Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Original Paper

Ubiquitous Embryonic Expression of the Norepinephrine Transporter

Ren Z.G.a · Pörzgen P.P.b · Youn Y.-H.a · Sieber-Blum M.a

Author affiliations

aDepartment of Cell Biology, Neurobiology and Anatomy, Medical College of Wisconsin, Milwaukee, Wisc., and bVollum Institute for Biomedical Research, Oregon Health Sciences University, Portland, Oreg., USA

Related Articles for ""

Dev Neurosci 2003;25:1–13

Do you have an account?

Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 9.00 *
EUR 8.00 *
USD 9.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.
Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00


Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: July 24, 2003
Issue release date: July 2003

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 1

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE

Abstract

We report that the norepinephrine transporter (NET) is expressed in avian and mouse embryos by numerous tissues that are derived from all three germ layers. In the nervous system, NET is expressed in the neuroepithelium of the brain and the spinal cord (ventral horn and floor plate), forming mesencephalic nuclei, neural crest, dorsal root ganglion, sympathetic ganglion and spinal nerve. Nonneuronal embryonic NET-expressing structures include the olfactory epithelium, the notochord, the somitic dermamyotome and mesenchymal cells in the limb bud. NET is expressed prominently in the cardiovascular system, including endothelial cells of forming blood vessels, the walls of the aorta and veins, the epicardium, myocardium and a subset of blood cells. The gut, lung buds, and in particular the kidneys, are intensely NET immunoreactive. Since neurotransmitters are known to affect proliferation, survival and differentiation of many mesenchymal cell types, NET function may be a physiologically relevant regulatory element in embryonic development. A working model is proposed for neurotransmitter transporter function in the embryo as a system for the concentration and targeted delivery of neurotransmitter.

© 2003 S. Karger AG, Basel


References

  1. Amara SG (1995): Monoamine transporters: Basic biology with clinical implications. Neuroscientist 1:259–267.
  2. Axelrod J (1965): The metabolism, storage, and release of catecholamines. Recent Prog Horm Res 21:597–619.
  3. Bohn LM, Xu F, Gainetdinov RR, Caron MG (2000): Potentiated opioid analgesia in norepinephrine transporter knock-out mice. J Neurosci 20:9040–9045.
  4. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, Gershon MD (2001): Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: Abnormal intestinal motility and the expression of cation transporters. J Neurosci 15:6348–6361.
  5. Dao HH, Lemay J, de Champlain J, de Bois D, Moreau P (2001): Norepinephrine-induced aortic hyperplasia and extracellular matrix deposition are endothelin-dependent. J Hypertens 19:1965–1973.
  6. Deng X-F, Rokosh DG, Simpson PC (2000): Autonomous and growth factor-induced hypertrophy in cultured neonatal mouse cardiac myocytes. Comparison with rat. Circ Res 87:781–788.
  7. Eisenhofer G (2001): The role of neuronal and extraneuronal plasma membrane transporters in the inactivation of peripheral catecholamines. Pharmacol Ther 91:35–62.
    External Resources
  8. Falkenburger BH, Barstow KL, Mintz IM (2001): Dendrodendritic inhibition through reversal of dopamine transport. Science 294:2465–2470.
  9. Fiorica-Howells E, Maroteaux L, Gershon, MD (2000): Serotonin and the 5-HT(2B) receptor in the development of enteric neurons. J Neurosci 20:294–305.
  10. Freeman JG, Ryan JJ, Shelburne CP, Bailey DP, Bouton, LA, Narasimhachari N, Domen J, Simeon N, Couderc F, Stewart JK (2001): Catecholamines in murine bone marrow derived mast cells. J Neuroimmunol 119:231–238.
  11. Galli A, Blakely RD, DeFelice LJ (1996): Norepinephrine transporters have channel modes of conduction. Proc Natl Acad Sci USA 93:8671–8676.
  12. Gerevich Z, Tretter L, Adam-Vizi V, Baranyi M, Kiss JP, Zelles T, Vizi ES (2001): Analysis of high intracellular [Na+]-induced release of [3H]noradrenaline in rat hippocampal slices. Neuroscience 104:761–768.
  13. Haller J, Bakos N, Rodriguiz RM, Caron MG, Wetsel WC, Liposits Z (2002): Behavioral responses to social stress in noradrenaline transporter knockout mice: effects on social behavior and depression. Brain Res Bull 58:279–284.
    External Resources
  14. Hallmann R, Mayer DN, Berg EL, Broermann R, Butcher EC (1995): Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood brain barrier. Dev Dyn 202:325–332
  15. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ, Saxena PR, Humphrey PPA (1994): International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol Rev 446:157–203.
  16. Iversen LL (1967): The Uptake and Storage of Noradrenaline in Sympathetic Nerves. New York, Cambridge University Press.
  17. Kirby ML, Gilmore SA (1972): A fluorescence study on the ability of the notochord to synthesize and store catecholamines in early chick embryos. Anat Rec 173:469–478.
  18. Kobayashi K, Morita S, Sawada H, Mizuguchi T, Yamada K, Nagatsu I, Hata T, Watanabe Y, Fujita K, Nagatsu T (1995): Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice. J Biol Chem 270:27235–27243.
  19. Kristufek D, Rudorfer W, Pifl C, Huck S (2002): Organic cation transporter mRNA and function in the rat superior cervical ganglion. J Physiol 15:117–134.
  20. Langeloh A, Bönisch H, Trendelenburg U (1987): The mechanism of the 3H-noradrenaline releasing effect of various substrates of uptake 1: Multifactorial induction of outward transport. Naunyn Schmiedebergs Arch Pharmacol 336:602–610.
  21. Lauder JM, Tamir H, Sadler TW (1988): Serotonin and morphogenesis. 1. Sites of serotonin uptake and -binding protein immunoreactivity in the midgestation mouse embryo. Development 102:709–720.
  22. Lauder JM, Wallace JA, Krebs H, Petrusz P (1980): Serotonin as a timing mechanism in neuroembryogenesis; in Brambilla F, Racagni G, de Wied D (eds): Progress in Psychoendocrinology. Amsterdam, Elsevier.
  23. Lo L, Tiveron MC, Anderson DJ (1998): MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125:609–620.
  24. Moiseiwitsch, RRD, Lauder JM (1995): Serotonin regulates mouse cranial neural crest migration. Proc Natl Acad Sci USA 92:7182–7186.
  25. Moron JA, Brockington A, Wise RA, Rocha BA, Hope BT (2002): Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: Evidence from knock-out mouse lines. J Neurosci 15:389–395.
  26. Newgreen DF, Allan IJ, Young HM, Southwell BR (1981): Accumulation of exogenous catecholamines in the neural tube and non-neuronal tissues of the early fowl embryo. Wilhelm Rouxs Arch 190:320–330.
  27. Nisoli E, Regianini L, Bulbarelli A, Briscinin L, Breacale R, Carruba MO (2001): Protective effects of noradrenaline against tumor necrosis factor-alpha-induced apoptosis in cultured rat brown adipocytes: Role of nitric oxide-induced heat shock protein 70 expression. Int J Obes Relat Metab Disord 25:1421–1430.
  28. Pacholczyk T, Blakely RD, Amara SG (1991): Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature 350:320–353.
  29. Panabieres F, Piechaczyk M, Rainer B, Dani C, Fort P, Riaad S,Marti L, Imbach JL, Jeanteur P, Blanchard, J-MM (1984): Complete nucleotide sequence of the messenger RNA coding for chicken muscle glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Commun 118:767–773.
  30. Pardanaud L, Altmann C, Kitos P, Dieterlen-Lievre F, Buck CA (1987): Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349.
  31. Paton DM (1973): Mechanisms of efflux of noradrenaline from adrenergic nerves in rabbit atria. Br J Pharmacol 49:6114–627.
  32. Pifl C, Singer EA (1999): Ion dependence of carrier-mediated release in dopamine or norepinephrine transporter-transfected cells questions the hypothesis of facilitated exchange diffusion. Mol Pharmacol 56:1047–1054.
  33. Pifl, C, Zezuela J, Spittler A, Kattinger A, Reither H, Caron MG, Hornykiewicz O (2001): Antiproliferative action of dopamine and norepinephrine in neuroblastoma cells expressing the human dopamine transporter. FASEB J 15:1607–1609.
  34. Pönicke K, Schlüter K-D, Heinroth-Hoffman I, Seyfarth T, Goldberg M, Osten B, Piper HM, Brodde O-E (2001): Noradrenaline-induced increase in protein synthesis in adult rat cardiomyocytes: Involvement of only α1A-adrenoceptors. Naunyn Schmiedebergs Arch Pharmacol 264:444–453.
    External Resources
  35. Portbury AL, Chikaraishi DM (2001): The role of norepinephrine and 3 adrenergic receptors in fetal development. Soc Neurosci Abstr 27:838.2.
  36. Povlock SL, Amara SG (1997): The structure and function of norepinephrine, dopamine and serotonin transporters; in Reith MEA (ed): Neurotransmitter Transporters, Structure, Function and Regulation. Totawa, Humane Press, pp 1–28.
  37. Reissmann E, Ernsberger U, Francis-West PH, Rueger D, Brickell PM, Rohrer H (1996): Involvement of bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 122:2079–2088.
  38. Ren ZG, Pörzgen PP, Zhang JM, Chen XR, Amara SG, Blakely RD, Sieber-Blum M (2001): Autocrine regulation of norepinephrine transporter expression. Mol Cell Neurosci 17:539–550.
  39. Rios M, Habecker B, Sasaoka T, Eisenhofer G, Tian H, Landis S, Chikaraishi D, Roffler-Tarnoff S (1999): Catecholamine synthesis is mediated by tyrosinase in the absence of tyrosine hydroxylase. J Neurosci 19:3519–3526.
  40. Rothman TP, Gershon MD, Holtzer H (1978): The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev Biol 65:322–341.
  41. Schomig A, Fischer S, Kurz T, Richardt G, Schomig E (1987): Nonexocytotic release of endogenous noradrenaline in the ischemic and anoxic rat heart: Mechanism and metabolic requirements. Circ Res 60:194–205.
  42. Schroeter S, Apparsundaram S, Wiley RG, Miner LAH, Sesack SR, Blakely RD (2000): Immunolocalization of the cocaine- and antidepressant-sensitive l-norepinephrine transporter. J Comp Neurol 420:211–232.
  43. Shuey DL, Sadler TW, Lauder JM (1992): Serotonin as a regulator of craniofacial morphogenesis: Site-specific malformations following exposure to serotonin uptake inhibitors. Teratology 46:367–378.
  44. Sieber-Blum M (1989): Inhibition of the adrenergic phenotype in cultured neural crest cells by norepinephrine uptake inhibitors. Dev Biol 136:372–380.
  45. Sieber-Blum M, Ren ZG (2000): Norepinephrine transporter expression and function in noradrenergic cell differentiation. Mol Cell Biochem 212:61–70.
    External Resources
  46. Singh K, Xiao L, Remondino A, Sawyer DB, Colucci WS (2001): Adrenergic regulation of cardiac myocyte apoptosis. J Cell Physiol 189:257–265.
  47. Snyder SH (1970): Putative neurotransmitters in the brain: Selective neuronal uptake, subcellular localization, and interactions with centrally acting drugs. Biol Psychiatry 2:367–389.
  48. Strudel G, Recasens M, Mandel P (1977): Identification de catecholamines et de serotonine dans les chordes d’embryons de poulet. CR Acad Sci Paris 284:967–969.
  49. Tessarollo L, Parada LF (1995): In situ hybridization. Methods Enzymol 254:419–430.
  50. Troadec JD, Marien M, Darios F, Hartmann A, Ruberg M, Colpaert F, Michel PP (2001): Noradrenaline provides long-term protection to dopaminergic neurons by reducing oxidative stress. J Neurochem 79:200–210.
  51. Uchida-Oka N, Sugimoto M (2001): Norepinephrine induces apoptosis in skin melanophores by attenuating cAMP-PKA signals via α2-adrenoceptors in the medaka, Oryzias latipes. Pigment Cell Res 14:356–361.
  52. Varley JE, Maxwell GD (1996): BMP-2 and BMP-4, but not BMP-6 increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84–94.
  53. Varley JE, Wehby RG, Rueger DC, Maxwell GD (1995): Number of adrenergic and islet-1 immunoreactive cells increased in avian trunk neural crest cultures in the presence of human recombinant osteogenic protein-1. Dev Dyn 203:434–437.
  54. Wallace JA (1982): Monoamines in the early chick embryo: Demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis. Am J Anat 165:261–276.
  55. Wang RX, Limbird LE (1997): Distribution of mRNA encoding three alpha 2-adrenergic receptor subtypes in the developing mouse embryo suggests a role for the alpha 2A subtype in apoptosis. Mol Pharmacol 52:1071–1080.
  56. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW, Wang YM, Caron MG (2000): Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3:465–471.
  57. Zhang JM, Dix J, Langtimm-Sedlak CJ, Trusk T, Schroeder B, Hoffmann R, Strosberg AD, Winslow JW, Sieber-Blum M (1997): Neurotrophin-3- and norepinephrine-mediated adrenergic differentiation and the inhibitory action of desipramine and cocaine. J Neurobiol 32:262–280.
  58. Zhang J-M, Sieber-Blum M (1992): Characterization of the norepinephrine uptake system and the role of norepinephrine in the expression of the adrenergic phenotype by quail neural crest cells in clonal culture. Brain Res 570:251–258.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: July 24, 2003
Issue release date: July 2003

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 1

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.