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
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...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Endocrinology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fendo.2022.891714/full |
| _version_ | 1811337410016968704 |
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| author | Tomer Abramov Tomer Abramov Saowaros Suwansa-ard Patricia Mirella da Silva Tianfang Wang Tianfang Wang Michael Dove Wayne O’Connor Laura Parker David A. Lovejoy Scott F. Cummins Scott F. Cummins Abigail Elizur |
| author_facet | Tomer Abramov Tomer Abramov Saowaros Suwansa-ard Patricia Mirella da Silva Tianfang Wang Tianfang Wang Michael Dove Wayne O’Connor Laura Parker David A. Lovejoy Scott F. Cummins Scott F. Cummins Abigail Elizur |
| author_sort | Tomer Abramov |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T17:54:29Z |
| format | Article |
| id | doaj.art-c349c82d92834122b750398d26cea2b0 |
| institution | Directory Open Access Journal |
| issn | 1664-2392 |
| language | English |
| last_indexed | 2024-04-13T17:54:29Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Endocrinology |
| spelling | doaj.art-c349c82d92834122b750398d26cea2b02022-12-22T02:36:33ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922022-06-011310.3389/fendo.2022.891714891714Teneurin and TCAP Phylogeny and Physiology: Molecular Analysis, Immune Activity, and Transcriptomic Analysis of the Stress Response in the Sydney Rock Oyster (Saccostrea glomerata) HemocytesTomer Abramov0Tomer Abramov1Saowaros Suwansa-ard2Patricia Mirella da Silva3Tianfang Wang4Tianfang Wang5Michael Dove6Wayne O’Connor7Laura Parker8David A. Lovejoy9Scott F. Cummins10Scott F. Cummins11Abigail Elizur12Centre for Bioinnovation, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaSchool of Science, Technology and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaCentre for Bioinnovation, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaInvertebrate Immunology and Pathology Laboratory, Department of Molecular Biology, Federal University of Paraíba, João Pessoa, BrazilCentre for Bioinnovation, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaSchool of Science, Technology and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaNew South Wales (NSW) Department of Primary Industries, Port Stephens Fisheries Institute, João Pessoa, Para´ıba, Taylors Beach, NSW, AustraliaNew South Wales (NSW) Department of Primary Industries, Port Stephens Fisheries Institute, João Pessoa, Para´ıba, Taylors Beach, NSW, AustraliaSchool of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW, AustraliaDepartment of Cell and Systems Biology, University of Toronto, Toronto, ON, CanadaCentre for Bioinnovation, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaSchool of Science, Technology and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaCentre for Bioinnovation, University of the Sunshine Coast, Sippy Downs, QLD, AustraliaTeneurin 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.https://www.frontiersin.org/articles/10.3389/fendo.2022.891714/fullteneurinTCAPstressmetabolismROSphagocytosis |
| spellingShingle | Tomer Abramov Tomer Abramov Saowaros Suwansa-ard Patricia Mirella da Silva Tianfang Wang Tianfang Wang Michael Dove Wayne O’Connor Laura Parker David A. Lovejoy Scott F. Cummins Scott F. Cummins Abigail Elizur 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 Frontiers in Endocrinology teneurin TCAP stress metabolism ROS phagocytosis |
| 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 |
| title_full | 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 |
| title_fullStr | 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 |
| title_full_unstemmed | 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 |
| title_short | 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 |
| title_sort | 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 |
| topic | teneurin TCAP stress metabolism ROS phagocytosis |
| url | https://www.frontiersin.org/articles/10.3389/fendo.2022.891714/full |
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