Apoptotic events induced by high glucose in human hepatoma HepG2 cells involve endoplasmic reticulum stress and MAPK’s activation

Molecular and Cellular Biochemistry

Volumn 399, Issue 1-2, 2015, Pages 113-122

  Jiang, Qiaoling ^a   Yuan, Yujun ^a,c   Zhou, Jiali ^a   Wu, Yan ^a   Zhou, Qing ^a,b   Gui, Shuyu ^b   Wang, Yuan ^a,b  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b Key Lab Genome Res of Anhui Prov   (China)

^c JIUJIANG UNIVERSITY   (China)

Author keywords

Apoptosis; ER stress; HepG2 cells; MAPKs; Oxidative stress

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 3; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P47; SYNAPTOPHYSIN; THIOCTIC ACID;

APOPTOSIS; ARTICLE; CATALYSIS; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; FLOW CYTOMETRY; GLUCOTOXICITY; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; OXIDATIVE STRESS; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; WESTERN BLOTTING; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GLUCOSE; HEP G2 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATIVE STRESS;

EID: 84916925614     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-014-2238-5     Document Type: Article

References (51)

1. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, Lin JK, Farzadfar F, Khang YH, Stevens GA, Rao M, Ali MK, Riley LM, Robinson CA, Ezzati M (2011) Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Blood Glucose) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country- years and 2.7 million participants. Lancet 378(9785):31–40
2. Global status report on noncommunicable diseases (2010) Geneva, World Health Organization
3. Liu BC, Song X, Lu XY, Li DT, Eaton DC, Shen BZ, Li XQ, Ma HP (2013) High glucose induces podocyte apoptosis by stimulating TRPC6 via elevation of reactive oxygen species. Biochim Biophys Acta 1833:1434–1442
4. Lakshmanana AP, Harimaa M, Suzukib K, Soetiknoa V, Nagatac M, Nakamuraa T, Takahashid T, Sonee H, Kawachif H, Watanabea K (2013) The hyperglycemia stimulated myocardial endoplasmic reticulum (ER) stress contributes to diabetic cardiomyopathy in the transgenic non-obese type 2 diabetic rats: a differential role of unfolded protein response (UPR) signaling proteins. Int J Bioche Cell Biol 45:438–447
5. Villarroel M, Garcia-Ramirez M, Corraliza L, Hernandez C, Simo R (2009) Effects of high glucose concentration on the barrier function and the expression of tight junction proteins in human retinal pigment epithelial cells. Exp Eye Res 89:913–920
6. Zhang KZ (2010) Integration of ER stress, oxidative stress and the inflammatory response in health and disease. Int J Clin Exp Med 3(1):33–40
7. Hayden MR, Tyagi SC, Kerklo MM, Nicolls MR (2005) Type 2 diabetes mellitus as a conformational disease. JOP 6:287–302
8. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7:880–885
9. Sari FR, Widyantoro B, Thandavarayan RA, Harima M, Lakshmanan AP, Zhang SS, Muslin AJ, Suzuki K, Kodama M, Watanabe K (2011) Attenuation of CHOP-mediated myocardial apoptosis in pressure-overloaded dominant negative p38α mitogen-activated protein kinase mice. Cell Physiol Biochem 27:487–496
10. Lakshmanan AP, Thandavarayan RA, Palaniyandi SS, Sari FR, Meilei H, Giridharan VV, Soetikno V, Suzuki K, Kodama M, Watanabe K (2011) Modulation of AT-1R/CHOP-JNK-Caspase12 pathway by olmesartan treatment attenuates ER stress-induced renal apoptosis in streptozotocin-induced diabetic mice. Eur J Pharm Sci 44:627–634
11. Liang SH, Zhang W, McGrath BC, Zhang P, Cavener DR (2006) PERK (eIF2alpha kinase) is required to activate the stress-activated MAPKs and induce the expression of immediate-early genes upon disruption of ER calcium homoeostasis. Biochem J 393:201–209
12. Logue SE, Cleary P, Saveljeva S, Samali A (2013) New directions in ER stress-induced cell death. Apoptosis 18(5):537–546
13. Matsukawa J, Matsuzawa A, Takeda K, Ichijo H (2004) The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136:261–265
14. Cargnello M, Roux PP (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75(1):50–83
15. Junttila MR, Li SP, Westermarck J (2008) Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J 22:954–965
16. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2(3):222–228
17. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16:1345–1355
18. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, Noguchi T, Matsuzawa A, Takeda K, Ichijo H (2008) ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22:1451–1464
19. Hetz CA (2007) ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid Redox Signal 9(12):2345–2355
20. Nemcova-Furstova V, Balusikova K, Sramek J, James RF, Kovar J (2013) Caspase-2 and JNK activated by saturated fatty acids are not involved in apoptosis induction but modulate ER stress in human pancreatic β-cells. Cell Physiol Biochem 31(2–3):277–289
21. Gu XM, Li K, Laybutt DR, He ML, Zhao HL, Chan JCN, Xu G (2010) Bip overexpression, but not CHOP inhibition, attenuates fatty-acid-induced endoplasmic reticulum stress and apoptosis in HepG2 liver cells. Life Sci 87:724–732
22. Zhang LL, Lai E, Teodoro T, Volchuk A (2009) GRP78, but not protein-disulfide isomerase, partially reverses hyperglycemia-induced inhibition of insulin synthesis and secretion in pancreatic β-cells. J Biol Chem 284(8):5289–5298
23. Mazumder S, Plesca D, Almasan A (2008) Caspase-3 activation is a critical determinant of genotoxic stress–induced apoptosis. Methods Mol Biol 414:13–21
24. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8(7):519–529
25. Chandrasekaran K, Swaminathan K, Chatterjee S, Dey A (2010) Apoptosis in HepG2 cells exposed to high glucose. Toxicol In Vitro 24(2):387–396
26. Matsuzawa A, Nishitoh H, Tobiume K, Takeda K, Ichijo H (2002) Physiological Roles of ASK1-Mediated Signal Transduction in Oxidative Stress- and Endoplasmic Reticulum Stress-Induced Apoptosis: advanced Findings from ASK1 Knockout Mice. Antioxid Redox Signal 4(3):415–425
27. Nagata Y, Todokoro K (1999) Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood 94(3):853–863
28. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2002) Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23(5):599–622
29. Deursen DV, Jansen H, Verhoeven AJM (2008) Glucose increases hepatic lipase expression in HepG2 liver cells through upregulation of upstream stimulatory factors 1 and 2. Diabetologia 51:2078–2087
30. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, Takashima S, Hirata A, Fujita M, Nagamachi Y, Nakatani T, Yutani C, Ozawa K, Ogawa S, Tomoike H, Hori M, Kitakaze M (2004) Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 110:705–712
31. Zhao LH, Ackerman SL (2006) Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 18(4):444–452
32. Yamagishi N, Ueda T, Mori A, Saito Y, Hatayama T (2012) Decreased expression of endoplasmic reticulum chaperone GRP78 in liver of diabetic mice. Biochem Biophys Res Commun 417:364–370
33. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381–389
34. Zinszner H, Kuroda M, Wang XZ, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995
35. Stankovic MN, Mladenovic D, Ninkovic M, Duricic I, Sobajic S, Jorgacevic B, Luka S, Vukicevic RJ, Radosavljevic TS (2014) The effects of a-lipoic acid on liver oxidative stress and free fatty acid composition in methionine-choline deficient diet-induced NAFLD. J Med Food 17(2):254–261
36. Elshazly SM, El-Moselhy MA, Barakat W (2014) Insights in the mechanism underlying the protective effect of α-lipoic acid against acetaminophen-hepatotoxicity. Eur J Pharmacol 726:116–123
37. Kim MY, Kim EJ, Kim YN, Choi C, Lee BH (2011) Effects of α-lipoic acid and L-carnosine supplementation on antioxidant activities and lipid profiles in rats. Nutr Res Pract 5:421–428
38. Shay KP, Moreau RF, Smith EJ, Smith AR, Hagen TM (2009) Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 1790:1149–1160
39. Hahm JR, Noh HS, Ha JH, Roh GS, Kim DR (2014) Alpha-lipoic acid attenuates adipocyte differentiation and lipid accumulation in 3T3-L1 cells via AMPK-dependent autophagy. Life Sci 100(2):125–132
40. Hinson JA, Pumford NR, Roberts DW (1995) Mechanisms of acetaminophen toxicity: immunochemical detection of drug-protein adducts. Drug Metab Rev 27(1–2):73–92
41. Rochette L, Ghibu S, Richard C, Zeller M, Cottin Y, Vergely C (2013) Direct and indirect antioxidant properties of α-lipoic acid and therapeutic potential. Mol Nutr Food Res 57:114–125
42. Higa A, Chevet E (2012) Redox signaling loops in the unfolded protein response. Cell Signal 24(8):1548–1555
43. Glover-Cutter KM, Lin S, Blackwell TK (2013) Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet 9(9):e1003701. doi:10.1371/journal.pgen.1003701
44. Liu HB, Xiao YL, Xiong CM, Wei AH, Ruan JL (2011) Apoptosis induced by a new flavonoid in human hepatoma HepG2 cells involves reactive oxygen species-mediated mitochondrial dysfunction and MAPK activation. Eur J Pharmacol 654:209–216
45. Pate T, Gores GJ, Kaufmann SH (1996) The role of proteases during apoptosis. FASEB J 10:587–597
46. Rojas-Rivera D, Caballero B, Zamorano S, Lisbona F, Hetz C (2010) Alternative functions of the BCL-2 protein family at the endoplasmic reticulum. Adv Exp Med Biol 687:33–47
47. Ghribi O, DeWitt DA, Forbes MS, Herman MM, Savory J (2001) Co-involvement of mitochondria and endoplasmic reticulum in regulation of apoptosis: changes in cytochrome c, Bcl-2 and Bax in the hippocampus of aluminum-treated rabbits. Brain Res 903(1–2):66–73
48. Korsmeyer SJ, Yin XM, Oltvai ZN, Veis-Novack DJ, Linette GP (1995) Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochim Biophys Acta 1271(1):63–66
49. Roux PP, Blenis J (2004) ERK and p38 MAPK-Activated Protein Kinases: a Family of Protein Kinases with Diverse Biological Functions. Microbiol Mol Biol Rev 68(2):320–344
50. Xia ZG, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270(5240):1326–1331
51. Szydlowska K, Gozdz A, Dabrowski M, Zawadzka M, Kaminska B (2010) Prolonged activation of ERK triggers glutamate-induced apoptosis of astrocytes: neuroprotective effect of FK506. J Neurochem 113(4):904–918