Advanced oxidation protein products induce apoptosis in podocytes through induction of endoplasmic reticulum stress

Journal of Physiology and Biochemistry

Volumn 71, Issue 3, 2015, Pages 455-470

  Rong, Guang ^a   Tang, Xun ^a   Guo, Tingting ^a   Duan, Na ^a   Wang, Yue ^a   Yang, Lei ^a   Zhang, Jun ^a   Liang, Xiujie ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Advanced oxidation protein products (AOPPs); Apoptosis; Endoplasmic reticulum stress; Podocyte; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ADVANCED GLYCATION END PRODUCT RECEPTOR; ADVANCED OXIDATION PROTEIN PRODUCT; CASPASE 12; CCAAT ENHANCER BINDING PROTEIN; CELL PROTEIN; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INOSITOL REQUIRING 1 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN BCL 2; PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; THAPSIGARGIN; UNCLASSIFIED DRUG; AGER PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; MOUSE; NONHUMAN; PODOCYTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN UNFOLDING; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHYSIOLOGY; UNFOLDED PROTEIN RESPONSE;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ADVANCED OXIDATION PROTEIN PRODUCTS; ANIMALS; APOPTOSIS; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; MICE; NADPH OXIDASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PODOCYTES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84939469548     PISSN: 11387548     EISSN: 18778755     Source Type: Journal    
DOI: 10.1007/s13105-015-0424-x     Document Type: Article

References (43)

1. Atabek ME, Keskin M, Yazici C, Kendirci M, Hatipoglu N, Koklu E, Kurtoglu S (2006) Protein oxidation in obesity and insulin resistance. Eur J Pediatr 165:753–756
2. Boussabbeh M, Ben Salem I, Prola A, Guilbert A, Bacha H, Abid-Essefi S, Lemaire C (2015) Patulin induces apoptosis through ROS-mediated endoplasmic reticulum stress pathway. Toxicol Sci 144:328–337
3. Cao Y, Hao Y, Li H, Liu Q, Gao F, Liu W, Duan H (2014) Role of endoplasmic reticulum stress in apoptosis of differentiated mouse podocytes induced by high glucose. Int J Mol Med 33:809–816
4. Chen S, He FF, Wang H, Fang Z, Shao N, Tian XJ, Liu JS, Zhu ZH, Wang YM, Wang S et al (2011) Calcium entry via TRPC6 mediates albumin overload-induced endoplasmic reticulum stress and apoptosis in podocytes. Cell Calcium 50:523–529
5. Chen Y, Liu CP, Xu KF, Mao XD, Lu YB, Fang L, Yang JW, Liu C (2008) Effect of taurine-conjugated ursodeoxycholic acid on endoplasmic reticulum stress and apoptosis induced by advanced glycation end products in cultured mouse podocytes. Am J Nephrol 28:1014–1022
6. Cheng YC, Chen CA, Chang JM, Chen HC (2015) Albumin overload down-regulates integrin-beta1 through reactive oxygen species-endoplasmic reticulum stress pathway in podocytes. J Biochem
7. Cybulsky AV (2010) Endoplasmic reticulum stress in proteinuric kidney disease. Kidney Int 77:187–193
8. Cybulsky AV, Takano T, Papillon J, Kitzler TM, Bijian K (2011) Endoplasmic reticulum stress in glomerular epithelial cell injury. Am J Physiol Ren Physiol 301:F496–F508
9. Dickhout JG, Krepinsky JC (2009) Endoplasmic reticulum stress and renal disease. Antioxid Redox Signal 11:2341–2352
10. Eid AA, Gorin Y, Fagg BM, Maalouf R, Barnes JL, Block K, Abboud HE (2009) Mechanisms of podocyte injury in diabetes: role of cytochrome P450 and NADPH oxidases. Diabetes 58:1201–1211
11. Gorlach A, Klappa P, Kietzmann T (2006) The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 8:1391–1418
12. Hou FF, Miyata T, Boyce J, Yuan Q, Chertow GM, Kay J, Schmidt AM, Owen WF (2001) beta(2)-Microglobulin modified with advanced glycation end products delays monocyte apoptosis. Kidney Int 59:990–1002
13. Inagi R (2010) Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 10:156–165
14. Iwao Y, Nakajou K, Nagai R, Kitamura K, Anraku M, Maruyama T, Otagiri M (2008) CD36 is one of important receptors promoting renal tubular injury by advanced oxidation protein products. Am J Physiol Ren Physiol 295:F1871–F1880
15. Jefferson JA, Shankland SJ, Pichler RH (2008) Proteinuria in diabetic kidney disease: a mechanistic viewpoint. Kidney Int 74:22–36
16. Kalousova M, Skrha J, Zima T (2002) Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus. Physiol Res Acad Sci Bohemoslovaca 51:597–604
17. Kitamura M (2008) Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces. Am J Physiol Ren Physiol 295:F323–F334
18. Li HY, Hou FF, Zhang X, Chen PY, Liu SX, Feng JX, Liu ZQ, Shan YX, Wang GB, Zhou ZM et al (2007) Advanced oxidation protein products accelerate renal fibrosis in a remnant kidney model. J Am Soc Nephrol JASN 18:528–538
19. Liu SX, Hou FF, Guo ZJ, Nagai R, Zhang WR, Liu ZQ, Zhou ZM, Zhou M, Xie D, Wang GB et al (2006) Advanced oxidation protein products accelerate atherosclerosis through promoting oxidative stress and inflammation. Arterioscler Thromb Vasc Biol 26:1156–1162
20. Lu TH, Su CC, Tang FC, Chen CH, Yen CC, Fang KM, Lee KI, Hung DZ, Chen YW (2015) Chloroacetic acid triggers apoptosis in neuronal cells via a reactive oxygen species-induced endoplasmic reticulum stress signaling pathway. Chem Biol Interact 225:1–12
21. Markan S, Kohli HS, Joshi K, Minz RW, Sud K, Ahuja M, Anand S, Khullar M (2009) Up regulation of the GRP-78 and GADD-153 and down regulation of Bcl-2 proteins in primary glomerular diseases: a possible involvement of the ER stress pathway in glomerulonephritis. Mol Cell Biochem 324:131–138
22. Martin-Gallan P, Carrascosa A, Gussinye M, Dominguez C (2003) Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic Biol Med 34:1563–1574
23. Nagai R, Hayashi CM, Xia L, Takeya M, Horiuchi S (2002) Identification in human atherosclerotic lesions of GA-pyridine, a novel structure derived from glycolaldehyde-modified proteins. J Biol Chem 277:48905–48912
24. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW (1997) Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99:342–348
25. Reidy K, Susztak K (2009) Epithelial-mesenchymal transition and podocyte loss in diabetic kidney disease. Am J Kidney Dis Off J Natl Kidney Found 54:590–593
26. Sady C, Jiang CL, Chellan P, Madhun Z, Duve Y, Glomb MA, Nagaraj RH (2000) Maillard reactions by alpha-oxoaldehydes: detection of glyoxal-modified proteins. Biochim Biophys Acta 1481:255–264
27. Santos CX, Tanaka LY, Wosniak J, Laurindo FR (2009) Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 11:2409–2427
28. Susztak K, Raff AC, Schiffer M, Bottinger EP (2006) Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55:225–233
29. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7:880–885
30. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13:184–190
31. Tang X, Rong G, Bu Y, Zhang S, Zhang M, Zhang J, Liang X (2015) Advanced oxidation protein products induce hypertrophy and epithelial-to-mesenchymal transition in human proximal tubular cells through induction of endoplasmic reticulum stress. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 35:816–828
32. Tao JL, Wen YB, Shi BY, Zhang H, Ruan XZ, Li H, Li XM, Dong WJ, Li XW (2012) Endoplasmic reticulum stress is involved in podocyte apoptosis induced by saturated fatty acid palmitate. Chin Med J 125:3137–3142
33. Wei XF, Zhou QG, Hou FF, Liu BY, Liang M (2009) Advanced oxidation protein products induce mesangial cell perturbation through PKC-dependent activation of NADPH oxidase. Am J Physiol Ren Physiol 296:F427–F437
34. Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, Jungers P, Descamps-Latscha B (1996) Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49:1304–1313
35. Witko-Sarsat V, Friedlander M, Nguyen Khoa T, Capeillere-Blandin C, Nguyen AT, Canteloup S, Dayer JM, Jungers P, Drueke T, Descamps-Latscha B (1998) Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. J Immunol (Baltim Md: 1950) 161:2524–2532
36. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656–2664
37. Xue X, Piao JH, Nakajima A, Sakon-Komazawa S, Kojima Y, Mori K, Yagita H, Okumura K, Harding H, Nakano H (2005) Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem 280:33917–33925
38. Zhang J, Qiu M, Ma Y, Bu Y, Yang L, Tang X (2014) Advanced oxidation protein products induce epithelial-to-mesenchymal transition in cultured human proximal tubular epithelial cells via oxidative stress. Nan Fang Yi Ke Da Xue Xue Bao J South Med Univ 34:659–663
39. Zhang J, Guo TT, Yang L, Du QS, Hua J, Liu RZ, Tang X (2012) Effect of arctiin on mouse podocyte epithelial-mesenchymal transition induced by advanced oxidation protein products. Nan Fang Yi Ke Da Xue Xue Bao J South Med Univ 32:379–382
40. Zheng YZ, Cao ZG, Hu X, Shao ZM (2014) The endoplasmic reticulum stress markers GRP78 and CHOP predict disease-free survival and responsiveness to chemotherapy in breast cancer. Breast Cancer Res Treat 145:349–358
41. Zhou LL, Hou FF, Wang GB, Yang F, Xie D, Wang YP, Tian JW (2009) Accumulation of advanced oxidation protein products induces podocyte apoptosis and deletion through NADPH-dependent mechanisms. Kidney Int 76:1148–1160
42. Zhou LL, Cao W, Xie C, Tian J, Zhou Z, Zhou Q, Zhu P, Li A, Liu Y, Miyata T et al (2012) The receptor of advanced glycation end products plays a central role in advanced oxidation protein products-induced podocyte apoptosis. Kidney Int 82:759–770
43. Zhou QG, Zhou M, Lou AJ, Xie D, Hou FF (2010) Advanced oxidation protein products induce inflammatory response and insulin resistance in cultured adipocytes via induction of endoplasmic reticulum stress. Cell Physiol Biochem 26:775–786