Differential Expression of Drosophila Transgelins Throughout Development.

Katerina M Vakaloglou,Maria Mouratidou,Athina Keramidioti,Christos G Zervas

doi:10.3389/fcell.2021.648568

Abstract

Transgelins are a conserved family of actin-binding proteins involved in cytoskeletal remodeling, cell contractility, and cell shape. In both mammals and Drosophila, three genes encode transgelin proteins. Transgelins exhibit a broad and overlapping expression pattern, which has obscured the precise identification of their role in development. Here, we report the first systematic developmental analysis of all Drosophila transgelin proteins, namely, Mp20, CG5023, and Chd64 in the living organism. Drosophila transgelins display overall higher sequence identity with mammalian TAGLN-3 and TAGLN-2 than with TAGLN. Detailed examination in different developmental stages revealed that Mp20 and CG5023 are predominantly expressed in mesodermal tissues with the onset of myogenesis and accumulate in the cytoplasm of all somatic muscles and heart in the late embryo. Notably, at postembryonic developmental stages, Mp20 and CG5023 are detected in the gut’s circumferential muscles with distinct subcellular localization: Z-lines for Mp20 and sarcomere and nucleus for CG5023. Only CG5023 is strongly detected in the adult fly in the abdominal, leg, and synchronous thoracic muscles. Chd64 protein is primarily expressed in endodermal and ectodermal tissues and has a dual subcellular localization in the cytoplasm and the nucleus. During the larval–pupae transition, Chd64 is expressed in the brain, eye, legs, halteres, and wings. In contrast, in the adult fly, Chd64 is expressed in epithelia, including the alimentary tract and genitalia. Based on the non-overlapping tissue expression, we predict that Mp20 and CG5023 mostly cooperate to modulate muscle function, whereas Chd64 has distinct roles in epithelial, neuronal, and endodermal tissues.

Highlights

Actin networks are fundamental cellular scaffolds that provide structural integrity in most cell types and modulate cellular contractility
Transgelin proteins are encoded by three genes that display differential tissue expression: (a) TAGLN which is abundantly expressed in visceral and vascular smooth muscle cells (LeesMiller et al, 1987; Lawson et al, 1997; Camoretti-Mercado et al, 1998; Assinder et al, 2009); (b) TAGLN2 which is expressed in a wide variety of tissues and organs including smooth muscle cells, lung epithelium, gut, ovary, nephrons, pancreas, and T cells of the immune system (Zhang et al, 2002; Na et al, 2015; Meng et al, 2017; Yin et al, 2019)
We compared the protein sequence of all three Drosophila transgelins with their mouse and human homologs and confirmed the strong conservation of both calponin homology domain (CH)-domain and CLR (Supplementary Figure 1A)

Summary

Introduction

Actin networks are fundamental cellular scaffolds that provide structural integrity in most cell types and modulate cellular contractility. Transgelins encompass an actin-binding protein family, well-conserved from yeast to human, implicated in cytoskeleton remodeling (Shapland et al, 1988; Assinder et al, 2009; Liu et al, 2020). Transgelin proteins are encoded by three genes that display differential tissue expression: (a) TAGLN (or SM22a) which is abundantly expressed in visceral and vascular smooth muscle cells (LeesMiller et al, 1987; Lawson et al, 1997; Camoretti-Mercado et al, 1998; Assinder et al, 2009); (b) TAGLN2 (or SM22β) which is expressed in a wide variety of tissues and organs including smooth muscle cells, lung epithelium, gut, ovary, nephrons, pancreas, and T cells of the immune system (Zhang et al, 2002; Na et al, 2015; Meng et al, 2017; Yin et al, 2019). TAGLN2 elevated expression has been associated with progression of colorectal cancer (Zhang et al, 2010; Elsafadi et al, 2020); (c) TAGLN3 ( known as NP22 or NP25) is predominantly expressed in the nervous system (Ren et al, 1994; Depaz and Wilce, 2006)

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