Abstract
Carassius RFamide (C-RFa) is a brain-gut peptide, isolated originally from the brain of a teleost fish, Japanese crucian carp (Carassius auratus langsdorfii). It is a novel FMRFamide-related peptide sharing homologies with mammalian prolactin-related peptide. We observed the localization of C-RFa-like immunoreactivity (C-RFa-IR) in the stomach, intestine, and pancreas of Japanese butterfly ray using an immunohistochemical technique. In the whole gastrointestinal tract, C-RFa-IR was observed in smooth muscle cells, and in the Meissner’s and Auerbach’s plexus ganglia. Furthermore, in the stomach C-RFa-IR was also observed at the bottom of the fundic glands in both the body and pyloric region. In the intestine C-RFa-IR was observed in epithelial cells at the tip of mucosal folds. In the pancreas, C-RFa-IR was observed in islet cells. Thus, we suggest that ray C-RFa may have functional roles in both peripheral neurotransmission and endocrine function of the gastroenteropancreatic system.
Similar content being viewed by others
References
Akiyoshi H, Inoue A, Fujimoto M (2005) Comparative immunohistochemical study of Carassius RFamide localization in teleost guts in different salinity habitats. Zool Sci 22:57–63
Barrington EJW (1972) The pancreas and intestine. In: Hardisty MW, Potter IC (eds) The biology of lampreys Vol 2. Academic Press, New York, pp 135–169
Boer HH, Schot LPC, Veenstra JA, Reichelt D (1980) Immunocytochemical identification of neural elements in the central nervous system of a snail, some insects, a fish and a mammal with an antiserum to molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell Tissue Res 213:21–27
Brownlee D, Holden-Dye L, Walker R (2000) The range and biological activity of FMRFamide-related peptides and classical neurotransmitters in nematodes. Adv Parasitol 45:109–180
Chartrel N, Dujardin C, Leprince J, Desrues L, Tonon MC, Cellier E, Cosette P, Jouenne T, Simonnet G, Vaudry H (2002) Isolation, characterization, and distribution of a novel neuropeptide, Rana RFamide (R-RFa), in the brain of the European green frog Rana esculenta. J Comp Neurol 448:111–127
Chiba A (2000) Immunohistochemical cell types in the terminal nerve ganglion of the cloudy dogfish, Scyliorhinus torazame, with special regard to neuropeptide Y/FMRFamide-immunoreactive cells. Neurosci Lett 286:195–198
Chiba A, Oka S, Honma Y (1991) Immunocytochemical distribution of FMRFamide-like substance in the brain of the cloudy dogfish, Scyliorhinus torazame. Cell Tissue Res 265:243–250
Clarke WC, Bern HA (1980) Comparative endocrinology of prolactin. In: Li CH (ed) Hormonal proteins and peptides Vol 8. Academic Press, New York, pp 105–197
Conlon JM, Bjenning C, Moon TW, Youson JH, Thim L (1991) Neuropeptide Y-related peptides from the pancreas of a teleostean (eel), holostean (bowfin) and elasmobranch (skate) fish. Peptides 12:221–226
Cottrell GA, Schot LP, Dockray GJ (1983) Identification and probable role of a single neurone containing the neuropeptide Helix FMRFamide. Nature 304:638–640
Cowden C, Stretton AO, Davis RE (1989) AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2:1465–1473
Crim JW, Jenkins AC, Brown MR (1992) A mosquito neuropeptide in a moth larva (Helicoverpa zea): relation to FMRFamide immunoreactivity. Tissue Cell 24:537–545
Dockray GJ (2004) The expanding family of RFamide peptides and their effects on feeding behavior. Exp Physiol 89:229–235
Dockray GJ, Vaillant C, Williams RG, Gayton RJ, Osborne NN (1981) Vertebrate brain-gut peptides related to FMRFamide and Met-enkephalin Arg6Phe7. Peptides 2:25–30
El-Salhy M (1984) Immunocytochemical investigation of the gastro-entero-pancreatic (GEP) neurohormonal peptides in the pancreas and gastrointestinal tract of the dogfish Squalus acanthias. Histochemistry 80:193–205
Epple A, Brinn JE (1987). The comparative physiology of the pancreatic islets. Springer-Verlag, Heidelberg
Evans BD, Pohl J, Kartsonis NA, Calabrese RL (1991) Identification of Rfamide neuropeptides in the medicinal leech. Peptides 12:897–908
Falkmer S, Östberg Y (1977) Comparative morphology of pancreatic islets in animals. In: Volk BW, Wellmann KF (eds), The diabetic pancreas. Plenum Press, New York, pp 15–59
Falkmer S, Carraway RE, El-Salhy M, Emdin SO, Grimelius L, Rehfeld JF, Reinecke M, Schwartz TW (1981) Phylogeny of the gastroenteropancreatic neuroendocrine system: a review. In: Grossman MI, Brazier MAB. Lechago J (eds), Cellular basis of chemical messengers in the digestive system. Academic Press, New York, pp 21–42
Favrel P, Lelong C, Mathieu M (1998) Structure of the cDNA encoding the precursor for the neuropeptide FMRFamide in the bivalve mollusc Mytilus edulis. Neuroreport 9:2961–2965
Fujimoto K, Ohta N, Yoshida M, Kobota I, Muneoka Y, Kobayashi M (1990) A novel cardio-excitatory peptide isolated from the atria of the African giant snail, Achatina fulica. Biochem Biophys Res Commun 167:777–783
Fujimoto K, Kubota I, Yoshida-Kamatani Y, Minakata H, Nomoto K, Yoshida M, Harada A, Muneoka Y, Kobayashi M (1991) Purification of achatin-I from the atria of the African giant snail, Achatina fulica, and its possible function. Biochem Biophys Res Commun 177:847–853
Fujimoto M, Takeshita K, Wang X, Takabatake I, Fujisawa Y, Teranishi H, Ohtani M, Muneoka Y, Ohta S (1998) Isolation and characterization of a novel bioactive peptide, Carassius RFamide (C-RFa), from the brain of the Japanese crucian carp. Biochem Biophys Res Commun 242:436–440
Fujita T, Yui R, Iwanaga T, Nishiitsutsuji-Uwo J, Endo Y, Yanaihara N (1981) Evolutionary aspects of “brain-gut peptides”: an immunohistochemical study. Peptides 2:123–131
Geary TG, Price DA, Bowman JW, Winterrowd CA, Mackenzie CD, Garrison RD, Williams JF, Friedman AR (1992) Two FMRFamide-like peptides from the free-living nematode panagrellus redivirus. Peptides 13:209–214
Grimmelikhuijzen CJ, Graff D (1986) Isolation of pyroGlu-Gly-Arg-Phe-NH2 (Antho-RFamide), a neuropeptide of sea anemones. Proc Natl Acad Sci USA 83:9817–9821
Grimmelikhuijzen CJ, Rinehart KL, Spencer AN (1992) Isolation of the neuropeptide less than Glu-Trp-Leu-Gly-Arg-Phe-NH2 (Pol-RFamide) from the hydromedusae Polyorchis penicillatus. Biochem Biophys Res Commun 16:375–382
Groome JR, Townley MA, Watson WH III (1994) Excitatory actions of FMRFamide-related peptides (FaRPs) on the neurogenic Limulus heart. Biol Bull 186:309–318
Hinuma S, Habata Y, Fujii R, Kawamata Y, Hosoya M, Fukusumi S, Kitada C, Masuo Y, Asano T,Matsumoto H, Sekiguchi M, Kurokawa T, Nishimura O, Onda H, Fujino M (1998) A prolactin-releasing peptide in the brain. Nature 393:272–276
Jönsson AC (1991). Regulatory peptides in the pancreas of two species of elasmobranchs and in the Brockmann bodies of four teleost species. Cell Tissue Res 266:163–172
Jönsson AC (1995) Endocrine cells with gastrin/cholecystokinin-like immunoreactivity in the pancreas of the spiny dogfish, Squalus acanthias. Regul Pept 59:67–78
Kamatani Y, Minakata H, Kenny PTM, Iwashita T, Watanabe K, Funase K, Ping Sun X, Yongsiri A, Hwi Kim K, Novales-Li P, Novales ET, Kanapi CG, Takeuchi H, Nomoto K (1989) Achatin-I, an endogenous neuroexcitatory tetrapeptide from Achatina fulica ferrusac containing a D-amino acid residue. Biochem Biophys Res Commun 160:1015–1020
Kim JB, Gadsbøll V, Whittaker J, Barton BA, Conlon JM (2000) Gastroenteropancreatic hormones (insulin, glucagon, somatostatin, multiple forms of PYY) from the pallid sturgeon, Scaphirhynchus albus (Acipenseriformes). Gen Comp Endocrinol 120:353–363
Koch G, Chen ML, Sharma R, Walker RJ (1993) The actions of RFamide neuroactive peptides on the isolated heart of the giant African snail, Achatina fulica. Comp Biochem Physiol C 106:359–365
Kuhlman JR, Li C, Calabrese RL (1985) FMRFamide-like substances in the leech. II. Bioactivity on the heartbeat system. J Neurosci 5:2310–2317
Lange AB, Cheung IL (1999) The modulation of skeletal muscle contraction by FMRFamide-related peptides of the locust. Peptides 20:1411–1418
Lange AB, Orchard I (1998) The effects of SchistoFLRFamide on contractions of locust midgut. Peptides 19:459–467
Li C, Kim K, Nelson LS (1999) FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res 848:26–34
López J, Cuesta N, Cuttitta F, Martīnez A (1999) Adrenomedullin in nonmammalian vertebrate pancreas: an immunocytochemical study. Gen Comp Endocrinol 115:309–322
Mercier AJ, Orchard I, TeBrugge V (1991) FMRFamide-like immunoreactivity in the crayfish nervous system. J Exp Biol 156:519–538
Moosler A, Rinehart KL, Grimmelikhuijzen CJ (1996) Isolation of four neuropeptides, the hydra-RFamides I–IV, from Hydra magnipapillata. Biochem Biophys Res Commun 229:596–602
Moosler A, Rinehart KL, Grimmelikhuijzen CJ (1997) Isolation of three novel neuropeptides, the Cyanea-RFamides I–III, from Scyphomedusae. Biochem Biophys Res Commun 236:743–749
Moriyama S, Ito T, Takahashi A, Amano M, Sower SA, Hirano T, Yamamori K, Kawauchi H (2002) A homolog of mammalian PRL-releasing peptide (fish arginyl-phenylalany-amide peptide) is a major hypothalamic peptide of PRL release in teleost fish. Endocrinology 143:2071–2079
Nambu JR, Murphy-Erdosh C, Andrews PC, Feistner GJ, Scheller RH (1988) Isolation and characterization of a Drosophila neuropeptide gene. Neuron 1:55–61
O’Gara BA, Brown PL, Dlugosch D, Kandiel A, Ku JW, Geier JK, Henggeler NC, Abbasi A, Kounalakis N (1999) Regulation of pharyngeal motility by FMRFamide and related peptides in the medicinal leech, Hirudo medicinalis. Invert Neurosci 4:41–53
Pearse AGE (1976) Peptides in brain and intestine. Nature 262:92–94
Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671
Raffa RB, Jacoby HI (1990) Effect of Phe-D-Met-Arg-Phe-NH2 and other Phe-Met-Arg-Phe-NH2 related peptides on mouse colonic propulsive motility: a structure-activity relationship study. J Pharmacol Exp Ther 254:809–814
Sakamoto T, Iwata K, Ando M (2002) Growth hormone and prolactin expression during environmental adaptation of gobies. Fish Sci 68 Supplement:757–760
Sakamoto T, Fujimoto M, Ando M (2003) Fishy tales of prolactin-releasing peptide. Int Rev Cytol 225:91–130
Salzet M, Bulet P, Wattez C, Malecha J (1994) FMRFamide-related peptides in the sex segmental ganglia of the pharyngobdellid leech, Erpobdella octoculata. Identification and involvement in the control of hydric balance. Eur J Biochem 221:269–275
Satake H, Minakata H, Wang X, Fujimoto M (1999) Characterization of a cDNA encoding a precursor of Carassius RFamide, structurally related to a mammalian prolactin-releasing peptide. FEBS Lett 446:247–250
Seale AP, Itoh T, Moriyama S, Takahashi A, Kawauchi H, Sakamoto T, Fujimoto M, Riley LG, Hirano T, Grau EG (2002) Isolation and characterization of a homologue of mammalian prolactin-releasing peptide from the tilapia brain and its effect on prolactin release from the tilapia pituitary. Gen Comp Endocrinol 125:328–339
Sekine Y, Yui R (1981) Immunohistochemical study of the pancreatic endocrine cells of the ray, Dasyatis akajei. Arch Histol Jpn 44:95–101
Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661–667
Ukena K, Koda A, Yamamoto K, Kobayashi T, Iwakoshi-Ukena E, Minakata H, Kikuyama S, Tsutsui K (2003) Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinology 144:3879–3884
Vallarino M, Salsotto-Cattaneo MT, Feuilloley M, Vaudry H (1991) Distribution of FMRFamide-like immunoreactivity in the brain of the elasmobranch fish Scyliorhinus canicula. Peptides 12:1321–1328
Van Noorden S, Pearse AGE (1974) Immunoreactive polypeptide hormones in the pancreas and gut of the lamprey. Gen Comp Endocrinol 23:311–324
Van Noorden S, Greenberg J, Pearse AGE (1972) Cytochemical and immunofluorescence investigations on polypeptide hormone localization in the pancreas and gut of the larval lamprey. Gen Comp Endocrinol 19:192–199
Wang X, Morishita F, Matsushima O, Fujimoto M (2000) Immunohistochemical localization of C-RFamide, a FMRF-related peptide, in the brain of the goldfish Carassius auratus. Zool Sci 17:1067–1074
Weiss S, Goldberg JI, Chohan KS, Stell WK, Drummond GI, Lukowiak K (1984) Evidence for FMRFamide as a neurotransmitter in the gill of Aplysia californica. J Neurosci 4:1994–2000
Youson JH and Al-Mahrouki AA (1999). Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fishes. Gen Comp Endocrinol 116:303–335
Yui R, Nagata Y, Fujita T (1988) Immunocytochemical studies on the islet and the gut of the arctic lamprey, Lampetra japonica. Arch Histol Cytol 51:109–119
Acknowledgments
We thank Dr. M. Fujimoto for permission to use his antibody against C-RFa. We also thank Mr. Kouji Tomimuro and Mr. Takeshi Kiyoi, Department of Biological Science, Shimane University, for technical assistance.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Inoue, A., Akiyoshi, H. An immunohistochemical study of Carassius RF amide in the stomach, intestine, and pancreas of the Japanese butterfly ray, Gymnura japonica . Ichthyol Res 57, 223–230 (2010). https://doi.org/10.1007/s10228-010-0156-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10228-010-0156-4