Diverse Roles of Axonemal Dyneins in Drosophila Auditory Neuron Function and Mechanical Amplification in Hearing

Somdatta Karak; Julie S Jacobs; Maike Kittelmann; Christian Spalthoff; Radoslaw Katana; Elena Sivan-Loukianova; Michael A Schon; Maurice J Kernan; Daniel F Eberl; Martin C Göpfert

doi:10.1038/srep17085

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Diverse Roles of Axonemal Dyneins in Drosophila Auditory Neuron Function and Mechanical Amplification in Hearing

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Diverse Roles of Axonemal Dyneins in Drosophila Auditory Neuron Function and Mechanical Amplification in Hearing

Somdatta Karak, Julie S Jacobs, Maike Kittelmann, Christian Spalthoff, Radoslaw Katana, Elena Sivan-Loukianova, Michael A Schon, Maurice J Kernan, Daniel F Eberl and Martin C Göpfert

Scientific reports, Vol.5(1), pp.17085-17085

11/26/2015

DOI: 10.1038/srep17085

PMCID: PMC4660584

PMID: 26608786

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Abstract

Much like vertebrate hair cells, the chordotonal sensory neurons that mediate hearing in Drosophila are motile and amplify the mechanical input of the ear. Because the neurons bear mechanosensory primary cilia whose microtubule axonemes display dynein arms, we hypothesized that their motility is powered by dyneins. Here, we describe two axonemal dynein proteins that are required for Drosophila auditory neuron function, localize to their primary cilia, and differently contribute to mechanical amplification in hearing. Promoter fusions revealed that the two axonemal dynein genes Dmdnah3 (=CG17150) and Dmdnai2 (=CG6053) are expressed in chordotonal neurons, including the auditory ones in the fly's ear. Null alleles of both dyneins equally abolished electrical auditory neuron responses, yet whereas mutations in Dmdnah3 facilitated mechanical amplification, amplification was abolished by mutations in Dmdnai2. Epistasis analysis revealed that Dmdnah3 acts downstream of Nan-Iav channels in controlling the amplificatory gain. Dmdnai2, in addition to being required for amplification, was essential for outer dynein arms in auditory neuron cilia. This establishes diverse roles of axonemal dyneins in Drosophila auditory neuron function and links auditory neuron motility to primary cilia and axonemal dyneins. Mutant defects in sperm competition suggest that both dyneins also function in sperm motility.

Ear - physiology

Axonemal Dyneins - metabolism

Male

Spermatozoa - metabolism

Drosophila Proteins - metabolism

Mutation - genetics

Drosophila melanogaster - metabolism

TRPV Cation Channels - metabolism

Animals

Epistasis, Genetic

Hearing - physiology

Neurons - metabolism

Auditory Pathways - metabolism

Details

Title: Subtitle: Diverse Roles of Axonemal Dyneins in Drosophila Auditory Neuron Function and Mechanical Amplification in Hearing
Creators: Somdatta Karak - Department of Cellular Neurobiology, University of Göttingen, 37077 Göttingen, Germany
Julie S Jacobs - Biology Department, University of Iowa, Iowa City, IA 52242
Maike Kittelmann - Department of Cellular Neurobiology, University of Göttingen, 37077 Göttingen, Germany
Christian Spalthoff - Department of Cellular Neurobiology, University of Göttingen, 37077 Göttingen, Germany
Radoslaw Katana - Department of Cellular Neurobiology, University of Göttingen, 37077 Göttingen, Germany
Elena Sivan-Loukianova - Biology Department, University of Iowa, Iowa City, IA 52242
Michael A Schon - Biology Department, University of Iowa, Iowa City, IA 52242
Maurice J Kernan - Department of Neurobiology and Behavior and Center for Developmental Genetics, Stony Brook University, Stony Brook, NY 11794
Daniel F Eberl - Biology Department, University of Iowa, Iowa City, IA 52242
Martin C Göpfert - Department of Cellular Neurobiology, University of Göttingen, 37077 Göttingen, Germany
Resource Type: Journal article
Publication Details: Scientific reports, Vol.5(1), pp.17085-17085
DOI: 10.1038/srep17085
PMID: 26608786
PMCID: PMC4660584
NLM abbreviation: Sci Rep
ISSN: 2045-2322
eISSN: 2045-2322
Publisher: England
Grant note: R01 DC011357 / NIDCD NIH HHS DC011357 / NIDCD NIH HHS P30 DC010362 / NIDCD NIH HHS
Language: English
Date published: 11/26/2015
Academic Unit: Iowa Neuroscience Institute; Biology; Internal Medicine
Record Identifier: 9983992100102771

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