Advertisement

Cell Stress and Chaperones

, Volume 23, Issue 4, pp 773–781 | Cite as

Antioxidant effect of myricitrin on hyperglycemia-induced oxidative stress in C2C12 cell

  • Akram Ahangarpour
  • Ali Akbar Oroojan
  • Layasadat Khorsandi
  • Maryam Kouchak
  • Mohammad Badavi
Original Paper

Abstract

Hyperglycemia induced oxidative stress inside the cells. Myricitrin, as an antioxidant plant-derived component, may be useful in hyperglycemia. Hence, the aim of this study was conducted to evaluate the antioxidant effects of myricitrin on hyperglycemia-induced oxidative damage in myotubes (C2C12 cells). In this experimental study, mouse myoblast cell line (C2C12) was obtained and divided into five groups: control, hyperglycemia, hyperglycemia + myricitrin 1, 3, and 10 μM. After treatment period for 48 h, cells were collected, homogenized, and centrifuged at 2000 rpm for 10 min. All samples were kept at − 80 °C until experimental and real-time PCR assessments were performed. Hyperglycemia increased malondialdehyde (MDA) (p < 0.05), total antioxidant capacity (TAC) (p < 0.001), and cellular apoptosis, and decreased levels of superoxide dismutase (SOD), catalase (CAT) (p < 0.01), myotube glycogen content (p < 0.05), glucose transporter type 4 (Glut-4), and cellular viability (p < 0.001). Myricitrin administration improved SOD (p < 0.05), CAT (p < 0.01), muscle cell’s glycogen content (p < 0.01), Glut-4 gene expression (p < 0.001), Thiazolyl blue tetrazolium bromide (MTT) (p < 0.05), and Bax to Bcl-2 ratio (p < 0.001), and reduced MDA (p < 0.05) compared to hyperglycemia group. In conclusion, hyperglycemic condition induced oxidative stress along with cellular apoptosis, and myricitrin improved these disorders. Also, low and moderate doses of myricitrin are more efficient on skeletal muscle cells exposed to hyperglycemic statues than a high concentration of this antioxidant agent.

Keywords

Myricitrin Hyperglycemia Oxidative stress Apoptosis C2C12 cell line 

Notes

Acknowledgements

This study is a part of the Ph.D. thesis of Ali Akbar Oroojan was labeled Cell & Molecular Research Center project (CMRC-9509) and was supported financially by the vice-chancellor of research affairs of Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.

Compliance with ethical standards

This research has been done in accordance with the principles and guidelines of Ahvaz Jundishapur University of Medical Sciences ethics committee with No. IR.AJUMS.REC.1395.136.

Conflicts of interest

The authors declare that they have no conflict of interest.

References

  1. Akan Z, Garip AI (2013) Antioxidants may protect cancer cells from apoptosis signals and enhance cell viability. Asian Pac J Cancer Prev 14(8):4611–4614CrossRefPubMedGoogle Scholar
  2. Aloud AA, Veeramani C, Govindasamy C, Alsaif MA, El Newehy AS, Al-Numair KS (2017) Galangin, a dietary flavonoid, improves antioxidant status and reduces hyperglycemia-mediated oxidative stress in streptozotocin-induced diabetic rats. Redox Rep 22(6):290–300CrossRefPubMedGoogle Scholar
  3. Annadurai T, Muralidharan AR, Joseph T, Hsu MJ, Thomas PA, Geraldine P (2012) Antihyperglycemic and antioxidant effects of a flavanone, naringenin, in streptozotocin-nicotinamide-induced experimental diabetic rats. J Physiol Biochem 68(3):307–318CrossRefPubMedGoogle Scholar
  4. Botha CJ, Clift SJ, Ferreira GCH, Masango MG (2017) Geigerin-induced cytotoxicity in a murine myoblast cell line (C2C12). Onderstepoort J Vet Res 84(1):e1–e7CrossRefPubMedGoogle Scholar
  5. Dimauro I, Pearson T, Caporossi D, Jackson MJ (2012) A simple protocol for the subcellular fractionation of skeletal muscle cells and tissue. BMC Research Notes 5:513–513CrossRefPubMedPubMedCentralGoogle Scholar
  6. Elkalaf M, Anděl M, Trnka J (2013) Low glucose but not galactose enhances oxidative mitochondrial metabolism in C2C12 myoblasts and myotubes. PLoS One 8(8):e70772CrossRefPubMedPubMedCentralGoogle Scholar
  7. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2003) Are oxidative stress- activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes 52(1):1–8CrossRefPubMedGoogle Scholar
  8. Fiorentino TV, Prioletta A, Zuo P, Folli F (2013) Hyperglycemia-induced oxidative stress and its role in diabetes mellitus related cardiovascular diseases. Curr Pharm Des 19(32):5695–5703CrossRefPubMedGoogle Scholar
  9. Gomez Perez M, Fourcade L, Mateescu MA, Paquin J (2017) Neutral Red versus MTT assay of cell viability in the presence of copper compounds. Anal Biochem 535(Supplement C):43–46CrossRefPubMedGoogle Scholar
  10. Gupta R, Mathur M, Bajaj VK, Katariya P, Yadav S, Kamal R, Gupta RS (2012) Evaluation of antidiabetic and antioxidant activity of Moringa oleifera in experimental diabetes. J Diabetes 4(2):164–171CrossRefPubMedGoogle Scholar
  11. Hasnan J, Yusoff M, Damitri T, Faridah A, Adenan A, Norbaini T (2010) Relationship between apoptotic markers (Bax and Bcl-2) and biochemical markers in type 2 diabetes mellitus. Singap Med J 51(1):50–55Google Scholar
  12. Hosseinzadeh R, Khorsandi K (2017) Methylene blue, curcumin and ion pairing nanoparticles effects on photodynamic therapy of MDA-MB-231 breast cancer cell. Photodiagn Photodyn Ther 18(Supplement C):284–294CrossRefGoogle Scholar
  13. Huang Q, Gao B, Wang L, Hu YQ, Lu WG, Yang L, Luo ZJ, Liu J (2014) Protective effects of myricitrin against osteoporosis via reducing reactive oxygen species and bone-resorbing cytokines. Toxicol Appl Pharmacol 280(3):550–560CrossRefPubMedGoogle Scholar
  14. Jain SK, McVie R, Bocchini JA (2006) Hyperketonemia (ketosis), oxidative stress and type 1 diabetes. Pathophysiology 13(3):163–170CrossRefPubMedGoogle Scholar
  15. Kabra DG, Gupta J, Tikoo K (2009) Insulin induced alteration in post-translational modifications of histone H3 under a hyperglycemic condition in L6 skeletal muscle myoblasts. Biochim Biophys Acta (BBA) - Mol Basis Dis 1792(6):574–583CrossRefGoogle Scholar
  16. Kang J, Boonanantanasarn K, Baek K, Woo KM, Ryoo H-M, Baek J-H, Kim G-S (2015) Hyperglycemia increases the expression levels of sclerostin in a reactive oxygen species- and tumor necrosis factor-alpha-dependent manner. J Periodontal Implant Sci 45(3):101–110CrossRefPubMedPubMedCentralGoogle Scholar
  17. Karbach S, Jansen T, Horke S, Heeren T, Scholz A, Coldewey M, Karpi A, Hausding M, Kröller-Schön S, Oelze M, Münzel T, Daiber A (2012) Hyperglycemia and oxidative stress in cultured endothelial cells—a comparison of primary endothelial cells with an immortalized endothelial cell line. J Diabetes Complicat 26(3):155–162CrossRefPubMedGoogle Scholar
  18. Kato M, Suwa A, Shimokawa T (2004) Glucose catabolic gene mRNA levels in skeletal muscle exhibit non-coordinate expression in hyperglycemic mice. Horm Metab Res 36(08):513–518CrossRefPubMedGoogle Scholar
  19. Kay CD, Hooper L, Kroon PA, Rimm EB, Cassidy A (2012) Relative impact of flavonoid composition, dose and structure on vascular function: a systematic review of randomised controlled trials of flavonoid-rich food products. Mol Nutr Food Res 56(11):1605–1616CrossRefPubMedGoogle Scholar
  20. Kim YB, Peroni OD, Aschenbach WG, Minokoshi Y, Kotani K, Zisman A, Kahn CR, Goodyear LJ, Kahn BB (2005) Muscle-specific deletion of the Glut4 glucose transporter alters multiple regulatory steps in glycogen metabolism. Mol Cell Biol 25(21):9713–9723CrossRefPubMedPubMedCentralGoogle Scholar
  21. Li W, Hu Z-F, Chen B, Ni G-X (2013) Response of C2C12 myoblasts to hypoxia: the relative roles of glucose and oxygen in adaptive cellular metabolism. Biomed Res Int 2013:326346PubMedPubMedCentralGoogle Scholar
  22. Lorente L, María MM, Pérez-Cejas A, Abreu-González P, Ramos L, Argueso M, Cáceres JJ, Solé-Violán J, Jiménez A (2016) Association between total antioxidant capacity and mortality in ischemic stroke patients. Ann Intensive Care 6:39CrossRefPubMedPubMedCentralGoogle Scholar
  23. Magistrelli P, Coppola R, Tonini G, Vincenzi B, Santini D, Borzomati D, Vecchio F, Valeri S, Castri F, Antinori A (2006) Apoptotic index or a combination of Bax/Bcl-2 expression correlate with survival after resection of pancreatic adenocarcinoma. J Cell Biochem 97(1):98–108CrossRefPubMedGoogle Scholar
  24. Matough FA, Budin SB, Hamid ZA, Alwahaibi N, Mohamed J (2012) The role of oxidative stress and antioxidants in diabetic complications. Sultan Qaboos Univ Med J 12(1):5–18CrossRefPubMedPubMedCentralGoogle Scholar
  25. Mohammadi-Farani A, Ghazi-Khansari M, Sahebgharani M (2014) Glucose concentration in culture medium affects mRNA expression of TRPV1 and CB1 receptors and changes capsaicin toxicity in PC12 cells. Iran J Basic Med Sci 17(9):673–378PubMedPubMedCentralGoogle Scholar
  26. Naudi A, Jove M, Ayala V, Cassanye A, Serrano J, Gonzalo H, Boada J, Prat J, Portero-Otin M, Pamplona R (2012) Cellular dysfunction in diabetes as maladaptive response to mitochondrial oxidative stress. Exp Diabetes Res 2012:696215CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ogawa N, Yamaguchi T, Yano S, Yamauchi M, Yamamoto M, Sugimoto T (2007) The combination of high glucose and advanced glycation end-products (AGEs) inhibits the mineralization of osteoblastic MC3T3-E1 cells through glucose-induced increase in the receptor for AGEs. Horm Metab Res 39(12):871–875CrossRefPubMedGoogle Scholar
  28. Park SY, Kim MH, Ahn JH, Lee SJ, Lee JH, Eum WS, Choi SY, Kwon HY (2014) The stimulatory effect of essential fatty acids on glucose uptake involves both Akt and AMPK activation in C2C12 skeletal muscle cells. Korean J Physiol Pharmacol 18(3):255–261CrossRefPubMedPubMedCentralGoogle Scholar
  29. Pereira M, Siba IP, Chioca LR, Correia D, Vital MABF, Pizzolatti MG, Santos ARS, Andreatini R (2011) Myricitrin, a nitric oxide and protein kinase C inhibitor, exerts antipsychotic-like effects in animal models. Prog Neuro-Psychopharmacol Biol Psychiatry 35(7):1636–1644CrossRefGoogle Scholar
  30. Pyun B-J, Kim YS, Lee I-S, Kim JS (2017) Homonoia riparia and its major component, myricitrin, inhibit high glucose-induced apoptosis of human retinal pericytes. Int Med Res 6(3):300–309CrossRefGoogle Scholar
  31. Safi SZ, Qvist R, Yan GOS, Ismail ISB (2014) Differential expression and role of hyperglycemia induced oxidative stress in epigenetic regulation of β1, β2 and β3-adrenergic receptors in retinal endothelial cells. BMC Med Genet 7:29–29Google Scholar
  32. Sak K (2014) Cytotoxicity of dietary flavonoids on different human cancer types. Pharmacogn Rev 8(16):122–146CrossRefPubMedPubMedCentralGoogle Scholar
  33. Schöneich C, Dremina E, Galeva N, Sharov V (2014) Apoptosis in differentiating C2C12 muscle cells selectively targets Bcl-2-deficient myotubes. Apoptosis 19(1):42–57CrossRefPubMedPubMedCentralGoogle Scholar
  34. Senesi P, Montesano A, Luzi L, Codella R, Benedini S, Terruzzi I (2016) Metformin treatment prevents sedentariness related damages in mice. J Diabetes Res 2016(8274689):30Google Scholar
  35. Sharma P, Singh R (2014) Effect of Momordica dioica fruit extract on antioxidant status in liver, kidney, pancreas, and serum of diabetic rats. Pharm Res 6(1):73–79Google Scholar
  36. Siu PM, Wang Y, Alway SE (2009) Apoptotic signaling induced by H(2)O(2)-mediated oxidative stress in differentiated C2C12 myotubes. Life Sci 84(13–14):468–481CrossRefPubMedPubMedCentralGoogle Scholar
  37. Son MJ, Miura Y, Yagasaki K (2015) Mechanisms for antidiabetic effect of gingerol in cultured cells and obese diabetic model mice. Cytotechnology 67(4):641–652CrossRefPubMedGoogle Scholar
  38. Uruno A, Yagishita Y, Katsuoka F, Kitajima Y, Nunomiya A, Nagatomi R, Pi J, Biswal SS, Yamamoto M (2016) Nrf2-mediated regulation of skeletal muscle glycogen metabolism. Mol Cell Biol 36(11):1655–1672CrossRefPubMedPubMedCentralGoogle Scholar
  39. Verzola D, Bertolotto MB, Villaggio B, Ottonello L, Dallegri F, Salvatore F, Berruti V, Gandolfo MT, Garibotto G, Deferrari G (2004) Oxidative stress mediates apoptotic changes induced by hyperglycemia in human tubular kidney cells. J Am Soc Nephrol 15(1 suppl):S85–S87CrossRefPubMedGoogle Scholar
  40. Zatalia SR, Sanusi H (2013) The role of antioxidants in the pathophysiology, complications, and management of diabetes mellitus. Acta Med Indones 45(2):141–147PubMedGoogle Scholar
  41. Zhang Y, Liu D (2011) Flavonol kaempferol improves chronic hyperglycemia-impaired pancreatic beta-cell viability and insulin secretory function. Eur J Pharmacol 670(1):325–332CrossRefPubMedGoogle Scholar
  42. Zhang B, Shen Q, Chen Y, Pan R, Kuang S, Liu G, Sun G, Sun X (2017) Myricitrin alleviates oxidative stress-induced inflammation and apoptosis and protects mice against diabetic cardiomyopathy. Sci Rep 7:44239CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Cell Stress Society International 2018

Authors and Affiliations

  • Akram Ahangarpour
    • 1
  • Ali Akbar Oroojan
    • 2
  • Layasadat Khorsandi
    • 3
  • Maryam Kouchak
    • 4
  • Mohammad Badavi
    • 5
  1. 1.Department of Physiology, Faculty of Medicine, Diabetes Research Center, Health Research InstituteAhvaz Jundishapur University of Medical SciencesAhvazIran
  2. 2.Department of Physiology, Faculty of MedicineStudent Research Committee of Ahvaz Jundishapur University of Medical SciencesAhvazIran
  3. 3.Department of Anatomical Sciences, Faculty of Medicine, Cell & Molecular Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran
  4. 4.Faculty of Pharmacy, Nanotechnology Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran
  5. 5.Department of Physiology, Faculty of Medicine, Physiology Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran

Personalised recommendations