Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus (original) (raw)

Abstract

D1 dopamine receptor localization was examined by immunohistochemistry using a polyclonal anti-peptide antibody which (i) immunoprecipitated a protein fragment encoded by a D1 receptor cDNA and (ii) on Western blots of solubilized striatal and hippocampal membranes recognized two proteins of approximately 50 kDa and 75 kDa, corresponding to reported sizes of D1 receptor proteins. Immunoreactivity overlapped with dopamine-containing pathways, patterns of D1 receptor binding, and mRNA expression. Staining was concentrated in prefrontal, cingulate, parietal, piriform, entorhinal, and hippocampal cortical areas and subcortically in the basal ganglia, amygdala, septal area, substantia inominata, thalamus, hypothalamus, and neurohypophysis. Prominent labeling was seen in the thalamic reticular nucleus, a region known to integrate ascending basal forebrain inputs with thalamocortical and corticothalamic pathways and in fiber bundles interconnecting limbic areas. In striatal neuropil, staining appeared in spines (heads and necks), at postsynaptic sites in dendrites, and in axon terminals; in the pars reticulata of the substantia nigra, labeling was prevalent in myelinated and unmyelinated axons and dendrites. These data provide direct evidence for the regional and subcellular distribution of D1 receptor protein in the brain and for its pre- and postsynaptic localization in the basal ganglia. The prominent immunoreactivity seen in the limbic system and thalamic reticular nucleus supports an important role for this receptor subtype in mediating integrative processes involved with learning, memory, and cognition.

11988

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altar C. A., Hauser K. Topography of substantia nigra innervation by D1 receptor-containing striatal neurons. Brain Res. 1987 Apr 28;410(1):1–11. doi: 10.1016/s0006-8993(87)80014-8. [DOI] [PubMed] [Google Scholar]
  2. Amlaiky N., Berger J. G., Chang W., McQuade R. J., Caron M. G. Identification of the binding subunit of the D1-dopamine receptor by photoaffinity crosslinking. Mol Pharmacol. 1987 Feb;31(2):129–134. [PubMed] [Google Scholar]
  3. Bunzow J. R., Van Tol H. H., Grandy D. K., Albert P., Salon J., Christie M., Machida C. A., Neve K. A., Civelli O. Cloning and expression of a rat D2 dopamine receptor cDNA. Nature. 1988 Dec 22;336(6201):783–787. doi: 10.1038/336783a0. [DOI] [PubMed] [Google Scholar]
  4. Carlson J. H., Bergstrom D. A., Walters J. R. Stimulation of both D1 and D2 dopamine receptors appears necessary for full expression of postsynaptic effects of dopamine agonists: a neurophysiological study. Brain Res. 1987 Jan 6;400(2):205–218. doi: 10.1016/0006-8993(87)90619-6. [DOI] [PubMed] [Google Scholar]
  5. Clark D., White F. J. D1 dopamine receptor--the search for a function: a critical evaluation of the D1/D2 dopamine receptor classification and its functional implications. Synapse. 1987;1(4):347–388. doi: 10.1002/syn.890010408. [DOI] [PubMed] [Google Scholar]
  6. Cortés R., Gueye B., Pazos A., Probst A., Palacios J. M. Dopamine receptors in human brain: autoradiographic distribution of D1 sites. Neuroscience. 1989;28(2):263–273. doi: 10.1016/0306-4522(89)90178-4. [DOI] [PubMed] [Google Scholar]
  7. Cortés R., Probst A., Palacios J. M. Decreased densities of dopamine D1 receptors in the putamen and hippocampus in senile dementia of the Alzheimer type. Brain Res. 1988 Dec 13;475(1):164–167. doi: 10.1016/0006-8993(88)90212-0. [DOI] [PubMed] [Google Scholar]
  8. Dawson T. M., Barone P., Sidhu A., Wamsley J. K., Chase T. N. The D1 dopamine receptor in the rat brain: quantitative autoradiographic localization using an iodinated ligand. Neuroscience. 1988 Jul;26(1):83–100. doi: 10.1016/0306-4522(88)90129-7. [DOI] [PubMed] [Google Scholar]
  9. Dearry A., Gingrich J. A., Falardeau P., Fremeau R. T., Jr, Bates M. D., Caron M. G. Molecular cloning and expression of the gene for a human D1 dopamine receptor. Nature. 1990 Sep 6;347(6288):72–76. doi: 10.1038/347072a0. [DOI] [PubMed] [Google Scholar]
  10. DiFiglia M., Christakos S., Aronin N. Ultrastructural localization of immunoreactive calbindin-D28k in the rat and monkey basal ganglia, including subcellular distribution with colloidal gold labeling. J Comp Neurol. 1989 Jan 22;279(4):653–665. doi: 10.1002/cne.902790411. [DOI] [PubMed] [Google Scholar]
  11. Dubois A., Savasta M., Curet O., Scatton B. Autoradiographic distribution of the D1 agonist [3H]SKF 38393, in the rat brain and spinal cord. Comparison with the distribution of D2 dopamine receptors. Neuroscience. 1986 Sep;19(1):125–137. doi: 10.1016/0306-4522(86)90010-2. [DOI] [PubMed] [Google Scholar]
  12. Fremeau R. T., Jr, Duncan G. E., Fornaretto M. G., Dearry A., Gingrich J. A., Breese G. R., Caron M. G. Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3772–3776. doi: 10.1073/pnas.88.9.3772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freund T. F., Powell J. F., Smith A. D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience. 1984 Dec;13(4):1189–1215. doi: 10.1016/0306-4522(84)90294-x. [DOI] [PubMed] [Google Scholar]
  14. Girault J. A., Spampinato U., Glowinski J., Besson M. J. In vivo release of [3H]gamma-aminobutyric acid in the rat neostriatum--II. Opposing effects of D1 and D2 dopamine receptor stimulation in the dorsal caudate putamen. Neuroscience. 1986 Dec;19(4):1109–1117. doi: 10.1016/0306-4522(86)90127-2. [DOI] [PubMed] [Google Scholar]
  15. Grandy D. K., Zhang Y. A., Bouvier C., Zhou Q. Y., Johnson R. A., Allen L., Buck K., Bunzow J. R., Salon J., Civelli O. Multiple human D5 dopamine receptor genes: a functional receptor and two pseudogenes. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9175–9179. doi: 10.1073/pnas.88.20.9175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grandy D. K., Zhang Y. A., Bouvier C., Zhou Q. Y., Johnson R. A., Allen L., Buck K., Bunzow J. R., Salon J., Civelli O. Multiple human D5 dopamine receptor genes: a functional receptor and two pseudogenes. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9175–9179. doi: 10.1073/pnas.88.20.9175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Joyce J. N., Lexow N., Bird E., Winokur A. Organization of dopamine D1 and D2 receptors in human striatum: receptor autoradiographic studies in Huntington's disease and schizophrenia. Synapse. 1988;2(5):546–557. doi: 10.1002/syn.890020511. [DOI] [PubMed] [Google Scholar]
  18. Kebabian J. W., Beaulieu M., Itoh Y. Pharmacological and biochemical evidence for the existence of two categories of dopamine receptor. Can J Neurol Sci. 1984 Feb;11(1 Suppl):114–117. doi: 10.1017/s0317167100046254. [DOI] [PubMed] [Google Scholar]
  19. Kelleher D. J., Rashidbaigi A., Ruoho A. E., Johnson G. L. Rapid vesicle reconstitution of alprenolol-Sepharose-purified beta 1-adrenergic receptors. Interaction of the purified receptor with N. J Biol Chem. 1983 Nov 10;258(21):12881–12885. [PubMed] [Google Scholar]
  20. Lidow M. S., Goldman-Rakic P. S., Gallager D. W., Rakic P. Distribution of dopaminergic receptors in the primate cerebral cortex: quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390. Neuroscience. 1991;40(3):657–671. doi: 10.1016/0306-4522(91)90003-7. [DOI] [PubMed] [Google Scholar]
  21. Mansour A., Meador-Woodruff J. H., Bunzow J. R., Civelli O., Akil H., Watson S. J. Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J Neurosci. 1990 Aug;10(8):2587–2600. doi: 10.1523/JNEUROSCI.10-08-02587.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mansour A., Meador-Woodruff J. H., Zhou Q. Y., Civelli O., Akil H., Watson S. J. A comparison of D1 receptor binding and mRNA in rat brain using receptor autoradiographic and in situ hybridization techniques. Neuroscience. 1991;45(2):359–371. doi: 10.1016/0306-4522(91)90233-e. [DOI] [PubMed] [Google Scholar]
  23. McVittie L. D., Ariano M. A., Sibley D. R. Characterization of anti-peptide antibodies for the localization of D2 dopamine receptors in rat striatum. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1441–1445. doi: 10.1073/pnas.88.4.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Molloy A. G., Waddington J. L. Dopaminergic behaviour stereospecific promoted by the D1 agonist R-SK & F 38393 and selectively blocked by the D1 antagonist SCH 23390. Psychopharmacology (Berl) 1984;82(4):409–410. doi: 10.1007/BF00427697. [DOI] [PubMed] [Google Scholar]
  25. Monsma F. J., Jr, Mahan L. C., McVittie L. D., Gerfen C. R., Sibley D. R. Molecular cloning and expression of a D1 dopamine receptor linked to adenylyl cyclase activation. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6723–6727. doi: 10.1073/pnas.87.17.6723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Niznik H. B., Jarvie K. R., Bzowej N. H., Seeman P., Garlick R. K., Miller J. J., Jr, Baindur N., Neumeyer J. L. Photoaffinity labeling of dopamine D1 receptors. Biochemistry. 1988 Oct 4;27(20):7594–7599. doi: 10.1021/bi00420a004. [DOI] [PubMed] [Google Scholar]
  27. Ongini E., Caporali M. G., Massotti M. Stimulation of dopamine D-1 receptors by SKF 38393 induces EEG desynchronization and behavioral arousal. Life Sci. 1985 Dec 16;37(24):2327–2333. doi: 10.1016/0024-3205(85)90025-6. [DOI] [PubMed] [Google Scholar]
  28. Pickel V. M., Beckley S. C., Joh T. H., Reis D. J. Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum. Brain Res. 1981 Nov 30;225(2):373–385. doi: 10.1016/0006-8993(81)90843-x. [DOI] [PubMed] [Google Scholar]
  29. Sawaguchi T., Goldman-Rakic P. S. D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science. 1991 Feb 22;251(4996):947–950. doi: 10.1126/science.1825731. [DOI] [PubMed] [Google Scholar]
  30. Schalling M., Djurfeldt M., Hökfelt T., Ehrlich M., Kurihara T., Greengard P. Distribution and cellular localization of DARPP-32 mRNA in rat brain. Brain Res Mol Brain Res. 1990 Feb;7(2):139–149. doi: 10.1016/0169-328x(90)90091-q. [DOI] [PubMed] [Google Scholar]
  31. Sidhu A. A novel affinity purification of D-1 dopamine receptors from rat striatum. J Biol Chem. 1990 Jun 15;265(17):10065–10072. [PubMed] [Google Scholar]
  32. Sokoloff P., Giros B., Martres M. P., Bouthenet M. L., Schwartz J. C. Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics. Nature. 1990 Sep 13;347(6289):146–151. doi: 10.1038/347146a0. [DOI] [PubMed] [Google Scholar]
  33. Steriade M., Domich L., Oakson G. Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance. J Neurosci. 1986 Jan;6(1):68–81. doi: 10.1523/JNEUROSCI.06-01-00068.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tourtellotte W. G., Van Hoesen G. W., Hyman B. T., Tikoo R. K., Damasio A. R. Alz-50 immunoreactivity in the thalamic reticular nucleus in Alzheimer's disease. Brain Res. 1990 May 7;515(1-2):227–234. doi: 10.1016/0006-8993(90)90600-g. [DOI] [PubMed] [Google Scholar]
  35. Van Tol H. H., Bunzow J. R., Guan H. C., Sunahara R. K., Seeman P., Niznik H. B., Civelli O. Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine. Nature. 1991 Apr 18;350(6319):610–614. doi: 10.1038/350610a0. [DOI] [PubMed] [Google Scholar]
  36. Zhou Q. Y., Grandy D. K., Thambi L., Kushner J. A., Van Tol H. H., Cone R., Pribnow D., Salon J., Bunzow J. R., Civelli O. Cloning and expression of human and rat D1 dopamine receptors. Nature. 1990 Sep 6;347(6288):76–80. doi: 10.1038/347076a0. [DOI] [PubMed] [Google Scholar]