Epigallocatechin gallate inhibits oxidative stress-induced DNA damage and apoptosis in MRL-Fas^lpr mice with autoimmune sialadenitis via upregulation of heme oxygenase-1 and Bcl-2

References

• Wheeler, M. L., and A. L. DeFranco. 2012. Prolonged production of reactive oxygen species. J. Immunol. 189: 4405–4416
   PubMed Web of Science ®Google Scholar
• Lam, G. Y., J. Huang, and J. H. Brumell. 2010. The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin. Immunopathol. 32: 415–430
   PubMed Web of Science ®Google Scholar
• Bedard, K., and K.-H. Krause. 2007. The NOX family of ROS-Generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87: 245–313
   PubMed Web of Science ®Google Scholar
• Frey, R. S., M. Ushio-Fukai, and A. B. Malik. 2009. NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid. Redox Signal 11: 791–810
   PubMed Web of Science ®Google Scholar
• Leto, T. L., S. Morand, D. Hurt, et al. 2009. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid. Redox Signal 11: 2607–2619
   PubMed Web of Science ®Google Scholar
• Sumimoto, H. 2008. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275: 3249–3277
   PubMed Web of Science ®Google Scholar
• Holmdahl, R., O. Sareila, A. Pizzolla, et al. 2012. Hydrogen peroxide as an immunological transmitter regulating autoreactive T cells. Antioxid. Redox Signal 18: 1463–1474
   PubMed Web of Science ®Google Scholar
• van der Vliet, A. 2008. NADPH oxidases in lung biology and pathology: host defense enzymes, and more. Free Radic. Biol. Med. 44: 938–955
   PubMed Web of Science ®Google Scholar
• Gaté, L., G. N. Ba, K. D. Tew, et al. 1999. Oxidative stress induced in pathologies: the role of antioxidants. Biomed. Pharmacother. 53: 169–180
   PubMed Web of Science ®Google Scholar
• Kundu, S., P. Ghosh, S. Datta, et al. 2012. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radic. Res. 46: 1482–1489
   PubMed Web of Science ®Google Scholar
• Alves, C. M., C. M. Marzocchi-Machado, and P. Louzada-junior, et al. 2008. Superoxide anion production by neutrophils is associated with prevalent clinical manifestations in systemic lupus erythematosus. Clin. Rheumatol. 27: 701–708
   PubMed Web of Science ®Google Scholar
• Servettaz, A., P. Guilpain, C. Goulvestre, et al. 2007. Radical oxygen species production induced by advanced oxidation protein products predicts clinical evolution and response to treatment in systemic sclerosis. Ann. Rheum. Dis. 66: 1202–1209
   PubMed Web of Science ®Google Scholar
• Fischer, M. T., R. Sharma, J. L. Lim, L. Haider, et al. 2012. NADPH oxidase expression in active multiple sclerosis lesion in relation to oxidative tissue damage and mitochondrial injury. Brain 135: 886–899
   PubMed Web of Science ®Google Scholar
• Padgett, L. E., K. A. Broniowska, P. O. Hansen, et al. 2013. The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann. N. Y. Acad. Sci. 1281: 16–35
   PubMed Web of Science ®Google Scholar
• Burek, C. L., and N. R. Rose. 2008. Autoimmune thyroiditis and ROS. Autoimmun. Rev. 7: 530–537
   PubMed Web of Science ®Google Scholar
• Pagono, G., G. Castello, and F. V. Pallardó. 2013. Sjögren’s syndrome-associated oxidative stress and mitochondrial dysfunction: prospects for chemoprevention trials. Free Radic. Res. 47: 71–73
   PubMed Web of Science ®Google Scholar
• Norheim, K. B., G. Jonsson, E. Harboe, et al. 2012. Oxidative stress, as measured by protein oxidation, is increased in primary Sjögren’s syndrome. Free Radic. Res. 46: 141–146
   PubMed Web of Science ®Google Scholar
• Ryo, K., H. Yamada, Y. Nakagawa, et al. 2006. Possible involvement of oxidative stress in salivary gland of patients with Sjögren’s syndrome. Pathobiology 73: 252–260
   PubMed Web of Science ®Google Scholar
• Zhou, L. L., F. F. Hou, G. B. Wang, et al. 2009. Accumulation of advanced oxidation protein products induces podocyte apoptosis and deletion through NADPH-dependent mechanisms. Kidney Int. 76: 1148–1160
   PubMed Web of Science ®Google Scholar
• Nishihara, M., M. Terada, J. Kamogawa, et al. 1999. Genetic basis of autoimmune sialadenitis in MRL/lpr lupus-prone mice. Arthritis Rheum. 42: 2616–2623
   PubMed Web of Science ®Google Scholar
• Nose, M. 2011. A polygene network model for the complex pathological phenol types of collagen disease. Pathol. Int. 61: 619–629
   PubMed Web of Science ®Google Scholar
• Kobayashi, H., Y. Tanaka, K. Asagiri, et al. 2010. The antioxidant effect of green tea catechin ameliorates experimental liver injury. Phytomedicine 17: 197–202
   PubMed Web of Science ®Google Scholar
• Hisamura, F., A. Kojima-Yuasa, X. Huang, et al. 2008. Synergistic effect of green tea polyphenols on their protection against FK506-induced cytotoxicity in renal cells. Am. J. Chin. Med. 36: 615–624
   PubMed Web of Science ®Google Scholar
• Kawai, Y., Y. Matsui, H. Kondo, et al. 2008. Galloylated catechins as potent inhibitors of hypochlorous acid-induced DNA damage. Chem. Res. Toxicol. 21: 1407–1414
   PubMed Web of Science ®Google Scholar
• Lin, B.-R., C.-Y. Yu, W.-C. Chen, et al. 2009. Green tea extract supplement reduces D-galactosamone-induced acute liver injury by inhibition of apoptotic and proinflammatory siganaling. J. Biomed. Sci. 16: 35. doi:10.1186/1423-0127-16-35
   PubMed Web of Science ®Google Scholar
• Park, H. J., D.-H. Shin, W. J. Chung, et al. 2006. Epigallocatechin gallate reduces hypoxia-induced apoptosis in human hepatoma cells. Life Sci. 78: 2826–2832
   PubMed Web of Science ®Google Scholar
• Jung, J. Y., C. R. Han, Y. J. Jeon, et al. 2007. Epigallocatechin gallate inhibits nitric oxide-induced apoptosis in rat PC12 cells. Neurosci. Lett. 411: 222–227
   PubMed Web of Science ®Google Scholar
• Sheng, R., Z. Gu, M. Xie, et al. 2007. EGCG inhibits cardiomyocyte apoptosis in pressure overload-induced cardiac hypertrophy and protects cardiomyocytes from oxidative stress in rats. Acta Pharmacol. Sin. 28: 191–201
   PubMed Web of Science ®Google Scholar
• Kim, H. R., R. Rajaiah, Q.-L. Wu, et al. 2008. Green tea protects rats against autoimmune arthritis by modulating disease-related immune events. J. Nutr. 138: 2111–2116
   PubMed Web of Science ®Google Scholar
• Haqqi, T. M., D. D. Anthony, S. Gupta, et al. 1999. Prevention of collagen-induced arthritis in mice by a plyphenolic fraction from green tea. Proc. Natl. Acad. Sci. USA. 96: 4524–4529
   PubMed Web of Science ®Google Scholar
• Aktas, O., T. Prozorovski, A. Smorodehenko, et al. 2004. Green tea epigallocatechin-3-gallate mediates T cellular NF-κB inhibition and exerts neuroprotection in autoimmune encephalomyelitis. J. Immunol. 173: 5794–5800
   PubMed Web of Science ®Google Scholar
• Fu, Z., W. Zhen, J. Yuskavage, et al. 2011. Epigallocatechin gallate delays the onset of type 1 diabetes in spontaneous non-obese diabetic mice. Br. J. Nutr. 105: 1218–1225
   PubMed Web of Science ®Google Scholar
• Sayama, K., I. Oguni, A. Tsbura, et al. 2003. Inhibitory effects of autoimmune disease by green tea in MRL-Faslprcg/Faslprcg mice. In Vivo 17: 545–552
   PubMed Web of Science ®Google Scholar
• Ohno, S., H. Yu, D. Dickinson, et al. 2012. Epigallocatechin-3-gallate modulates antioxidant and DNA repair-related proteins in exocrine glands of a primary Sjogren’s syndrome mouse model prior to disease onset. Autoimmunity 45: 540–546
   PubMed Web of Science ®Google Scholar
• Gillespie, K., I. Kodani, D. P. Dickinson, et al. 2008. Effect of oral consumption of green tea polyphenol EGCG in a murine model for human Sjogren’s syndrome, an autoimmune disease. Life Sci. 83: 581–588
   PubMed Web of Science ®Google Scholar
• Hsu, S. D., D. Dickinson, H. Qin, et al. 2007. Green tea polyphenols reduce autoimmune symptoms in murine model for human Sjogren’s syndrome and protect human salivary acinar cells from TNF-α-induced cytotoxicity. Autoimmunity 40: 138–147
   PubMed Web of Science ®Google Scholar
• Wu, C. C., M. C. Hsu, C. W. Hsieh, et al. 2006. Upregulation of heme oxygenase-1 by epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathway. Life Sci. 78: 2889–2897
   PubMed Web of Science ®Google Scholar
• Ryter, S. W., J. Alam, and A. M. K. Choi. 2006. Heme sxygenase-1/Carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86: 583–650
   PubMed Web of Science ®Google Scholar
• Dolinnaya N. G., E. A. Kubareva, E. A. Romanova, et al. 2012. Thymidine glycol: the effect on DNA molecular structure and enzymatic processing. Biochimie 95: 134–147
   PubMed Web of Science ®Google Scholar
• Ito, K., T. Yano, Y. Morodomi, et al. 2012. Serum antioxidant capacity and oxidative injury to pulmonary DNA in never-smokers with primary lung cancer. Anticancer Res. 32: 1063–1068
   PubMed Web of Science ®Google Scholar
• Watanabe, I., M. Toyoda, J. Okuda, et al. 1999. Detection of apoptotic cells in human colorectal cancer by two different in situ methods: antibody against single-stranded DNA and terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick end-labeling (TUNEL) methods. Jpn. J. Cancer Res. 90: 188–193
   PubMedGoogle Scholar
• Frankfurt, O. S., J. A. Robb, E. V. Sugarbaker, et al. 1996. Monoclonal antibody to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. Exp. Cell Res. 226: 387–397
   PubMed Web of Science ®Google Scholar
• Kimura, T., H. Fukui, A. Sekikawa, et al. 2008. Involvement of REG Iα protein in the regeneration of ductal epithelial cells in the minor salivary glands of patients with Sjögren’s syndrome. Clin. Exp. Immunol. 155: 16–20
   PubMed Web of Science ®Google Scholar
• Konstantinidou A. E., N. Givalos, H. Gakiopoulou, et al. 2007. Caspase-3 immunohistochemical expression is a marker of apoptosis, increased grade and early recurreence in intracranial meningiomas. Apoptosis 12: 695–705
   PubMed Web of Science ®Google Scholar
• Shu, K-X., B. Li, and L-X. Wu. 2007. The p53 network: p53 and its downstream genes. Colloid Surf. B-Biointerfaces 55: 10–18
   PubMed Web of Science ®Google Scholar
• Chipuk, J. E., and D. R. Green. 2006. Dissection p53-dependent apoptosis. Cell Death Differ. 13: 994–1002
   PubMed Web of Science ®Google Scholar
• Hoffmann, M. H., S. Trembreau, S. Muller, et al. 2010. Nucleic acid-associated autoantigens: pathogenic involvement and therapeutic potential. J. Autoimmun. 34: J178–J206
   PubMed Web of Science ®Google Scholar
• Bolstad, A. I., H. G. Eiken, B. Rosenlund, et al. 2003. Increased salivary gland tissue expression of Fas, Fas ligand, cytotoxic T lymphocyte- associated antigen 4, and programmed cell death 1 in primary Sjögren’s syndrome. Arthritis Rheum. 48: 174–185
   PubMed Web of Science ®Google Scholar
• Kubo, M., H. Ihn, Y. Asano, et al. 2002. Prevalence of 52-kd and 60-kd Ro/SS-A autoantibodies in Japanese patients with polymyositis/dermatomyositis. J. Am. Acad. Dermatol. 47: 148–151
   PubMed Web of Science ®Google Scholar
• Choubey, D. 2012. Interferon-inducible Ifi200-family genes as modifiers of lupus susceptibility. Immunol. Lett. 147: 10–17
   PubMed Web of Science ®Google Scholar
• Choubey, D., and R. Panchanathan. 2008. Interferon-inducible Ifi200-family genes in systemic lupus erythematosus. Immunol. Lett. 119: 32–41
   PubMed Web of Science ®Google Scholar
• Ichii, O., A. Kamikawa, S. Otsuka, et al. 2010. Overexpression of interferon-activated gene 202 (Ifi202) correlates with the progression of autoimmune glomerulonephritis associated with the MRL chromosome 1. Lupus 19: 897–905
   PubMed Web of Science ®Google Scholar
• Pérez, P., J.-M. Anaya, S. Aguilera, et al. 2009. Gene expression and chromosomal location for susceptibility to Sjögren’s syndrome. J. Autoimmun. 33: 99–108
   PubMed Web of Science ®Google Scholar
• Uchida, K., Y. Akita, K. Matsuo, et al. 2005. Identification of specific autoantigens in Sjögren’s syndrome by SEREX. Immunology 116: 53–63
   PubMed Web of Science ®Google Scholar
• Kotsias, F., E. Hoffmann, S. Amigorena, et al. 2013. Reactive oxygen species production in the phagosome: impact on antigen presentation in dendritic cells. Antioxid. Redox Signal. 18: 714–729
   PubMed Web of Science ®Google Scholar
• Ckless, K., S. R. Hodgkins, J. L. Ather, et al. 2011. Epithelial, dendritic, and CD4+ T cell regulation of and by reactive oxygen and nitrogen species in allergic sensitization. Bioch. Biophys. Acta 1810: 1025–1034
   PubMed Web of Science ®Google Scholar
• Wang, Y., B. Qiao, Y. Wang, et al. 2006. Autoantibodies closely relate to the elevation level of in vivo hydrogen peroxide and tissue damage in systemic lupus erythematosus. DNA Cell Biol. 25: 563–570
   PubMed Web of Science ®Google Scholar
• Saito, K., S. Mori, F. Date, et al. 2013. Sjögren’s syndrome-like autoimmune sialadenitis in MRL-Faslpr mice is associated with expression of glucocorticoid-induced TNF receptor-related protein (GITR) ligand and 4-1BB ligand. Autoimmunity 46: 231–237
   PubMed Web of Science ®Google Scholar
• Tsunawaki, S., S. Nakamura, Y. Ohyama, et al. 2002. Possible function of salivary gland epithelial cells as nonprofessional antigen-presenting cells in the development of Sjögren’s syndrome. J. Rheumatol. 29: 1884–1896
   PubMed Web of Science ®Google Scholar
• Hayashi, Y., N. Haneji, and H. Hamano. 1996. Cytokine gene expression and autoantibody production in Sjögren’s syndrome of/lpr mice. Autoimmunity 23: 269–277
   PubMed Web of Science ®Google Scholar
• Sakamoto, M., M. Miyazaki, S. Mori, et al. 1999. Anti-cytoplasmic autoantibodies reactive with epithelial cells of the salivary gland in sera from patients with Sjögren’s syndrome: their disease- and organ-specificities. J. Oral Pathol. Med. 28: 20–25
   PubMed Web of Science ®Google Scholar
• McArthur, C., Y. Wang, P. Veno, et al. 2002. Intracellular trafficking and surface expression of SS-A (Ro), SS-B (La), poly(ADP-ribose) polymerase and α-fodrin autoantibodies during apoptosis in human salivary gland cells induced by tumour necrosis factor-α. Arch. Oral Biol. 47: 443–448
   PubMed Web of Science ®Google Scholar
• Jimenez. F., S. Aiba-Masago, I. Al Hashimi, et al. 2002. Activated caspase 3 and cleaved poly(ADP-ribose)polymerase in salivary epithelium suggest a pathologenetic mechanism for Sjögren’s syndrome. Rheumatology 41: 338–342
   PubMed Web of Science ®Google Scholar
• Tapinos N. I., M. Polihronis, and H. M. Moutosopoulos. 1999. Lymphoma development in Sjögren’s syndrome. Novel p53 mutations. Arthritis Rheum. 42: 1466–1472
   PubMedGoogle Scholar
• Polihronis, M., N. I. Tapinos, S. E. Theocharis, et al. 1998. Modes of epithelial cell death and repair in Sjögren’s syndrome (SS). Clin. Exp. Immunol. 114: 485–490
   PubMed Web of Science ®Google Scholar
• Fan, S., M. Qi, Y. Yu, et al. 2012. p53 activation plays a crucial role in silibinin induced ROS generation via PUMA and JNK. Free Radic. Res. 46: 310–319
   PubMed Web of Science ®Google Scholar
• Wang, G., H. Li, and F. Khan. 2012. Differential oxidative modification of proteins in MRL+/+ and MRL/lprmice: increased formation of lipid peroxidation-derived aldehyde-protein adducts may contribute to accelerated onset of autoimmune response. Free Radic. Res. 46: 1472–1481
   PubMed Web of Science ®Google Scholar
• Li, H.-L., Y. Huang, C.-N. Zhang, et al. 2006. Epigallocathechin-3 gallate inhibits cardiac hypertrophy through blocking reactive species-dependent and -independent signal pathway. Free Radic. Biol. Med. 40: 1756–1775
   PubMed Web of Science ®Google Scholar
• Kweon, M.-H., V. M. Adhami, J.-S. Lee, et al. 2006. Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J. Biol. Chem. 281: 33761–33772
   PubMed Web of Science ®Google Scholar
• Li, X., M. G. Schwacha, I. H. Chaudry, et al. 2008. Heme oxygenase-1 protects against neutrophil-mediated intestinal damage by down-regulation of neutrophil p47phox and p67phox activity and production in a two-hit model of alcohol introxication and burn injury. J. Immunol. 180: 6933–6940
   PubMed Web of Science ®Google Scholar
• Taillé, C., J. El-Benna, S. Lanone, et al. 2004. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity down-regulating cytochrome b558 expression via the reduction of heme availability. J. Biol. Chem. 279: 28681–28688
   PubMed Web of Science ®Google Scholar
• Orozco-Ibarra, M., A. M. Estrada-Sánchez, L. Massieu, et al. 2009. Heme oxygenase-1 induction prevents neuronal damage triggered during mitochondrial inhibition: role of CO and bilirubin. Int. J. Biochem. Cell Biol. 41: 1304–1314
   PubMed Web of Science ®Google Scholar
• Goodman, A. I., R. Olszanecki, L. M. Yang, et al. 2007. Heme oxygenase-1 protects against radiocontrast-induced acute kidney injury by regulating anti-apoptotic proteins. Kidney Int. 72: 945–953
   PubMed Web of Science ®Google Scholar
• Hsu, S., D. P. Dickinson, H. Qin, et al. 2005. Inhibition of autoantigen expression by (-)-epigallocatechin-3-gallate (the major constituent of green tea) in normal human cells. J. Pharmacol. Exp. Ther. 315: 805–811
   PubMed Web of Science ®Google Scholar
• Nobuhara, Y., S. Kawano, G. Kageyama, et al. 2007. Is SS-A/Ro52 a hydrogen peroxide-sensitive signaling molecule? Antioxid. Redox Signal. 9: 385–391
   PubMed Web of Science ®Google Scholar
• Jauharoh S. N. A., J. Saegusa, T. Sugimoto, et al. 2012. SS-A/Ro52 promotes apoptosis by regulating Bcl-2 production. Biochem. Biophys. Res. Commun. 417: 582–587
   PubMed Web of Science ®Google Scholar
• Casciola-Rosen, L. A., G. Anhalt, A. Rosen, et al. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179: 1317–1330
   PubMed Web of Science ®Google Scholar
• Wen, Y., D.-H. Yan, B. Spohn, et al. 2000. Tumor suppression and sensitization to tumor necrosis factor α-induced apoptosis by an interferon-inducible protein, p202, in breast. Cancer Res. 60: 42–46
   PubMed Web of Science ®Google Scholar
• Henriksson, G., M. Brant, A. Sallmyr, et al. 2002. Enhabced DNA damage-induced p53 peptide phosphorylation and cell-cycle arrest in Sjögren’s syndrome cells. Eur. J. Clin. Invest. 32: 458–465
   PubMed Web of Science ®Google Scholar
• Sisto, M., S. Lisi, D. Castellana, et al. 2006. Autoantibodies from Sjögren’s syndrome induce activation of both the intrinsic and extrinsic apoptotic pathways in human salivary gland cell line A-253. J. Autoimmun. 27: 38–49
   PubMed Web of Science ®Google Scholar