The Drosophila tamou gene, a component of the activating pathway of extramacrochaetae expression, encodes a protein homologous to mammalian cell-cell junction-associated protein ZO-1.

Abstract

In Drosophila sensory organ development, the balance of activities between proneural genes and repressor genes defines a proneural cluster as a population of competent cells for neural development. In this study, we report the isolation and analysis of the tamou [tain) gene that encodes a cell-cell junction-associated protein, which is homologous to mammalian ZO-1, a member of the membrane-associated guanylate kinase homolog family. The tarn mutation reduces the transcription of a repressor gene, extramacrochaetae, and causes enlargement of a proneural cluster where supernumerary precursor cells emerge, resulting in extra mechanosensory organs in the fly. These results suggest that the membrane-associated Tam protein is involved in the signaling pathway that activates emc expression.[Key Woids: Diosophila-, sensory organ formation; MAGUK protein; emc gene; ZO-1 homolog; signal transduction] Received March 15, 1996; revised version accepted May 30, 1996.The Diosophila peripheral nervous system comprises several types of sensory organs, including external mech anosensory and chemosensory organs, internal tension receptors, and touch receptors. The distribution patterns and position-dependent specifications of these sensory organs are highly reproducible (Ghysen 1980;Vandervorst and Ghysen 1980). The position of a sensory organ in the adult fly depends on the birthplace of its precursor, the sensory organ precursor (SOP) cell, which is singled out from a small group of cells called a proneural cluster in the imaginal disc. It has been shown that Diosophila sensory organ development is programmed genetically, and the framework of the genetic cascade involved has been described (Ghysen and Dambly-Chaudiere 1989;Romani et al. 1989;Cubas et al. 1991;Skeath and Carroll 1991;Campuzano and Modolell 1992;Ghysen et al. 1993). According to the scheme, cells expressing the pro neural genes acquire the potential to initiate neural de velopment, and this proneural gene activity is regulated negatively by the repressor genes. A gain-of-function mutation of the proneural gene or a loss-of-function mu-'These authois contributed equally to this work. ^Present addtess: Fujirebio, Inc., Tokyo 192, Japan. ^Corresponding author. tation of the repressor gene causes expansion of the pro neural cluster and yields extra SOP cells, resulting in supernumerary sensory organs in the fly, whereas a lossof-function mutation of the proneural gene or a gain-offunction mutation of the repressor gene has the opposite effect (Jan and Jan 1990;Ghysen et al. 1993). Thus, a balance between the activities of the proneural and re pressor genes to set up a normal proneural cluster is im portant for ensuring the formation of SOP.All known proneural genes, daughteiless [da], atonal, and achaete [ac], scute [sc], lethal of scute, and asense of the achaete-scute complex, encode basic helix-loop-he lix (bHLH) transcription factors (Villares and Cabrera 1987;Alonso and Cabrera 1988; Gaudy et al. 1988;Cronmiller et al. 1988;Gonzalez et al. 1989;Jarman et al...

Emc, a negative HLH regulator with multiple functions in Drosophila development

“…The polychaetoid (pyd) mutation (also called Tamou, a Japanese term for`hairy') gives rise to ectopic SOs resembling the phenotype of insu ciency of emc (Chen et al, 1996;Takahisa et al, 1996). Moreover, Pyd and emc mutations act synergistically in the development of extra veins and SOs (Takahisa et al, 1996).…”

“…Moreover, Pyd and emc mutations act synergistically in the development of extra veins and SOs (Takahisa et al, 1996). pyd ectopic bristles are due to the formation of additional SMCs (Chen et al, 1996;Takahisa et al, 1996) which appear to result from reduced transcription of emc in pyd mutant discs (Takahisa et al, 1996).…”

“…Moreover, Pyd and emc mutations act synergistically in the development of extra veins and SOs (Takahisa et al, 1996). pyd ectopic bristles are due to the formation of additional SMCs (Chen et al, 1996;Takahisa et al, 1996) which appear to result from reduced transcription of emc in pyd mutant discs (Takahisa et al, 1996). Pyd is a PDZ domain protein whose sequence is closely related to mammalian Zona occludens proteins ZO-1, ZO-2 and ZO-3, members of the membrane-associated guanylate kinase homologue (MAGUK) family (reviewed in Dimitratos et al, 1999).…”

“…Pyd is a PDZ domain protein whose sequence is closely related to mammalian Zona occludens proteins ZO-1, ZO-2 and ZO-3, members of the membrane-associated guanylate kinase homologue (MAGUK) family (reviewed in Dimitratos et al, 1999). Since Pyd is associated with septate and adherens junctions (Takahisa et al, 1996;Wie and Ellis, 2001), its role in emc regulation cannot be a direct one. The presence of multiple protein ± protein interaction domains in PDZ proteins allows them to act as sca olding components to organize protein complexes (Dimitratos et al, 1999).…”

“…The presence of multiple protein ± protein interaction domains in PDZ proteins allows them to act as sca olding components to organize protein complexes (Dimitratos et al, 1999). Accordingly, it has been suggested that Pyd participates in a signaling pathway that ultimately activates emc expression (Takahisa et al, 1996).…”