Casein glycomacropeptide-derived peptide IPPKKNQDKTE ameliorates high glucose-induced insulin resistance in HepG2 cells via activation of AMPK signaling

Molecular Nutrition and Food Research

Volumn 61, Issue 2, 2017, Pages

  Song, Jia Jia ^a   Wang, Qian ^a   Du, Min ^b   Li, Tian Ge ^a   Chen, Bin ^c   Mao, Xue Ying ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c China Astronaut Research and Training Center   (China)

Author keywords

Akt; AMPK; Casein glycomacropeptide; HepG2 cells; Insulin resistance

Indexed keywords

CASEIN; CASEINOMACROPEPTIDE; GLUCOSE; GLUCOSE 6 PHOSPHATASE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3BETA; GSK3B PROTEIN, HUMAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ILE-PRO-PRO-LYS-LYS-ASN-GLN-ASP-LYS-THR-GLU; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; PCK2 PROTEIN, HUMAN; PEPTIDE; PEPTIDE FRAGMENT; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PROTEIN KINASE B;

CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEP-G2 CELL LINE; HUMAN; HYDROLYSIS; INSULIN RESISTANCE; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; CASEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; GLUCOSE-6-PHOSPHATASE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3 BETA; HEP G2 CELLS; HUMANS; HYDROLYSIS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; PEPTIDE FRAGMENTS; PEPTIDES; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84987617630     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201600301     Document Type: Article

References (50)

1. Chen, L., Magliano, D. J., Zimmet, P. Z., The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat. Rev. Endocrinol. 2012, 8, 228–236.
2. Jatav, R. K., Kumbhare, M. B., Chennamaneni, R., Cutaneous manifestations of diabetes mellitus in adult patients of telangana region of South India. Eur. J. Acad. Essays 2014, 1, 38–44.
3. Deshpande, A. D., Harris-Hayes, M., Schootman, M., Epidemiology of diabetes and diabetes-related complications. Phys. Ther. 2008, 88, 1254–1264.
4. Ding, M., Bhupathiraju, S. N., Chen, M., van Dam, R. M. et al., Caffeinated and decaffeinated coffee consumption and risk of type 2 diabetes: a systematic review and a dose-response meta-analysis. Diabetes Care 2014, 37, 569–586.
5. Herrera, B. M., Lockstone, H. E., Taylor, J. M., Wills, Q. F. et al., MicroRNA-125a is over-expressed in insulin target tissues in a spontaneous rat model of Type 2 Diabetes. BMC Med. Genomics 2009, 2, 1–11.
6. Cao, J., Li, X., Liu, Y., Leng, F. et al., Bioassay-based isolation and identification of phenolics from sweet cherry that promote active glucose consumption by HepG2 cells. J. Food Sci. 2015, 80, C234–C240.
7. Boonloh, K., Kukongviriyapan, U., Pannangpetch, P., Kongyingyoes, B. et al., Rice bran protein hydrolysates prevented interleukin-6-and high glucose-induced insulin resistance in HepG2 cells. Food Funct. 2015, 6, 566–573.
8. Jin, M., Shi, G., Tang, S., Qiao, W. et al., Flavonoids from Tetrastigma obtectum enhancing glucose consumption in insulin-resistance HepG2 cells via activating AMPK. Fitoterapia 2013, 90, 240–246.
9. Liu, T., Shi, C., Gao, R., Sun, H. et al., Irisin inhibits hepatic gluconeogenesis and increases glycogen synthesis via the PI3K/Akt pathway in type 2 diabetic mice and hepatocytes. Clin. Sci. 2015, 129, 839–850.
10. Dujic, T., Causevic, A., Bego, T., Malenica, M. et al., Organic cation transporter 1 variants and gastrointestinal side effects of metformin in patients with Type 2 diabetes. Diabetic Med. 2015, 1–4.
11. Cariou, B., Charbonnel, B., Staels, B., Thiazolidinediones and PPARγ agonists: time for a reassessment. Trends Endocrin. Met. 2012, 23, 205–215.
12. Ma, X., Zhou, F., Chen, Y., Zhang, Y. et al., A polysaccharide from Grifola frondosa relieves insulin resistance of HepG2 cell by Akt-GSK-3 pathway. Glycoconjugate J. 2014, 31, 355–363.
13. Kwon, E., Jung, U. J., Park, T., Yun, J. W. et al., Luteolin attenuates hepatic steatosis and insulin resistance through the interplay between the liver and adipose tissue in mice with diet-induced obesity. Diabetes 2015, 64, 1658–1669.
14. Udenigwe, C. C., Bioinformatics approaches, prospects and challenges of food bioactive peptide research. Trends Food Sci. Tech. 2014, 36, 137–143.
15. Royle, P. J., McIntosh, G. H., Clifton, P. M., Whey protein isolate and glycomacropeptide decrease weight gain and alter body composition in male Wistar rats. Brit. J. Nutr. 2008, 100, 88–93.
16. Keogh, J. B., Clifton, P., The effect of meal replacements high in glycomacropeptide on weight loss and markers of cardiovascular disease risk. Am. J. Clin. Nutr. 2008, 87, 1602–1605.
17. Sawin, E. A., De Wolfe, T. J., Aktas, B., Stroup, B. M. et al., Glycomacropeptide is a prebiotic that reduces Desulfovibrio bacteria, increases cecal short-chain fatty acids, and is anti-inflammatory in mice. Am. J. Physiol. Gastr. L. 2015, 309, G590–G601.
18. Xu, S., Mao, X., Cheng, X., Chen, B., Ameliorating effects of casein glycomacropeptide on obesity induced by high-fat diet in male Sprague-Dawley rats. Food Chem. Toxicol. 2013, 56, 1–7.
19. Xu, S. P., Mao, X. Y., Ren, F. Z., Che, H. L., Attenuating effect of casein glycomacropeptide on proliferation, differentiation, and lipid accumulation of in vitro Sprague-Dawley rat preadipocytes. J. Dairy Sci. 2011, 94, 676–683.
20. Cheng, X., Gao, D., Chen, B., Mao, X., Endotoxin-binding peptides derived from casein glycomacropeptide inhibit lipopolysaccharide-stimulated inflammatory responses via blockade of NF-κB activation in macrophages. Nutrients 2015, 7, 3119–3137.
21. 2-induced oxidative stress in RAW 264.7 macrophages via ROS-dependent heme oxygenase-1 expression. RSC Adv. 2015, 5, 4511–4523.
22. Zang, M., Zuccollo, A., Hou, X., Nagata, D. et al., AMP-activated protein kinase is required for the lipid-lowering effect of metformin in insulin-resistant human HepG2 cells. J. Biol. Chem. 2004, 279, 47898–47905.
23. Cordero-Herrera, I., Martín, M. Á., Goya, L., Ramos, S., Cocoa flavonoids attenuate high glucose-induced insulin signalling blockade and modulate glucose uptake and production in human HepG2 cells. Food Chem. Toxicol. 2014, 64, 10–19.
24. Zou, C., Wang, Y., Shen, Z., 2-NBDG as a fluorescent indicator for direct glucose uptake measurement. J. Biochem. Bioph. Met. 2005, 64, 207–215.
25. Bartlett, P. J., Gaspers, L. D., Pierobon, N., Thomas, A. P., Calcium-dependent regulation of glucose homeostasis in the liver. Cell Calcium 2014, 55, 306–316.
26. Yin, J., Gao, Z., Liu, D., Liu, Z. et al., Berberine improves glucose metabolism through induction of glycolysis. Am. J. Physiol. Endoc. M. 2008, 294, E148-156.
27. Huang, Q., Chen, L., Teng, H., Song, H. et al., Phenolic compounds ameliorate the glucose uptake in HepG2 cells' insulin resistance via activating AMPK: Anti-diabetic effect of phenolic compounds in HepG2 cells. J. Funct. Foods 2015, 19, 487–494.
28. Dong, Y., Gao, G., Fan, H., Li, S. et al., Activation of the liver X receptor by agonist TO901317 improves hepatic insulin resistance via suppressing reactive oxygen species and JNK pathway. PLoS One 2015, 10, 1–20.
29. Chen, C., Lee, T., Kwok, C., Hsu, Y. et al., Major urinary protein 1 interacts with cannabinoid receptor type 1 in fatty acid-induced hepatic insulin resistance in a mouse hepatocyte model. Biochem. Biophys. Res. Co. 2015, 460, 1063–1068.
30. Perry, R. J., Samuel, V. T., Petersen, K. F., Shulman, G. I., The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature 2014, 510, 84–91.
31. Kim, K. M., Lee, K., Lee, G. Y., Jin, H. et al., Anti-diabetic efficacy of KICG1338, a novel glycogen synthase kinase-3β inhibitor, and its molecular characterization in animal models of type 2 diabetes and insulin resistance. Mol. Cell. Endocrinol. 2015, 409, 1–10.
32. Zheng, T., Yang, X., Wu, D., Xing, S. et al., Salidroside ameliorates insulin resistance through activation of a mitochondria-associated AMPK/PI3K/Akt/GSK3β pathway. Brit. J. Pharmacol. 2015, 172, 3284–3301.
33. Sajan, M. P., Ivey, R. A., Farese, R. V., BMI-related progression of atypical PKC-dependent aberrations in insulin signaling through IRS-1, Akt, FoxO1 and PGC-1α in livers of obese and type 2 diabetic humans. Metabolism 2015, 64, 1454–1465.
34. Zhang, Y., Hai, J., Cao, M., Zhang, Y. et al., Silibinin ameliorates steatosis and insulin resistance during non-alcoholic fatty liver disease development partly through targeting IRS-1/PI3K/Akt pathway. Int. Immunopharmacol. 2013, 17, 714–720.
35. Copps, K. D., White, M. F., Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia 2012, 55, 2565–2582.
36. Lin, C. L., Lin, J. K., Epigallocatechin gallate (EGCG) attenuates high glucose-induced insulin signaling blockade in human hepG2 hepatoma cells. Mol. Nutr. Food Res. 2008, 52, 930–939.
37. Bhuvaneswari, S., Anuradha, C. V., Astaxanthin prevents loss of insulin signaling and improves glucose metabolism in liver of insulin resistant mice. Can. J. Physiol. Pharm. 2012, 90, 1544–1552.
38. Sharma, B., Kim, H., Rhyu, D., extract ameliorates insulin resistance and regulates glucose metabolism in C57BL/KsJ-db/db mice via PI3K/AKT signaling pathway in myocytes. J. Transl. Med. 2015, 1, 1–10.
39. Coughlan, K. A., Valentine, R. J., Ruderman, N. B., Saha, A. K., AMPK activation: a therapeutic target for type 2 diabetes? Diabetes Metab. Syndr. Obes. Tar. Ther. 2014, 7, 241–253.
40. Jayanthy, G., Subramanian, S., RA abrogates hepatic gluconeogenesis and insulin resistance by enhancing IRS-1 and AMPK signalling in experimental type 2 diabetes. RSC Adv. 2015, 5, 44053–44067.
41. Cordero-Herrera, I., Mart, I. M. I. A.A., Goya, L., Ramos, S., Cocoa flavonoids protect hepatic cells function against high glucose-induced oxidative stress. Relevance of MAPKs. Mol. Nutr. Food Res. 2015, 59, 597–609.
42. Lammi, C., Zanoni, C., Arnoldi, A., IAVPGEVA, I. A. V.P T G V. A., LPYP, three peptides from soy glycinin, modulate cholesterol metabolism in HepG2 cells through the activation of the LDLR-SREBP2 pathway. J. Funct. Foods. 2015, 14, 469–478.
43. Guo, Y., Ma, C., Li, C., Wu, J. et al., Screening and identification of a specific peptide binding to hepatocellular carcinoma cells from a phage display peptide library. J. Pept. Sci. 2014, 20, 196–202.
44. Sarmadi, B. H., Ismail, A., Antioxidative peptides from food proteins: a review. Peptides 2010, 31, 1949–1956.
45. Udenigwe, C. C., Aluko, R. E., Food protein-derived bioactive peptides: production, processing, and potential health benefits. J. Food Sci. 2012, 77, R11-R24.
46. Lyapina, L. A., Myasoedov, N. F., Grigor Eva, M. E., Shubina, T. A. et al., The modern concept of the regulatory role of peptides of the glyproline family in the correction of hemostasis system function during development of diabetes mellitus. Biol. Bull. 2013, 40, 386–393.
47. 2 in rats with associated metabolic disorders. B. Exp. Biol. Med. 2014, 156, 338–341.
48. Sawada, Y., Sakamoto, Y., Toh, M., Ohara, N. et al., Milk-derived peptide Val-Pro-Pro (VPP) inhibits obesity-induced adipose inflammation via an angiotensin-converting enzyme (ACE) dependent cascade. Mol. Nutr. Food Res. 2015, 59, 2502–2510.
49. Lammi, C., Zanoni, C., Arnoldi, A., Three peptides from soy glycinin modulate glucose metabolism in human hepatic HepG2 cells. Int. J. Mol. Sci. 2015, 16, 27362–27370.
50. Zhang, Z., Lu, J., Zheng, Y., Wu, D. et al., Purple sweet potato color attenuates hepatic insulin resistance via blocking oxidative stress and endoplasmic reticulum stress in high-fat-diet-treated mice. J. Nutr. Biochem. 2013, 24, 1008–1018.