Lack of dopaminergic inputs elongates the primary cilia of striatal neurons

Ko Miyoshi, Kyosuke Kasahara, Shinki Murakami, Mika Takeshima, Natsuko Kumamoto, Asako Sato, Ikuko Miyazaki, Shinsuke Matsuzaki, Toshikuni Sasaoka, Taiichi Katayama, Masato Asanuma

Research output: Contribution to journalArticle

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Abstract

In the rodent brain, certain G protein-coupled receptors and adenylyl cyclase type 3 are known to localize to the neuronal primary cilium, a primitive sensory organelle protruding singly from almost all neurons. A recent chemical screening study demonstrated that many compounds targeting dopamine receptors regulate the assembly of Chlamydomonas reinhardtii flagella, structures which are analogous to vertebrate cilia. Here we investigated the effects of dopaminergic inputs loss on the architecture of neuronal primary cilia in the rodent striatum, a brain region that receives major dopaminergic projections from the midbrain. We first analyzed the lengths of neuronal cilia in the dorsolateral striatum of hemiparkinsonian rats with unilateral lesions of the nigrostriatal dopamine pathway. In these rats, the striatal neuronal cilia were significantly longer on the lesioned side than on the non-lesioned side. In mice, the repeated injection of reserpine, a dopamine-depleting agent, elongated neuronal cilia in the striatum. The combined administration of agonists for dopamine receptor type 2 (D2) with reserpine attenuated the elongation of striatal neuronal cilia. Repeated treatment with an antagonist of D2, but not of dopamine receptor type 1 (D1), elongated the striatal neuronal cilia. In addition, D2-null mice displayed longer neuronal cilia in the striatum compared to wild-type controls. Reserpine treatment elongated the striatal neuronal cilia in D1-null mice but not in D2-null mice. Repeated treatment with a D2 agonist suppressed the elongation of striatal neuronal cilia on the lesioned side of hemi-parkinsonian rats. These results suggest that the elongation of striatal neuronal cilia following the lack of dopaminergic inputs is attributable to the absence of dopaminergic transmission via D2 receptors. Our results provide the first evidence that the length of neuronal cilia can be modified by the lack of a neurotransmitter's input.

Original languageEnglish
Article numbere97918
JournalPLoS One
Volume9
Issue number5
DOIs
Publication statusPublished - May 15 2014

Fingerprint

Corpus Striatum
Cilia
Reserpine
cilia
Neurons
Rats
Elongation
neurons
Dopamine Receptors
Dopamine
Brain
Dopamine Agonists
G-Protein-Coupled Receptors
Adenylyl Cyclases
reserpine
Neurotransmitter Agents
Screening
mice
dopamine
brain

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Miyoshi, K., Kasahara, K., Murakami, S., Takeshima, M., Kumamoto, N., Sato, A., ... Asanuma, M. (2014). Lack of dopaminergic inputs elongates the primary cilia of striatal neurons. PLoS One, 9(5), [e97918]. https://doi.org/10.1371/journal.pone.0097918

Lack of dopaminergic inputs elongates the primary cilia of striatal neurons. / Miyoshi, Ko; Kasahara, Kyosuke; Murakami, Shinki; Takeshima, Mika; Kumamoto, Natsuko; Sato, Asako; Miyazaki, Ikuko; Matsuzaki, Shinsuke; Sasaoka, Toshikuni; Katayama, Taiichi; Asanuma, Masato.

In: PLoS One, Vol. 9, No. 5, e97918, 15.05.2014.

Research output: Contribution to journalArticle

Miyoshi, K, Kasahara, K, Murakami, S, Takeshima, M, Kumamoto, N, Sato, A, Miyazaki, I, Matsuzaki, S, Sasaoka, T, Katayama, T & Asanuma, M 2014, 'Lack of dopaminergic inputs elongates the primary cilia of striatal neurons', PLoS One, vol. 9, no. 5, e97918. https://doi.org/10.1371/journal.pone.0097918
Miyoshi K, Kasahara K, Murakami S, Takeshima M, Kumamoto N, Sato A et al. Lack of dopaminergic inputs elongates the primary cilia of striatal neurons. PLoS One. 2014 May 15;9(5). e97918. https://doi.org/10.1371/journal.pone.0097918
Miyoshi, Ko ; Kasahara, Kyosuke ; Murakami, Shinki ; Takeshima, Mika ; Kumamoto, Natsuko ; Sato, Asako ; Miyazaki, Ikuko ; Matsuzaki, Shinsuke ; Sasaoka, Toshikuni ; Katayama, Taiichi ; Asanuma, Masato. / Lack of dopaminergic inputs elongates the primary cilia of striatal neurons. In: PLoS One. 2014 ; Vol. 9, No. 5.
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