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Tytuł:
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The Kunitz-type serine protease inhibitor Spint2 is required for cellular cohesion, coordinated cell migration and cell survival during zebrafish hatching gland development.
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Autorzy:
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Hatzold J; Institute of Zoology - Developmental Biology, University of Cologne, Cologne, Germany. Electronic address: .
Wessendorf H; Institute of Zoology - Developmental Biology, University of Cologne, Cologne, Germany.
Pogoda HM; Institute of Zoology - Developmental Biology, University of Cologne, Cologne, Germany.
Bloch W; Institute of Cardiology and Sports Medicine, German Sport University Cologne, Cologne, Germany.
Hammerschmidt M; Institute of Zoology - Developmental Biology, University of Cologne, Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany; Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, Cologne, Germany.
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Źródło:
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Developmental biology [Dev Biol] 2021 Aug; Vol. 476, pp. 148-170. Date of Electronic Publication: 2021 Apr 04.
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Typ publikacji:
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Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
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Język:
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English
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Imprint Name(s):
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Publication: San Diego, CA : Elsevier
Original Publication: New York.
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MeSH Terms:
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Cell Adhesion/*physiology
Proteinase Inhibitory Proteins, Secretory/*genetics
Serine Proteinase Inhibitors/*metabolism
Animals ; Cadherins ; Cell Adhesion/genetics ; Cell Adhesion Molecules/genetics ; Cell Movement/physiology ; Cell Survival/physiology ; Epidermis/metabolism ; Epithelial Cells/metabolism ; Gene Expression/genetics ; Gene Expression Regulation, Developmental/genetics ; Membrane Glycoproteins/genetics ; Membrane Glycoproteins/metabolism ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Organogenesis ; Proteinase Inhibitory Proteins, Secretory/metabolism ; Serine Proteinase Inhibitors/genetics ; Zebrafish/embryology ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism
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Grant Information:
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R01 GM063904 United States GM NIGMS NIH HHS; R56 GM063904 United States GM NIGMS NIH HHS
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Contributed Indexing:
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Keywords: Cell death; Cohesion; Collective cell migration; E-cadherin; Hatching gland; Morphogenesis; Spint2; Zebrafish
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Substance Nomenclature:
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0 (Cadherins)
0 (Cell Adhesion Molecules)
0 (Membrane Glycoproteins)
0 (Membrane Proteins)
0 (Proteinase Inhibitory Proteins, Secretory)
0 (Serine Proteinase Inhibitors)
0 (Zebrafish Proteins)
0 (spint1a protein, zebrafish)
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Entry Date(s):
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Date Created: 20210407 Date Completed: 20211012 Latest Revision: 20220802
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Update Code:
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20240104
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PubMed Central ID:
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PMC8820232
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DOI:
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10.1016/j.ydbio.2021.03.017
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PMID:
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33826923
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We have previously shown that the Kunitz-type serine protease inhibitor Spint1a, also named Hai1a, is required in the zebrafish embryonic epidermis to restrict the activity of the type II transmembrane serine protease (TTSP) Matriptase1a/St14a, thereby ensuring epidermal homeostasis. A closely related Kunitz-type inhibitor is Spint2/Hai2, which in mammals plays multiple developmental roles that are either redundant or non-redundant with those of Spint1. However, the molecular bases for these non-redundancies are not fully understood. Here, we study spint2 during zebrafish development. It is co-expressed with spint1a in multiple embryonic epithelia, including the outer/peridermal layer of the epidermis. However, unlike spint1a, spint2 expression is absent from the basal epidermal layer but present in hatching gland cells. Hatching gland cells derive from the mesendodermal prechordal plate, from where they undergo a thus far undescribed transit into, and coordinated sheet migration within, the interspace between the outer and basal layer of the epidermis to reach their final destination on the yolk sac. Hatching gland cells usually survive their degranulation that drives embryo hatching but die several days later. In spint2 mutants, cohesion among hatching gland cells and their collective intra-epidermal migration are disturbed, leading to a discontinuous organization of the gland. In addition, cells undergo precocious cell death before degranulation, so that embryos fail to hatch. Chimera analyses show that Spint2 is required in hatching gland cells, but not in the overlying periderm, their potential migration and adhesion substrate. Spint2 acts independently of all tested Matriptases, Prostasins and other described Spint1 and Spint2 mediators. However, it displays a tight genetic interaction with and acts at least partly via the cell-cell adhesion protein E-cadherin, promoting both hatching gland cell cohesiveness and survival, in line with formerly reported effects of E-cadherin during morphogenesis and cell death suppression. In contrast, no such genetic interaction was observed between Spint2 and the cell-cell adhesion molecule EpCAM, which instead interacts with Spint1a. Our data shed new light onto the mechanisms of hatching gland morphogenesis and hatching gland cell survival. In addition, they reveal developmental roles of Spint2 that are strikingly different from those of Spint1, most likely due to differences in the expression patterns and relevant target proteins.
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