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In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)

BACKGROUND: The importance of visual sense in Hymenopteran social behavior is suggested by the existence of a Hymenopteran insect-specific neural circuit related to visual processing and the fact that worker honeybee brain changes morphologically according to its foraging experience. To analyze mole...

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Autores principales: Kaneko, Kumi, Hori, Sayaka, Morimoto, Mai M., Nakaoka, Takayoshi, Paul, Rajib Kumar, Fujiyuki, Tomoko, Shirai, Kenichi, Wakamoto, Akiko, Tsuboko, Satomi, Takeuchi, Hideaki, Kubo, Takeo
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2821913/
https://www.ncbi.nlm.nih.gov/pubmed/20169065
http://dx.doi.org/10.1371/journal.pone.0009213
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author Kaneko, Kumi
Hori, Sayaka
Morimoto, Mai M.
Nakaoka, Takayoshi
Paul, Rajib Kumar
Fujiyuki, Tomoko
Shirai, Kenichi
Wakamoto, Akiko
Tsuboko, Satomi
Takeuchi, Hideaki
Kubo, Takeo
author_facet Kaneko, Kumi
Hori, Sayaka
Morimoto, Mai M.
Nakaoka, Takayoshi
Paul, Rajib Kumar
Fujiyuki, Tomoko
Shirai, Kenichi
Wakamoto, Akiko
Tsuboko, Satomi
Takeuchi, Hideaki
Kubo, Takeo
author_sort Kaneko, Kumi
collection PubMed
description BACKGROUND: The importance of visual sense in Hymenopteran social behavior is suggested by the existence of a Hymenopteran insect-specific neural circuit related to visual processing and the fact that worker honeybee brain changes morphologically according to its foraging experience. To analyze molecular and neural bases that underlie the visual abilities of the honeybees, we used a cDNA microarray to search for gene(s) expressed in a neural cell-type preferential manner in a visual center of the honeybee brain, the optic lobes (OLs). METHODOLOGY/PRINCIPAL FINDINGS: Expression analysis of candidate genes using in situ hybridization revealed two genes expressed in a neural cell-type preferential manner in the OLs. One is a homologue of Drosophila futsch, which encodes a microtubule-associated protein and is preferentially expressed in the monopolar cells in the lamina of the OLs. The gene for another microtubule-associated protein, tau, which functionally overlaps with futsch, was also preferentially expressed in the monopolar cells, strongly suggesting the functional importance of these two microtubule-associated proteins in monopolar cells. The other gene encoded a homologue of Misexpression Suppressor of Dominant-negative Kinase Suppressor of Ras 2 (MESK2), which might activate Ras/MAPK-signaling in Drosophila. MESK2 was expressed preferentially in a subclass of neurons located in the ventral region between the lamina and medulla neuropil in the OLs, suggesting that this subclass is a novel OL neuron type characterized by MESK2-expression. These three genes exhibited similar expression patterns in the worker, drone, and queen brains, suggesting that they function similarly irrespective of the honeybee sex or caste. CONCLUSIONS: Here we identified genes that are expressed in a monopolar cell (Amfutsch and Amtau) or ventral medulla-preferential manner (AmMESK2) in insect OLs. These genes may aid in visualizing neurites of monopolar cells and ventral medulla cells, as well as in analyzing the function of these neurons.
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spelling pubmed-28219132010-02-19 In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.) Kaneko, Kumi Hori, Sayaka Morimoto, Mai M. Nakaoka, Takayoshi Paul, Rajib Kumar Fujiyuki, Tomoko Shirai, Kenichi Wakamoto, Akiko Tsuboko, Satomi Takeuchi, Hideaki Kubo, Takeo PLoS One Research Article BACKGROUND: The importance of visual sense in Hymenopteran social behavior is suggested by the existence of a Hymenopteran insect-specific neural circuit related to visual processing and the fact that worker honeybee brain changes morphologically according to its foraging experience. To analyze molecular and neural bases that underlie the visual abilities of the honeybees, we used a cDNA microarray to search for gene(s) expressed in a neural cell-type preferential manner in a visual center of the honeybee brain, the optic lobes (OLs). METHODOLOGY/PRINCIPAL FINDINGS: Expression analysis of candidate genes using in situ hybridization revealed two genes expressed in a neural cell-type preferential manner in the OLs. One is a homologue of Drosophila futsch, which encodes a microtubule-associated protein and is preferentially expressed in the monopolar cells in the lamina of the OLs. The gene for another microtubule-associated protein, tau, which functionally overlaps with futsch, was also preferentially expressed in the monopolar cells, strongly suggesting the functional importance of these two microtubule-associated proteins in monopolar cells. The other gene encoded a homologue of Misexpression Suppressor of Dominant-negative Kinase Suppressor of Ras 2 (MESK2), which might activate Ras/MAPK-signaling in Drosophila. MESK2 was expressed preferentially in a subclass of neurons located in the ventral region between the lamina and medulla neuropil in the OLs, suggesting that this subclass is a novel OL neuron type characterized by MESK2-expression. These three genes exhibited similar expression patterns in the worker, drone, and queen brains, suggesting that they function similarly irrespective of the honeybee sex or caste. CONCLUSIONS: Here we identified genes that are expressed in a monopolar cell (Amfutsch and Amtau) or ventral medulla-preferential manner (AmMESK2) in insect OLs. These genes may aid in visualizing neurites of monopolar cells and ventral medulla cells, as well as in analyzing the function of these neurons. Public Library of Science 2010-02-16 /pmc/articles/PMC2821913/ /pubmed/20169065 http://dx.doi.org/10.1371/journal.pone.0009213 Text en Kaneko et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kaneko, Kumi
Hori, Sayaka
Morimoto, Mai M.
Nakaoka, Takayoshi
Paul, Rajib Kumar
Fujiyuki, Tomoko
Shirai, Kenichi
Wakamoto, Akiko
Tsuboko, Satomi
Takeuchi, Hideaki
Kubo, Takeo
In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title_full In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title_fullStr In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title_full_unstemmed In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title_short In Situ Hybridization Analysis of the Expression of Futsch, Tau, and MESK2 Homologues in the Brain of the European Honeybee (Apis mellifera L.)
title_sort in situ hybridization analysis of the expression of futsch, tau, and mesk2 homologues in the brain of the european honeybee (apis mellifera l.)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2821913/
https://www.ncbi.nlm.nih.gov/pubmed/20169065
http://dx.doi.org/10.1371/journal.pone.0009213
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