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Combinatorial topography and cell-type specific regulation of the ERK pathway by dopaminergic agonists in the mouse striatum

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Abstract

Therapeutic agents and drugs of abuse regulate the extracellular signal-regulated kinase (ERK) cascade signaling in the medium-sized spiny neurons (MSNs) of the striatum. However, whether this regulation is associated with specific cortical and thalamic inputs has never been studied. We used Drd2-EGFP BAC-transgenic mice to undertake a topographical and cell-type specific analysis of ERK phosphorylation and two of its downstream targets histone H3 and ribosomal protein S6 (rS6) in the dorsal striatum following injection of SKF81297 (D1R-like agonist), quinpirole (D2R-like agonist) or apomorphine (non selective DA receptor agonist). In striatal areas receiving inputs from the cingulate/prelimbic, visual and auditory cortex, SKF81297 treatment increased phosphorylation of ERK, histone H3 and rS6 selectively in EGFP-negative MSNs of Drd2-EGFP mice. In contrast, no regulation was found in striatal region predominantly targeted by the sensorimotor and motor cortex. Apomorphine slightly enhanced ERK and rS6, but not histone H3 phosphorylation. This regulation occurred exclusively in EGFP-negative neurons mostly in striatal sectors receiving connections from the insular, visual and auditory cortex. Quinpirole administration inhibited basal ERK activation but did not change histone H3 and rS6 phosphorylation throughout the rostrocaudal axis of the dorsal striatum. This anatomo-functional study indicates that D1R and D2R agonists produce a unique topography and cell-type specific regulation of the ERK cascade signaling in the mouse striatum, and that those patterns are closely associated with particular cortical and thalamic inputs. This work evidences the need of a precise identification of the striatal areas under study to further understand striatal plasticity.

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Abbreviations

A:

Auditory cortex

AI:

Agranular insular cortex

Cg:

Cingulate cortex

CL:

Centrolateral nucleus

D1R:

Dopamine 1 receptor

D2R:

Dopamine 2 receptor

EGFP:

Enhanced green fluorescent protein

ERK:

Extracellular signal-regulated kinase

H3:

Histone H3

IL:

Infralimbic cortex

IMD:

Intermediodorsal nucleus

LO:

Lateral orbital cortex

M1/M2:

Motor cortex

MGm:

Medial geniculate nucleus

MSNs:

Medium-sized spiny neurons

PC:

Paracentral nucleus

PFdl:

Dorsolateral parafascicular nucleus

PFvl:

Ventral lateral parafascicular nucleus

PFm:

Medial parafascicular nucleus

PIL:

Posterior intralaminar nucleus

PL:

Prelimbic cortex

PV:

Paraventricular nucleus

rS6:

Ribosomal protein S6

S:

Somatosensory cortex

V:

Visual cortex

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Acknowledgments

This work was supported by Inserm and grants from ATIP-Avenir (Inserm), Sanofi-Aventis R&D and from the Agence Nationale de la Recherche (ANR-2010-JCJC-1412) to Emmanuel Valjent. Giuseppe Gangarossa was supported by a Short-Term fellowship (Ambassade de France). We thank Dr Dimitri De Bundel for comments on the manuscript. We are grateful to Laurent Fagni (Institut de Génomique Fonctionnelle) for providing the transgenic mice used in this study. We thank Fredéric Gallardo and Florence Arnal for animal care, breeding and genotyping.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Institut de Génomique Fonctionnelle, Inserm U661, CNRS UMR 5203, 34094, Montpellier Cedex 05, France

    Giuseppe Gangarossa, Julie Perroy & Emmanuel Valjent

  2. Inserm U661, Montpellier, France

    Giuseppe Gangarossa, Julie Perroy & Emmanuel Valjent

  3. CNRS UMR 5203, Montpellier, France

    Giuseppe Gangarossa, Julie Perroy & Emmanuel Valjent

  4. Université Montpellier I & II, Montpellier, France

    Giuseppe Gangarossa, Julie Perroy & Emmanuel Valjent

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  1. Giuseppe Gangarossa
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  2. Julie Perroy
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  3. Emmanuel Valjent
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Correspondence to Emmanuel Valjent.

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Supplementary Table 1 (DOCX 14 kb)

429_2012_405_MOESM2_ESM.tif

Supplemental Figure 1. Identification of EGFP-expressing striatal neurons in Drd2-EGFP mice. Parvalbumin immunoreactivity (cyan) was detected together with EGFP (green) and DARPP-32 (red) immunoreactivity in the dorsal striatum of Drd2-EGFP mice in a triple fluorescence analysis. Arrowheads (yellow) indicate the position of parvalbumin-positive GABAergic interneurons. Arrows (yellow) indicate the position of cholinergic interneurons, which can be detected in Drd2-EGFP mice (Bertran-Gonzalez et al. 2008; Matamales et al. 2009). Scale bar 30 µm (TIFF 716 kb)

429_2012_405_MOESM3_ESM.tif

Supplemental Figure 2. SKF81297 induces ERK activation in DARPP-32-expressing neurons. P-ERK immunoreactivity (red) was detected together with DARPP-32 (blue) and EGFP (green) immunoreactivity in the striatal sector receiving afferents from the cingulate cortex of Drd2-EGFP mice treated with vehicle or SKF81297 (5 mg/kg) in a triple fluorescence analysis. Arrowheads (yellow) illustrate P-ERK/DARPP-32-positive cells and the complete lack of co-localization with EGFP-expressing neurons revealing that SKF81297-induced ERK activation is restricted in D1R-containing MSNs. Scale bar: 50 µm (TIFF 893 kb)

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Gangarossa, G., Perroy, J. & Valjent, E. Combinatorial topography and cell-type specific regulation of the ERK pathway by dopaminergic agonists in the mouse striatum. Brain Struct Funct 218, 405–419 (2013). https://doi.org/10.1007/s00429-012-0405-6

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