A unique talin homologue with a villin headpiece-like domain is required for multicellular morphogenesis in Dictyostelium

Abstract

Molecules involved in the interaction between the extracellular matrix, cell membrane and cytoskeleton are of central importance in morphogenesis. Talin is a large cytoskeletal protein with a modular structure consisting of an amino-terminal membrane-interacting domain, with sequence similarities to members of the band 4.1 family, and a carboxy-terminal region containing F-actin-binding and vinculin-binding domains [1] [2]. It also interacts with the cytoplasmic tail of beta integrins which, on the external face of the membrane, bind to extracellular matrix proteins [3]. The possible roles of talin in multicellular morphogenesis in development remain largely unexplored. In Dictyostelium, a eukaryotic microorganism capable of multicellular morphogenesis, a talin homologue (TALA) has previously been identified and shown to play an important role in cell-to-substrate adhesion and maintenance of normal elastic properties of the cell [4] [5] [6]. Here, we describe a second talin homologue (TALB) that is required for multicellular morphogenesis in the development of Dictyostelium. Unlike any other talin characterised to date, it contains an additional carboxy-terminal domain homologous to the villin headpiece.

Paxillin is required for cell-substrate adhesion, cell sorting and slug migration duringDictyosteliumdevelopment

“…8D,G). It is thought that upper cup cells are especially important in the elevation of the spore mass from the substrate and it may be that these cells need to make especially strong cell-cell and possibly cell matrix contacts (Tsujioka et al, 1999). However, the rescue experiments where paxB was expressed from prestalk-and prespore-specific promoters showed that paxB expression needs to be expressed in prespore and prestalk cells to be able to achieve a complete rescue of development, especially slug migration, showing that all cells in the slug actively contribute to the migration of the slug.…”

“…Actin-rich membrane fragments are left behind by migrating cells (Uchida and Yumura, 2004). Dictyostelium contains no known focal adhesion kinase, but it contains two talin homologues (talA and talB) that have been shown to be important for multicellular development (Kreitmeier et al, 1995;Niewöhner et al, 1997;Tsujioka et al, 1999;Tsujioka et al, 2004). Deletion of talB results in mound arrest.…”

ForC, a novel type of formin family protein lacking an FH1 domain, is involved in multicellular development inDictyostelium discoideum

“…Unlike the case of the gelation factor/α-actinin double mutant and the TalB mutant (Tsujioka et al, 1999;Witke et al, 1992), culmination in ∆forC cells could not be rescued by mixing them with wild-type cells. The lack of a synergy effect suggests that ∆forC cells were sorted out of wild-type cells within aggregates.…”

“…In some mutants, proper function can be restored through synergetic effects elicited by mixing the defective mutants with wild-type cells (Tsujioka et al, 1999;Witke et al, 1992). To test whether adding wild-type cells would rescue the developmental function of ∆forC cells, we allowed ∆forC cells to develop on MES agar plates after mixing them with wild-type cells at various ratios (Fig.…”

“…For instance, a double mutant lacking the actin crosslinking proteins, gelation factor and α-actinin, is unable to develop much beyond the mound stage, even though spore differentiation occurs normally (Witke et al, 1992). Cells lacking TalB, one of the two Dictyostelium homologues of talin, also stop at the mound stage, again despite normal spore differentiation (Tsujioka et al, 1999). Myosin II null mutants also arrest at the mound stage, though in this case viable spores are not formed (De Lozanne and Spudich, 1987;Knecht and Loomis, 1987).…”