Ghrelin increases food intake, swimming activity and growth in juvenile brown trout (Salmo trutta)

Physiology and Behavior

Volumn 124, Issue , 2014, Pages 15-22

  Tinoco, Ana B ^b   Näslund, Joacim ^a   Delgado, María J ^b   de Pedro, Nuria ^b   Johnsson, Jörgen I ^a   Jönsson, Elisabeth ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Aggression; Food intake; Ghrelin; Growth; Salmo trutta; Swimming activity

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; DOPAMINE; GHRELIN; MESSENGER RNA; NEUROPEPTIDE Y; NORADRENALIN; SEROTONIN; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; BIOGENIC AMINE; DRUG IMPLANT;

AGGRESSION; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BODY GROWTH; BODY WEIGHT; BRAIN STEM; BROWN TROUT; CONTROLLED STUDY; ENZYME ACTIVITY; FOOD INTAKE; FORAGING; GROWTH ACCELERATION; GROWTH RATE; HYPOTHALAMUS; IMPLANTATION; JUVENILE; LIPID ANALYSIS; LIPID METABOLISM; LIPID STORAGE; LIVER; MOTIVATION; MUSCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SWIMMING; TELENCEPHALON; ANIMAL; BIOSYNTHESIS; BRAIN; DRUG EFFECTS; DRUG IMPLANT; EATING; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TROUT;

AGGRESSION; ANIMALS; BIOGENIC MONOAMINES; BODY WEIGHT; BRAIN; DRUG IMPLANTS; EATING; GHRELIN; LIPID METABOLISM; LIVER; MUSCLES; NEUROPEPTIDE Y; SWIMMING; TROUT;

EID: 84887792460     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.10.034     Document Type: Article

References (59)

1. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1994, 402:656-660.
2. Geelissen S.M., Beck I.M., Darras V.M., Kuhn E.R., Van der Geyten S. Distribution and regulation of chicken growth hormone secretagogue receptor isoforms. Gen Comp Endocrinol 2003, 134:167-174.
3. Chan C.B., Cheng C.H. Identification and functional characterization of two alternatively spliced growth hormone secretagogue receptor transcripts from the pituitary of black seabream Acanthopagrus schlegeli. Mol Cell Endocrinol 2004, 214:81-95.
4. Kaiya H., Mori T., Miyazato M., Kangawa K. Ghrelin receptor (GHS-R)-like receptor and its genomic organisation in rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol A 2009, 153:438-450.
5. Kaiya H., Miura T., Matsuda K., Miyazato M., Kangawa K. Two functional growth hormone secretagogue receptor (ghrelin receptor) type 1a and 2a in goldfish, Carassius auratus. Mol Cell Endocrinol 2010, 327:25-39.
6. Kaiya H., Kojima M., Hosoda H., Moriyama S., Takahashi A., Kawauchi H., et al. Peptide purification, complementary deoxyribonucleic acid (DNA) and genomic DNA cloning, and functional characterization of ghrelin in rainbow trout. Endocrinology 2003, 144:5215-5226.
7. Kaiya H., Kojima M., Hosoda H., Riley L.G., Hirano T., Grau E.G., et al. Amidated fish ghrelin: purification, cDNA cloning in the Japanese eel and its biological activity. J Endocrinol 2003, 176:415-423.
8. Murashita K., Kurokawa T., Nilsen T.O., Rönnestad I. Ghrelin, cholesystokinin, and peptide YY in Atlantic salmon (Salmo salar): molecular cloning and tissue expression. Gen Comp Endocrinol 2009, 160:223-235.
9. Unniappan S., Lin X., Cervini L., Rivier J., Kaiya H., Kangawa K., et al. Goldfish ghrelin: molecular characterization of the complementary deoxyribonucleic acid, partial gene structure and evidence for its stimulatory role in food intake. Endocrinology 2002, 143:4143-4146.
10. Kaiya H., Miyazato M., Kangawa K. Recent advances in the phylogenetic study of ghrelin. Peptides 2011, 32:2155-2174.
11. Kaiya H., Miyazato M., Kangawa K., Peter R.E., Unniappan S. Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp Biochem Physiol A 2008, 149:109-128.
12. Nakazato M., Murakami N., Date Y., Kojima M., Matsuo H., Kangawa K., et al. A role for ghrelin in the central regulation of feeding. Nature 2001, 409:194-198.
13. Tschöp M., Smiley D.L., Heiman M.L. Ghrelin induces adiposity in rodents. Nature 2000, 407:908-913.
14. Jerlhag E., Egecioglu E., Dickson S.L., Andersson M., Svensson L., Engel J.A. Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol 2006, 11:45-54.
15. Perelló M., Sakata I., Birnbaum S., Chuang J.C., Osborne-Lawrence S., Rovinsky S.A., et al. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry 2010, 67:880-886.
16. Carlini V.P., Monzon M.E., Varas M.M., Cragnolini A.B., Schioth H.B., Scimonelli T.N., et al. Ghrelin increases anxiety-like behavior and memory retention in rats. Biochem Biophys Res Commun 2002, 299:739-743.
17. Kamegai J., Tamura H., Shimizu T., Ishii S., Sugihara H., Wakabayashi I. Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti related protein mRNA levels and body weight in rats. Diabetes 2001, 50:2438-2443.
18. Seoane L.M., Lopez M., Tovar S., Casanueva F.F., Senaris R., Dieguez C. Agouti related peptide, neuropeptide Y and somatostatin-producing neurons are targets for ghrelin actions in the rat hypothalamus. Endocrinology 2003, 144:544-551.
19. Picha M.E., Strom C.N., Riley L.G., Walker A.A., Won E.T., Johnstone W.M., et al. Plasma ghrelin and growth hormone regulation in response to metabolic state in hybrid striped bass: effects of feeding, ghrelin and insulin-like growth factor-I on in vivo and in vitro GH secretion. Gen Comp Endocrinol 2009, 161:365-372.
20. Ran X., Li W., Lin H. Rat ghrelin stimulates GH release and GH mRNA expression in the pituitary of orange-spotted grouper, Epinephelus coioides. Fish Physiol Biochem 2004, 30:95-102.
21. Miura T., Maruyama K., Shimakura S., Kaiya H., Uchiyama M., Kangawa K., et al. Regulation of food intake in the goldfish by interaction between ghrelin and orexin. Peptides 2007, 28:1207-1213.
22. Miura T., Maruyama K., Shimakura S., Kaiya H., Uchiyama M., Kangawa K., et al. Neuropeptide Y mediates ghrelin-induced feeding in the goldfish, Carassius auratus. Neurosci Lett 2006, 407:279-283.
23. Riley L.G., Fox B.K., Kaiya H., Hirano T., Grau E.G. Long-term treatment of ghrelin stimulates feeding, fat deposition, and alters the GH/IGF-I axis in the tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 2005, 142:234-240.
24. Unniappan S., Canosa L.F., Peter R.E. Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 2004, 79:100-108.
25. Gao Y.J., Tian L.X., Yang H.J., Liang G.Y., Yue Y.R., Liu Y.J. The influence of ghrelin and des-ghrelin on feed intake, growth performance and hypothalamic NPY mRNA expression of grouper Epinephelus coioides. Aquaculture 2012, 364-365:19-24.
26. Jönsson E., Kaiya H., Björnsson B.Th. Ghrelin decreases food intake in juvenile rainbow trout (Oncorhynchus mykiss) through the central anorexigenic corticotropin-releasing factor system. Gen Comp Endocrinol 2010, 166:39-46.
27. Shepherd B.S., Johnson J.K., Silverstein J.T., Parhar I.S., Vijayan M.M., McGuire A., et al. Endocrine and orexigenic actions of growth hormone secretagogues in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 2007, 146:390-399.
28. Saito E.S., Kaiya H., Tachibana T., Tomonaga S., Denbow D.M., Kangawa K., et al. Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chicks. Regul Pept 2005, 125:201-208.
29. Jönsson E., Forsman A., Einarsdottir I.E., Kaiya H., Ruohonen K., Björnsson B.Th. Plasma ghrelin levels in rainbow trout in response to fasting, feeding and food composition, and effects of ghrelin on voluntary food intake. Comp Biochem Physiol A 2007, 147:1116-1124.
30. Kitazawa T., Kaiya H., Taneike T. Contractile effect of ghrelin-related peptides on the chicken gastrointestinal tract in vitro. Peptides 2007, 28:617-624.
31. Olsson C., Holbrook J.D., Bompadre G., Jönsson E., Hoyle C.H.V., Sanger G.J., et al. Identification of genes for the ghrelin and motilin receptors and a novel related gene in fish, and stimulation of intestinal motility in zebrafish (Danio rerio) by ghrelin and motilin. Gen Comp Endocrinol 2008, 155:217-226.
32. Jerlhag E. Systemic administration of ghrelin induces conditioned place preference and stimulates accumbal dopamine. Addict Biol 2008, 13:358-363.
33. Tang-Christensen M., Vrang N., Ortmann S., Bidlingmaier M., Horvath T.L., Tschöp M. Central administration of ghrelin and agouti-related protein (83-132) increases food intake and decreases spontaneous locomotor activity in rats. Endocrinology 2004, 145:4645-4652.
34. Yahashi S., Kang K.S., Kaiya H., Matsuda K. GHRP-6 mimics ghrelin-induced stimulation of food intake and suppression of locomotor activity in goldfish. Peptides 2012, 34:324-328.
35. Mason S.T. Catecholamines and behaviour 1984, Cambridge University Press, Cambridge.
36. Winberg S., Nilsson G. Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp Biochem Physiol C 1993, 106:597-614.
37. Kang K.S., Yahashi S., Matsuda K. The effects of ghrelin on energy balance and psychomotor activity in a goldfish model: an overview. Int J Pept 2011, 2011:171034.
38. Johansson V., Winberg S., Jönsson E., Hall D., Björnsson B.Th. Peripherally administered growth hormone increases brain dopaminergic activity and swimming in rainbow trout. Horm Behav 2004, 46:436-443.
39. Jönsson E., Johansson V., Björnsson B.Th., Winberg S. Central nervous system actions of growth hormone on brain monoamine levels and behavior of juvenile rainbow trout. Horm Behav 2003, 43:367-374.
40. Johnsson J.I., Winberg S., Sloman K.A. Social interactions. Behav Physiol Fish 2006, vol. 24:151-196. Elsevier Academic Press, New York. K.A. Sloman, R.W. Wilson, S. Balshine (Eds.).
41. Jönsson E., Björnsson B.Th. Physiological functions of growth hormone in fish with special reference to its influence on behaviour. Fish Sci 2002, 68:742-774.
42. Kadri S., Thorpe J.E., Metcalfe N.B. Anorexia in one-sea-winter Atlantic salmon (Salmo salar) during summer, associated with sexual maturation. Aquaculture 1997, 151:405-409.
43. Metcalfe N.B., Thorpe J.E. Anorexia and defended energy levels in overwintering juvenile salmon. J Anim Ecol 1992, 61:175-181.
44. Johnsson J.I., Nöbbelin F., Bohlin T. Territorial competition among wild brown trout fry: effects of ownership and body size. J Fish Biol 1999, 54:469-472.
45. Jenkins T.M. Social structure position choice and microdistribution of two trout species (Salmo trutta and Salmo gairdneri) resident in mountain streams. Anim Behav Monogr 1969, 2:57-123.
46. Kalleberg H. Observations in a stream tank of territoriality and competition in juvenile salmon and trout (Salmo salar L. and S. trutta L.). Rept Instr Freshw Res Drottningholm 1958, 39:55-98.
47. Brockmark S., Adriaenssens B., Johnsson J.I. Less is more: density influences the development of behavioural life skills in trout. Proc R Soc B 2010, 277:3035-3043.
48. Schwartz D.M., Wolins N.E. A simple and rapid method to assay triacylglycerol in cells and tissues. J Lipid Res 2007, 48:2514-2520.
49. Neregård L., Sundt-Hansen L., Björnsson B.Th., Johnsson J.I. Growth hormone affects behaviour of wild brown trout Salmo trutta in territorial owner-intruder conflicts. J Fish Biol 2008, 73:2341-2351.
50. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J Biol Chem 1951, 193:265-275.
51. Tinoco A.B., Nisembaum L.G., Isorna E., Delgado M.J., de Pedro N. Leptins and leptin receptor expression in the goldfish (Carassius auratus). Regulation by food intake and fasting/overfeeding conditions. Peptides 2012, 34:329-335.
52. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
53. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
54. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(δδC(T)) method. Methods 2001, 25:402-408.
55. Keen-Rhinehart E., Bartness T.J. Peripheral ghrelin injections stimulate food intake, foraging, and food hoarding in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 2004, 288:R716-R722.
56. Hanson K.C., Abizaid A., Cooke S.J. Causes and consequences of voluntary anorexia during the parental care period of wild male smallmouth bass (Micropterus dolomieu). Horm Behav 2009, 56:5039.
57. Jönsson E., Johansson I.J., Björnsson B.Th. Growth hormone increases predation exposure of rainbow trout. Proc R Soc Lond B Biol Sci 1996, 263:647-651.
58. Jönsson E., Johnsson J.I., Björnsson B.Th. Growth hormone increases aggressive behavior in juvenile rainbow trout. Horm Behav 1998, 33:9-15.
59. Date Y., Murakami N., Toshinai K., Matsukura S., Niijima A., Matsuo H., et al. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 2002, 123:1120-1128.