Teneurin and TCAP Phylogeny and Physiology: Molecular Analysis, Immune Activity, and Transcriptomic Analysis of the Stress Response in the Sydney Rock Oyster (Saccostrea glomerata) Hemocytes

Tomer Abramov; Saowaros Suwansa-Ard; Patricia Mirella da Silva; Tianfang Wang; Michael Dove; Wayne O'Connor; Laura Parker; David A Lovejoy; Scott F Cummins; Abigail Elizur

doi:10.3389/fendo.2022.891714

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Teneurin and TCAP Phylogeny and Physiology: Molecular Analysis, Immune Activity, and Transcriptomic Analysis of the Stress Response in the Sydney Rock Oyster (Saccostrea glomerata) Hemocytes

Journal article

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Teneurin and TCAP Phylogeny and Physiology: Molecular Analysis, Immune Activity, and Transcriptomic Analysis of the Stress Response in the Sydney Rock Oyster (Saccostrea glomerata) Hemocytes

Tomer Abramov, Saowaros Suwansa-Ard, Patricia Mirella da Silva, Tianfang Wang, Michael Dove, Wayne O'Connor, Laura Parker, David A Lovejoy, Scott F Cummins and Abigail Elizur

Frontiers in Endocrinology , Vol.13, pp.1-19

2022

DOI: https://doi.org/10.3389/fendo.2022.891714

PMID: 35784537

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Abstract

teneurin

TCAP

stress

metabolism

ROS

phagocytosis

hemocytes

oyster

Teneurin C-terminal associated peptide (TCAP) is an ancient bioactive peptide that is highly conserved in metazoans. TCAP administration reduces cellular and behavioral stress in vertebrate and urochordate models. There is little information for invertebrates regarding the existence or function of a TCAP. This study used the Sydney rock oyster (SRO) as a molluscan model to characterize an invertebrate TCAP, from molecular gene analysis to its physiological effects associated with hemocyte phagocytosis. We report a single teneurin gene (and 4 teneurin splice variants), which encodes a precursor with TCAP that shares a vertebrate-like motif, and is similar to that of other molluscan classes (gastropod, cephalopod), arthropods and echinoderms. TCAP was identified in all SRO tissues using western blotting at 1-2 different molecular weights (~22 kDa and ~37kDa), supporting precursor cleavage variation. In SRO hemolymph, TCAP was spatially localized to the cytosol of hemocytes, and with particularly high density immunoreactivity in granules. Based on ‘pull-down’ assays, the SRO TCAP binds to GAPDH, suggesting that TCAP may protect cells from apoptosis under oxidative stress. Compared to sham injection, the intramuscular administration of TCAP (5 pmol) into oysters modulated their immune system by significantly reducing hemocyte phagocytosis under stress conditions (low salinity and high temperature). TCAP administration also significantly reduced hemocyte reactive oxygen species production at ambient conditions and after 48 h stress, compared to sham injection. Transcriptomic hemocyte analysis of stressed oysters administered with TCAP demonstrated significant changes in expression of genes associated with key metabolic, protective and immune functions. In summary, this study established a role for TCAP in oysters through modulation of physiological and molecular functions associated with energy conservation, stress and cellular defense.

Details

Title: Teneurin and TCAP Phylogeny and Physiology: Molecular Analysis, Immune Activity, and Transcriptomic Analysis of the Stress Response in the Sydney Rock Oyster (Saccostrea glomerata) Hemocytes
Authors: Tomer Abramov (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Saowaros Suwansa-Ard (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Patricia Mirella da Silva (Author) - Universidade Federal da Paraíba
Tianfang Wang (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Michael Dove (Author) - New South Wales Department of Primary Industries
Wayne O'Connor (Author) - New South Wales Department of Primary Industries
Laura Parker (Author) - UNSW Australia
David A Lovejoy (Author) - University of Toronto
Scott F Cummins (Author) - University of the Sunshine Coast, Queensland, School of Science, Technology and Engineering
Abigail Elizur (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Publication details: Frontiers in Endocrinology , Vol.13, pp.1-19
Publisher: Frontiers Research Foundation
Date published: 2022
DOI: 10.3389/fendo.2022.891714
ISSN: 1664-2392
PMID: 35784537
Copyright note: © 2022 Abramov, Suwansa-ard, da Silva, Wang, Dove, O’Connor, Parker, Lovejoy, Cummins and Elizur. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Data Availability: The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi. nlm.nih.gov/, PRJNA804582.
Grants: The basis of oyster resilience to global environmental change, IN190100051, Australian Research Council (Australia, Canberra) - ARC
Future Oysters CRC-P, 0980024282, Cooperative Research Centres
Organisation Unit: GeneCology Research Centre - Legacy; School of Science, Technology and Engineering; Centre for Bioinnovation
Language: English
Record Identifier: 99654998702621
Output Type: Journal article

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Web Of Science research areas: Endocrinology & Metabolism

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