Skip to main content

Localization and characterization of neuropeptide Y-like peptides in the brain and islet organ of the anglerfish (Lophius americanus)

Cell and Tissue Research volume 257, pages 303–311 (1989)Cite this article

Summary

Results from a previous report demonstrate that more than one molecular form of neuropeptide Y-like peptide may be present in the islet organ of the anglerfish (Lophius americanus). Most of the neuropeptide Y-like immunoreactive material was anglerfish peptide YG, which is expressed in a subset of islet cells, whereas an additional neuropeptide Y-like peptide(s) was localized in islet nerves. To learn more about the neuropeptide Y-like peptides in islet nerves, we have employed immunohistochemical and biochemical methods to compare peptides found in anglerfish islets and brain. Using antisera that selectively react with either mammalian forms of neuropeptide Y or with anglerfish peptide YG, subsets of neurons were found in the brain that labelled with only one or the other of the antisera. In separate sections, other neurons that were labelled with either antiserum exhibited similar morphologies. Peptides from brains and islets were subjected to gel filtration and reverse-phase high performance liquid chromatography. Radioimmunoassays employing either the neuropeptide Y or peptide YG antisera were used to examine chromatographic eluates. Immunoreactive peptides having retention times of human neuropeptide Y and porcine neuropeptide Y were identified in extracts of both brain and islets. This indicates that peptides structurally similar to both of these peptides from the neuropeptide Y-pancreatic polypeptide family are expressed in neurons of anglerfish brain and nerve fibers of anglerfish islets. The predominant form of neuropeptide Y-like peptide in islets was anglerfish peptide YG. Neuropeptide Y-immunoreactive peptides from islet extracts that had chromatographic retention times identical to human neuropeptide Y and porcine neuropeptide Y were present in much smaller quantities. These results are consistent with the hypothesis that peptides having significant sequence homology with human neuropeptide Y and porcine neuropeptide Y are present in the nerve fibers that permeate the islet.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Adrian TE, Allen JM, Bloom SR, Ghatei MA, Rossor MN, Roberts GW, Crow TJ, Tatemoto K, Polak JM (1983) Neuropeptide Y distribution in the human brain. Nature 306:584–586

    Google Scholar 

  • Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow J, Bloom SR, Polak JM (1983) Neuropeptide Y distribution in the rat brain. Science 221:877–879

    Google Scholar 

  • Alwmark A, Ahren B (1987) Phentolamine reverses NPY-induced inhibition of insulin secretion in isolated rat islets. Eur J Pharmacol 135:307–311

    Google Scholar 

  • Andrews PC, Hawke D, Shively JE, Dixon JE (1985) A nonamidated peptide homologous to porcine peptide YY and neuropeptide YY. Endocrinology 116:2677–2681

    Google Scholar 

  • Balasubramaniam A, Andrews PC, Rigel DF, Dixon JE, Jackson RL, Fischer JE (1988) Synthesis of anglerfish peptide YG (APY). In: Peptides. Marshall GR (ed) Chemistry and Biology: Proceedings of the Tenth American Peptide Symposium, Leiden: ESCOM, pp 181–183

    Google Scholar 

  • Beal MF, Chattha GK, Martin JB (1986) A comparison of regional somatostatin and neuropeptide Y distribution in rat striatum and brain. Brain Res 377:240–245

    Google Scholar 

  • Beal MF, Mazurek MF, Martin JB (1987) A comparison of somatostatin and neuropeptide Y distribution in monkey brain. Brain Res 405:213–219

    Google Scholar 

  • Braford MR, Northcutt RG (1983) Organization of the diencephalon and pretectum of the ray-finned fishes. In: Davis RE, Northcutt RG (eds) Fish neurobiology. University of Michigan Press, Ann Arbor, Mich., Vol 2, pp 117–163

    Google Scholar 

  • Cailliez D, Danger JM, Polak JM, Pelletier G, Andersen AC, Leboulenger F, Vaudry H (1987) Co-distribution of neuropeptide Y and its C-terminal flanking peptide in the brain and pituitary of the frog Rana ridibunda. Neurosci Lett 74:163–168

    Google Scholar 

  • Carlei F, Allen JM, Bishop AE, Bloom SR, Polak JM (1985) Occurrence, distribution and nature of neuropeptide Y in the rat pancreas. Experientia 41:1554–1557

    Google Scholar 

  • Chronwall BM, Chase TN, O'Donohue TL (1984) Coexistence of neuropeptide Y and somatostatin in rat and human cortical and rat hypothalamic neurons. Neurosci Lett 52:213–217

    Google Scholar 

  • Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL (1985) The anatomy of neuropeptide-Y containing neurons in rat brain. Neuroscience 15:1159–1181

    Google Scholar 

  • Clark JT, Kalra PS, Crowley WR, Kalra SP (1984) Neuropeptide Y and human pancreatic polypeptide stimulate feeding behavior in rats. Endocrinology 115:427–429

    Google Scholar 

  • Corder R, Lowry PJ, Emson PC, Gaillard RC (1985) Chromatographic characterization of the circulating neuropeptide Y immunoreactivity from patients with phaeochromocytoma. Regul Pept 10:91–97

    Google Scholar 

  • Danger JM, Guy J, Benyamina M, Jegou S, Leboulenger F, Cote J, Tonon MC, Pelletier G, Vaudry H (1985) Localization and identification of neuropeptide Y (NPY)-like immunoreactivity in the frog brain. Peptides 6:1225–1236

    Google Scholar 

  • Ekblad E, Wahlestedt C, Ekelund M, Hakanson R, Sundler F (1984) Neuropeptide Y in the gut and pancreas: Distribution and possible vasomotor function. Front Horm Res 12:85–90

    Google Scholar 

  • Everitt BJ, Hokfelt T, Terenius L, Tatemoto K, Mutt V, Goldstein M (1984) Differential coexistence of neuropeptide Y (NPY)-like immunoreactivity with catecholamines in the central nervous system of the rat. Neuroscience 11:443–462

    Google Scholar 

  • Greenwood FC, Hunter WM, Glover JS (1963) The preparation of 131I-labelled growth hormone of high specific activity. Biochem J 89:114–118

    Google Scholar 

  • Lindh B, Hökfelt T, Elfvin LG, Terenius L, Fahrenkrug J, Elde R, Goldstein M (1986) Topography of NPY-, somatostatin-, and VIP-immunoreactive, neuronal subpopulations in the guinea pig celiac-superior mesenteric ganglion and their projection to the pylorus. J Neurosci 6:2371–2383

    Google Scholar 

  • Liu D, Desiderio DM (1987) Reversed-phase high performance liquid chromatographic-radioreceptor assay of human cerebrospinal fluid neuropeptides: Maximizing recovery of picomoles of peptides and minimizing memory. J Chromatogr 422:61–71

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom SR, Goldstein M (1982) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477–480

    Google Scholar 

  • McDonald JK (1988) Neuropeptide Y and related substances. In: Nelson J (ed) CRC critical reviews in neurobiology. CRC Press, Boca Raton, Fla., Vol 4(1): 97–135

    Google Scholar 

  • McDonald JK, Dees WL, Ahmed C, Noe BD, Ojeda SR (1987a) Biochemical and immunocytochemical characterization of neuropeptide Y in the immature rat ovary. Endocrinology 120:1703–1710

    Google Scholar 

  • McDonald JK, Koenig JI, Gibbs DM, Collins P, Noe BD (1987b) High concentrations of neuropeptide Y in pituitary portal blood of rats. Neuroendocrinology 46:538–541

    Google Scholar 

  • McDonald JK, Greiner F, Wood JG, Noe BD (1987c) Oxytocinlike immunoreactive nerves are associated with insulin-containing cells in pancreatic islets of anglerfish (Lophius americanus). Cell Tissue Res 249:7–12

    Google Scholar 

  • McDonald JK, Tigges J, Tigges M, Reich CR (1988a) Developmental study of neuropeptide Y-like immunoreactivity in the neurohypophysis and intermediate lobe of the rhesus monkey (Macaca mulatta). Cell Tissue Res 254:499–509

    Google Scholar 

  • McDonald JK, Han C, Noe BD, Abel PW (1988b) High levels of NPY in rabbit cerebrospinal fluid and immunohistochemical analysis of possible sources. Brain Res 463:259–267

    Google Scholar 

  • McLachlan EM, Llewellyn-Smith IJ (1986) The immunohistochemical distribution of neuropeptide Y in lumbar pre- and paravertebral sympathetic ganglia of the guinea pig. J Auton Nerv Syst 17:313–324

    Google Scholar 

  • McLean IW, Nakane PK (1974) Periodate lysine paraformaldehyde fixative: A new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083

    Google Scholar 

  • Moltz JH, McDonald JK (1985) Neuropeptide Y: Direct and indirect action on insulin secretion in the rat. Peptides 6:1155–1159

    Google Scholar 

  • Noe BD, McDonald JK, Greiner F, Wood JG, Andrews PC (1986) Anglerfish islets contain NPY immunoreactive nerves and produce the NPY analog aPY. Peptides 7:147–154

    Google Scholar 

  • Parent A (1983) The monoamine-containing neuronal systems in the teleostean brain. In: Davis RE, Northcutt RG (eds) Fish neurobiology. University of Michigan Press, Ann Arbor, Mich., Vol 2, pp 285–315

    Google Scholar 

  • Pelletier G, Desy L, Kerkerian L, Cote J (1984) Immunocytochemical localization of neuropeptide Y (NPY) in the human hypothalamus. Cell Tissue Res 238:203–205

    Google Scholar 

  • Pettersson M, Ahren B, Lundquist I, Bottcher G, Sundler F (1987a) Neuropeptide Y: Intrapancreatic neuronal localization and effects on insulin secretion in the mouse. Cell Tissue Res 248:43–48

    Google Scholar 

  • Pettersson M, Lundquist I, Ahren B (1987b) Neuropeptide Y and calcitonin gene related peptide effects on glucagon and insulin secretion in the mouse. Endocr Res 13:407–417

    Google Scholar 

  • Reiner A, Oliver JR (1987) Somatostatin and neuropeptide Y are almost exclusively found in the same neurons in the telencephalon of turtles. Brain Res 426:149–156

    Google Scholar 

  • Sabatino FD, Murnane JM, Hoffman RA, McDonald JK (1987) Distribution of neuropeptide Y-like immunoreactivity in the hypothalamus of the adult golden hamster. J Comp Neurol 257:93–104

    Google Scholar 

  • Smith Y, Parent A (1986) Neuropeptide Y-immunoreactive neurons in the striatum of cat and monkey: Morphological characteristics, intrinsic organization and co-localization with somatostatin. Brain Res 372:241–252

    Google Scholar 

  • Sundler F, Moghimzadeh E, Håkanson R, Ekelund M, Emson P (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide-Y immunoreactivity. Cell Tissue Res 230:487–493

    Google Scholar 

  • Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y — a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Google Scholar 

  • Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β endorphin. Science 213:1394–1397

    Google Scholar 

  • Vallarino M, Danger JM, Fasolo A, Pelletier G, Saint-Pierre S, Vaudry H (1988) Distribution and characterization of neuropeptide Y in the brain of an elasmobranch fish. Brain Res 448:67–76

    Google Scholar 

  • Vigh-Teichmann V, Vigh B, Aros B (1976) Cerebrospinal fluidcontacting neurons, ciliated perikarya and “peptidergic” synapses in the magnocellular preoptic nucleus of teleostean fishes. Cell Tissue Res 165:397–413

    Google Scholar 

  • Watson AHD (1980) The distribution of aminergic neurones and their projections in the brain of the teleost, Myoxocephalus scorpius. Cell Tissue Res 208:299–312

    Google Scholar 

Download references

Author information

Author notes

  1. Jaroslaw Calka

    Present address: Department of Animal Anatomy, Agricultural and Technical University, Olsztyn, Kortowo, Poland

Affiliations

  1. Department of Anatomy and Cell Biology, Emory University School of Medicine, 30322, Atlanta, Georgia, USA

    Bryan D. Noe, Sharon L. Milgram, Jaroslaw Calka & John K. McDonald

  2. Division of Gastrointestinal Hormones, University of Cincinnati Medical Center, Cincinnati, Ohio, USA

    A. Balasubramaniam

  3. Department of Biochemistry, Purdue University, West Lafayette, Indiana, USA

    P. C. Andrews

  4. Marine Biological Laboratory, Woods Hole, Massachusetts, USA

    Bryan D. Noe & Sharon L. Milgram

Authors
  1. Bryan D. Noe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sharon L. Milgram
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Balasubramaniam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. C. Andrews
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jaroslaw Calka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John K. McDonald
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Noe, B.D., Milgram, S.L., Balasubramaniam, A. et al. Localization and characterization of neuropeptide Y-like peptides in the brain and islet organ of the anglerfish (Lophius americanus). Cell Tissue Res. 257, 303–311 (1989). https://doi.org/10.1007/BF00261834

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00261834

Key words

  • Neuropeptide Y
  • Anglerfish peptide YG
  • Brain
  • Pancreas, endocrine, innervation
  • Immunohistochemistry
  • Radioimmunoassay
  • High performance liquid chromatography
  • Anglerfish, Lophius americanus (Teleostei)