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Ishige okamurae reduces blood glucose levels in high-fat diet mice and improves glucose metabolism in the skeletal muscle and pancreas

  • Yang, Hye-Won (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Son, Myeongjoo (Department of Anatomy & Cell Biology, Gachon University College of Medicine) ;
  • Choi, Junwon (Department of Anatomy & Cell Biology, Gachon University College of Medicine) ;
  • Oh, Seyeon (Functional Cellular Networks Laboratory, Lee Gil Ya Cancer and Diabetes Institute, Gachon University) ;
  • Jeon, You-Jin (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University) ;
  • Byun, Kyunghee (Department of Anatomy & Cell Biology, Gachon University College of Medicine) ;
  • Ryu, Bo Mi (Department of Marine Life Science, School of Marine Biomedical Sciences, Jeju National University)
  • Received : 2020.05.21
  • Accepted : 2020.07.24
  • Published : 2020.09.30

Abstract

Brown alga (Ishige okamurae; IO) dietary supplements have been reported to possess anti-diabetic properties. However, the effects of IO supplements have not been evaluated on glucose metabolism in the pancreas and skeletal muscle. C57BL/6 N male mice (age, 7 weeks) were arranged in five groups: a chow diet with 0.9% saline (NFD/saline group), high-fat diet (HFD) with 0.9% saline (HFD/saline group). high-fat diet with 25 mg/kg IO extract (HFD/25/IOE). high-fat diet with 50 mg/kg IO extract (HFD/50/IOE), and high-fat diet with 75 mg/kg IO extract (HFD/75/IOE). After 4 weeks, the plasma, pancreas, and skeletal muscle samples were collected for biochemical analyses. IOE significantly ameliorated glucose tolerance impairment and fasting and 2 h blood glucose level in HFD mice. IOE also stimulated the protein expressions of the glucose transporters (GLUTs) including GLUT2 and GLUT4 and those of their related transcription factors in the pancreases and skeletal muscles of HFD mice, enhanced glucose metabolism, and regulated blood glucose level. Our results suggest Ishige okamurae extract may reduce blood glucose levels by improving glucose metabolism in the pancreas and skeletal muscle in HFD-induced diabetes.

Keywords

References

  1. Bell GI, Polonsky KS. Diabetes mellitus and genetically programmed defects in ${\beta}$-cell function. Nature. 2001;414:788. https://doi.org/10.1038/414788a
  2. Bonny C, Roduit R, Gremlich S, Nicod P, Thorens B, Waeber G. The loss of GLUT2 expression in the pancreatic ${\beta}$-cells of diabetic db/db mice is associated with an impaired DNA-binding activity of islet-specific trans-acting factors. Mol Cell Endocrinol. 1997;135:59-65. https://doi.org/10.1016/S0303-7207(97)00190-1
  3. Bringhenti I, Moraes-Teixeira JA, Cunha MR, Ornellas F, Mandarim-de-Lacerda CA, Aguila MB. Maternal obesity during the preconception and early life periods alters pancreatic development in early and adult life in male mouse offspring. PLOS ONE. 2013;8:e55711. https://doi.org/10.1371/journal.pone.0055711
  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. Carey DG, Jenkins AB, Campbell LV, Freund J, Chisholm DJ. Abdominal fat and insulin resistance in normal and overweight women: direct measurements reveal a strong relationship in subjects at both low and high risk of NIDDM. Diabetes. 1996;45:633-8. https://doi.org/10.2337/diab.45.5.633
  6. Cerf ME. High fat diet modulation of glucose sensing in the beta-cell. Med Sci Monit. 2006;13:RA12-7.
  7. Chang L, Chiang S-H, Saltiel AR. Insulin signaling and the regulation of glucose transport. Mol Med. 2004;10:65. https://doi.org/10.2119/2005-00029.Saltiel
  8. Epstein PN, Boschero AC, Atwater I, Cai X, Overbeek PA. Expression of yeast hexokinase in pancreatic beta cells of transgenic mice reduces blood glucose, enhances insulin secretion, and decreases diabetes. Proc Natl Acad Sci USA. 1992;89:12038-42. https://doi.org/10.1073/pnas.89.24.12038
  9. Folli F, Okada T, Perego C, Gunton J, Liew CW, Akiyama M, D’Amico A, La Rosa S, Placidi C, Lupi R. Altered insulin receptor signalling and ${\beta}$-cell cycle dynamics in type 2 diabetes mellitus. PLOS ONE. 2011;6:e28050. https://doi.org/10.1371/journal.pone.0028050
  10. Frantz EDC, Crespo-Mascarenhas C, Barreto-Vianna ARC, Aguila MB, Mandarim-de-Lacerda CA. Renin-angiotensin system blockers protect pancreatic islets against diet-induced obesity and insulin resistance in mice. PLOS ONE. 2013;8:e67192. https://doi.org/10.1371/journal.pone.0067192
  11. Fukumoto H, Seino S, Imura H, Seino Y, Bell GI. Characterization and expression of human HepG2/erythrocyte glucose-transporter gene. Diabetes. 1988;37: 657-61. https://doi.org/10.2337/diab.37.5.657
  12. Giugliano D, Ceriello A, Esposito K. Glucose metabolism and hyperglycemia. Am J Clin Nutr. 2008;87:217S-22S. https://doi.org/10.1093/ajcn/87.1.217S
  13. Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9:367. https://doi.org/10.1038/nrm2391
  14. Hamza N, Berke B, Cheze C, Agli A-N, Robinson P, Gin H, Moore N. Prevention of type 2 diabetes induced by high fat diet in the C57BL/6 J mouse by two medicinal plants used in traditional treatment of diabetes in the east of Algeria. J Ethnopharmacol. 2010;128:513-8. https://doi.org/10.1016/j.jep.2010.01.004
  15. Hashimoto N, Kido Y, Uchida T, Matsuda T, Suzuki K, Inoue H, Matsumoto M, Ogawa W, Maeda S, Fujihara H. $PKC{\lambda}$ regulates glucose-induced insulin secretion through modulation of gene expression in pancreatic ${\beta}$ cells. J Clin Investig. 2005;115:138-45. https://doi.org/10.1172/JCI22232
  16. Heo S-J, Hwang J-Y, Choi J-I, Han J-S, Kim H-J, Jeon Y-J. Diphlorethohydroxycarmalol isolated from Ishige okamurae, a brown algae, a potent ${\alpha}$-glucosidase and ${\alpha}$-amylase inhibitor, alleviates postprandial hyperglycemia in diabetic mice. Eur J Pharmacol. 2009;615:252-6. https://doi.org/10.1016/j.ejphar.2009.05.017
  17. Herman MA, Kahn BB. Glucose transport and sensing in the maintenance of glucose homeostasis and metabolic harmony. J Clin Investig. 2006;116:1767-75. https://doi.org/10.1172/JCI29027
  18. Honors MA, Hargrave SL, Kinzig KP. Glucose tolerance in response to a high-fat diet is improved by a high-protein diet. Obesity. 2012;20:1859-65. https://doi.org/10.1038/oby.2011.297
  19. Hull R, Kodama K, Utzschneider K, Carr D, Prigeon R, Kahn S. Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: evidence for specificity of impaired beta cell adaptation. Diabetologia. 2005;48:1350-8. https://doi.org/10.1007/s00125-005-1772-9
  20. Kiuru P, MV DA, Muller CD, Tammela P, Vuorela H, Yli-Kauhaluoma J. Exploring marine resources for bioactive compounds. Planta Med. 2014;80:1234-46. https://doi.org/10.1055/s-0034-1383001
  21. Konrad D, Bilan PJ, Nawaz Z, Sweeney G, Niu W, Liu Z, Antonescu CN, Rudich A, Klip A. Need for GLUT4 activation to reach maximum effect of insulinmediated glucose uptake in brown adipocytes isolated from GLUT4mycexpressing mice. Diabetes. 2002;51:2719-26. https://doi.org/10.2337/diabetes.51.9.2719
  22. Lee S-H, Park M-H, Heo S-J, Kang S-M, Ko S-C, Han J-S, Jeon Y-J. Dieckol isolated from Ecklonia cava inhibits ${\alpha}$-glucosidase and ${\alpha}$-amylase in vitro and alleviates postprandial hyperglycemia in streptozotocin-induced diabetic mice. Food Chem Toxicol. 2010;48:2633-7. https://doi.org/10.1016/j.fct.2010.06.032
  23. Matveyenko AV, Gurlo T, Daval M, Butler AE, Butler PC. Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPPinduced ${\beta}$-cell endoplasmic reticulum stress. Diabetes. 2009;58:906-16. https://doi.org/10.2337/db08-1464
  24. Min K-H, Kim H-J, Jeon Y-J, Han J-S. Ishige okamurae ameliorates hyperglycemia and insulin resistance in C57BL/KsJ-db/db mice. Diabetes Res Clin Pract. 2011;93:70-6. https://doi.org/10.1016/j.diabres.2011.03.018
  25. Murugan AC, Karim MR, Yusoff MBM, Tan SH, Asras MFBF, Rashid SS. New insights into seaweed polyphenols on glucose homeostasis. Pharm Biol. 2015;53: 1087-97. https://doi.org/10.3109/13880209.2014.959615
  26. Nicolino M, Claiborn KC, Senee V, Boland A, Stoffers DA, Julier C. A novel hypomorphic PDX1 mutation responsible for permanent neonatal diabetes with subclinical exocrine deficiency. Diabetes. 2010;59:733-40. https://doi.org/10.2337/db09-1284
  27. Nishiumi S, Bessyo H, Kubo M, Aoki Y, Tanaka A, Yoshida K-I, Ashida H. Green and black tea suppress hyperglycemia and insulin resistance by retaining the expression of glucose transporter 4 in muscle of high-fat diet-fed C57BL/6 J mice. J Agric Food Chem. 2010;58:12916-23. https://doi.org/10.1021/jf102840w
  28. Ratner RE. Controlling postprandial hyperglycemia. Am J Cardiol. 2001;88:26-31. https://doi.org/10.1016/S0002-9149(01)01834-3
  29. Riant E, Waget A, Cogo H, Arnal J-F, Burcelin R, Gourdy P. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology. 2009;150:2109-17. https://doi.org/10.1210/en.2008-0971
  30. Rines AK, Sharabi K, Tavares CD, Puigserver P. Targeting hepatic glucose metabolism in the treatment of type 2 diabetes. Nat Rev Drug Discov. 2016;15:786. https://doi.org/10.1038/nrd.2016.151
  31. Ryu B, Jiang Y, Kim H-S, Hyun J-M, Lim S-B, Li Y, Jeon Y-J. Ishophloroglucin A, a novel phlorotannin for standardizing the anti-${\alpha}$-glucosidase activity of Ishige okamurae. Mar Drugs. 2018;16:436. https://doi.org/10.3390/md16110436
  32. Sanjeewa KA, Lee WW, Kim J-I, Jeon Y-J. Exploiting biological activities of brown seaweed Ishige okamurae Yendo for potential industrial applications: a review. J Appl Phycol. 2017;29:3109-19. https://doi.org/10.1007/s10811-017-1213-4
  33. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev. 2007;87:507-20. https://doi.org/10.1152/physrev.00024.2006
  34. Schultze SM, Hemmings BA, Niessen M, Tschopp O. PI3K/AKT, MAPK and AMPK signalling: protein kinases in glucose homeostasis. Expet Rev Mol Med. 2012;14.
  35. Shan W-F, B-q C, Zhu S-j, Jiang L, Zhou Y-F. Effects of GLUT4 expression on insulin resistance in patients with advanced liver cirrhosis. J Zhejiang Univ Sci B. 2011;12:677. https://doi.org/10.1631/jzus.B1100001
  36. Sharifuddin Y, Chin Y-X, Lim P-E, Phang S-M. Potential bioactive compounds from seaweed for diabetes management. Mar Drugs. 2015;13:5447-91. https://doi.org/10.3390/md13085447
  37. Shepherd PR, Withers DJ, Siddle K. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem J. 1998;333:471-90. https://doi.org/10.1042/bj3330471
  38. Sun Q, Nie S, Wang L, Yang F, Meng Z, Xiao H, Xiang B, Li X, Fu X, Wang S. Factors that affect pancreatic islet cell autophagy in adult rats: evaluation of a calorie-restricted diet and a high-fat diet. PLOS ONE. 2016;11:e0151104. https://doi.org/10.1371/journal.pone.0151104
  39. Suzuki R, Tobe K, Terauchi Y, Komeda K, Kubota N, Eto K, Yamauchi T, Azuma K, Kaneto H, Taguchi T. Pdx1 expression in Irs2-deficient mouse ${\beta}$-cells is regulated in a strain-dependent manner. J Biol Chem. 2003;278:43691-8. https://doi.org/10.1074/jbc.M307004200
  40. Tremblay F, Lavigne C, Jacques H, Marette A. Defective insulin-induced GLUT4 translocation in skeletal muscle of high fat-fed rats is associated with alterations in both Akt/protein kinase B and atypical protein kinase C ($\zeta$/${\lambda}$) activities. Diabetes. 2001;50:1901-10. https://doi.org/10.2337/diabetes.50.8.1901
  41. Tsuchiya Y, Hatakeyama H, Emoto N, Wagatsuma F, Matsushita S, Kanzaki M. Palmitate-induced down-regulation of sortilin and impaired GLUT4 trafficking in C2C12 myotubes. J Biol Chem. 2010;285:34371-81. https://doi.org/10.1074/jbc.M110.128520
  42. Tsuneki H, Ishizuka M, Terasawa M, Wu J-B, Sasaoka T, Kimura I. Effect of green tea on blood glucose levels and serum proteomic patterns in diabetic (db/db) mice and on glucose metabolism in healthy humans. BMC Pharmacol. 2004;4:18. https://doi.org/10.1186/1471-2210-4-18
  43. Waeber G, Thompson N, Nicod P, Bonny C. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol Endocrinol. 1996;10:1327-34. https://doi.org/10.1210/mend.10.11.8923459
  44. Wiegand S, Dannemann A, Krude H, Gruters A. Impaired glucose tolerance and type 2 diabetes mellitus: a new field for pediatrics in Europe. Int J Obes. 2005;29:S136. https://doi.org/10.1038/sj.ijo.0803081
  45. Yamashita Y, Wang L, Tinshun Z, Nakamura T, Ashida H. Fermented tea improves glucose intolerance in mice by enhancing translocation of glucose transporter 4 in skeletal muscle. J Agric Food Chem. 2012;60:11366-71. https://doi.org/10.1021/jf303597c
  46. Yang H-W, Son M, Choi J, Oh S, Jeon Y-J, Byun K, Ryu B. Effect of ishophloroglucin A, a component of Ishige okamurae, on glucose homeostasis in the pancreas and muscle of high fat diet-fed mice. Mar Drugs. 2019;17:608. https://doi.org/10.3390/md17110608

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