Universität zu Köln

Hatzold, Julia ORCID: 0000-0002-5491-1921, Wessendorf, Heike, Pogoda, Hans-Martin, Bloch, Wilhelm and Hammerschmidt, Matthias (2021). The Kunitz-type serine protease inhibitor Spint2 is required for cellular cohesion, coordinated cell migration and cell survival during zebrafish hatching gland development. Dev. Biol., 476. S. 148 - 171. SAN DIEGO: ACADEMIC PRESS INC ELSEVIER SCIENCE. ISSN 1095-564X

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Abstract

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.

Item Type:	Journal Article
Creators:	Creators Email ORCID ORCID Put Code Hatzold, Julia UNSPECIFIED orcid.org/0000-0002-5491-1921 UNSPECIFIED Wessendorf, Heike UNSPECIFIED UNSPECIFIED UNSPECIFIED Pogoda, Hans-Martin UNSPECIFIED UNSPECIFIED UNSPECIFIED Bloch, Wilhelm UNSPECIFIED UNSPECIFIED UNSPECIFIED Hammerschmidt, Matthias UNSPECIFIED UNSPECIFIED UNSPECIFIED
URN:	urn:nbn:de:hbz:38-574539
DOI:	10.1016/j.ydbio.2021.03.017
Journal or Publication Title:	Dev. Biol.
Volume:	476
Page Range:	S. 148 - 171
Date:	2021
Publisher:	ACADEMIC PRESS INC ELSEVIER SCIENCE
Place of Publication:	SAN DIEGO
ISSN:	1095-564X
Language:	English
Faculty:	Unspecified
Divisions:	Unspecified
Subjects:	no entry
Uncontrolled Keywords:	Keywords Language FACTOR ACTIVATOR INHIBITOR; ANCHORAGE-INDEPENDENT GROWTH; E-CADHERIN; EPITHELIAL INTEGRITY; TRANSGENIC ZEBRAFISH; MOLECULAR PATHWAYS; EXPRESSION; MATRIPTASE; CANCER; METASTASIS Multiple languages Developmental Biology Multiple languages
URI:	http://kups.ub.uni-koeln.de/id/eprint/57453