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Non-cell-autonomous control of denticle diversity in the Drosophila embryo.

ABSTRACT: Certain Drosophila embryonic epidermal cells construct actin-based protrusions, called denticles, which exhibit stereotyped, column-specific differences in size, density and hook orientation. This precise denticle pattern is conserved throughout all drosophilids yet studied, and screening for mutations that affect this pattern has been used to identify genes involved in development and signaling. However, how column-specific differences are specified and the mechanism(s) involved have remained elusive. Here, we show that the transcription factor Stripe is required for multiple aspects of this column-specific denticle pattern, including denticle hook orientation. The induction of stripe expression in certain denticle field cells appears to be the primary mechanism by which developmental pathways assign denticle hook orientation. Furthermore, we show that the cytoskeletal linker protein Short stop (Shot) functions both cell-autonomously and non-autonomously to specify denticle hook orientation via interaction with the microtubule cytoskeleton. We propose that stripe mediates its effect on hook orientation, in part, via upregulation of shot.

SUBMITTER: Dilks SA

PROVIDER: S-EPMC2847471 | biostudies-literature | 2010 Apr

REPOSITORIES: biostudies-literature

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Non-cell-autonomous control of denticle diversity in the Drosophila embryo.

Dilks Stacie A SA DiNardo Stephen S

Development (Cambridge, England) 20100401 8

Certain Drosophila embryonic epidermal cells construct actin-based protrusions, called denticles, which exhibit stereotyped, column-specific differences in size, density and hook orientation. This precise denticle pattern is conserved throughout all drosophilids yet studied, and screening for mutations that affect this pattern has been used to identify genes involved in development and signaling. However, how column-specific differences are specified and the mechanism(s) involved have remained e ...[more]

PMID: 20332154

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Project description:During central nervous system (CNS) development neural stem cells (Neuroblasts, NBs) have to acquire an identity appropriate to their location. In thoracic and abdominal segments of Drosophila, the expression pattern of Bithorax-Complex Hox genes is known to specify the segmental identity of NBs prior to their delamination from the neuroectoderm. Compared to the thoracic, ground state segmental units in the head region are derived to different degrees, and the precise mechanism of segmental specification of NBs in this region is still unclear. We identified and characterized a set of serially homologous NB-lineages in the gnathal segments and used one of them (NB6-4 lineage) as a model to investigate the mechanism conferring segment-specific identities to gnathal NBs. We show that NB6-4 is primarily determined by the cell-autonomous function of the Hox gene Deformed (Dfd). Interestingly, however, it also requires a non-cell-autonomous function of labial and Antennapedia that are expressed in adjacent anterior or posterior compartments. We identify the secreted molecule Amalgam (Ama) as a downstream target of the Antennapedia-Complex Hox genes labial, Dfd, Sex combs reduced and Antennapedia. In conjunction with its receptor Neurotactin (Nrt) and the effector kinase Abelson tyrosine kinase (Abl), Ama is necessary in parallel to the cell-autonomous Dfd pathway for the correct specification of the maxillary identity of NB6-4. Both pathways repress CyclinE (CycE) and loss of function of either of these pathways leads to a partial transformation (40%), whereas simultaneous mutation of both pathways leads to a complete transformation (100%) of NB6-4 segmental identity. Finally, we provide genetic evidences, that the Ama-Nrt-Abl-pathway regulates CycE expression by altering the function of the Hippo effector Yorkie in embryonic NBs. The disclosure of a non-cell-autonomous influence of Hox genes on neural stem cells provides new insight into the process of segmental patterning in the developing CNS.

Dataset Information

Non-cell-autonomous control of denticle diversity in the Drosophila embryo.

Publications

Non-cell-autonomous control of denticle diversity in the Drosophila embryo.

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