18381446
61. Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Dearth RK, Cui X, Kim H-J, Kuiatse I, Lawrence NA, Zhang X, Divisova J, Britton OL, Mohsin S, Allred DC, Hadsell DL, Lee AV, Mol Cell Biol 2006 26 9302 9314 10.1128/MCB.00260-06 17030631
62. T-antigen of human polyomavirus JC cooperates withIGF-IR signaling system in cerebellar tumors of the childhood-medulloblastomas. Khalili K, Del Valle L, Wang JY, Darbinian N, Lassak A, Safak M, Reiss K, Anticancer Res 2003 23 3A 2035 2041 12894576
63. Association of insulin receptor substrate 1 with simian virus 40 large T antigen. Fei ZL, D'Ambrosio C, Li S, Surmacz E, Baserga R, Mol Cell Biol 1995 15 4232 4239 7542742
64. IRS-4 mediates protein kinase B signaling during insulin stimulation without promoting antiapoptosis. Uchida T, Myers MG, White MF, Mol Cell Biol 2000 20 126 138 10.1128/MCB.20.1.126-138.2000 10594015
65. Overexpression of insulin receptor substrate-1, but not insulin receptor substrate-2, protects a T cell Hybridoma from activation-induced cell death. Li L, Qi X, Williams M, Shi Y, Keegan AD, J Immunol 2002 168 6215 6223 12055235