Autophagy regulates insulin resistance following endoplasmic reticulum stress in diabetes

Journal of Physiology and Biochemistry

Volumn 71, Issue 2, 2015, Pages 319-327

  Zhang, Ning ^a   Cao, Ming ming ^a   Liu, Han ^a   Xie, Guang ying ^a   Li, Yan bo ^a  

^a THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; Diabetes; Endoplasmic reticulum stress; Hepatic cell; Insulin resistance

Indexed keywords

ANIMAL; AUTOPHAGY; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INSULIN RESISTANCE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CELL SURVIVAL; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HUMANS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS;

EID: 84939984285     PISSN: 11387548     EISSN: 18778755     Source Type: Journal    
DOI: 10.1007/s13105-015-0384-1     Document Type: Review

References (65)

1. Back SH, Kaufman RJ (2012) Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem 81:767–793
2. B’chir W, Maurin AC, Carraro V, Averous J, Jousse C, Muranishi Y, Parry L, Stepien G, Fafournoux P, Bruhat A (2013) The eIF2a/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res 41:7683–7699
3. Bernales S, McDonald KL, Walter P (2006) Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4:e423
4. Bernales S, Schuck S, Walter P (2007) ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3:285–287
5. Chakrabarti A, Chen AW, Varner JD (2011) A review of the mammalian unfolded protein response. Biotechnol Bioeng 108:2777–2793
6. Chen P, Cescon M, Bonaldo P (2014) Autophagy-mediated regulation of macrophages and its applications for cancer. Autophagy 10:192–200
7. Chen ZF, Li YB, Han JY, Wang J, Yin JJ, Li JB, Tian H (2011) The double-edged effect of autophagy in pancreatic beta cells and diabetes. Autophagy 7:12–16
8. Choi SE, Lee SM, Lee YJ, Li LJ, Lee SJ, Lee JH, Kim Y, Jun HS, Lee KW, Kang Y (2009) Protective role of autophagy in palmitate-induced INS-1 beta-cell death. Endocrinology 150:126–134
9. Cnop M, Foufelle F, Velloso LA (2012) Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med 18:59–68
10. Codogno P, Meijer AJ (2010) Autophagy: a potential link between obesity and insulin resistance. Cell Metab 11:449–451
11. Das G, Shravage BV, Baehrecke EH (2012) Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a008813
12. Deegan S, Saveljeva S, Gorman AM, Samali A (2013) Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress. Cell Mol Life Sci 70:2425–2441
13. Ding WX, Ni HM, Gao W, Hou YF, Melan MA, Chen X, Stolz DB, Shao ZM, Yin XM (2007) Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 282:4702–4710
14. Ebato C, Uchida T, Arakawa M, Komatsu M, Ueno T, Komiya K, Azuma K, Hirose T, Tanaka K, Kominami E et al (2008) Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab 8:325–332
15. Flamment M, Hajduch E, Ferré P, Foufelle F (2012) New insights into ER stress-induced insulin resistance. Trends Endocrinol Metab 23:381–390
16. Fouillet A, Levet C, Virgone A, Robin M, Dourlen P, Rieusset J, Belaidi E, Ovize M, Touret M, Nataf S et al (2012) ER stress inhibits neuronal death by promoting autophagy. Autophagy 8:915–926
17. Fujimoto K, Hanson PT, Tran H, Ford EL, Han Z, Johnson JD, Schmidt RE, Green KG, Wice BM, Polonsky KS (2009) Autophagy regulates pancreatic beta cell death in response to Pdx1 deficiency and nutrient deprivation. J Biol Chem 284:27664–27673
18. Fujitani Y, Kawamori R, Watada H (2009) The role of autophagy in pancreatic beta-cell and diabetes. Autophagy 5:280–282
19. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G (2007) Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14:1237–1243
20. Gonzalez CD, Lee MS, Marchetti P, Pietropaolo M, Towns R, Vaccaro MI, Watada H, Wiley JW (2011) The emerging role of autophagy in the pathophysiology of diabetes mellitus. Autophagy 7:2–11
21. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H et al (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885–889
22. He C, Zhu H, Li H, Zou MH, Xie Z (2013) Dissociation of Bcl-2–beclin1 complex by activated AMPK enhances cardiac autophagy and protects against cardiomyocyte apoptosis in diabetes. Diabetes 62:1270–1281
23. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH (2006) Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1α-Mediated NF-κB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26:3071–3084
24. Hwang SL, Li X, Lee JY, Chang HW (2012) Improved insulin sensitivity by rapamycin is associated with reduction of mTOR and S6K1 activities in L6 myotubes. Biochem Biophys Res Commun 418:402–407
25. Jung HS, Chung KW, Won Kim J, Kim J, Komatsu M, Tanaka K, Nguyen YH, Kang TM, Yoon KH, Kim JW et al (2008) Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab 8:318–324
26. Jung HS, Lee MS (2009) Macroautophagy in homeostasis of pancreatic β-cell. Autophagy 5:241–243
27. Kato H, Nakajima S, Saito Y, Takahashi S, Katoh R, Kitamura M (2012) mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1–JNK pathway. Cell Death Differ 19:310–320
28. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141
29. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y et al (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169:425–434
30. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T (2007) ER stress (PERK/eIF2a phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14:230–239
31. Kovsan J, Blüher M, Tarnovscki T, Klöting N, Kirshtein B, Madar L, Shai I, Golan R, Harman-Boehm I, Schön MR et al (2011) Altered autophagy in human adipose tissues in obesity. J Clin Endocrinol Metab 96:E268–E277
32. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ (2007) Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50:752–763
33. Lee J, Ozcan U (2014) unfolded protein response signaling and metabolic diseases. J Biol Chem 289:1203–1211
34. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS (2008) The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 15:1460–1471
35. Liu HY, Han J, Cao SY, Hong T, Zhuo D, Shi J, Liu Z, Cao W (2009) Hepatic autophagy is suppressed in the presence of insulin resistance and hyperinsulinemia. J Biol Chem 284:31484–31492
36. Martino L, Masini M, Novelli M, Beffy P, Bugliani M, Marselli L, Masiello P, Marchetti P, De Tata V (2012) Palmitate activates autophagy in INS-1E β-cells and in isolated rat and human pancreatic Islets. PLoS One 7:e36188
37. Masini M, Bugliani M, Lupi R, del Guerra S, Boggi U, Filipponi F, Marselli L, Masiello P, Marchetti P (2009) Autophagy in human type 2 diabetes pancreatic beta cells. Diabetologia 52:1083–1086
38. Mizushima N (2005) The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ 12:1535–1541
39. Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873
40. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741
41. Mizushima N, Levine B (2010) Autophagy in mammalian development and differentiation. Nat Cell Biol 12:823–830
42. Nuñez CE, Rodrigues VS, Gomes FS, Moura RF, Victorio SC, Bombassaro B, Chaim EA, Pareja JC, Geloneze B, Velloso LA et al (2013) Defective regulation of adipose tissue autophagy in obesity. Int J Obes 37:1473–1480
43. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K et al (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220–9231
44. Ost A, Svensson K, Ruishalme I, Brännmark C, Franck N, Krook H, Sandström P, Kjolhede P, Strålfors P (2010) Attenuated mTOR signaling and enhanced autophagy in adipocytes from obese patients with type 2 diabetes. Mol Med 16:235–246
45. Ota T, Gayet C, Ginsberg HN (2008) Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents. J Clin Invest 118:316–332
46. Ozcan U, Ozcan L, Yilmaz E, Düvel K, Sahin M, Manning BD, Hotamisligil GS (2008) Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol Cell 29:541–551
47. Oz-Levi D, Gelman A, Elazar Z, Lancet D (2013) TECPR2 A new autophagy link for neurodegeneration. Autophagy 9:801–802
48. Park SW, Ozcan U (2013) Potential for therapeutic manipulation of the UPR in disease. Semin Immunopathol 35:351–373
49. Peng G, Li LH, Liu YB, Pu J, Zhang SY, Yu JH, Zhao JJ, Liu PS (2011) Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 152:2206–2218
50. Pereira MJ, Palming J, Rizell M, Aureliano M, Carvalho E, Svensson MK, Eriksson JW (2012) mTOR inhibition with rapamycin causes impaired insulin signaling and glucose uptake in human subcutaneous and omental adipocytes. Mol Cell Endocrinol 355:96–105
51. Qin L, Wang Z, Tao L, Wang Y (2010) ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 6:239–247
52. Qiu W, Su Q, Rutledge AC, Zhang J, Adeli K (2009) Glucosamine-induced endoplasmic reticulum stress attenuates apolipoprotein B100 synthesis via PERK signaling. J Lipid Res 50:1814–1823
53. Rouschop KM, Wouters BG (2009) Regulation of autophagy through multiple independent 337 hypoxic signaling pathways. Curr Mol Med 9:417–424
54. Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Lorente M, Egia A, Vázquez P, Blázquez C, Torres S, García S et al (2009) Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest 119:1359–1372
55. Samuel VT, Shulman GI (2012) Mechanisms for insulin resistance: common threads and missing links. Cell 148:852–871
56. Satoo K, Noda NN, Kumeta H, Fujioka Y, Mizushima N, Ohsumi Y, Inagaki F (2009) The structure of Atg4B–LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J 28:1341–1350
57. Shimoda M, Kanda Y, Hamamoto S, Tawaramoto K, Hashiramoto M, Matsuki M, Kaku K (2011) The human glucagon-like peptide-1 analogue liraglutide preserves pancreatic beta cells via regulation of cell kinetics and suppression of oxidative and endoplasmic reticulum stress in a mouse model of diabetes. Diabetologia 54:1098–1108
58. Shi WY, Xiao D, Wang L, Dong LH, Yan ZX, Shen ZX, Chen SJ, Chen Y, Zhao WL (2012) Therapeutic metformin/AMPK activation blocked lymphoma cell growth via inhibition of mTOR pathway and induction of autophagy. Cell Death Dis 3:e275
59. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664–666
60. Wu YT, Tan HL, Huang Q, Ong CN, Shen HM (2009) Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy. Autophagy 5:824–834
61. Xi H, Kurtoglu M, Liu H, Wangpaichitr M, You M, Liu X, Savaraj N, Lampidis TJ (2011) 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion. Cancer Chemother Pharmacol 67:899–910
62. Xu L, Spinas GA, Niessen M (2010) ER stress in adipocytes inhibits insulin signaling, represses lipolysis, and alters the secretion of adipokines without inhibiting glucose transport. Horm Metab Res 42:643–651
63. Yang L, Li P, Fu S, Calay ES, Hotamisligil GS (2010) Defective hepatic autophagy in obesity promotes er stress and causes insulin resistance. Cell Metab 11:467–478
64. Zhou L, Zhang J, Fang Q, Liu M, Liu X, Jia W, Dong LQ, Liu F (2009) Autophagy-mediated insulin receptor down-regulation contributes to endoplasmic reticulum stress-induced insulin resistance. Mol Pharmacol 76:596–603
65. Zhou Z, Wu S, Li X, Xue Z, Tong J (2010) Rapamycin induces autophagy and exacerbates metabolism associated complications in a mouse model of type 1 diabetes. Indian J Exp Biol 48:31–38