Skip to main content
Book cover

Opioids pp 711–727Cite as

Ontogeny of Mammalian Opioid Systems

  • Chapter
  • 412 Accesses

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 104 / 1))

Abstract

At least two of the three distinct genes encoding peptides with opioid activity are expressed during prenatal development not only in the CNS and endocrine cells, but also in specific peripheral tissues. Although it is not yet known whether any of the opioid peptides derived from these opioid precursors are required for normal development, any prospective action requires not only gene activation, but also appropriate maturation of numerous cellular functions including biosynthesis, posttranslational processing, and regulation of synthesis and secretion. In addition, the cognate receptor(s) for presumptive bioactive peptides must be present and active. In this review, we will synthesize the information available on prenatal expression of all three opioid systems, proopiomelanocortin (POMC), proenkephalin (PENK), and prodynorphin (PDYN), but will focus on differentiation of POMC cells in the rodent pituitary where the most complete information is available. Relevant studies and reviews beyond the scope of this review will be cited as appropriate, and the authors apologize in advance for being unable to cite or discuss in detail all relevant work because of space limitations.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Allen RG, Pintar JE, Stack J, Kendall JW (1984) Biosynthesis and processing of proopiomelanocortin-derived peptides during fetal pituitary development. Dev Biol 102: 43–50

    Article  PubMed  CAS  Google Scholar 

  • Attali B, Saya D, Vogel Z (1990) Pre- and postnatal development of opiate receptor subtypes in rat spinal cord. Dev Brain Res 53: 97–102

    Article  CAS  Google Scholar 

  • Bowie EP, Ishikawa H, Shiino M, Rennels EG (1978) An immunocytochemical study of a rat pituitary multipotential clone. J Histochem Cytochem 26: 94–97

    Article  PubMed  CAS  Google Scholar 

  • Capecchi MR (1989) The new mouse genetics - altering the genome by gene targeting. Trends Gen 5:70–76 Chen C–LC, Chang CC, Kreiger DT, Bardin CW (1986) Expression and regulation of proopiomelanocortin-like gene in ovary and placenta: comparison with the testes. Endocrinology 118: 2382–2389

    Google Scholar 

  • Couly GF, LeDouarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras: I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110: 422–439

    Google Scholar 

  • Coyle KT, Pert CB (1976) Ontogenetic development of [3H]naloxone binding in the rat brain. Neuropharmacology 15: 555–560

    Article  PubMed  CAS  Google Scholar 

  • Davis MD, Lichtensteiger W, Schlumpf M, Bruinink A (1984) Early postnatal development of pituitary intermediate lobe control in the rat by dopamine neurons. Neuroendocrinology 39: 1–12

    Article  PubMed  CAS  Google Scholar 

  • Dunlap CE III, Christ GJ, Rose JC (1986) Characterization of opioid receptor binding in adult and fetal sheep brain regions. Dev Brain Res 24: 279–285

    Article  CAS  Google Scholar 

  • Dupouy JP (1980) Differentiation of MSH-containing, ACTH-containing and LPH- containing cells in the hypophysis during embryonic and fetal development. Int Rev Cytol 68: 197–249

    Article  PubMed  CAS  Google Scholar 

  • Dupouy JP, Chatelain A (1984) In-vitro effects of corticosterone, synthetic ovine corticotrophin releasing factor and arginine vasopressin on the release of adrenocorticotrophin by fetal rat pituitary glands. J Endocrinol 101: 339–344

    Article  PubMed  CAS  Google Scholar 

  • Durand P, Cathiard A-M, Dacheuxz F, Naaman S, Saez JM (1986) In vitro stimulation and inhibition of adrenocorticotrophin release by pituitary cells from ovine fetuses and lambs. Endocrinology 118: 11387–11394

    Article  Google Scholar 

  • Eagleson GW, Jenks BG, Overbecke AP (1986) The pituitary adrenocorticotropes originate from neural ridge tissue in Xenopus laevis. J Embryol Exp Morphol 95: 1–14

    PubMed  CAS  Google Scholar 

  • Elkabes S, Loh YP, Nieburgs A, Wray S (1989) Prenatal ontogenesis of proopiomelanocortin in the mouse central nervous system and pituitary gland: an in situ hybridization and immunocytochemical study. Dev Brain Res 46: 85–95

    Article  CAS  Google Scholar 

  • Fink G, Smith GD (1971) Ultrastructural features of the developing hypothalamo- hypophysial axis in the rat. A corrolative study. Z Zellforsch Mikrosk Anat 119: 208–226

    Google Scholar 

  • Gizang-Ginsberg E, Wolgemuth D (1987) Expression of the proopiomelanocortin gene is developmentally regulated and affected by germ cells in the male mouse reproductive system. Proc Natl Acad Sci USA 84: 1600–1604

    Article  PubMed  CAS  Google Scholar 

  • Glydon RSJ (1957) The development of the blood supply of the pituitary in the albino rat, with special reference to the portal vessels. J Anat 91: 237–244

    PubMed  CAS  Google Scholar 

  • Goland RS, Wardlaw SL, Stark RI, Brown LS Jr, Frantz AG (1986) High levels of corticotropin–releasing hormone in human plasma during pregnancy, labour and delivery. J Clin Endocrinol Metab 63: 1199–1203

    Article  PubMed  CAS  Google Scholar 

  • Grino M, Young WS III, Burgunder J–M (1989) Ontogeny of expression of the corticotropin-releasing factor gene in the hypothalamic paraventricular nucleus and of the proopiomelanocortin gene in rat pituitary. Endocrinology 124: 60–68

    Article  PubMed  CAS  Google Scholar 

  • Hammer GD, Fairchild–Harkness V, Low MJ (1990) Pituitary specific and hormonally regulated gene expression directed by the rat proopiomelanocortin promoter in transgenic mice. Mol Endocrinol 4: 1689–1697

    CAS  Google Scholar 

  • Hammer RP Jr (1985) Ontogeny of opiate receptors in the rat medial preoptic area: critical periods in regional development. Int J Dev Neurosci 3: 541 – 548

    Article  CAS  Google Scholar 

  • Hanuoka Y (1967) The effects of posterior hypothalectomy upon the growth and metamorphosis of the tadpole of Rana pipiens. Gen Comp Endocrinol 8:417–431

    Google Scholar 

  • Hauser KF, McLaughlin PJ, Zagon IS (1989) Endogenous opioid systems and the regulation of dendritic growth and spine formation. J Comp Neurol 281: 13–22

    Article  PubMed  CAS  Google Scholar 

  • Hayes WP, Loh YP (1990) Correlated onset and patterning of proopiomelanocortin gene expression in embryonic Xenopus brain and pituitary. Development 110: 747–757

    PubMed  CAS  Google Scholar 

  • Hemming FJ, Begeot M, Dubois MP, Dubois PM (1983) Ultrastructural identification of corticotropes of the fetal rat. In-vivo and in-vitro immunocytochemistry. Cell Tissue Res 234: 427–437

    Google Scholar 

  • Hotta M, Shibasaki T, Akitsugu M, Imaki T, Demura H, Ohno H, Daikoku S, Benoit R, Ling N, Shizume K (1988) Ontogeny of pituitary responsiveness to corticotropin-releasing hormone in rat. Regul Pept 21: 245–252

    Article  PubMed  CAS  Google Scholar 

  • Howells RD, Kilpatrick DL, Bailey LD, Noe M, Udenfriend S (1986) Proenkephalin mRNA in rat heart. Proc Natl Acad Sci USA 83: 1960–1963

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H, Suzuki J, Sasano N, Niizuma H (1988) The development and morphogenesis of the human pituitary gland. Anat Embryol (Berl) 178: 327–336

    Article  CAS  Google Scholar 

  • Kent JL, Pert CB, Herkenham M (1982) Ontogeny of opiate receptors in rat forebrain: visualization by in vitro autoradiography. Dev Brain Res 2: 487–504

    Article  Google Scholar 

  • Keshet E, Polakiewicz D, Itin A, Ornoy A, Rosen H (1989) Proenkephalin A is expressed in mesodermal lineages during organogenesis. EMBO J 8: 2917–2923

    PubMed  CAS  Google Scholar 

  • Kew D, Kilpatrick DL (1990) Widespread organ expression of the rat proenkephalin gene during early postnatal development. Mol Endocrinol 4: 337–340

    Article  PubMed  CAS  Google Scholar 

  • Khachaturian H, Alessi NE, Munfakh N, Watson SJ (1983) Ontogeny of opioid and related peptides in the rat CNS and pituitary: an immunocytochemical study. Life Sci 33: 61–64

    Article  PubMed  CAS  Google Scholar 

  • Khachaturian H, Lewis ME, Schafer MKH, Watson SJ (1985a) Anatomy of the CNS opioid systems. Trends Neurosci 8: 111–119

    Article  CAS  Google Scholar 

  • Khachaturian H, Lewis ME, Alessi NE, Watson SJ (1985b) Time of origin peptide- containing neurons in the rat hypothalamus. J Comp Neurol 236: 538–546

    Article  PubMed  CAS  Google Scholar 

  • Khorram O, McCann SM (1984) Pre- and postnatal developmental changes in hypothalamic and pituitary content of α–melanocyte-stimulating hormone and somatostatin in the rat. Biol Neonate 46: 80–88

    Article  PubMed  CAS  Google Scholar 

  • Kornblum HI, Hurlbut DE, Leslie FM (1987) Postnatal development of multiple opioid receptors in rat brain. Dev Brain Res 37: 21–41

    Article  CAS  Google Scholar 

  • Liotta AS, Kreiger DT (1980) In vitro biosynthesis and comparative posttranslational processing of immunoreactive precursor corticotropin/β-endorphin by human placental and pituitary cells. Endocrinology 106: 1504–1511

    Article  PubMed  CAS  Google Scholar 

  • Loh YP, Eskay RL, Brownstein M (1980) a-MSH-like peptides in rat brain: identification and changes in level during development. Biochem Biophys Res Comm 94:916–923

    Google Scholar 

  • Lord JAH, Waterfield AA, Hughes J, Kosterlitz HW (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267: 495–499

    Article  PubMed  CAS  Google Scholar 

  • Lugo DI (1989) Proopiomelanocortin gene expression and peptide secretion in the developing rat pituitary gland. PhD thesis, Columbia University

    Google Scholar 

  • Lugo DI, Roberts JL, Pintar JE (1989) Analysis of proopiomelanocortin gene expression during prenatal development of the rat pituitary gland. Mol Endocrinol 1313–1324

    Google Scholar 

  • Melner MH, Low KG, Allen RG, Nielson CP, Young SL, Saneto RP (1990) The regulation of proenkephalin expression in a distinct population of glial cells. EMBO J 9: 791–796

    PubMed  CAS  Google Scholar 

  • Milcovic K, Milcovic S (1962) Studies of the pituitary-adrenocortical system in the fetal rat. Endocrinology 71: 799–802

    Article  Google Scholar 

  • Mulchahey JJ, DiBlasio AM, Martin MC, Blumenfeld Z, Jaffe RB (1987) Hormone production and peptide regulation of the human fetal pituitary gland. Endocr Rev 8: 406–412

    Article  PubMed  CAS  Google Scholar 

  • Nakane PR, Setalo G, Mazurkiewicz JE (1977) The origin of ACTH cells in rat anterior pituitary. Ann NY Acad Sci 297: 201–204

    Article  PubMed  CAS  Google Scholar 

  • Negm IM (1971) The vascular blood supply of the pituitary and its development. Acat Anat (Basel) 80: 601–619

    Google Scholar 

  • Palmer MR, Miller RJ, Olson L, Seiger A (1982) Prenatal ontogeny of neurons with enkephalin-like immunoreactivity in the rat central nervous system: an immunohistochemical mapping investigation. Med Biol 60: 61–88

    PubMed  CAS  Google Scholar 

  • Pelletier G, Leclerc R, Labric F, Cote J, Chretien M, Lis M (1977) Immunohistochemical localization of lipotropic hormone in the pituitary gland. Endocrinology 100: 770–776

    Article  PubMed  CAS  Google Scholar 

  • Petrillo P, Tavani A, Verotta D, Robson LE, Kosterlitz HW (1987) Differential postnatal development of μ-δ- and ĸ-opioid binding sites in rat brain. Dev Brain Res 31: 53–58

    Article  CAS  Google Scholar 

  • Pintar JE, Lugo DI (1987) Proopiomelanocortin gene expression, prohormone processing, and secretion during fetal rat pituitary development. Ann NY Acad Sci 512: 318–327

    Article  PubMed  CAS  Google Scholar 

  • Pintar JE, Schachter BS, Herman AT, Durgerian S, Kreiger DT (1984) Characterization and localization of proopiomelanocortin messenger RNA in the adult rat testes. Science 225: 632–634

    Article  PubMed  CAS  Google Scholar 

  • Polakiewicz RD, Rosen H (1990) Regulated expression of proenkephalin A during ontogenic development of mesenchymal derivative tissues. Mol Cell Biol 10: 736–742

    PubMed  CAS  Google Scholar 

  • Potter E, Behan DP, Fischer WH, Linton EA, Lowry PJ, Vale WW (1991) Cloning and characterization of the cDNAs for human and rat corticotropin releasing factor-binding proteins. Nature 349: 423–426

    Article  PubMed  CAS  Google Scholar 

  • Rosen H, Polakiewicz R (1989) Postnatal expression of opioid genes in rat brain. Dev Brain Res 46: 123–129

    Article  CAS  Google Scholar 

  • Rundle SE, Funder JW (1988) Ontogeny of corticotropin-releasing factor and arginine vasopressin in the rat. Neuroendocrinology 47: 374–378

    Article  PubMed  CAS  Google Scholar 

  • Sato SM, Mains RE (1985) Posttranslational processing of proadrenocorticotropin/ endorphin-derived peptides during postnatal development in the rat pituitary. Endocrinology 117: 773–786

    Article  PubMed  CAS  Google Scholar 

  • Sato SM, Mains RE (1986) Regulation of adrenocorticotropin/endorphin-related peptide secretion in neonatal rat pituitary cultures. Endocrinology 119: 793–801

    Article  PubMed  CAS  Google Scholar 

  • Schmitt G, Stoeckel ME, Koch B (1981) Evidence for a possible dopaminergic control of pituitary alpha–MSH during ontogenesis in mice. Neuroendocrinology 33: 306–311

    Article  PubMed  CAS  Google Scholar 

  • Schwartz JP, Simantov R (1988) Developmental expression of proenkephalin mRNA in rat striatum and in striatal cultures. Dev Brain Res 40: 311–314

    Article  CAS  Google Scholar 

  • Schwind JL (1928) The development of the hypophysis cerebri of the albino rat. Am J Anat 41: 295–319

    Article  Google Scholar 

  • Scott REM, Autelitano DJ, Lugo DI, Blum M, Roberts JL, Pintar JE (1990) Developmental changes in levels of proopiomelanocortin intron A-containing heterogeneous nuclear RNA and mature messenger RNA in the anterior and neurointermediate lobes of the rat pituitary. Mol Endocrinol 4: 812–820

    Article  PubMed  CAS  Google Scholar 

  • Seidah NG, Markinkiewicz M, Benjannet S, Gaspar L, Beaubien G, Mattei MG, Lazure C, Mbikay M, Chretien M (1991) Cloning and primary sequence of a mouse candidate prohormone convertase PCI homologous to PC2, furin, and Kex2: distinct chromosome localization and messenger RNA distribution in brain and pituitary compared to PC2. Mol Endocrinol 5: 111–122

    Article  PubMed  CAS  Google Scholar 

  • Seizinger BR, Liebisch DC, Grimm C, Herz A (1984) Ontogenetic development of the proenkephalin B (=pro-dynorphin) opioid peptide system in the rat pituitary. Neuroendocrinology 39: 414–422

    Article  PubMed  CAS  Google Scholar 

  • Setalo G, Nakane P (1972) Studies on the functional differentiation of cells in fetal anterior pituitary glands of rats with peroxidase labelled antibody method. Anat Rec 172: 403–404

    Google Scholar 

  • Shaha C, Liotta AS, Kreiger DT, Bardin CW (1984) The ontogeny of immunoreactive P–endorphin in fetal, neonatal, and pubertal testes from mouse and human. Endocrinology 114:1584–1591 Shiino M, Ishikawa H, Rennels EG (1978) Accumulation of secretory granules in pituitary clonal cells derived from the epithelium of Rathke’s pouch. Cell Tissue Res 186: 53–61

    Google Scholar 

  • Shinoda H, Marini AM, Losi C, Schwartz JP (1989) Brain expression and gene specificity of neuropeptide gene expression in cultured astrocytes. Science 245: 415–417

    Article  PubMed  CAS  Google Scholar 

  • Spain JW, Roth BL, Coscia CJ (1985) Differential ontogeny of multiple opioid receptors (μ, δ, and ĸ). J Neurosci 5: 584–588

    PubMed  CAS  Google Scholar 

  • Spruce BA, Curtis R, Wilkin GP, Glover DM (1990) A neuropeptide precursor in cerebellum: proenkephalin exists in subpopulations of both neurons and astrocytes. EMBO J 9: 1787–1795

    PubMed  CAS  Google Scholar 

  • Stoeckel ME, Hindelang-Gertner C, Porte A (1979) Embryonic development and secretory differentiation in the pars tuberalis of the mouse hypophysis. Cell Tissue Res 198: 465–476

    Article  PubMed  CAS  Google Scholar 

  • Svalander C (1974) Ultrastructure of the fetal rat adenohypophysis. Acta Endocrinol [Suppl] (Copenh) 188: 1–114

    CAS  Google Scholar 

  • Swaab DF, Visser M, Tilders FJH (1976) Stimulation of intra-uterine growth in rat by melanocyte-stimulating hormone. J Endocrinol 70: 445–455

    Article  PubMed  CAS  Google Scholar 

  • Szabo K, Csanyi K (1982) The vascular architecture of the developing pituitary- median eminence complex in the rat. Cell Tissue Res 224: 563–577

    Article  PubMed  CAS  Google Scholar 

  • Tavani A, Robson LE, Kosterltz HW (1985) Differential postnatal development of μ-, δ- and ĸ-opioid binding sites in mouse brain. Dev Brain Res 23: 306–309

    Article  CAS  Google Scholar 

  • Tecott LH, Rubenstein JLR, Paxino G, Evans CJ, Eberwine JH, Valentino KL (1989) Developmental expression of proenkephalin mRNA and peptides in rat striatum. Dev Brain Res 49: 75–86

    Article  CAS  Google Scholar 

  • Tilders H, Parker CR, Barnea A, Porter JC (1981) The major immunoreactive melanocyte-stimulating hormone (α-MSH)-like substance found in human fetal pituitary tissue is not MSH but may be desacetyl MSH (adrenocorticotropin 1-13NH2). J Clin Endocrinol Metab 52: 319–323

    Article  PubMed  CAS  Google Scholar 

  • Vilijn MH, Vaysse PJJ, Zukin RS, Kessler JA (1988) Expression of preproenkephalin mRNA by cultured astrocytes and neurons. Proc Natl Acad Sci USA 85: 6551–6555

    Article  PubMed  CAS  Google Scholar 

  • Watanabe YG, Daikoku S (1979) An immunohistochemical study on the histogenesis of adenohypophysial cells in fetal rats. Dev Biol 68: 557–567

    Article  PubMed  CAS  Google Scholar 

  • Watkins WB, Choy VJ (1979) Maturation of the hypothalamo-neurohypophysial system. Neurophysin, vasopressin and oxytocin in the median eminance of the developing rat brain. Cell Tissue Res 197: 337–346

    Google Scholar 

  • Yoshida Y (1966) Electron microscopy of the anterior pituitary gland under normal and different experimental conditions. Exp Pathol 1: 439–454

    Google Scholar 

  • Zagon IS, Rhodes RE, McLaughlin PJ (1985) Distribution of enkephalin immunoreactivity in germinative cells of developing rat cerebellum. Science 227: 1049–1051

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Pintar, J.E., Scott, R.E.M. (1993). Ontogeny of Mammalian Opioid Systems. In: Herz, A., Akil, H., Simon, E.J. (eds) Opioids. Handbook of Experimental Pharmacology, vol 104 / 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-77460-7_28

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-77460-7_28

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-77462-1

  • Online ISBN: 978-3-642-77460-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics