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      Src family kinases-mediated negative regulation of sperm acrosome reaction in chickens ( Gallus gallus domesticus)

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          Abstract

          The acrosome reaction (AR) is a strictly-regulated, synchronous exocytosis that is required for sperm to penetrate ova. This all-or-nothing process occurs only once in the sperm lifecycle through a sequence of signaling pathways. Spontaneous, premature AR therefore compromises fertilization potential. Although protein kinase A (PKA) pathways play a central role in AR across species, the signaling network used for AR induction is poorly understood in birds. Mechanistic studies of mammalian sperm AR demonstrate that PKA activity is downstreamly regulated by Src family kinases (SFKs). Using SFK inhibitors, our study shows that in chicken sperm, SFKs play a role in the regulation of PKA activity and spontaneous AR without affecting motility. Furthermore, we examined the nature of SFK phosphorylation using PKA and protein tyrosine phosphatase inhibitors, which demonstrated that unlike in mammals, SFK phosphorylation in birds does not occur downstream of PKA and is primarily regulated by calcium-dependent tyrosine phosphatase activity. Functional characterization of SFKs in chicken sperm showed that SFK activation modulates the membrane potential and plays a role in inhibiting spontaneous AR. Employing biochemical isolation, we also found that membrane rafts are involved in the regulation of SFK phosphorylation. This study demonstrates a unique mechanism for regulating AR induction inherent to avian sperm that ensure fertilization potential despite prolonged storage.

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          Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4

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            Lipid rafts and signal transduction.

            Signal transduction is initiated by complex protein-protein interactions between ligands, receptors and kinases, to name only a few. It is now becoming clear that lipid micro-environments on the cell surface -- known as lipid rafts -- also take part in this process. Lipid rafts containing a given set of proteins can change their size and composition in response to intra- or extracellular stimuli. This favours specific protein-protein interactions, resulting in the activation of signalling cascades.
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              Src family kinases, key regulators of signal transduction.

              The Src family of protein tyrosine kinases (SFKs) plays key roles in regulating signal transduction by a diverse set of cell surface receptors in the context of a variety of cellular environments. SFKs have evolved many ingenious molecular strategies to couple receptors with the cytoplasmic signaling machinery. The contributions to this issue of ONCOGENE describe how this machinery regulates fundamental cellular processes, including cell growth, differentiation, cell shape, migration and survival, and specialized cell signals. The pleiotropic functions of Src and Src family members underscore the importance of these kinases and explain why many of the members of this family have been identified as cellular oncogenes. In this volume, we have attempted to provide the reader with an overview of the current understanding of the function of Src family kinases in the regulation of selected cellular signaling pathways.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: InvestigationRole: Resources
                Role: Resources
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 November 2020
                2020
                : 15
                : 11
                : e0241181
                Affiliations
                [1 ] Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
                [2 ] Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
                Cleveland Clinic, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-1828-9554
                Article
                PONE-D-20-09659
                10.1371/journal.pone.0241181
                7660528
                33180820
                f87a9cad-08bf-41ef-a7ec-04d24db3d004
                © 2020 Priyadarshana et al

                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 credited.

                History
                : 15 April 2020
                : 6 October 2020
                Page count
                Figures: 7, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000646, Japan Society for the Promotion of Science London;
                Award ID: 15K07761
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 17KK0150
                Award Recipient :
                AA received funding for this work from the Japan Society of the Promotion of Science (JSPS) (Project No. 15K07761 and 17KK0150) and from the Sustainable Food Security Research Project in the form of an operational grant from the National University Corporation, Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Germ Cells
                Sperm
                Biology and Life Sciences
                Biochemistry
                Proteins
                Post-Translational Modification
                Phosphorylation
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Fowl
                Gamefowl
                Chickens
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Birds
                Fowl
                Gamefowl
                Chickens
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Poultry
                Chickens
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Birds
                Poultry
                Chickens
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Membrane Potential
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Membrane Potential
                Hyperpolarization
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Amino Acids
                Aromatic Amino Acids
                Tyrosine
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Amino Acids
                Aromatic Amino Acids
                Tyrosine
                Biology and Life Sciences
                Biochemistry
                Proteins
                Amino Acids
                Aromatic Amino Acids
                Tyrosine
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Amino Acids
                Hydroxyl Amino Acids
                Tyrosine
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Amino Acids
                Hydroxyl Amino Acids
                Tyrosine
                Biology and Life Sciences
                Biochemistry
                Proteins
                Amino Acids
                Hydroxyl Amino Acids
                Tyrosine
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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