Advanced oxidation protein products induce apoptosis of human chondrocyte through reactive oxygen species-mediated mitochondrial dysfunction and endoplasmic reticulum stress pathways

Fundamental and Clinical Pharmacology

Volumn 31, Issue 1, 2017, Pages 64-74

  Ye, Wenbin ^a   Zhu, Siyuan ^a   Liao, Congrui ^a   Xiao, Jun ^a   Wu, Qian ^a   Lin, Zhen ^a   Chen, Jianting ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

advanced oxidation protein products; apoptosis; endoplasmic reticulum stress; human chondrocyte; mitochondria membrane potential; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ADVANCED OXIDATION PROTEIN PRODUCT; CASPASE; REACTIVE OXYGEN METABOLITE; SERUM ALBUMIN;

ADULT; AGED; APOPTOSIS; ARTICLE; CHONDROCYTE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; CELL CULTURE; CELL CULTURE TECHNIQUE; DRUG EFFECTS; METABOLISM; MIDDLE AGED; MITOCHONDRION; PATHOLOGY; RHEUMATOID ARTHRITIS;

ADVANCED OXIDATION PROTEIN PRODUCTS; AGED; APOPTOSIS; ARTHRITIS, RHEUMATOID; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHONDROCYTES; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SERUM ALBUMIN;

EID: 84982206821     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/fcp.12229     Document Type: Article

References (38)

1. Hitchon C.A., El-Gabalawy H.S. Oxidation in rheumatoid arthritis. Arthritis. Res. Ther. (2004) 6 265–278.
2. Reinheckel T., Nedelev B., Prause J. et al. Occurrence of oxidatively modified proteins: an early event in experimental acute pancreatitis. Free Radic. Biol. Med. (1998) 24 393–400.
3. DeAtley S.M., Aksenov M.Y., Aksenova M.V., Carney J.M., Butterfield D.A. Adriamycin induces protein oxidation in erythrocyte membranes. Pharmacol. Toxicol. (1998) 83 62–68.
4. Witko-Sarsat V., Friedlander M., Capeillere-Blandin C. et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. (1996) 49 1304–1313.
5. Witko-Sarsat V., Friedlander M., Nguyen Khoa T. et al. Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. J. Immunol. (1998) 161 2524–2532.
6. Baskol G., Demir H., Baskol M. et al. Investigation of protein oxidation and lipid peroxidation in patients with rheumatoid arthritis. Cell Biochem. Funct. (2006) 24 307–311.
7. Guo Z.J., Niu H.X., Hou F.F. et al. Advanced oxidation protein products activate vascular endothelial cells via a RAGE-mediated signaling pathway. Antioxid. Redox Signal. (2008) 10 1699–1712.
8. Wu Q., Zhong Z.M., Zhu S.Y. et al. Advanced oxidation protein products induce chondrocyte apoptosis via receptor for advanced glycation end products-mediated, redox-dependent intrinsic apoptosis pathway. Apoptosis (2016) 21 36–50.
9. Sun Y., Zhang T., Li L., Wang J. Induction of apoptosis by hypertension via endoplasmic reticulum stress. Kidney Blood Press. Res. (2015) 40 41–51.
10. Rainbolt T.K., Saunders J.M., Wiseman R.L. Stress-responsive regulation of mitochondria through the ER unfolded protein response. Trends Endocrinol. Metab. (2014) 25 528–537.
11. Urra H., Dufey E., Lisbona F., Rojas-Rivera D., Hetz C. When ER stress reaches a dead end. Biochim. Biophys. Acta (2013) 1833 3507–3517.
12. Rizzuto R., De Stefani D., Raffaello A., Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. (2012) 13 566–578.
13. Uehara Y., Hirose J., Yamabe S. et al. Endoplasmic reticulum stress-induced apoptosis contributes to articular cartilage degeneration via C/EBP homologous protein. Osteoarthritis Cartilage (2014) 22 1007–1017.
14. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. (2007) 9 2277–2293.
15. Adams J.M., Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene (2007) 26 1324–1337.
16. Green D., Kroemer G. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. (1998) 8 267–271.
17. Javadov S., Kuznetsov A. Mitochondrial permeability transition and cell death: the role of cyclophilin d. Front. Physiol. (2013) 4 76.
18. Rasola A., Bernardi P. Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium (2011) 50 222–233.
19. Zamzami N., Larochette N., Kroemer G. Mitochondrial permeability transition in apoptosis and necrosis. Cell Death Differ. (2005) 12(Suppl 2) 1478–1480.
20. Kim J.S., He L., Lemasters J.J. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem. Biophys. Res. Commun. (2003) 304 463–470.
21. Bolisetty S., Jaimes E.A. Mitochondria and reactive oxygen species: physiology and pathophysiology. Int. J. Mol. Sci. (2013) 14 6306–6344.
22. Shiraishi H., Okamoto H., Yoshimura A., Yoshida H. ER stress-induced apoptosis and caspase-12 activation occurs downstream of mitochondrial apoptosis involving Apaf-1. J. Cell Sci. (2006) 119 3958–3966.
23. Alderman C.J., Shah S., Foreman J.C., Chain B.M., Katz D.R. The role of advanced oxidation protein products in regulation of dendritic cell function. Free Radic. Biol. Med. (2002) 32 377–385.
24. Singh R., Ahmed S., Islam N., Goldberg V.M., Haqqi T.M. Epigallocatechin-3-gallate inhibits interleukin-1beta-induced expression of nitric oxide synthase and production of nitric oxide in human chondrocytes: suppression of nuclear factor kappaB activation by degradation of the inhibitor of nuclear factor kappaB. Arthritis Rheum. (2002) 46 2079–2086.
25. Ahmed S., Wang N., Lalonde M., Goldberg V.M., Haqqi T.M. Green tea polyphenol epigallocatechin-3-gallate (EGCG) differentially inhibits interleukin-1 beta-induced expression of matrix metalloproteinase-1 and -13 in human chondrocytes. J. Pharmacol. Exp. Ther. (2004) 308 767–773.
26. Rasheed Z., Anbazhagan A.N., Akhtar N., Ramamurthy S., Voss F.R., Haqqi T.M. Green tea polyphenol epigallocatechin-3-gallate inhibits advanced glycation end product-induced expression of tumor necrosis factor-alpha and matrix metalloproteinase-13 in human chondrocytes. Arthritis. Res. Ther. (2009) 11 R71.
27. Akhtar N., Rasheed Z., Ramamurthy S., Anbazhagan A.N., Voss F.R., Haqqi T.M. MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. Arthritis Rheum. (2010) 62 1361–1371.
28. Cottet-Rousselle C., Ronot X., Leverve X., Mayol J.F. Cytometric assessment of mitochondria using fluorescent probes. Cytometry A (2011) 79 405–425.
29. Ye Y.C., Wang H.J., Yu L., Tashiro S., Onodera S., Ikejima T. RIP1-mediated mitochondrial dysfunction and ROS production contributed to tumor necrosis factor alpha-induced L929 cell necroptosis and autophagy. Int. Immunopharmacol. (2012) 14 674–682.
30. Yu H., Ye W.B., Zhong Z.M., Ding R.T., Chen J.T. Effect of advanced oxidation protein products on articular cartilage and synovium in a rabbit osteoarthritis model. Orthop. Surg. (2015) 7 161–167.
31. Rao R.V., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ. (2004) 11 372–380.
32. Pinton P., Giorgi C., Siviero R., Zecchini E., Rizzuto R. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene (2008) 27 6407–6418.
33. Meyer J.W., Holland J.A., Ziegler L.M., Chang M.M., Beebe G., Schmitt M.E. Identification of a functional leukocyte-type NADPH oxidase in human endothelial cells: a potential atherogenic source of reactive oxygen species. Endothelium (1999) 7 11–22.
34. Gorlach A., Brandes R.P., Nguyen K., Amidi M., Dehghani F., Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ. Res. (2000) 87 26–32.
35. Seno T., Inoue N., Gao D. et al. Involvement of NADH/NADPH oxidase in human platelet ROS production. Thromb. Res. (2001) 103 399–409.
36. Zafarullah M., Li W.Q., Sylvester J., Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cell. Mol. Life Sci. (2003) 60 6–20.
37. Aruoma O.I., Halliwell B., Hoey B.M., Butler J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic. Biol. Med. (1989) 6 593–597.
38. Nakagawa S., Arai Y., Mazda O. et al. N-acetylcysteine prevents nitric oxide-induced chondrocyte apoptosis and cartilage degeneration in an experimental model of osteoarthritis. J. Orthop. Res. (2010) 28 156–163.