Immunohistochemical Localization of AMPA-type Glutamate Receptor Subunits in the Striatum of Rhesus Monkey

Overview

Journal Brain Res

Specialty Neurology

Date 2010 May 13

PMID 20460117

Citations 14

Authors

Yun-Ping Deng

Evan Shelby

Anton J Reiner

Affiliations

Soon will be listed here.

Abstract

Corticostriatal and thalamostriatal projections utilize glutamate as their neurotransmitter. Their influence on striatum is mediated, in part, by ionotropic AMPA-type glutamate receptors, which are heteromers composed of GluR1-4 subunits. While the cellular localization of AMPA-type subunits in the basal ganglia has been well characterized in rodents, the cellular localization of AMPA subunits in primate basal ganglia is not. We thus carried out immunohistochemical studies of GluR1-4 distribution in rhesus monkey basal ganglia in conjunction with characterization of each major neuron type. In striatum, about 65% of striatal neurons immunolabeled for GluR1, 75%-79% immunolabeled for GluR2 or GluR2/3, and only 2.5% possessed GluR4. All neurons the large size of cholinergic interneurons (mean diameter 26.1 microm) were moderately labeled for GluR1, while all neurons in the size range of parvalbuminergic interneurons (mean diameter 13.8 microm) were intensely rich in GluR1. Additionally, somewhat more than half of the neurons in the size range of projection neurons (mean diameter 11.6 microm) immunolabeled for GluR1, and about one third of these were very rich in GluR1. About half of the neurons the size of cholinergic interneurons were immunolabeled for GluR2, and the remainder of the neurons that were immunolabeled for GluR2 coincided with projection neurons in size and shape (GluR2 diameter=10.7 microm), indicating that the vast majority of striatal projection neurons possess immunodectible GluR2. Similar results were observed with GluR2/3 immunolabeling. Half of the neurons the size of cholinergic interneurons immunolabeled for GluR4 and seemingly all neurons in the size range of parvalbuminergic interneurons possessed GluR4. These results indicate that AMPA receptor subunit combinations for striatal projection neurons in rhesus monkey are similar to those for the corresponding neuron types in rodents, and thus their AMPA responses to glutamate are likely to be similar to those demonstrated in rodents.

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References

Bennett B, Bolam J . Two populations of calbindin D28k-immunoreactive neurones in the striatum of the rat. Brain Res. 1993; 610(2):305-10. DOI: 10.1016/0006-8993(93)91414-n. View

Tomiyama M, Palacios J, Cortes R, Vilaro M, Mengod G . Distribution of AMPA receptor subunit mRNAs in the human basal ganglia: an in situ hybridization study. Brain Res Mol Brain Res. 1997; 46(1-2):281-9. DOI: 10.1016/s0169-328x(97)00022-3. View

Anderson K, Chen Q, Veenman C, Reiner A . Relative survival of striatal projection neurons and interneurons after intrastriatal injection of quinolinic acid in rats. Exp Neurol. 1994; 129(1):37-56. DOI: 10.1006/exnr.1994.1145. View

Chen Q, Surmeier D, Reiner A . NMDA and non-NMDA receptor-mediated excitotoxicity are potentiated in cultured striatal neurons by prior chronic depolarization. Exp Neurol. 1999; 159(1):283-96. DOI: 10.1006/exnr.1999.7135. View

Sager C, Tapken D, Kott S, Hollmann M . Functional modulation of AMPA receptors by transmembrane AMPA receptor regulatory proteins. Neuroscience. 2008; 158(1):45-54. DOI: 10.1016/j.neuroscience.2007.12.046. View

Chen Q, Veenman L, Knopp K, Yan Z, Medina L, Song W . Evidence for the preferential localization of glutamate receptor-1 subunits of AMPA receptors to the dendritic spines of medium spiny neurons in rat striatum. Neuroscience. 1998; 83(3):749-61. DOI: 10.1016/s0306-4522(97)00452-1. View

Mullen R, Buck C, Smith A . NeuN, a neuronal specific nuclear protein in vertebrates. Development. 1992; 116(1):201-11. DOI: 10.1242/dev.116.1.201. View

Tallaksen-Greene S, Albin R . Localization of AMPA-selective excitatory amino acid receptor subunits in identified populations of striatal neurons. Neuroscience. 1994; 61(3):509-19. DOI: 10.1016/0306-4522(94)90430-8. View

Zimmermann L, Schwaller B . Monoclonal antibodies recognizing epitopes of calretinins: dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium. 2002; 31(1):13-25. DOI: 10.1054/ceca.2001.0255. View

10.

Popoli P, Pintor A, Domenici M, Frank C, Tebano M, Pezzola A . Blockade of striatal adenosine A2A receptor reduces, through a presynaptic mechanism, quinolinic acid-induced excitotoxicity: possible relevance to neuroprotective interventions in neurodegenerative diseases of the striatum. J Neurosci. 2002; 22(5):1967-75. PMC: 6758877. View

11.

Iihara K, Joo D, Henderson J, Sattler R, Taverna F, Lourensen S . The influence of glutamate receptor 2 expression on excitotoxicity in Glur2 null mutant mice. J Neurosci. 2001; 21(7):2224-39. PMC: 6762387. View

12.

BRIZZEE K, Ordy J, Kaack B . Early appearance and regional differences in intraneuronal and extraneuronal lipofuscin accumulation with age in the brain of a nonhuman primate (Macaca mulatta). J Gerontol. 1974; 29(4):366-81. DOI: 10.1093/geronj/29.4.366. View

13.

Saper C . Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol. 1996; 364(1):5. DOI: 10.1002/(SICI)1096-9861(19960101)364:1<5::AID-CNE1>3.0.CO;2-9. View

14.

Martin L, Blackstone C, Huganir R, Price D . The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J Neurosci. 1993; 13(2):782-92. PMC: 6576641. View

15.

Feldmeyer D, Kask K, Brusa R, Kornau H, Kolhekar R, Rozov A . Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat Neurosci. 1999; 2(1):57-64. DOI: 10.1038/4561. View

16.

Deng Y, Albin R, Penney J, Young A, Anderson K, Reiner A . Differential loss of striatal projection systems in Huntington's disease: a quantitative immunohistochemical study. J Chem Neuroanat. 2004; 27(3):143-64. DOI: 10.1016/j.jchemneu.2004.02.005. View

17.

VUILLET J, Kerkerian L, Kachidian P, Bosler O, Nieoullon A . Ultrastructural correlates of functional relationships between nigral dopaminergic or cortical afferent fibers and neuropeptide Y-containing neurons in the rat striatum. Neurosci Lett. 1989; 100(1-3):99-104. DOI: 10.1016/0304-3940(89)90667-8. View

18.

DiFiglia M . Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci. 1990; 13(7):286-9. DOI: 10.1016/0166-2236(90)90111-m. View

19.

Richardson P, Dixon A, Lee K, Bell M, Cox P, Williams R . Correlating physiology with gene expression in striatal cholinergic neurones. J Neurochem. 2000; 74(2):839-46. DOI: 10.1046/j.1471-4159.2000.740839.x. View

20.

Petralia R, Wenthold R . Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol. 1992; 318(3):329-54. DOI: 10.1002/cne.903180309. View