Home LiteratureArticle Details
PMID: 3357895 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

D1-type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 85 ·No. 8 ·1988-04-00 ·Pages 2839-43

Lankford KL, DeMello FG, Klein WL

Abstract

Precedent exists for the early development and subsequent down-regulation of neurotransmitter receptor systems in the vertebrate central nervous system, but the function of such embryonic receptors has not been established. Here we show that stimulation of early-developing dopamine receptors in avian retina cells greatly inhibits the motility of neuronal growth cones. Neurons from embryonic chicken retinas were cultured in low-density monolayers, and their growth cones were observed with phase-contrast or video-enhanced-contrast-differential-interference-contrast (VEC-DIC) microscopy. Approximately 25% of the neurons responded to micromolar dopamine with a rapid reduction in filopodial activity followed by a flattening of growth cones and retraction of neurites. The response occurred at all ages examined (embryonic day-8 retinal neurons cultured on polylysine-coated coverslips for 1-7 days), although neurite retraction was greatest in younger cultures. Effects of dopamine on growth cone function could be reversed by haloperidol or (+)-SCH 23390, whereas forskolin elicited a response similar to dopamine; these data show the response was receptor-mediated, acting through a D1-type system, and are consistent with the use of cAMP as a second messenger. The experiments provide strong support for the hypothesis that neurotransmitters, besides mediating transynaptic signaling in the adult, may have a role in neuronal differentiation as growth regulators.

MeSH Terms
Adenylyl Cyclases/metabolism Animals Cell Differentiation Cells, Cultured Chick Embryo Colforsin/pharmacology Dopamine/pharmacology Dopamine Antagonists Growth Inhibitors Morphogenesis Receptors, Dopamine/physiology Retina/cytology,growth & development
Chemicals
Dopamine Antagonists Growth Inhibitors Receptors, Dopamine Colforsin Adenylyl Cyclases Dopamine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lankford K L
Department of Neurobiology and Physiology, Northwestern University, Evanston, IL 60201.
DeMello F G
Klein W L
References (58)
58 references, click to expand
  1. Ca2+ and pH affect the neurite formation in cultured mollusc isolated neurones.
    Brain Res. 1983 Oct 3;276(1):43-50 PMID: 6627000
  2. Studies on the mechanism determining the course of nerve fibers in tissue culture. I. The reaction of the growth cone to various obstructions.
    Z Zellforsch Mikrosk Anat. 1959;51:108-22 PMID: 14425885
  3. DARPP-32, a dopamine- and adenosine 3':5'-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. I. Regional and cellular distribution in the rat brain.
    J Neurosci. 1984 Jan;4(1):84-98 PMID: 6319627
  4. Differential ontogenesis of D1 and D2 dopaminergic receptors in the chick embryo retina.
    Brain Res. 1984 Feb;314(2):217-23 PMID: 6200189
  5. New neuronal growth factors.
    Annu Rev Neurosci. 1984;7:149-70 PMID: 6143526
  6. Embryonic development of monoaminergic neurons in the chick retina.
    J Comp Neurol. 1984 Apr 10;224(3):437-44 PMID: 6425366
  7. Blockers of calcium permeability inhibit neurite extension and formation of neuromuscular synapses in cell culture.
    Brain Res. 1984 Jun;316(2):263-70 PMID: 6467017
  8. Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons.
    Science. 1984 Nov 2;226(4674):561-4 PMID: 6093252
  9. Perturbation of the direction of neurite growth by pulsed and focal electric fields.
    J Neurosci. 1984 Dec;4(12):2939-47 PMID: 6502213
  10. Novel organization of microtubules in cultured central nervous system neurons: formation of hairpin loops at ends of maturing neurites.
    J Neurosci. 1984 Dec;4(12):3002-13 PMID: 6502218
  11. Two dopamine receptors: biochemistry, physiology and pharmacology.
    Life Sci. 1984 Dec 3;35(23):2281-96 PMID: 6390056
  12. The role of centralized computer services in faculty evaluation.
    Comput Nurs. 1986 Nov-Dec;4(6):259-64 PMID: 3641647
  13. Topographical organization of the dopamine-dependent adenylate cyclase of the chick embryo retina.
    Brain Res. 1985 Feb 25;328(1):59-63 PMID: 2982467
  14. Expression of A1 adenosine receptors modulating dopamine-dependent cyclic AMP accumulation in the chick embryo retina.
    J Neurochem. 1985 Mar;44(3):845-51 PMID: 2579199
  15. Neuron-specific growth cone properties as seen in identified neurons of Helisoma.
    J Neurosci Res. 1985;13(1-2):135-47 PMID: 3973929
  16. Guidance of neurite outgrowth by pathways of substratum-adsorbed laminin.
    J Neurosci Res. 1985;13(1-2):213-20 PMID: 3973933
  17. Growth cones and the formation of central and peripheral neurites by sensory neurones in amphibian embryos.
    J Neurosci Res. 1985;13(1-2):23-38 PMID: 3871863
  18. Response of nerve growth cone to focal electric currents.
    J Neurosci Res. 1985;13(1-2):245-56 PMID: 3973935
  19. Phosphorylation of the calcium antagonist receptor of the voltage-sensitive calcium channel by cAMP-dependent protein kinase.
    Proc Natl Acad Sci U S A. 1985 Apr;82(8):2528-32 PMID: 2581248
  20. In vitro phosphorylation of microtubule-associated protein 2: differential effects of cyclic AMP analogues.
    J Neurochem. 1985 Oct;45(4):1218-22 PMID: 2993522
  21. Binding of [3H]SCH23390 in rat brain: regional distribution and effects of assay conditions and GTP suggest interactions at a D1-like dopamine receptor.
    J Neurochem. 1985 Nov;45(5):1601-11 PMID: 2864398
  22. Differentiation of neuronal growth cones: specialization of filopodial tips for adhesive interactions.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8256-60 PMID: 3865227
  23. Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors.
    J Neurochem. 1986 Apr;46(4):1006-21 PMID: 2869104
  24. Suppression of neurite elongation and growth cone motility by electrical activity.
    Science. 1986 Jun 27;232(4758):1638-40 PMID: 3715470
  25. Neurosciences advance in basic and clinical realms.
    Science. 1986 Dec 12;234(4782):1324-6 PMID: 2431480
  26. Surface movements during the growth of single explanted neurons.
    Proc Natl Acad Sci U S A. 1970 Apr;65(4):905-10 PMID: 5266160
  27. A protein binding assay for adenosine 3':5'-cyclic monophosphate.
    Proc Natl Acad Sci U S A. 1970 Sep;67(1):305-12 PMID: 4318781
  28. Cell locomotion, nerve elongation, and microfilaments.
    Dev Biol. 1973 Feb;30(2):427-40 PMID: 4703680
  29. Selective growth of sympathetic nerve fibers to explants of normally densely innervated autonomic effector organs in tissue culture.
    Dev Biol. 1973 Apr;31(2):362-79 PMID: 4799092
  30. On the synaptogenic sequence in the chick retina.
    Anat Rec. 1974 Jul;179(3):297-301 PMID: 4837763
  31. The stimulation of calcium transport in cardiac sarcoplasmic reticulum by adenosine 3':5'-monophosphate-dependent protein kinase.
    J Biol Chem. 1974 Oct 10;249(19):6174-80 PMID: 4371608
  32. Phosphorylation of a 22,000-dalton component of the cardiac sarcoplasmic reticulum by adenosine 3':5'-monophosphate-dependent protein kinase.
    J Biol Chem. 1975 Apr 10;250(7):2640-7 PMID: 235523
  33. Cell-to-substratum adhesion and guidance of axonal elongation.
    Dev Biol. 1975 May;44(1):92-101 PMID: 1132591
  34. The role of microtubules in the growth and stabilization of nerve fibers.
    Ann N Y Acad Sci. 1975 Jun 30;253:535-44 PMID: 167634
  35. Receptor-mediated shifts in cGMP and cAMP levels in neuroblastoma cells.
    Proc Natl Acad Sci U S A. 1975 Sep;72(9):3472-6 PMID: 171662
  36. Differentiation of chick embryo neuroretina cells in monolayer cultures. An ultrastructural study. I. Seven-day retina.
    Cell Tissue Res. 1977 Dec 13;185(2):159-73 PMID: 563768
  37. The ontogeny of dopamine-dependent increase of adenosine 3',5'-cyclic monophosphate in the chick retina.
    J Neurochem. 1978 Oct;31(4):1049-53 PMID: 212530
  38. Chemotactic response of nerve fiber elongation to nerve growth factor.
    Dev Biol. 1978 Sep;66(1):183-96 PMID: 751835
  39. Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation.
    Exp Cell Res. 1979 Nov;124(1):127-38 PMID: 499378
  40. Inhibition of microtubule assembly by phosphorylation of microtubule-associated proteins.
    Biochemistry. 1980 May 27;19(11):2472-9 PMID: 7387985
  41. Neurite outgrowth induced by the substrate associated material from nonneuronal cells.
    Dev Biol. 1980 Sep;79(1):247-52 PMID: 7409323
  42. Calcium conductances in Purkinje cell dendrites: their role in development and integration.
    Prog Brain Res. 1979;51:323-34 PMID: 551484
  43. Characterization of the turning response of dorsal root neurites toward nerve growth factor.
    J Cell Biol. 1980 Dec;87(3 Pt 1):546-54 PMID: 6257725
  44. Polyornithine-attached neurite-promoting factors (PNPFs). Culture sources and responsive neurons.
    Brain Res. 1981 Feb 9;206(1):129-44 PMID: 7470880
  45. Optical recording of calcium action potentials from growth cones of cultured neurons with a laser microbeam.
    Science. 1981 Jun 5;212(4499):1164-7 PMID: 7233210
  46. Oriented extracellular channels and axonal guidance in the embryonic chick retina.
    Dev Biol. 1981 May;84(1):41-50 PMID: 7250501
  47. Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3363-7 PMID: 6267587
  48. Studies on the localization of newly added membrane in growing neurites.
    J Neurobiol. 1981 Nov;12(6):591-8 PMID: 7310397
  49. Neural retina development in vitro. Effects of tissue extracts on cell survival and neuritic development in purified neuronal cultures.
    Dev Neurosci. 1982;5(1):40-53 PMID: 7106016
  50. Regulation of dopamine- and adenosine-dependent adenylate cyclase systems of chicken embryo retina cells in culture.
    Proc Natl Acad Sci U S A. 1982 Sep;79(18):5708-12 PMID: 6291061
  51. Localization of voltage-sensitive calcium channels along developing neurites: their possible role in regulating neurite elongation.
    Dev Biol. 1982 Dec;94(2):351-65 PMID: 6295852
  52. The classification of dopamine receptors: relationship to radioligand binding.
    Annu Rev Neurosci. 1983;6:43-71 PMID: 6220666
  53. Short-latency local actions of nerve growth factor at the growth cone.
    Proc Natl Acad Sci U S A. 1983 May;80(9):2789-93 PMID: 6302705
  54. Neuronal growth cones.
    Annu Rev Physiol. 1983;45:567-80 PMID: 6342524
  55. Ultrastructural networks in growth cones and neurites of cultured central nervous system neurons.
    Proc Natl Acad Sci U S A. 1983 Sep;80(18):5779-83 PMID: 6577454
  56. Membrane biogenesis in the sprouting neuron. I. Selective transfer of newly synthesized phospholipid into the growing neurite.
    J Cell Biol. 1983 Oct;97(4):1038-42 PMID: 6194160
  57. A transient embryonic dopamine receptor inhibits growth cone motility and neurite outgrowth in a subset of avian retina neurons.
    Neurosci Lett. 1987 Mar 31;75(2):169-74 PMID: 2952906
  58. DARPP-32, a dopamine- and adenosine 3':5'-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization.
    J Neurosci. 1984 Jan;4(1):111-24 PMID: 6319625
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.85.8.2839
Published
1988-04-00
Pages
2839-43
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC280095
Subset
IM
Grants
NICHD NIH HHS · HD07068 · United States
NINDS NIH HHS · NS21234 · United States
External Links
PubMed source DOI: 10.1073/pnas.85.8.2839 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2