The Nkd EF-hand domain modulates divergent wnt signaling outputs in zebrafish

Autumn N Marsden; Sarah W Derry; Igor Schneider; C Anthony Scott; Trudi A Westfall; Lindy K Brastrom; Madeline A Shea; Deborah V Dawson; Diane C Slusarski

doi:10.1016/j.ydbio.2017.11.012

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The Nkd EF-hand domain modulates divergent wnt signaling outputs in zebrafish

Journal article

Peer reviewed

The Nkd EF-hand domain modulates divergent wnt signaling outputs in zebrafish

Autumn N Marsden, Sarah W Derry, Igor Schneider, C Anthony Scott, Trudi A Westfall, Lindy K Brastrom, Madeline A Shea, Deborah V Dawson and Diane C Slusarski

Developmental biology, Vol.434(1), pp.63-73

02/01/2018

DOI: 10.1016/j.ydbio.2017.11.012

PMID: 29180104

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Abstract

Wnt proteins regulate diverse biological responses by initiating two general outcomes: β-catenin-dependent transcription and β-catenin-independent activation of signaling cascades, the latter including modulation of calcium and regulation of cytoskeletal dynamics (Planar Cell Polarity, PCP). It has been difficult to elucidate the mechanisms by which Wnt signals are directed to effect one or the other outcome due to shared signaling proteins between the β-catenin-dependent and -independent pathways, such as the Dishevelled binding protein Naked. While all Naked paralogs contain a putative calcium-binding domain, the EF-Hand, Drosophila Naked does not bind calcium. Here we find a lineage-specific evolutionary change within the Drosophila Naked EF-hand that is not shared with other insects or vertebrates. We demonstrate the necessary role of the EF-hand for Nkd localization changes in calcium fluxing cells and using in vivo assays, we identify a role for the zebrafish Naked EF-hand in PCP but not in β-catenin antagonism. In contrast, Drosophila-like Nkd does not function in PCP, but is a robust antagonist of Wnt/β-catenin signaling. This work reveals that the zebrafish Nkd1 EF-hand is essential to balance Wnt signaling inputs and modulate the appropriate outputs, while the Drosophila-like EF-Hand primarily functions in β-catenin signaling.

Carrier Proteins - genetics

Animals

Carrier Proteins - metabolism

Calcium - metabolism

Zebrafish Proteins - metabolism

Calcium Signaling - physiology

Zebrafish - metabolism

Wnt Signaling Pathway - physiology

Zebrafish Proteins - genetics

Zebrafish - genetics

Details

Title: Subtitle: The Nkd EF-hand domain modulates divergent wnt signaling outputs in zebrafish
Creators: Autumn N Marsden - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Sarah W Derry - Department of Biology, University of Iowa, Iowa City, IA 52242, USA; Drake University, Des Moines, IA 50311, USA
Igor Schneider - Department of Biology, University of Iowa, Iowa City, IA 52242, USA; Instituto de Ciencias Biologicas, Universidade Federal do Para, Belem 66075-110, Brazil
C Anthony Scott - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Trudi A Westfall - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Lindy K Brastrom - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Madeline A Shea - Department of Biochemistry, University of Iowa, UA 52242, USA
Deborah V Dawson - Departments of Pediatric Dentistry&Biostatistics, University of Iowa, Iowa City 52242, USA
Diane C Slusarski - Department of Biology, University of Iowa, Iowa City, IA 52242, USA. Electronic address: diane-slusarski@uiowa.edu
Resource Type: Journal article
Publication Details: Developmental biology, Vol.434(1), pp.63-73
DOI: 10.1016/j.ydbio.2017.11.012
PMID: 29180104
NLM abbreviation: Dev Biol
ISSN: 0012-1606
eISSN: 1095-564X
Publisher: United States
Grant note: DOI: 10.13039/100000968, name: American Heart Association
Language: English
Date published: 02/01/2018
Academic Unit: Molecular Physiology and Biophysics; Iowa Neuroscience Institute; Biostatistics; Biology; Pediatric Dentistry; Biochemistry and Molecular Biology
Record Identifier: 9983991999602771

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