DOI QR코드

DOI QR Code

Padina arborescens extract protects high glucose-induced apoptosis in pancreatic ${\beta}$ cells by reducing oxidative stress

  • Park, Mi Hwa (Department of Food and Nutrition, College of Medical and Life Science, Silla University) ;
  • Han, Ji-Sook (Department of Food Science and Nutrition, Pusan National University)
  • Received : 2013.10.21
  • Accepted : 2014.04.25
  • Published : 2014.10.01

Abstract

BACKGROUND/OBJECTIVES: This study investigated whether Padina arborescens extract (PAE) protects INS-1 pancreatic ${\beta}$ cells against glucotoxicity-induced apoptosis. MATERIALS/METHODS: Assays, including cell viability, lipid peroxidation, generation of intracellular ROS, NO production, antioxidant enzyme activity and insulin secretion, were conducted. The expressions of Bax, Bcl-2, and caspase-3 proteins in INS-1 cells were evaluated by western blot analysis, and apoptosis/necrosis induced by high glucose was determined by analysis of FITC-Annexin V/PI staining. RESULTS: Treatment with high concentrations of glucose induced INS-1 cell death, but PAE at concentrations of 25, 50 or $100{\mu}g/ml$ significantly increased cell viability. The treatment with PAE dose dependently reduced the lipid peroxidation and increased the activities of antioxidant enzymes reduced by 30 mM glucose, while intracellular ROS levels increased under conditions of 30 mM glucose. PAE treatment improved the secretory responsiveness following stimulation with glucose. The results also demonstrated that glucotoxicity-induced apoptosis is associated with modulation of the Bax/Bcl-2 ratio. When INS-1 cells were stained with Annexin V/PI, we found that PAE reduced apoptosis by glucotoxicity. CONCLUSIONS: In conclusion, the present study indicates that PAE protects against high glucose-induced apoptosis in pancreatic ${\beta}$ cells by reducing oxidative stress.

Keywords

References

  1. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 2004;279:42351-4. https://doi.org/10.1074/jbc.R400019200
  2. Zurova-Nedelcevova J, Navarova J, Drabikova K, Jancinova V, Petrikova M, Bernatova I, Kristova V, Snirc V, Nosal'ova V, Sotnikova R. Participation of reactive oxygen species in diabetes-induced endothelial dysfunction. Neuro Endocrinol Lett 2006;27 Suppl 2:168-71.
  3. Mandrup-Poulsen T, Helqvist S, Wogensen LD, Molvig J, Pociot F, Johannesen J, Nerup J. Cytokine and free radicals as effector molecules in the destruction of pancreatic beta cells. Curr Top Microbiol Immunol 1990;164:169-93.
  4. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. ${\beta}$-cell deficit and increased ${\beta}$-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-10. https://doi.org/10.2337/diabetes.52.1.102
  5. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005;54:1615-25. https://doi.org/10.2337/diabetes.54.6.1615
  6. Heo SJ, Park EJ, Lee KW, Jeon YJ. Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol 2005;96:1613-23. https://doi.org/10.1016/j.biortech.2004.07.013
  7. Pal Singh I, Bharate SB. Phloroglucinol compounds of natural origin. Nat Prod Rep 2006;23:558-91. https://doi.org/10.1039/b600518g
  8. Park MH, Han JS. Protective effect of Padina arborescens extract against high glucose-induced oxidative damage in human umbilical vein endothelial cells. Prev Nutr Food Sci 2013;18:11-7. https://doi.org/10.3746/pnf.2013.18.1.011
  9. Park MH, Han JS. Hypoglycemic effect of Padina arborescens extract in streptozotocin-induced diabetic mice. Prev Nutr Food Sci 2012;17:239-44. https://doi.org/10.3746/pnf.2012.17.4.239
  10. Fautz R, Husein B, Hechenberger C. Application of the neutral red assay (NR assay) to monolayer cultures of primary hepatocytes: rapid colorimetric viability determination for the unscheduled DNA synthesis test (UDS). Mutat Res 1991;253:173-9. https://doi.org/10.1016/0165-1161(91)90130-Z
  11. Wang H, Joseph JA. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 1999;27:612-6. https://doi.org/10.1016/S0891-5849(99)00107-0
  12. Fraga CG, Leibovitz BE, Tappel AL. Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic Biol Med 1988;4:155-61. https://doi.org/10.1016/0891-5849(88)90023-8
  13. Nath J, Powledge A. Modulation of human neutrophil inflammatory responses by nitric oxide: studies in unprimed and LPS-primed cells. J Leukoc Biol 1997;62:805-16. https://doi.org/10.1002/jlb.62.6.805
  14. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974;47:469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  15. Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121-6. https://doi.org/10.1016/S0076-6879(84)05016-3
  16. Lawrence RA, Burk RF. Glutathione peroxidase activity in seleniumdeficient rat liver. Biochem Biophys Res Commun 1976;71:952-8. https://doi.org/10.1016/0006-291X(76)90747-6
  17. Green CD, Jump DB, Olson LK. Elevated insulin secretion from liver X receptor-activated pancreatic ${\beta}$-cells involves increased de novo lipid synthesis and triacylglyceride turnover. Endocrinology 2009; 150:2637-45. https://doi.org/10.1210/en.2008-1039
  18. Yamabe N, Kang KS, Goto E, Tanaka T, Yokozawa T. Beneficial effect of Corni Fructus, a constituent of Hachimi-jio-gan, on advanced glycation end-product-mediated renal injury in streptozotocintreated diabetic rats. Biol Pharm Bull 2007;30:520-6. https://doi.org/10.1248/bpb.30.520
  19. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 2008;36:343-7. https://doi.org/10.1042/BST0360343
  20. Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 2004;53 Suppl 1:S119-24. https://doi.org/10.2337/diabetes.53.2007.S119
  21. Tiedge M, Lortz S, Munday R, Lenzen S. Complementary action of antioxidant enzymes in the protection of bioengineered insulinproducing RINm5F cells against the toxicity of reactive oxygen species. Diabetes 1998;47:1578-85. https://doi.org/10.2337/diabetes.47.10.1578
  22. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 2002;23:599-622. https://doi.org/10.1210/er.2001-0039
  23. Del Guerra S, Grupillo M, Masini M, Lupi R, Bugliani M, Torri S, Boggi U, Del Chiaro M, Vistoli F, Mosca F, Del Prato S, Marchetti P. Gliclazide protects human islet beta-cells from apoptosis induced by intermittent high glucose. Diabetes Metab Res Rev 2007;23: 234-8. https://doi.org/10.1002/dmrr.680
  24. Robertson R, Zhou H, Zhang T, Harmon JS. Chronic oxidative stress as a mechanism for glucose toxicity of the beta cell in type 2 diabetes. Cell Biochem Biophys 2007;48:139-46. https://doi.org/10.1007/s12013-007-0026-5
  25. Kong Q, Lin CL. Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell Mol Life Sci 2010;67:1817-29. https://doi.org/10.1007/s00018-010-0277-y
  26. Kappus H. Oxidative stress in chemical toxicity. Arch Toxicol 1987;60:144-9. https://doi.org/10.1007/BF00296968
  27. Du X, Stocklauser-Farber K, Rosen P. Generation of reactive oxygen intermediates, activation of NF-kappaB, and induction of apoptosis in human endothelial cells by glucose: role of nitric oxide synthase? Free Radic Biol Med 1999;27:752-63. https://doi.org/10.1016/S0891-5849(99)00079-9
  28. Messmer UK, Reed UK, Brune B. Bcl-2 protects macrophages from nitric oxide-induced apoptosis. J Biol Chem 1996;271:20192-7. https://doi.org/10.1074/jbc.271.33.20192
  29. McDaniel ML, Kwon G, Hill JR, Marshall CA, Corbett JA. Cytokines and nitric oxide in islet inflammation and diabetes. Proc Soc Exp Biol Med 1996;211:24-32. https://doi.org/10.3181/00379727-211-43950D
  30. Kaneto H, Fujii J, Myint T, Miyazawa N, Islam KN, Kawasaki Y, Suzuki K, Nakamura M, Tatsumi H, Yamasaki Y, Taniguchi N. Reducing sugars trigger oxidative modification and apoptosis in pancreatic beta-cells by provoking oxidative stress through the glycation reaction. Biochem J 1996;320:855-63. https://doi.org/10.1042/bj3200855
  31. Tajiri Y, Grill V. Aminoguanidine exerts a beta-cell functionpreserving effect in high glucose-cultured beta-cells (INS-1). Int J Exp Diabetes Res 2000;1:111-9. https://doi.org/10.1155/EDR.2000.111
  32. Grankvist K, Marklund S, Täljedal IB. Superoxide dismutase is a prophylactic against alloxan diabetes. Nature 1981;294:158-60. https://doi.org/10.1038/294158a0
  33. Benhamou PY, Moriscot C, Richard MJ, Beatrix O, Badet L, Pattou F, Kerr-Conte J, Chroboczek J, Lemarchand P, Halimi S. Adenovirusmediated catalase gene transfer reduces oxidant stress in human, porcine and rat pancreatic islets. Diabetologia 1998;41:1093-100. https://doi.org/10.1007/s001250051035
  34. Krause MS, McClenaghan NH, Flatt PR, de Bittencourt PI, Murphy C, Newsholme P. L-arginine is essential for pancreatic beta-cell functional integrity, metabolism and defense from inflammatory challenge. J Endocrinol 2011;211:87-97. https://doi.org/10.1530/JOE-11-0236
  35. Moriscot C, Pattou F, Kerr-Conte J, Richard MJ, Lemarchand P, Benhamou PY. Contribution of adenoviral-mediated superoxide dismutase gene transfer to the reduction in nitric oxide-induced cytotoxicity on human islets and INS-1 insulin-secreting cells. Diabetologia 2000;43:625-31. https://doi.org/10.1007/s001250051351
  36. Fariss MW, Chan CB, Patel M, Van Houten B, Orrenius S. Role of mitochondria in toxic oxidative stress. Mol Interv 2005;5:94-111. https://doi.org/10.1124/mi.5.2.7
  37. Antonsson B, Martinou JC. The Bcl-2 protein family. Exp Cell Res 2000;256:50-7. https://doi.org/10.1006/excr.2000.4839
  38. Porter AG, Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999;6:99-104. https://doi.org/10.1038/sj.cdd.4400476

Cited by

  1. Aloe-Emodin Protects RIN-5F (Pancreatic β-cell) Cell from Glucotoxicity via Regulation of Pro-Inflammatory Cytokine and Downregulation of Bax and Caspase 3 vol.24, pp.1, 2016, https://doi.org/10.4062/biomolther.2015.056
  2. Morin exerts cytoprotective effects against oxidative stress in C2C12 myoblasts via the upregulation of Nrf2-dependent HO-1 expression and the activation of the ERK pathway vol.39, pp.2, 2016, https://doi.org/10.3892/ijmm.2016.2837
  3. Baicalein induces apoptosis via ROS-dependent activation of caspases in human bladder cancer 5637 cells vol.49, pp.3, 2016, https://doi.org/10.3892/ijo.2016.3606
  4. The Cytoprotective Effect of Petalonia binghamiae Methanol Extract against Oxidative Stress in C2C12 Myoblasts: Mediation by Upregulation of Heme Oxygenase-1 and Nuclear Factor-Erythroid 2 Related Factor 2 vol.13, pp.5, 2015, https://doi.org/10.3390/md13052666
  5. Protective Effect of Siegesbeckia orientalis on Pancreatic β-Cells under High Glucose-Induced Glucotoxicity vol.11, pp.22, 2014, https://doi.org/10.3390/app112210963
  6. Root extracts of Anacardium occidentale reduce hyperglycemia and oxidative stress in vitro vol.7, pp.1, 2014, https://doi.org/10.1186/s40816-021-00293-1