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Developmental study of neuropeptide Y-like immunoreactivity in the neurohypophysis and intermediate lobe of the rhesus monkey (Macaca mulatta)

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Summary

The purpose of this study was to examine the development and distribution of neuropeptide Y-immunoreactive fibers in the neurohypophysis of the rhesus monkey (Macaca mulatta) throughout life and the relationship of these fibers to the hypothalamo-hypophyseal portal vasculature. In rhesus monkeys, which varied in age from fetal life to 34 years, neuropeptide Y-immunoreactive fibers were present at all ages examined. In adult monkeys, varicose neuropeptide Y-labeled fibers were concentrated in the upper infundibular stem in association with capillary loops of the portal vasculature and the long portal vessels. Other fibers travelled down the infundibular stem and were distributed at the junction of the lower infundibular stem and infundibular process in the vicinity of the short portal vessels. In the infundibular process, neuropeptide Y-immunoreactive fibers were concentrated along the border of the intermediate lobe. Other stained fibers were sparsely distributed in the infundibular process and were often associated with small vessels. Neuropeptide Y-immunoreactivity was also located in a few fibers and cells of the intermediate lobe. Very few labeled fibers were seen in the fetal neurohypophysis, but their number increased gradually during the first postnatal year. At two years of age, a high density of stained fibers was observed, especially in the infundibular process. The number of axons in the infundibular process was lower at 12 years and continued to decline until 34 years of age. Neuropeptide Y may modulate hormone release at these sites and may also be released directly into vessels in the infundibular process. The close association of neuropeptide Y-labeled fibers with capillaries of the portal vasculature strongly suggests that neuropeptide Y is released into the portal blood of monkeys throughout life and may influence hormone secretion from the anterior pituitary gland.

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References

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

    Google Scholar 

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

    Google Scholar 

  • Anthony ELP, King JC, Stopa EG (1984) Immunocytochemical localization of LHRH in the median eminence, infundibular stalk, and neurohypophysis. Cell Tissue Res 236:5–14

    Google Scholar 

  • Barry J (1977) Immunofluorescence study of LRF neurons in man. Cell Tissue Res 181:1–14

    Google Scholar 

  • Barry J, Carette B (1975) Immunofluorescence study of LRF neurons in primates. Cell Tissue Res 164:163–178

    Google Scholar 

  • Bergland RM, Page RB (1978) Can the pituitary secrete directly to the brain? (Affirmative anatomical evidence). Endocrinology 102:1325–1338

    Google Scholar 

  • Cailliez D, Danger JM, Andersen AC, Polak JM, Pelletier G, Kawamura K, Kikuyama S, Vaudry H (1987a) Neuropeptide Y (NPY)-like immunoreactive neurons in the brain and pituitary of the amphibian Rana catesbeiana. Zool Sci 4:123–134

    Google Scholar 

  • Cailliez D, Danger JM, Polak JM, Pelletier G, Andersen AC, Leboulenger F, Vaudry H (1987b) 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 

  • 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 

  • Ciofi P, Croix D, Tramu G (1987) Coexistence of hGHRF and NPY immunoreactivities in neurons of the arcuate nucleus of the rat. Neuroendocrinology 45:425–428

    Google Scholar 

  • Crowley WR, Kalra SP (1987) Neuropeptide Y stimulates the release of luteinizing hormone-releasing hormone from medial basal hypothalamus in vitro: modulation by ovarian steroids. Neuroendocrinology 46:97–103

    Google Scholar 

  • Crowley WR, Tessel RE, O'Donohue TL, Adler BA, Kalra SP (1985) Effects of ovarian hormones on the concentrations of immunoreactive neuropeptide Y in discrete brain regions of the female rat: correlation with serum luteinizing hormone (LH) and median eminence LH-releasing hormone. Endocrinology 117:1151–1155

    Google Scholar 

  • Crowley WR, Hassid A, Kalra SP (1987) Neuropeptide Y enhances the release of luteinizing hormone (LH) induced by LH-releasing hormone. Endocrinology 120:941–945

    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 

  • Danger JM, Leboulenger F, Guy J, Tonon MC, Benyamina M, Martel JC, Pierre SS, Pelletier G, Vaudry H (1986) Neuropeptide Y in the intermediate lobe of the frog pituitary acts as an alpha-MSH-release inhibiting factor. Life Sci 39:1183–1192

    Google Scholar 

  • Daniel PM, Prichard MML (1975) Studies of the hypothalamus and pituitary gland. Acta Endocrinol 80 [Suppl201]:1–216

    Google Scholar 

  • De Quidt ME, Emson PC (1986a) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system — I. Radioimmunoassay and chromatographic characterization. Neuroscience 18:527–543

    Google Scholar 

  • De Quidt ME, Emson PC (1986b) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system — II. Immunohistochemical analysis. Neuroscience 18:545–618

    Google Scholar 

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

    Google Scholar 

  • Foster GA, Schultzberg M (1984) Immunohistochemical analysis of the ontogeny of neuropeptide Y immunoreactive neurons in foetal rat brain. Int J Dev Neurosci 2:387–407

    Google Scholar 

  • Foster GA, Schultzberg M, Goldstein M (1984) Differential and independent manifestation within co-containing neurons of neuropeptide Y and tyrosine hydroxylase during ontogeny of the rat central nervous system. Neurochem Int 6:761–771

    Google Scholar 

  • Goldsmith PC, Song T (1987) The gonadotropin-releasing hormone containing ventral hypothalamic tract in the fetal rhesus monkey (Macaco mulatta). J Comp Neurol 257:130–139

    Google Scholar 

  • Hökfelt T, Lundberg JM, Lagercrantz H, Tatemoto K, Mutt V, Lindberg J, Terenius L, Everitt BJ, Fuxe K, Agnati L, Goldstein M (1983a) Occurrence of neuropeptide Y (NPY)-like immunoreactivity in catecholamine neurons in the human medulla oblongata. Neurosci Lett 36:217–222

    Google Scholar 

  • Hökfelt T, Lundberg JM, Tatemoto K, Mutt V, Terenius L, Polak J, Bloom S, Sasek C, Elde R, Goldstein M (1983b) Neuropeptide Y (NPY) and FMRF-amide neuropeptide like immunoreactivities in catecholamine neurons of the rat medulla oblongata. Acta Physiol Scand 117:315–318

    Google Scholar 

  • Hooi SC, Richardson GS, McDonald JK, Allen JM, Koenig JI (1988) Changes in central and peripheral neuropeptide Y (NPY) and vasopressin (AVP) with a hyperosmotic stimulus in the rat. 70th Annual Meeting of the Endocrine Soc [Abstr] 1167, 312

    Google Scholar 

  • Kalra SP, Crowley WR (1984) Norepinephrine-like effects of neuropeptide Y on LH release in the rat. Life Sci 35:1173–1176

    Google Scholar 

  • Kerkerian L, Guy J, Lefevre G, Pelletier G (1985) Effects of neuropeptide Y (NPY) on the release of anterior pituitary hormones in the rat. Peptides 6:1201–1204

    Google Scholar 

  • Khorram O, Roselli CE, Ellinwood WE, Spies HG (1987a) The measurement of neuropeptide Y in discrete hypothalamic and limbic regions of male rhesus macaques with a human NPY-directed antiserum. Peptides 8:159–163

    Google Scholar 

  • Khorram O, Pau KYF, Spies HG (1987b) Bimodal effects of neuropeptide Y on hypothalamic release of gonadotropin-releasing hormone in conscious rabbits. Neuroendocrinology 45:290–297

    Google Scholar 

  • King JC, Anthony ELP (1984) LHRH neurons and their projections in humans and other mammals: species comparisons. Peptides 5 [Suppl1]:195–207

    Google Scholar 

  • King JC, Anthony ELP, Fitzgerald DM, Stopa EG (1985) Luteinizing hormone-releasing hormone neurons in human preoptic/hypothalamus: differential intraneuronal localization of immunoreactive forms. J Clin Endocrinol Metab 60:88–97

    Google Scholar 

  • McDonald JK (1988) Neuropeptide Y and related substances. In: Nelson J (ed) CRC critical reviews in neurobiology. CRC Press, Boca Raton, FL (in press)

    Google Scholar 

  • McDonald JK, Lumpkin MD, Samson WK, McCann SM (1984) Third ventricular injections of neuropeptide Y decrease LH and growth hormone secretions in ovariectomized rats. Soc Neurosci [Abstr] 10, 1214

    Google Scholar 

  • McDonald JK, Lumpkin MD, Samson WK, McCann SM (1985) Neuropeptide Y affects secretion of luteinizing hormone and growth hormone in ovariectomized rats. Proc Natl Acad Sci USA 82:561–564

    Google Scholar 

  • McDonald JK, Collins P, Reich CA (1986) Neonatal injections of MSG inhibit the development of neuropeptide Y in the rat hypothalamus and posterior pituitary. Soc Neurosci [Abstr] 12, 1523

    Google Scholar 

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

    Google Scholar 

  • McDonald JK, Dees WL, Ahmed C, Noe BD, Ojeda SR (1987b) 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 (1987c) High concentrations of neuropeptide Y in pituitary portal blood of rats. Neuroendocrinology 46:538–541

    Google Scholar 

  • McDonald JK, Lumpkin MD, DePaolo LV (1988) Neuropeptide Y suppresses pulsatile LH release in ovariectomized rats. 70th Annual Meeting of the Endocrine Soc [Abstr] 1165, 312

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Morel G, Leneveu E, Tonon MC, Pelletier G, Vaudry H, Dubois PM (1985) Subcellular localization of thyrotropin-releasing hormone (TRH)-and neuropeptide Y (NPY)- like immunoreactivity in the neurointermediate lobe of the frog pituitary. Peptides 6:1085–1091

    Google Scholar 

  • Page RB (1986) The pituitary portal system. Current Topics in Neuroendocrinology 7:1–47

    Google Scholar 

  • Papadopoulos GC, Karamanlidis AN, Michaloudi H, Dinopoulos A, Antonopoulos J, Parnavelas JG (1985) The coexistence of oxytocin and corticotropin-releasing factor in the hypothalamus: an immunocytochemical study in the rat, sheep and hedgehog. Neurosci Lett 62:213–218

    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 

  • Sabatino FD, McDonald JK (1987) Neuropeptide Y affects the release of LHRH from the median eminence in vitro. Soc Neurosci [Abstr] 13, 1310

    Google Scholar 

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

    Google Scholar 

  • Samson WK, McDonald JK, Lumpkin MD (1985) Naloxone-induced dissociation of oxytocin and prolactin release. Neuroendocrinology 40:68–71

    Google Scholar 

  • Shen CL, Moore RY (1985) NPY localization in monkey hypothalamus. Soc Neurosci [Abstr] 11, 682

    Google Scholar 

  • Silverman AJ, Antunes JL, Ferin M, Zimmerman EA (1977) The distribution of luteinizing hormone-releasing hormone (LHRH) in the hypothalamus of the rhesus monkey. Light microscopic studies using immunoperoxidase technique. Endocrinology 101:134–142

    Google Scholar 

  • Smith Y, Parent A, Kerkerian L, Pelletier G (1985) Distribution of neuropeptide Y immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus). J Comp Neurol 236:71–89

    Google Scholar 

  • Sutton S, Toyama T, Otto S, Plotsky P (1987) Presence of neuropeptide Y (NPY) in hypophysial portal plasma: analysis of putative central and adenohypophysial actions. 69th Annual Meeting of the Endocrine Soc [Abstr] 733, 204

    Google Scholar 

  • Tigges J, McDonald JK, Tigges M (1986) Neuropeptide Y-like immunoreactivity in the neurohypophysis of rhesus monkey and orangutan. Soc Neurosci [Abstr] 12, 294

    Google Scholar 

  • Tigges J, McDonald JK, Tigges M (1987) Neuropeptide Y-like immunoreactivity in the hypothalamus of the young rhesus monkey. Soc Neurosci [Abstr] 13, 1579

    Google Scholar 

  • Verburg-van Kemenade BM, Jenks BG, Danger JM, Vaudry H, Pelletier G, Saint-Pierre S (1987) An NPY-like peptide may function as MSH-release inhibiting factor in Xenopus laevis. Peptides 8:61–67

    Google Scholar 

  • Woodhams PL, Allen YS, McGovern J, Allen JM, Bloom SR, Balazs R, Polak JM (1985) Immunohistochemical analysis of the early ontogeny of the neuropeptide Y system in rat brain. Neuroscience 15:173–202

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Yerkes Regional Primate Research Center, Emory University School of Medicine, Atlanta, Georgia, USA

    John K. McDonald, Johannes Tigges, Margarete Tigges & Caroline Reich

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  1. John K. McDonald
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  2. Johannes Tigges
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  3. Margarete Tigges
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  4. Caroline Reich
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McDonald, J.K., Tigges, J., Tigges, M. et al. 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 (1988). https://doi.org/10.1007/BF00226499

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