Cite this paper:
LI Shengjie, HAN Linqiang, BAI Junjie, MA Dongmei, QUAN Yingchun, FAN Jiajia, JIANG Peng, YU Lingyun. Cloning, tissue distribution and effects of fasting on pituitary adenylate cyclase-activating polypeptide in largemouth bass[J]. Journal of Oceanology and Limnology, 2015, 33(2): 328-338

Cloning, tissue distribution and effects of fasting on pituitary adenylate cyclase-activating polypeptide in largemouth bass

LI Shengjie, HAN Linqiang, BAI Junjie, MA Dongmei, QUAN Yingchun, FAN Jiajia, JIANG Peng, YU Lingyun
Pearl River Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, China Ministry of Agriculture, Guangzhou 510380, China
Abstract:
Pituitary adenylate cyclase activating polypeptide (PACAP) has a wide range of biological functions. We cloned the full-length cDNAs encoding PACAP and PACAP-related peptide (PRP) from the brain of largemouth bass (Micropterus salmoides) and used real-time quantitative PCR to detect PRP-PACAP mRNA expression. The PRP-PACAP cDNA has two variants expressed via alternative splicing: a long form, which encodes both PRP and PACAP, and a short form, which encodes only PACAP. Sequence analysis results are consistent with a higher conservation of PACAP than PRP peptide sequences. The expression of PACAP-long and PACAP-short transcripts was highest in the forebrain, followed by the medulla, midbrain, pituitary, stomach, cerebellum, intestine, and kidney; however, these transcripts were either absent or were weakly expressed in the muscle, spleen, gill, heart, fatty tissue, and liver. The level of PACAP-short transcript expression was significantly higher than expression of the long transcript in the forebrain, cerebella, pituitary and intestine, but lower than that of the long transcript in the stomach. PACAP-long and PACAP-short transcripts were first detected at the blastula stage of embryogenesis, and the level of expression increased markedly between the muscular contraction stage and 3 d post hatch (dph). The expression of PACAP-long and PACAP-short transcripts decreased significantly in the brain following 4 d fasting compared with the control diet group. The down-regulation effect was enhanced as fasting continued. Conversely, expression levels increased significantly after 3 d of re-feeding. Our results suggest that PRP-PACAP acts as an important factor in appetite regulation in largemouth bass.
Key words:    pituitary adenylate cyclase activating polypeptide (PACAP)|PACAP-related peptide|largemouth bass|gene expression|fasting   
Received: 2014-05-05   Revised: 2014-06-28
Tools
PDF (465 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LI Shengjie
Articles by HAN Linqiang
Articles by BAI Junjie
Articles by MA Dongmei
Articles by QUAN Yingchun
Articles by FAN Jiajia
Articles by JIANG Peng
Articles by YU Lingyun
References:
Bai J, Li S, Deng G, Xie J. 2009. Status of aquaculture and breeding technology of largemouth bass in China. Scientific Fish Farming, (6): 15-16. (in Chinese)
Bai J, Lutz-Carrillo D J, Quan Y, Liang S. 2008. Taxonomic status and genetic diversity of cultured largemouth bass Micro pterus salmoides in China. Aquaculture, 278 (1-4): 27-30.
Cardoso J C R, Vieira F A, Gomes A S, Power D M. 2007. PACAP, VIP and their receptors in the metazoa: insights about the origin and evolution of the ligand-receptor pair. Peptides, 28 (9): 1 902-1 919.
Carpio Y, Lugo J M, León K, Morales R, Estrada M P. 2008. Novel function of recombinant pituitary adenylate cyclase-activating polypeptide as stimulator of innate immunity in African catfish (Clarias gariepinus) fry. Fish Shellfish Immun., 25 (4): 439-445.
Chance W T, Thompson H, Thomas I, Fischer J E. 1995. Anorectic and neurochemical effects of pituitary adenylate cyclase activating polypeptide in rats. Peptides, 16 (8): 1 511-1 516.
Chua Jr S C, Brown A W, Kim J, Hennessey K L, Leibel R L, Hirsch J. 1991. Food deprivation and hypothalamic neuropeptide gene expression: effects of strain background and the diabetes mutation. Mol. Brain Res., 11 (3): 291- 299.
Enes P, Panserat S, Kaushik S, Oliva-Teles A. 2009. Nutritional regulation of hepatic glucose metabolism in fi sh. Fish Physiol. Biochem., 35 (3): 519-539.
Holmberg A, Schwerte T, Pelster B, Holmgren S. 2004. Ontogeny of the gut motility control system in zebrafi sh Danio rerio embryos and larvae. J. Exp. Biol., 207 (23): 4 085-4 094.
Ji X S, Chen S L, Jiang Y L, Xu T J, Yang J F, Tian Y S. 2011. Growth differences and differential expression analysis of pituitary adenylate cyclase activating polypeptide (PACAP) and growth hormone-releasing hormone (GHRH) between the sexes in half-smooth tongue sole Cynoglossus semilaevis. Gen. Comp. Endocr., 170 (1): 99-109.
Jiang Y, Li W S, Xie J, Lin H R. 2003. Sequence and expression of a cDNA encoding both pituitary adenylate cyclase activating polypeptide and growth hormone-releasing hormone in grouper (Epinephelus coioides). Acta Biochimica et Biophysica Sinica, 35 (9): 864-872.
Jozsa R, Nemeth J, Tamas A, Hollosy T, Lubics A, Jakab B, Olah A, Lengvari I, Arimura A, Reglödi D. 2006. Shortterm fasting differentially alters PACAP and VIP levels in the brains of rat and chicken. Ann. NY Acad. Sci., 1070 (1): 354-358.
Kassahn K S, Dang V T, Wilkins S J, Perkins A C, Ragan M A. 2009. Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Res., 19 (8): 1 404-1 418.
Krueckl S L, Sherwood N M. 2001. Developmental expression, alternative splicing and gene copy number for the pituitary adenylate cyclase-activating polypeptide (PACAP) and growth hormone-releasing hormone (GRF) gene in rainbow trout. Mol. Cell. Endocrinol., 182 (1): 99-108.
Lee L T O, Siu F K Y, Tam J K V, Lau I T Y, Wong A O L, Lin M, Vaudry H, Chow B K C. 2007. Discovery of growth hormone-releasing hormones and receptors in nonmammalian vertebrates. P. Natl. Acad. Sci. USA, 104 (7): 2 133.
Lee L, Tam J, Chan D W, Chow B. 2009. Molecular cloning and mRNA distribution of pituitary adenylate cyclaseactivating polypeptide (PACAP)/PACAP-related peptide in the lungfi sh. Ann. Ny Acad. Sci., 1163 (1): 209-214.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC t method. Methods, 25 (4): 402-408.
Lu G, Moriyama E N. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Brief Bioinfor., 5 (4): 378-388.
Lugo J M, Oliva A, Morales A, Reyes O, Garay H E, Herrera F, Cabrales A, Pérez E, Estrada M P. 2010. The biological role of pituitary adenylate cyclase-activating polypeptide (PACAP) in growth and feeding behavior in juvenile fi sh. J. Pept. Sci., 16 (11): 633-643.
Maria Lugo J, Tafalla C, Leceta J, Gomariz R P, Estrada M P. 2011. Differential expression pattern of pituitary adenylate cyclase-activating polypeptide (PACAP) alternative splicing variants and its receptors in the immune system of rainbow trout (Oncorhynchus mykiss). Fish Shellfi sh Immun., 30 (2): 734-738.
Matsuda K, Azuma M, Maruyama K, Shioda S. 2013. Neuroendocrine control of feeding behavior and psychomotor activity by pituitary adenylate cyclaseactivating polypeptide (PACAP) in vertebrates. Obes. Res. Clin. Pract., 7 (1): e1-e7.
Matsuda K, Kashimoto K, Higuchi T, Yoshida T, Uchiyama M, Shioda S, Arimura A, Okamura T. 2000. Presence of pituitary adenylate cyclase-activating polypeptide (PACAP) and its relaxant activity in the rectum of a teleost, the stargazer, Uranoscopus japonicus. Peptides, 21 (6): 821-827.
Matsuda K, Maruyama K, Miura T, Uchiyama M, Shioda S. 2005a. Anorexigenic action of pituitary adenylate cyclaseactivating polypeptide (PACAP) in the goldfi sh: feedinginduced changes in the expression of mRNAs for PACAP and its receptors in the brain, and locomotor response to central injection. Neurosci. Lett., 386 (1): 9-13.
Matsuda K, Maruyama K, Nakamachi T, Miura T, Shioda S. 2006. Effects of pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal polypeptide on food intake and locomotor activity in the goldfi sh, Carassius auratus. Ann. Ny Acad. Sci., 1070 (1): 417-421.
Matsuda K, Maruyama K, Nakamachi T, Miura T, Uchiyama M, Shioda S. 2005b. Inhibitory effects of pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) on food intake in the goldfi sh, Carassius auratus. Peptides, 26 (9): 1 611-1 616.
Matsuda K, Maruyama K. 2007. Regulation of feeding behavior by pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal polypeptide (VIP) in vertebrates. Peptides, 28 (9): 1 761- 1 766.
Miyata A, Arimura A, Dahl R R, Minamino N, Uehara A, Jiang L. 1989. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Bioph. Res. Co., 164 (1): 567- 574.
Morley J E, Horowitz M, Morley P M K, Flood J F. 1992. Pituitary adenylate cyclase activating polypeptide (PACAP) reduces food intake in mice. Peptides, 13 (6): 1 133-1 135.
Nakata M, Yada T. 2007. PACAP in the glucose and energy homeostasis: physiological role and therapeutic potential. Curr. Pharm. Design, 13 (11): 1 105-1 112.
Nam B, Moon J, Kim Y, Kong H J, Kim W, Kim D, Jee Y J, Lee S. 2013. Structural and functional characterization of pituitary adenylyl cyclase-activating polypeptide (PACAP)/PACAP-related peptide (PRP) and its receptor in olive flounder (Paralichthys olivaceus). Comp. Biochem. Phys. B, 164 (1): 18-28.
Narnaware Y K, Peter R E. 2001. Effects of food deprivation and refeeding on neuropeptide Y (NPY) mRNA levels in goldfi sh. Comp. Biochem. Phys. B, 129 (2): 633-637.
Ogi K, Kimura C, Onda H, Arimura A, Fujino M. 1990. Molecular cloning and characterization of cDNA for the precursor of rat pituitary adenylate cyclase activating polypeptide (PACAP). Biochem. Bioph. Res. Co., 173 (3): 1 271-1 279.
Olsson C, Holmgren S. 2000. PACAP and nitric oxide inhibit contractions in the proximal intestine of the atlantic cod, Gadus morhua. J. Exp. Bio l., 203 (3): 575-583.
Panserat S, Plagnes-Juan E, Kaushik S. 2001. Nutritional regulation and tissue specifi city of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol., 204 (13): 2 351-2 360.
Parker D B, Power M E, Swanson P, Rivier J, Sherwood N M. 1997. Exon skipping in the gene encoding pituitary adenylate cyclase-activating polypeptide in salmon alters the expression of two hormones that stimulate growth hormone release. Endocrinology, 138 (1): 414-423.
Sherwood N M, Krueckl S L, McRory J E. 2000. The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr. Rev., 21 (6): 619-670.
Tachibana T, Saito E S, Takahashi H, Saito S, Tomonaga S, Boswell T, Furuse M. 2004. Anorexigenic effects of pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide in the chick brain are mediated by corticotrophin-releasing factor. Regul. Peptides, 120 (1): 99-105.
Tachibana T, Tomonaga S, Oikawa D, Saito S, Takagi T, Saito E, Boswell T, Furuse M. 2003. Pituitary adenylate cyclase activating polypeptide and vasoactive intestinal peptide inhibit feeding in the chick brain by different mechanisms. Neurosci. Lett., 348 (1): 25-28.
Tam J K V, Lee L T O, Chow B K C. 2007. PACAP-related peptide (PRP)—Molecular evolution and potential functions. Peptides, 28 (9): 1 920-1 929.
Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol., 24 (8): 1 596-1 599.
Thompson J D, Higgins D G, Gibson T J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specifi c gap penalties and weight matrix choice. Nucleic Acids Res., 22 (22): 4 673-4 680.
Valassi E, Scacchi M, Cavagnini F. 2008. Neuroendocrine control of food intake. Nutr. Metab. Cardiovas., 18 (2): 158-168.
Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow B K C, Hashimoto H, Galas L. 2009. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol. Rev., 61 (3): 283-357.
Vaughan J M, Rivier J, Spiess J, Peng C, Chang J P, Peter R E, Vale W. 1992. Isolation and characterization of hypothalamic growth-hormone releasing factor from common carp, Cyprinus carpio. Neuroendocrinology, 56 (4): 539-549.
Volkoff H, Xu M, MacDonald E, Hoskins L. 2009. Aspects of the hormonal regulation of appetite in fish with emphasis on goldfi sh, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp. Biochem. Phys. A, 153 (1): 8-12.
Wu S, Adams B A, Fradinger E A, Sherwood N M. 2006. Role of two genes encoding PACAP in early brain development in zebrafi sh. Ann. Ny Acad. Sci., 1070 (1): 602-621.
Xu M, Long L, Chen L, Qin J, Zhang L, Yu N, Li E. 2012. Cloning and differential expression pattern of pituitary adenylyl cyclase-activating polypeptide and the PACAPspecifi c receptor in darkbarbel catfish Pelteobagrus vachelli. Comp. Biochem. Phys. B, 161 : 41-53.
Xu M, Volkoff H. 2009. Cloning, tissue distribution and effects of food deprivation on pituitary adenylate cyclase activating polypeptide (PACAP)/PACAP-related peptide (PRP) and preprosomatostatin 1 (PPSS 1) in Atlantic cod (Gadus morhua). Peptides, 30 (4): 766-776.
Copyright © Haiyang Xuebao