Immunohistochemical and immunological detection of ghrelin and leptin in rainbow trout Oncorhynchus mykiss and murray cod Maccullochella peelii peelii as affected by different dietary fatty acids

Microscopy Research and Technique

Volumn 75, Issue 6, 2012, Pages 771-780

  Varricchio, Ettore ^a   Russo, Finizia ^a   Coccia, Elena ^a   Turchini, Giovanni ^b   Francis, David ^c   De Girolamo, Paolo ^d   Paolucci, Marina ^a  

^a Geological and Environmental Sciences   (Italy)

^b DEAKIN UNIVERSITY   (Australia)

^c AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Diets; Feeding; Fish oil; Gastrointestinal tract; Peptides; Secreting cells; Teleosts

Indexed keywords

BLOOD; CYTOLOGY; FISH; OLIVE OIL; PALM OIL; SUNFLOWER OIL;

CELL-BE; CELL/B.E; CELL/BE; FISH OIL; GASTROINTESTINAL TRACT; GHRELIN; LEPTINS; RAINBOW TROUT; SECRETING CELL; TELEOST;

CELLS;

HELIANTHUS; MACCULLOCHELLA PEELII PEELII; ONCORHYNCHUS MYKISS; TELEOSTEI;

EID: 84861348204     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.21124     Document Type: Article

References (73)

1. Anubhuti AS. 2006. The role of neuropeptides in appetite regulation and obesity-Review. Neuropeptide 40: 375-401.
2. Arcamone N, Neglia S, Gargiulo G, Esposito V, Varricchio E, Battaglini P, De Girolamo P, Russo F. 2009. Distribution of ghrelin peptide in the gastrointestinal tract of stomachless and stomach-containing teleosts. Microsc Res Tech 72: 525-533.
3. Bjørbæk C, Kahn BB. 2004. Leptin signalling in the central nervous system and in the periphery. Recent Prog Horm Res 59: 305-331.
4. Boguszewski CL, Paz-Filho G, Velloso LA. 2010. Neuroendocrine body weight regulation: Integration between fat tissue, gastrointestinal tract, and the brain. Endokrynol Pol 61: 194-206.
5. Bosi G, Di Giancamillo A, Arrighi S, Domeneghini C. 2004. An immunohistochemical study on the neuroendocrine system in the alimentary canal of the brown trout, Salmo trutta, L., 1758. Gen Comp Endocrinol 138: 166-181.
6. Brennan AM, Mantzoros CS. 2006. Drug Insight: The role of leptin in human physiology and pathophysiology-Emerging clinical applications. Nat Clin Pract Endocrinol Metab 2: 318-327.
7. Breves JP, Veillette PA, Specker JL. 2009. Ghrelin in the summer flounder: Immunolocalization to the gastric glands and action on plasma cortisol levels. Comp Biochem Physiol A Mol Integr Physiol 152: 268-272.
8. Brown PB, Hart SD. 2010. Soybean oil and other n-6 polyunsaturated fatty acid-rich vegetable oils. In: Turchini GM, Ng WK, Tocher DR, editors. Fish oil replacement and alternative lipid sources in aquaculture feeds. Boca Raton, FL, USA: CRC Press, Taylor & Francis Group. pp. 133-160.
9. Chan CB, Cheng CHK. 2004. Identification and functional characterization of two alternatively spliced growth hormone secretagogue receptor transcripts from the pituitary of black seabream Acanthopagrus schlegeli. Mol Cell Endocrinol 214: 81-95.
10. Chen X, Li D, Yin J, Ding Y, Zhang H, Zhang H, Yi G. 2006. Regulation of dietary energy level and oil source on leptin and its long form receptor mRNA expression of the adipose tissues in growing pigs. Domest Anim Endocrinol 31: 269-283.
11. Cummings DE, Foster KE. 2003. Ghrelin-leptin tango in body-weight regulation. Gastroenterology 124: 1532-1535.
12. Date Y, Nakazato M, Hashiguchi S, Dezaki K, Mondal MS, Hosoda H, Kojima M, Kangawa K, Arima T, Matsuo H, Yada T, Matsukura S. 2002. Ghrelin is present in pancreatic alpha-cells of humans and rats and stimulates insulin secretion. Diabetes 51: 124-129.
13. Dziedzic B, Szemraj J, Bartkowiak J, Walczewska A. 2007. Various dietary fats differentially change the gene expression of neuropeptides involved in body weight regulation in rats. J Neuroendocrinol 19: 364-373.
14. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, Flier JS, Saper CB, Elmquist JK. 1999. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23: 775-786.
15. Feltrin KL, Patterson M, Ghatei MA, Bloom SR, Meyer JH, Horowitz M, Feinle-Bisset C. 2006. Effect of fatty acid chain length on suppression of ghrelin and stimulation of PYY, GLP-2 and PP secretion in healthy men. Peptides 27: 1638-1643.
16. Foster-Schubert KE, McTiernan A, Frayo RS, Schwartz RS, Rajan KB, Yasui Y, Tworoger SS, Cummings DE. 2005. Human plasma ghrelin levels increase during a one-year exercise program. J Clin Endocrinol Metab 90: 820-825.
17. Friedman JM, Halaas JL. 1998. Leptin and the regulation of body weight in mammals. Nature 395: 763-770.
18. Frøiland E, Murashita K, Jørgensen EH, Kurokawa T. 2010. Leptin and ghrelin in anadromous Arctic charr: Cloning and change in expressions during a seasonal feeding cycle. Gen Comp Endocrinol 165: 136-143.
19. Gaigé S, Abysique A, Bouvier M. 2003. Effects of leptin on cat intestinal motility. J Phisiol 546: 267-277.
20. Ganga R, Bell JG, Montero D, Robaina L, Caballero MJ, Izquierdo MS. 2005. Effect of dietary lipids on plasma fatty acid profiles and prostaglandin and leptin production in gilthead seabream (Sparus aurata). Comp Biochem Physiol B Biochem Mol Biol 142: 410-418.
21. Gormsen LC, Gjedsted J, Gjedde S, Vestergaard ET, Christiansen JS, Jorgensen JO, Nielsen S. 2006. Free fatty acids decrease circulating ghrelin concentrations in humans. Eur J Endocrinol 154: 667-673.
22. Guilmeau S, Buyse M, Tsocas A, Laigneau JP, Bado A. 2003. Duodenal leptin stimulates cholecystokinin secretion: Evidence of a positive leptin-cholecystokinin feedback loop. Diabetes 52: 1664-1672.
23. Hynes GR, Heshka J, Chadee K, Jones PJ. 2003. Effects of dietary fat type and energy restriction on adipose tissue fatty acid composition and leptin production in rats. J Lipid Res 44: 893-901.
24. Jobling M, Larsen AV, Andreassen B, Olsen RL. 2002. Adiposity and growth of post-smolt Atlantic salmon Salmo salar L. Aquaculture Res 33: 533-541.
25. Johnson RM, Johnson TM, Londraville RL. 2000. Evidence for leptin expression in fishes. J Exp Zool 286: 718-724.
26. Johnsson E, Forsman A, Einarsdottir IE, Kaiya H, Ruohonen K, Bjornsson BT. 2007. 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 Mol Integr Physiol 147: 1116-1124.
27. Kageyama H, Takenoya F, Shiba K, Shioda S. 2010. Neuronal circuits involving ghrelin in the hypothalamus-mediated regulation of feeding. Neuropeptides 44: 133-138.
28. Kaiya H, Kojima M, Hosoda H, Riley LG, Hirano T, Grau EG, Kangawa K. 2003a. Amidated fish ghrelin: Purification, cDNA cloning in the Japanese eel and its biological activity. J Endocrinol 176: 415-423.
29. Kaiya H, Kojima M, Hosoda H, Moriyama S, Takahashi A, Kawauchi H, Kangawa K. 2003b. Peptide purification, complementary deoxyribonucleic acid (DNA) and genomic DNA cloning, and functional characterization of ghrelin in rainbow trout. Endocrinology 144: 5215-5226.
30. Kaiya H, Kojima M, Hosoda H, Riley LG, Hirano T, Grau EG, Kangawa K. 2003c. Identification of tilapia ghrelin and its effects on growth hormone and prolactin release in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol B Biochem Mol Biol 135: 421-429.
31. Kaiya H, Small BC, Bilodeau AL, Shepherd BS, Kojima M, Hosoda H, Kangawa K. 2005. Purification, cDNA cloning, and characterization of ghrelin in channel catfish, Ictalurus punctatus. Gen Comp Endocrinol 143: 201-210.
32. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. 1999. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402: 656-660.
33. Kurokawa T, Murashita K. 2009. Genomic characterization of multiple leptin genes and a leptin receptor gene in the Japanese medaka, Oryzias latipes. Gen Comp Endocrinol 161: 229-237.
34. Kurokawa T, Uji S, Suzuki T. 2005. Identification of cDNA coding for a homologue to mammalian leptin from pufferfish, Takifugu rubripes. Peptides 26: 745-750.
35. Liu Q, Chen Y, Copeland D, Ball H, Duff RJ, Rockich B, Londraville RL. 2010. Expression of leptin receptor gene in developing and adult zebrafish. Gen Comp Endocrinol 166: 346-355.
36. Londraville RL, Duvall CS. 2002. Murine leptin injections increase intracellular fatty acid binding protein in green sunfish (Lepomis cyanellus). Gen Comp Endocrinol 129: 56-62.
37. Lostao MP, Urdaneta E, Martínez-Ansó E, Barber A, Martínez JA. 1998. Presence of leptin receptor in rat small intestine and leptin effect on sugar absorption. FEBS Lett 423: 302-306.
38. Manning AJ, Murray HM, Gallant JW, Matsuoka MP, Radford E, Douglas SE. 2008. Ontogenetic and tissue-specific expression of preproghrelin in the Atlantic halibut, Hippoglossus hippoglossus. J Endocrinol 196: 181-192.
39. Margetic S, Gazzola C, Pegg GG, Hill RA. 2002. Leptin: A review of its peripheral actions and interactions. Int J Obes Relat Metab Disord 26: 1407-1433.
40. McCormick SD. 2009. Evolution of the hormonal control of animal performance: insights from the seaward migration of salmon. Integr Comp Biol 49: 408-422.
41. Masuzaki H, Ogawa Y, Hosoda K, Kawada T, Fushiki T, Nakao K. 1995. Augmented expression of the obese gene in the adipose tissue from rats fed high-fat diet. Biochem Biophys Res Commun 216: 355-359.
42. Matsuda K, Kang KS, Sakashita A, Yahashi S, Vaudry H. 2011. Behavioral effect of neuropeptides related to feeding regulation in fish. Ann NY Acad Sci 1220: 117-126.
43. Morton NM, Emilsson V, Liu YL, Cawthorne MA 1998. Leptin action in intestinal cells. J Biol Chem 273: 26194-26201.
44. Murashita K, Uji S, Yamamoto T, Rønnestad I, Kurokawa T. 2008. Production of recombinant leptin and its effects on food intake in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 150: 377-384.
45. Muruzabal FJ, Frühbeck G, Gomez-Ambrosi J, Archanco M, Burrell MA. 2002. Immunocytochemical detection of leptin in non-mammalian vertebrate stomach. Gen Comp Endocrinol 128: 149-152.
46. Näslund E, Hellström PM. 2007. Appetite signalling: From gut peptides and enteric nerves to brain. Physiol Behav 92: 256-262.
47. Nishi Y, Hiejima H, Hosoda H, Kaiya H, Mori K, Fukue Y, Yanase T. 2005. Ingested medium-chain fatty acids are directly utilized for the acyl modification of ghrelin. Endocrinology 146: 2255-2264.
48. Nogueiras R, Tschöp MH, Zigman JM. 2008. Central nervous system regulation of energy metabolism: Ghrelin versus leptin. Ann NY Acad Sci 1126: 14-19.
49. Olsson C, Holbrook JD, Bompadre G, Jönsson E, Hoyle CH, Sanger GJ, Holmgren S, Andrews PL. 2008. 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 155: 217-226.
50. Overduin J, Frayo RS, Grill HJ, Kaplan JM, Cummings DE. 2005. Role of the duodenum and macronutrient type in ghrelin regulation. Endocrinology 146: 845-850.
51. Parhar IS, Sato H, Sakuma Y. 2003. Ghrelin gene in cichlid fish is modulated by sex and development. Biochem Biophys Res Commun 305: 169-175.
52. Pearson PY, O'Connor DM, Schwartz MZ. 2001. Novel effect of leptin on small intestine adaptation. J Surg Res 97: 192-195.
53. Peyron-Caso E, Taverna M, Guerre-Millo M, Véronèse A, Pacher N, Slama G, Rizkalla SW. 2002. Dietary (n-3) polyunsaturated fatty acids up-regulate plasma leptin in insulin-resistant rats. J Nutr 132: 2235-2240.
54. Picó C, Sánchez J, Oliver P, Palou A. 2002. Leptin production by the stomach is up-regulated in obese (fa/fa) Zucker rats. Obes Res 10: 932-938.
55. Reichardt F, Krueger D, Schemann M. 2011. Leptin excites enteric neurons of guinea-pig submucous and myenteric plexus. Neurogastroenterol Motil 128: 149-152.
56. Reseland JE, Haugen F, Hollung K, Solvoll K, Halvorsen B, Brude IR, Nenseter MS, Christiansen EN, Drevon CA. 2001. Reduction of leptin gene expression by dietary polyunsaturated fatty acids. J Lipid Res 42: 743-750.
57. Rønnestad I, Nilsen TO, Murashita K, Angotzi AR, Gamst Moen AG, Stefansson SO, Kling P, Thrandur Björnsson B, Kurokawa T. 2010. Leptin and leptin receptor genes in Atlantic salmon: Cloning, phylogeny, tissue distribution and expression correlated to long-term feeding status. Gen Comp Endocrinol 168: 55-70.
58. Rossi AS, Lombardo YB, Lacorte JM, Chicco AG, Rouault C, Slama G, Rizkalla SW. 2005. Dietary fish oil positively regulates plasma leptin and adiponectin levels in sucrose-fed, insulin-resistant rats. Am J Physiol Regul Integr Comp Physiol 289: 486-495.
59. Russo F, De Girolamo P, Neglia S, Gargiulo A, Arcamone N, Gargiulo G, Varricchio E. 2011. Immunohistochemical and immunochemical characterization of the distribution of leptin-like proteins in the gastroenteric tract of two teleosts (Dicentrarchus labrax and Carassius auratus L.) with different feeding habits. Microsc Res Technol 78: 714-719.
60. Sakata I, Mori T, Kaya H, Yamazaki M, Kangawa K, Inoue K, Sakai T. 2004. Localization of ghrelin-producing cells in the stomach of the rainbow trout (Oncorhynchus mykiss). Zool Sci 21: 757-762.
61. Solcia E, Rindi G, Buffa R, Fiocca R, Cappella C. 2000. Gastric endocrine cells: Types, function and growth. Regul Pept 93: 31-35.
62. Terova G, Rimoldi S, Bernardini G, Gornati R, Saroglia M. 2008. Sea bass ghrelin: Molecular cloning and mRNA quantification during fasting and refeeding. Gen Comp Endocrinol 155: 341-351.
63. Turchini GM, Paolucci M. 2010. Leptin and lipid metabolism in fish. In: Paolucci M, editor. Leptin in non-mammalian vertebrates. Transworld Reasearch Network: Kerala, India. pp. 151-172.
64. Turchini GM, Bente E, Torstensen BE, Ng W-K. 2009. Fish oil replacement in finfish nutrition. Rev Aquaculture 1: 10-57.
65. Turchini GM, Francis DS, Senadheera SPSD, Thanuthong T, De Silva SS. 2011. Fish oil replacement with different vegetable oils in Murray cod: Evidence of an "omega-3 sparing effect" by other dietary fatty acids. Aquaculture 315: 250-259.
66. Unniappan S, Peter RE. 2005. Structure, distribution and physiological functions of ghrelin in fish. Comp Biochem Physiol A Mol Integr Physiol 140: 396-408.
67. Unniappan S, Lin X, Cervini L, Rivier J, Kaiya H, Kangawa K, Peter RE. 2002. Goldfish ghrelin: molecular characterization of the complementary deoxyribonucleic acid, partial gene structure and evidence for its stimulatory role in food intake. Endocrinology 143: 4143-4146.
68. Unniappan S, Canosa LF, Peter RE. 2004. 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 79: 100-108.
69. Volkoff H, Canosa LF, Unniappan S, Cerdá-Reverter JM, Bernier NJ, Kelly SP, Peter RE. 2005. Neuropeptides and the control of food intake in fish. Gen Comp Endocrinol 142: 3-19.
70. Williams DL, Grill HJ, Cummings DE, Kaplan JM. 2003. Vagotomy dissociates short- and long-term controls of circulating ghrelin. Endocrinology 144: 5184-5187.
71. Yarandi SS, Hebbar G, Sauer CG, Cole CR, Ziegler TR. 2011. Diverse roles of leptin in the gastrointestinal tract: Modulation of motility, absorption, growth, and inflammation. Nutrition 27: 269-275.
72. Yeung CM, Chan CB, Woo NY, Cheng CH. 2006. Seabream ghrelin: cDNA cloning, genomic organization and promoter studies. J Endocrinol 189: 365-379.
73. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. 1994. Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432.