Sardine protein diet increases plasma glucagon-like peptide-1 levels and prevents tissue oxidative stress in rats fed a high-fructose diet

Molecular Medicine Reports

Volumn 12, Issue 5, 2015, Pages 7017-7026

  Madani, Zohra ^a   Sener, Abdullah ^b   Malaisse, Willy J ^b   Dalila, Ait Yahia ^a  

^a UNIVERSITY OF ORAN   (Algeria)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

Author keywords

Antioxidant enzymes; Fructose; Lipid peroxidation; Metabolic syndrome; Rat; Sardine protein; Tissues

Indexed keywords

CATALASE; CREATININE; FRUCTOSE; GLUCAGON LIKE PEPTIDE 1; GLUTATHIONE PEROXIDASE; HYDROPEROXIDE; URIC ACID; ALPHA TOCOPHEROL; ASCORBIC ACID; CASEIN; FISH PROTEIN; GLUCOSE BLOOD LEVEL; HYDROGEN PEROXIDE; NITRIC OXIDE; SUPEROXIDE DISMUTASE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; GLUCAGON BLOOD LEVEL; GLUCAGON LIKE PEPTIDE 1 BLOOD LEVEL; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RESISTANCE; LIPID DIET; MALE; METABOLIC SYNDROME X; NONHUMAN; OBESITY; OXIDATIVE STRESS; PROTEIN BLOOD LEVEL; PROTEIN DIET; RAT; SARDINE; ANALYSIS; ANIMAL; BLOOD; CALORIC INTAKE; DIET; DRUG EFFECTS; ENZYMOLOGY; ISOLATION AND PURIFICATION; KIDNEY; LIVER; METABOLISM; WISTAR RAT;

ALPHA-TOCOPHEROL; ANIMALS; ASCORBIC ACID; BLOOD GLUCOSE; CASEINS; CATALASE; DIET; ENERGY INTAKE; FISH PROTEINS; FRUCTOSE; GLUCAGON-LIKE PEPTIDE 1; HYDROGEN PEROXIDE; KIDNEY; LIVER; MALE; NITRIC OXIDE; OBESITY; OXIDATIVE STRESS; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 84943627461     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2015.4324     Document Type: Article

References (58)

1. Wong ND: Metabolic syndrome: Cardiovascular risk assessment and management. Am J Cardiovasc Drugs 7: 259-272, 2007.
2. Després JP, Lemieux I, Bergeron J, Pibarot Ph, Mathieu P, Larose E, Rodés-Cabau J, Bertrand OF and Poirier P: Abdominal obesity and the metabolic syndrome: Contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol 28: 1039-1049, 2008.
3. Misra A and Khurana L: Obesity and the metabolic syndrome in developing countries. J Clin Endocrinol Metab 93 (Suppl 1): S9-S30, 2008.
4. Tappy L and Lê KA: Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 90: 23-46, 2010.
5. Le KA and Tappy L: Metabolic effects of fructose. Curr Opin Clin Nutr Metab Care 9: 469-475, 2006.
6. Yokozawa T, Kim HJ and Cho EJ: Gravinol ameliorates high-fructose-induced metabolic syndrome through regulation of lipid metabolism and proinflammatory state in rats. J Agric Food Chem 56: 5026-5032, 2008.
7. Kelley GL, Allan G, and Azhar S: High dietary fructose induces a hepatic stress response resulting in cholesterol and lipid dysregulation. Endocrinology 145: 548-555, 2004. http://dx-doi-org/10-1210/en-2003-1167.
8. Nkondjock A and Receveur O: Fish-seafood consumption, obesity, and risk of type 2 diabetes: An ecological study. Diabetes Metab 29: 635-642, 2003.
9. Ramel A, Martinez A, Kiely M, Morais G, Bandarra NM and Thorsdottir I: Beneficial effects of long-chain n-3 fatty acids included in an energy-restricted diet on insulin resistance in overweight and obese European young adults. Diabetologia 51: 1261-1268, 2008.
10. Delarue J, LeFoll C, Corporeau C and Lucas D: N-3 long chain polyunsaturated fatty acids: A nutritional tool to prevent insulin resistance associated to type 2 diabetes and obesity. Reprod Nutr Dev 44: 289-299, 2004.
11. Ebbesson SO, Ebbesson LO, Swenson M, Kennish JM and Robbins DC: A successful diabetes prevention study in Eskimos: The Alaska Siberia project. Int J Circumpolar Health 64: 409-424, 2005.
12. Lombardo YB, Hein G and Chicco A: Metabolic syndrome: Effects of n-3 PUFAs on a model of dyslipidemia, insulin resistance and adiposity. Lipids 42: 427-437, 2007.
13. Noriega-Lopez L, Tovar AR, Gonzalez-Granillo M, Hernandez-Pando R, Escalante B, Santillan-Doherty P and Torres N: Pancreatic insulin secretion in rats fed a soy protein high fat diet depends on the interaction between the amino acid pattern and isoflavones. J Biol Chem 282: 20657-20666, 2007.
14. Ascencio C, Torres N, Isoard-Acosta F, Gomez-Perez FJ, Hernandez-Pando R and Tovar AR: Soy protein affects serum insulin and hepatic SREBP-1 mRNA and reduces fatty liver in rats. J Nutr 134: 522-529, 2004.
15. Lavigne C, Tremblay F, Asselin G, Jacques H and Marette A: Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol Endocrinol Metab 281: E62-E71, 2001.
16. Mellouk Z, Ait Yahia D, Boukortt FO, Benaicha N, Madani Z and Bouchenak M: Dietary sardine (Sardina pilchardus) protein attenuates hyperglycemia and hyperlipidemia and ameliorates tissue morphology changes in streptozotocin-induced diabetic rats. Metab Funct Res Diab 2: 45-54, 2009.
17. Ait-Yahia D, Madani S, Prost E, Prost J, Bouchenak M and Belleville J: Tissue antioxidant status differs in spontaneously hypertensive rats fed fish protein or casein. J Nutr 133: 479-482, 2003.
18. Tremblay F, Lavigne C, Jacques H and Marette A: Dietary cod protein restores insulin-induced activation of phosphatidylinositol 3-kinase/Akt and GLUT4 translocation to the T-tubules in skeletal muscle of high-fat-fed obese rats. Diabetes 52: 29-37, 2003.
19. Ouellet V, Weisnagel SJ, Marois J, Bergeron J, Julien P, Gougeon R, Tchernof A, Holub BJ and Jacques H: Dietary cod protein reduces plasma C-reactive protein in insulin-resistant men and women. J Nutr 138: 2386-2391, 2008.
20. Undeland I, Kelleher SD and Hultin HO: Recovery of functional proteins from herring (Clupea harengus) light muscle by an acid or alkaline solubilization process. J Agric Food Chem 50: 7371-7379, 2002.
21. Kjeldahl JZ: A new method for the determination of nitrogen in organic bodies. Analytical Chemistry 22: 366, 1883.
22. Soxhlet FRV: The gravimetric determination of milk fat. Dingler's Polytechnic J 232: 461-465, 1879 (In German).
23. Council of European Communities: Council instructions about the protection of living animals used in scientific investigations. Official J. L358 of 18.12.1986; Corrigendum Official J. L 117 of 05.05.1987.
24. Bergmeyer HU, Berndt E, Schmidt F and Stork H: D-glucose determination with hexokinase and glucose 6-phosphate dehydrogenase. In: Methods of Enzymatic Analysis. Bergmeyer HU (ed). Vol 3. Academic Press, New York, pp1190-1201, 1974.
25. Leclercq-Meyer V, Marchand J, Woussen-Colle MC, Giroix MH and Malaisse WJ: Multiple effects of leucine on glucagon, insulin, and somatostatin secretion from the perfused rat pancreas. Endocrinology 116: 1168-1174, 1985.
26. Lowry OH, Rosebrough NJ, Farr AL and Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
27. Quintanilha AT, Packer L, Davies JM, Racanelli TL and Davies KJA: Membrane effects of vitamin E deficiency: Bioenergetic and surface charge density studies of skeletal muscle and liver mitochondria. Ann NY Acad Sci 393 (1 Vitamin E): 32-47, 1982.
28. Eymard S and Genot C: A modified xylenol orange method to evaluate formation of lipid hydroperoxides during storage and processing of small pelagic fish. Eur J Lipid Sci Technol 105: 497-501, 2003.
29. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S and Stadtman ER: Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464-478, 1990.
30. Cortas NK and Wakid NW: Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin Chem 36: 1440-1443, 1990.
31. Aebi H: Catalase. In: Methods of Enzymatic Analysis. Bergmeyer HU (ed). 2nd edition. Verlag Chemie Weinheim, pp673-684, 1974.
32. Baker H, Frank O, Angelis B and Feingold S: Plasma tocopherol in man at various times after ingesting free or acetylated tocopherol. Nutr Rep Int 21: 531-536, 1980.
33. Liddell JR, Dringen R, Crack PJ and Robinson SR: Glutathione peroxidase 1 and a high cellular glutathione concentration are essential for effective organic hydroperoxide detoxification in astrocytes. Glia 54: 873-879, 2006.
34. Stanhope KL and Havel PJ. Fructose consumption: Potential mechanisms for its effects to increase visceral adiposity and induce dyslipidemia and insulin resistance. Curr Opin Lipidol 19: 16-24, 2008.
35. Lim JS, Mietus-Snyder M, Valente A, Schwarz JM and Lustig RH: The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol 7: 251-264, 2010.
36. Ahangarpour A, Mohammadian M and Dianat M: Antidiabetic effect of hydroalcholic urticadioica leaf extract in male rats with fructose-induced insulin resistance. Iran J Med Sci 37: 181-186, 2012.
37. Hsieh FC, Lee CL, Chai CY, Chen WT, Lu YC and Wu CS: Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr Metab (Lond) 10: 35, 2013.
38. Borzoei S, Neovius M, Barkeling B, Teixeira-Pinto A and Rossner S: A comparison of effects of fish and beef protein on satiety in normal weight men. Eur J Clin Nutr 60: 897-902, 2006.
39. Pilon G, Ruzzin J, Rioux LE, Lavigne C, White PJ, Froyland L, Jacques H, Bryl P, Beaulieu L and Marette A: Differential effects of various fish proteins in altering body weight, adiposity, inflammatory status, and insulin sensitivity in high-fat-fed rats. Metabolism 60: 1122-1130, 2011.
40. Ouellet V, Marois J, Weisnagel SJ and Jacques H: Dietary cod protein improves insulin sensitivity in insulin-resistant men and women: A randomized controlled trial. Diabetes Care 30: 2816-2821, 2007.
41. Creutzfeldt W and Ebert R: New developments in the incretin concept. Diabetologia 28: 565-573. 1985.
42. Kieffer TJ and Habener JF: The glucagon-like peptides. Endocr Rev 20: 876-913, 1999.
43. Larsen J, Hylleberg B, Ng K and Damsbo P: Glucagon-like peptide-1 infusion must be maintained for 24 h/day to obtain acceptable glycemia in type 2 diabetic patients who are poorly controlled on sulphonylurea treatment. Diabetes Care 24: 1416-1421, 2001.
44. Nauck MA, Heimesaat MM, Orskov C, Holst JJ, Ebert R and Creutzfeldt W: Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest 91: 301-307, 1993.
45. Elahi D, McAloon-Dyke M, Fukagawa NK, Meneilly GS, Sclater AL, Minaker KL,Habener JF and Andersen DK: The insulinotropic actions of glucosedependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (7-37) in normal and diabetic subjects. Regul Pept 51: 63-74. 1994.
46. Kjems LL, Holst JJ, Volund A and Madsbad S: The influence of GLP-1 on glucose-stimulated insulin secretion: Effects on beta-cell sensitivity in type 2 and nondiabetic subjects. Diabetes 52: 380-386, 2003.
47. Holst JJ: The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439, 2007.
48. Lynch CJ, Hutson SM, Patson BJ, Vaval A and Vary TC: Tissue-specific effects of chronic dietary leucine and norleucine supplementation on protein synthesis in rats. Am J Physiol Endocrinol Metab 283: E824-E835, 2002.
49. Lavigne C, Marette A and Jacques H: Cod and soy proteins compared with casein improve glucose tolerance and insulin sensitivity in rats. Am J Physiol Endocrinol Metab 278: E491-E500, 2000.
50. Natarajan Sulochana K, Lakshmi S, Punitham R, Arokiasamy T, Sukumar B and Ramakrishnan S: Effect of oral supplementation of free amino acids in type 2 diabetic patients-A pilot clinical trial. Med Sci Monit 8: CR131-CR137, 2002.
51. Reddy SS, Ramatholisamma P, Karuna R and Saralakumari D: Preventive effect of Tinospora cordifolia against high-fructose diet-induced insulin resistance and oxidative stress in male Wistar rats. Food Chem Toxicol 47: 2224-2229, 2009.
52. Sakai M, Oimomi M and Kasuga M: Experimental studies on the role of fructose in the development of diabetic complications. Kobe J Med Sci 48: 125-136, 2002.
53. Nandhini AT, Thirunavukkarasu V, Ravichandran MK and Anuradha CV: Effect of taurine on biomarkers of oxidative stress in tissues of fructose-fed insulin-resistant rats. Singapore Med J 46: 82-87, 2005.
54. Chevion M, Berenshtein E and Stadtman ER: Human studies related to protein oxidation: Protein carbonyl content as a marker of damage. Free Rad Res 33: Suppl:S99-S108, 2000.
55. Boukortt FO, Girard A, Prost JL, Ait-Yahia D, Bouchenak M and Belleville J: Fish protein improves the total antioxidant status of streptozotocin-induced diabetes in spontaneously hypertensive rat. Med Sci Monit 10: BR397-BR404, 2004.
56. Sun YX, Hu SJ, Zhang XH, Sun J, Zhu CH and Zhang ZJ: Plasma levels of vWF and NO in patients with metabolic syndrome and their relationship with metabolic disorders. Zhejiang Da Xue Xue Bao Yi Xue Ban 35: 315-318, 2006 (In Chinese).
57. Simão ANC, Lozovoy MAB, Simão TNC, Dichi JB, Matsuo T and Dichi I: Nitric oxide enhancement and blood pressure decrease in patients with metabolic syndrome using soy protein or fish oil. Arq Bras Endocrinol Metabol 54: 540-545, 2010.
58. Bai Y, Sun L, Yang T, Sun K, Chen J and Hui R: Increase in fasting vascular endothelial function after short-term oral L-arginine is effective when baseline flow-mediated dilation is low: A meta-analysis of randomized controlled trials. Am J Clin Nutr 89: 77-84, 2009.