Glucose homeostasis is impaired by a paradoxical interaction between metformin and insulin in carnivorous rainbow trout

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 6, 2009, Pages

  Polakof, S ^a,b,c,d   Skiba Cassy, S ^a,b,c   Panserat, S ^a,b,c  

^a Unite mixte INRA IFREMER Universite Bordeaux 1 UMR Nuage   (France)

^b IFREMER   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d UNIVERSITY OF VIGO   (Spain)

Author keywords

Fish; Glucose metabolism; Insulin; Liver; Metformin; Muscle

Indexed keywords

BOVINE INSULIN; GLUCOSE; GLYCOGEN; INSULIN; INSULIN PLUS METFORMIN; MESSENGER RNA; METFORMIN; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG EFFECT; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; HYPOGLYCEMIA; INSULIN RESISTANCE; LIPOGENESIS; LIVER LEVEL; MUSCLE LEVEL; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; RAINBOW TROUT; SIGNAL TRANSDUCTION; SUSTAINED DRUG RELEASE;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BLOOD GLUCOSE; FOOD HABITS; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLYCOLYSIS; HOMEOSTASIS; HYPOGLYCEMIC AGENTS; INFUSION PUMPS, IMPLANTABLE; INJECTIONS, INTRAPERITONEAL; INSULIN; INSULIN RESISTANCE; LIPOGENESIS; LIVER; LIVER GLYCOGEN; METFORMIN; MUSCLE, SKELETAL; ONCORHYNCHUS MYKISS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 72449208700     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00369.2009     Document Type: Article

References (41)

1. Amini H, Ahmadiani A, Gazerani P. Determination of metformin in human plasma by high-performance liquid chromatography. J Chromatogr B Biomed Appl 824: 319-322, 2005. (Pubitemid 41215613)
2. Bergot F. Effects of dietary carbohydrates and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri Richardson). Comp Biochem Physiol A 64: 543-547, 1979.
3. Daniel JR, Hagmeyer KO. Metformin and insulin: is there a role for combination therapy? Ann Pharmacother 31: 474-480, 1997. (Pubitemid 27155252)
4. Díaz M, Capilla E, Planas JV. Physiological regulation of glucose transporter (GLUT4) protein content in brown trout (Salmo trutta) skeletal muscle. J Exp Biol 210: 2346-2351, 2007. (Pubitemid 47080212)
5. Díaz M, Vraskou Y, Gutiérrez J, Planas JV. Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiation and regulation by insulin and IGF-I. Am J Physiol Regul Integr Comp Physiol 296: R794-R800, 2009.
6. El-Maghrabi MR, Lange AJ, Kummel L, Pilkis SJ. The rat fructose-1,6-bisphosphatase gene. Structure and regulation of expression. J Biol Chem 266: 2115-2120, 1991. (Pubitemid 21909037)
7. Elo B, Villano CM, Govorko D, White LA. Larval zebrafish as a model for glucose metabolism: expression of phosphoenolpyruvate carboxykinase as a marker for exposure to anti-diabetic compounds. J Mol Endocrinol 38: 433-440, 2007. (Pubitemid 46723259)
8. Giannarelli R, Aragona M, Coppelli A, Del Prato S. Reducing insulin resistance with metformin: the evidence today. Diabetes Metab 29: 6S28-6S35, 2003. (Pubitemid 37187088)
9. Hassan SSM, Mahmoud WH, Elmosallamy MAF, Othman AHM. Determination of metformin in pharmaceutical preparations using potentiometry, spectrofluorimetry and UV-visible spectrophotometry. Anal Chim Acta 378: 299-311, 1999.
10. Hemre GI, Mommsen TP, Krogdahl Å. Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8: 175-194, 2002. (Pubitemid 135716052)
11. Hertz Y, Epstein N, Abraham M, Madar Z, Hepher B, Gertler A. Effects of metformin on plasma insulin, glucose metabolism and protein synthesis in the common carp (Cyprinus carpio L.). Aquaculture 80: 175-187, 1989.
12. Hundal HS, Ramlal T, Reyes R, Leiter LA, Klip A. Cellular mechanism of metformin action involves glucose transporter translocation from an intracellular pool to the plasma membrane in L6 muscle cells. Endocrinology 131: 1165-1173, 1992.
13. Johnson AB, Webster JM, Sum CF, Heseltine L, Argyraki M, Cooper BG, Taylor R. The impact of metformin therapy on hepatic glucose production and skeletal muscle glycogen synthase activity in overweight type II diabetic patients. Metabolism 42: 1217-1222, 1993. (Pubitemid 23292702)
14. Joshi SR. Metformin: old wine in new bottle - evolving technology and therapy in diabetes. J Assoc Physicians India 53: 963-972, 2005.
15. Jucker BM, Barucci N, Shulman GI. Metabolic control analysis of insulin-stimulated glucose disposal in rat skeletal muscle. Am J Physiol Endocrinol Metab 277: E505-E512, 1999. (Pubitemid 29458211)
16. Keppler D, Decker K, Bergmeyer HU. Glycogen determination with amyloglucosidase. In: Methods of Enzymatic Analysis. New York: Academic, 1974, p. 1127-1131.
17. Kirchner S, Seixas P, Kaushik S, Panserat S. Effects of low protein intake on extra-hepatic gluconeogenic enzyme expression and peripheral glucose phosphorylation in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 140: 333-340, 2005. (Pubitemid 40092692)
18. Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefevre F, Medale F. Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 294: R1154-R1164, 2008.
19. Massillon D, Barzilai N, Chen W, Hu M, Rossetti L. Glucose regulates in vivo glucose-6-phosphatase gene expression in the liver of diabetic rats. J Biol Chem 271: 9871-9874, 1996. (Pubitemid 26131536)
20. Mommsen TP, Plisetskaya EM. Insulin in fishes and agnathans: history, structure, and metabolic regulation. Rev Aquat Sci 4: 225-259, 1991.
21. Moon TW. Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B-Biochem Mol Biol 129: 243-249, 2001.
22. Moon TW, Foster GD. Tissue carbohydrate metabolism, gluconeogenesis and hormonal and environmental influences. In: Biochemistry and molecular biology of fishes, edited by Hochachka PW and Mommsen TP. Amsterdam: Elsevier, 1995, p. 65-100.
23. Navarro I, Capilla E, Castillo A, Albalat A, Diκaz M, Gallardo MA, Blasco J, Planas JV, Gutiérrez J, Reinecke M, Zaccone G, Kapoor BG. Insulin metabolic effects in fish tissues. In: Fish Endocrinology. Enfield, NH: Science Publishers, 2006, p. 15-48.
24. Olsvik PA, Lie KK, Jordal AE, Nilsen TO, Hordvik I. Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon [Online]. BMC Mol Biol 6: 21, 2005. (Pubitemid 41715729)
25. Palmer TN, Ryman BE. Studies on oral glucose intolerance in fish. J Fish Biol 4: 311-319, 1972.
26. Panserat S, Médale F, Blin C, Brèque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S. Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilhead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278: R1164-R1170, 2000. (Pubitemid 30366443)
27. Panserat S, Plagnes-Juan E, Brèque J, Kaushik S. Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohybrates in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204: 359-365, 2001. (Pubitemid 32116911)
28. Panserat S, Plagnes-Juan E, Kaushik S. Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204: 2351-2360, 2001. (Pubitemid 34869499)
29. Panserat S, Skiba-Cassy S, Seiliez I, Lansard M, Plagnes-Juan E, Vachot C, Aguirre P, Larroquet L, Chavergnac G, Médale F, Corraze G, Kaushik S, Moon TW. Metformin improves postprandial glucose homeostasis in rainbow trout fed dietary carbohydrates: a link with the induction of hepatic lipogenic capacities? Am J Physiol Regul Integr Comp Physiol 297: R707-R715, 2009.
30. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR [Online]. Nucleic Acids Res 29: e45, 2001.
31. Plagnes-Juan E, Lansard M, Seiliez I, Medale F, Corraze G, Kaushik S, Panserat S, Skiba-Cassy S. Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J Exp Biol 211: 2510-2518, 2008.
32. Polakof S, Míguez JM, Moon TW, Soengas JL. Evidence for the presence of a glucosensor in hypothalamus, hindbrain, and Brockmann bodies of rainbow trout. Am J Physiol Regul Integr Comp Physiol 292: R1657-R1666, 2007. (Pubitemid 46557831)
33. Sarnblad S, Kroon M, Aman J. Metformin as additional therapy in adolescents with poorly controlled type 1 diabetes: randomised placebo-controlled trial with aspects on insulin sensitivity. Eur J Endocrinol 149: 323-329, 2003. (Pubitemid 37304703)
34. Scarpello JH, Howlett HC. Metformin therapy and clinical uses. Diab Vasc Dis Res 5: 157-167, 2008.
35. Scott DK, O'Doherty RM, Stafford JM, Newgard CB, Granner DK. The repression of hormone-activated PEPCK gene expression by glucose is insulin-independent but requires glucose metabolism. J Biol Chem 273: 24145-24151, 1998.
36. Seiliez I, Gabillard JC, Skiba-Cassy S, García-Serrana D, Gutiérrez J, Kaushik S, Panserat S, Tesseraud S. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 295: R329-R335, 2008.
37. Setter SM, Iltz JL, Thams J, Campbell RK. Metformin hydrochloride in the treatment of type 2 diabetes mellitus: a clinical review with a focus on dual therapy. Clin Ther 25: 2991-3026, 2003. (Pubitemid 38096142)
38. Stumvoll M, Nurjhan N, Perriello G, Dailey G, Gerich JE. Metabolic effects of metformin in non-insulin-dependent diabetes mellitus. N Engl J Med 333: 550-554, 1995.
39. White MF. Metformin and insulin meet in a most atypical way. Cell Metab 9: 485-487, 2009.
40. Wilson RP. Utilization of dietary carbohydrate by fish. Aquaculture 124: 67-80, 1994.
41. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174, 2001. (Pubitemid 32995375)