Evidence for a gut-brain axis used by glucagon-like peptide-1 to elicit hyperglycaemia in fish

Journal of Neuroendocrinology

Volumn 23, Issue 6, 2011, Pages 508-518

  Polakof, S ^a,b,c   Miguez J M ^a   Soengas, J L ^a  

^a UNIVERSITY OF VIGO   (Spain)

^b CRNH AUVERGNE   (France)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Brain; Fish; GLP 1; Glucose homeostasis; Glucose sensing; Neuropeptides

Indexed keywords

CAPSAICIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TRANSPORTER 2; INCRETIN; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.1; MESSENGER RNA; NEUROPEPTIDE; PROOPIOMELANOCORTIN; SULFONYLUREA DERIVATIVE; SULPHONYLUREA RECEPTOR LIKE; UNCLASSIFIED DRUG;

ARTICLE; CLINICAL ASSESSMENT; ENERGY; ENZYME ACTIVITY; FOOD INTAKE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; HYPERGLYCEMIA; HYPOTHALAMUS; IN VITRO STUDY; IN VIVO STUDY; LIVER; METABOLITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAINBOW TROUT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHOMBENCEPHALON; SPLANCHNIC NERVE; VAGUS NERVE;

ANIMALS; BLOOD GLUCOSE; BRAIN; CAPSAICIN; FISH DISEASES; FISHES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCAGON-LIKE PEPTIDE 1; GLUCONEOGENESIS; HYPERGLYCEMIA; INFUSIONS, INTRAVENTRICULAR; LIVER; ONCORHYNCHUS MYKISS; RANDOM ALLOCATION; SIGNAL TRANSDUCTION;

EID: 79955971663     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02137.x     Document Type: Article

References (53)

1. Migrenne S, Marsollier N, Cruciani-Guglielmacci C, Magnan C. Importance of the gut-brain axis in the control of glucose homeostasis. Curr Opin Pharmacol 2006; 6: 592-597.
2. Romijn JA, Corssmit EP, Havekes LM, Pijl H. Gut-brain axis. Curr Opin Clin Nutr Metab Care 2008; 11: 518-521.
3. Knauf C, Cani PD, Kim DH, Iglesias MA, Chabo C, Waget A, Colom A, Rastrelli S, Delzenne NM, Drucker DJ, Seeley RJ, Burcelin R. Role of central nervous system glucagon-like peptide-1 receptors in enteric glucose sensing. Diabetes 2008; 57: 2603-2612.
4. Irwin DM, Wong J. Trout and chicken proglucagon: alternative splicing generates mRNA transcripts encoding glucagon-like peptide 2. Mol Endocrinol 1995; 9: 267-277.
5. Kieffer TJ, Habener JF. The glucagon-like peptides. Endocr Rev 1999; 20: 876-913.
6. Plisetskaya EM, Mommsen TP. Glucagon and glucagon-like peptides in fishes. Int Rev Cytol 1996; 168: 187-257.
7. Irwin DM, Satkunarajah M, Wen Y, Brubaker PL, Pederson RA, Wheeler MB. The Xenopus proglucagon gene encodes novel GLP-1-like peptides with insulinotropic properties. Proc Natl Acad Sci USA 1997; 94: 7915-7920.
8. Lam CK, Chari M, Lam TK. CNS regulation of glucose homeostasis. Physiology (Bethesda) 2009; 24: 159-170.
9. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 2007; 87: 1409-1439.
10. Jin SL, Han VK, Simmons JG, Towle AC, Lauder JM, Lund PK. Distribution of glucagonlike peptide I (GLP-I), glucagon, and glicentin in the rat brain: an immunocytochemical study. J Comp Neurol 1988; 271: 519-532.
11. Yamamoto H, Lee CE, Marcus JN, Williams TD, Overton JM, Lopez ME, Hollenberg AN, Baggio L, Saper CB, Drucker DJ, Elmquist JK. Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J Clin Invest 2002; 110: 43-52.
12. Burcelin R, Serino M, Cabou C. A role for the gut-to-brain GLP-1-dependent axis in the control of metabolism. Curr Opin Pharmacol 2009; 9: 744-752.
13. Moon TW. Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B Biochem Mol Biol 2001; 129: 243-249.
14. Mommsen TP, Busby ER, Reinecke M, Zaccone G, Kapoor BG. Glucagon and friends. Fish Endocrinology. Enfield: Science Publishers, 2006: 223-256.
15. Mommsen TP. Glucagon-like peptide-1 in fishes: the liver and beyond. Am Zool 2000; 40: 259-268.
16. Richards MP, McMurtry JP. The avian proglucagon system. Gen Comp Endocrinol 2009; 163: 39-46.
17. Sarkar S, Subhedar N. Glucagon-like inmunoreactivity in the forebrain and pituitary of the teleost, Clarias batrachus (Linn.). Gen Comp Endocrinol 2001; 121: 23-31.
18. Cheung R, Andrews PC, Plisetskaya EM, Youson JH. Immunoreactivity to peptides belonging to the pancreatic polypeptide family (NPY, aPY, PP, PYY) and to glucagon-like peptide in the endocrine pancreas and anterior intestine of adult lampreys, Petromyzon marinus: an immunohistochemical study. Gen Comp Endocrinol 1991; 81: 51-63.
19. Polakof S, Alvarez R, Soengas JL. Gut glucose metabolism in rainbow trout: implications in glucose homeostasis and glucosensing capacity. Am J Physiol Regul Integr Comp Physiol 2010; 299: R19-R32.
20. Sundby A, Eliassen K, Blom AK, Asgard T. Plasma insulin, glucagon, glucagon-like peptide and glucose levels in response to feeding, starvation and life long restricted feed ration in salmonids. Fish Physiol Biochem 1991; 9: 253-259.
21. Plisetskaya EM, Ottolenghi C, Sheridan MA, Mommsen TP, Gorbman A. Metabolic effects of salmon glucagon and glucagon-like peptide in coho and chinook salmon. Gen Comp Endocrinol 1989; 73: 205-216.
22. Mommsen TP, Moon TW. Metabolic response of teleost hepatocytes to glucagon-like peptide and glucagon. J Endocrinol 1990; 126: 109-118.
23. Silverstein JT, Bondareva VM, Leonard JB, Plisetskaya EM. Neuropeptide regulation of feeding in catfish, Ictalurus punctatus: a role for glucagon-like peptide-1 (GLP-1)? Comp Biochem Physiol B Biochem Mol Biol 2001; 129: 623-631.
24. 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 2007; 292: R1657-R1666.
25. Conde-Sieira M, Agulleiro MJ, Aguilar AJ, Miguez JM, Cerda-Reverter JM, Soengas JL. Effect of different glycaemic conditions on gene expression of neuropeptides involved in control of food intake in rainbow trout; interaction with stress. J Exp Biol 2010; 213: 3858-3865.
26. Plisetskaya EM, Duguay S, Schrgibman MP, Scanes CE, Pang P. Pancreatic Hormones and Metabolism in Ectotherm Vertebrates: Current Views. New York, NY: Academic Press, 1993: 266-287.
27. Burnstock G. The innervation of the gut of the brown trout Salmo trutta. Q J Microsc Sci 1959; 100: 199-220.
28. Lutz TA, Althaus J, Rossi R, Scharrer E. Anorectic effect of amylin is not transmitted by capsaicin-sensitive nerve fibers. Am J Physiol Regul Integr Comp Physiol 1998; 274: R1777-R1782.
29. Polakof S, Soengas JL. Involvement of lactate in glucose metabolism and glucosensing function in selected tissues of rainbow trout. J Exp Biol 2008; 211: 1075-1086.
30. Keppler D, Decker K, Bergmeyer HU. Glycogen determination with amyloglucosidase. Methods of Enzymatic Analysis. New York, NY: Academic Press, 1974: 1127-1131.
31. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem 1985; 150: 76-85.
32. Polakof S, Míguez JM, Soengas JL. Dietary carbohydrates induce changes in glucosensing capacity and food intake of rainbow trout. Am J Physiol Regul Integr Comp Physiol 2008; 295: R478-R489.
33. Polakof S, Panserat S, Plagnes-Juan E, Soengas JL. Altered dietary carbohydrates significantly affect gene expression of the major glucosensing components in Brockmann bodies and hypothalamus of rainbow trout. Am J Physiol Regul Integr Comp Physiol 2008; 295: R1077-R1088.
34. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.
35. Yeung CM, Mojsov S, Mok PY, Chow BK. Isolation and structure-function studies of a glucagon-like peptide 1 receptor from goldfish Carassius auratus: identification of three charged residues in extracellular domains critical for receptor function. Endocrinology 2002; 143: 4646-4654.
36. Ottolenghi C, Puviani AC, Gavioli ME, Fabbri E, Brighenti L, Plisetskaya EM. Glycogenolytic action of glucagon-family peptides and epinephrine on catfish hepatocytes. Fish Physiol Biochem 1989; 6: 387-394.
37. Tachibana T, Oikawa D, Adachi N, Boswell T, Furuse M. Intracerebroventricular injection of glucagon-like peptide-1 changes lipid metabolism in chicks. Comp Biochem Physiol A Mol Integr Physiol 2007; 147: 1104-1108.
38. Larsen PJ, Tang-Christensen M, Jessop DS. Central administration of glucagon-like peptide-1 activates hypothalamic neuroendocrine neurons in the rat. Endocrinology 1997; 138: 4445-4455.
39. Perez-Tilve D, Gonzalez-Matias L, Aulinger BA, Alvarez-Crespo M, Gil-Lozano M, Alvarez E, Andrade-Olivie AM, Tschop MH, D'Alessio DA, Mallo F. Exendin-4 increases blood glucose levels acutely in rats by activation of the sympathetic nervous system. Am J of Physiol Endocrinol Metab 2010; 298: e1088-1096.
40. Christel CM, Denardo DF. Absence of exendin-4 effects on postprandial glucose and lipids in the Gila monster, Heloderma suspectum. J Comp Physiol B Biochem Syst Environ Physiol 2007; 177: 129-134.
41. Esteban FJ, Jimenez A, Barroso JB, Pedrosa JA, del Moral ML, Rodrigo J, Peinado MA. The innervation of rainbow trout (Oncorhynchus mykiss) liver: protein gene product 9.5 and neuronal nitric oxide synthase immunoreactivities. J Anat 1998; 193: 241-249.
42. Moon TW. Hormones and fish hepatocyte metabolism: "the good, the bad and the ugly!". Comp Biochem Physiol B Biochem Mol Biol 2004; 139: 335-345.
43. Dockray GJ. The versatility of the vagus. Physiol Behav 2009; 97: 531-536.
44. Nakabayashi H, Nishizawa M, Nakagawa A, Takeda R, Niijima A. Vagal hepatopancreatic reflex effect evoked by intraportal appearance of tGLP-1. Am J Physiol Endocrinol Metab 1996; 271: E808-E813.
45. Soengas JL, Polakof S, Chen X, Sangiao-Alvarellos S, Moon TW. Glucokinase and hexokinase expression and activities in rainbow trout tissues: changes with food deprivation and refeeding. Am J Physiol Regul Integr Comp Physiol 2006; 291: R810-R821.
46. Levin BE, Routh VH, Kang L, Sanders NM, Dunn-Meynell AA. Neuronal glucosensing. What do we know after 50years? Diabetes 2004; 53: 2521-2528.
47. Heijboer AC, Pijl H, Van den Hoek AM, Havekes LM, Romijn JA, Corssmit EP. Gut-brain axis: regulation of glucose metabolism. J Neuroendocrinol 2006; 18: 883-894.
48. Furuse M, Matsumoto M, Okumura J, Sugahara K, Hasegawa S. Intracerebroventricular injection of mammalian and chicken glucagon-like peptide-1 inhibits food intake of the neonatal chick. Brain Res 1997; 755: 167-169.
49. Sandoval DA, Bagnol D, Woods SC, D'Alessio DA, Seeley RJ. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008; 57: 2046-2054.
50. Grill HJ, Hayes MR. The nucleus tractus solitarius: a portal for visceral afferent signal processing, energy status assessment and integration of their combined effects on food intake. Int J Obes 2009; 33: S11-S15.
51. Irwin DM, Wong K. Evolution of new hormone function: loss and gain of a receptor. J Hered 2005; 96: 205-211.
52. Polakof S, Skiba-Cassy S, Choubert G, Panserat S. Insulin-induced hypoglycaemia is co-ordinately regulated by liver and muscle during acute and chronic insulin stimulation in rainbow trout (Oncorhynchus mykiss). J Exp Biol 2010; 213: 1443-1452.
53. Sandoval D. CNS GLP-1 regulation of peripheral glucose homeostasis. Physiol Behav 2008; 94: 670-674.