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      How Drosophila melanogaster Forms its Mechanoreceptors

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          Abstract

          A strictly determined number of external sensory organs, macrochaetes, acting as mechanoreceptors, are orderly located on drosophila head and body. Totally, they form the bristle pattern, which is a species-specific characteristic of drosophila.

          Each mechanoreceptor comprises four specialized cells derived from the single sensory organ precursor (SOP) cell. The conserved bristle pattern combined with a comparatively simple structure of each mechanosensory organ makes macrochaetes a convenient model for studying the formation spatial structures with a fixed number of elements at certain positions and the mechanism underlying cell differentiation.

          The macrochaete morphogenesis consists of three stages. At the first stage, the proneural clusters segregate from the massive of ectodermal cells of the wing imaginal disc. At the second stage, the SOP cell is determined and its position in the cluster is specified. At the third stage, the SOP cell undergoes two asymmetric divisions, and the daughter cells differentiate into the components of mechanoreceptor: shaft, socket, bipolar neuron, and sheath.

          The critical factor determining the neural pathway of cell development is the content of proneural proteins, products of the achaete-scute ( AS-C) gene complex, reaching its maximum in the SOP cell.

          The experimental data on the main genes and their products involved in the control of bristle pattern formation are systematized. The roles of achaete-scute complex, EGFR and Notch signaling pathways, and selector genes in these processes are considered. An integral scheme describing the functioning of the system controlling macrochaete development in D. melanogaster is proposed based on analysis of literature data.

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          Most cited references124

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          Notch signaling: from the outside in.

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            Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila.

            The senseless (sens) gene is required for proper development of most cell types of the embryonic and adult peripheral nervous system (PNS) of Drosophila. Sens is a nuclear protein with four Zn fingers that is expressed and required in the sensory organ precursors (SOP) for proper proneural gene expression. Ectopic expression of Sens in many ectodermal cells causes induction of PNS external sensory organ formation and is able to recreate an ectopic proneural field. Hence, sens is both necessary and sufficient for PNS development. Our data indicate that proneural genes activate sens expression. Sens is then in turn required to further activate and maintain proneural gene expression. This feedback mechanism is essential for selective enhancement and maintenance of proneural gene expression in the SOPs.
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              Calcium depletion dissociates and activates heterodimeric notch receptors.

              Notch receptors participate in a highly conserved signaling pathway that regulates morphogenesis in multicellular animals. Maturation of Notch receptors requires the proteolytic cleavage of a single precursor polypeptide to produce a heterodimer composed of a ligand-binding extracellular domain (N(EC)) and a single-pass transmembrane signaling domain (N(TM)). Notch signaling has been correlated with additional ligand-induced proteolytic cleavages, as well as with nuclear translocation of the intracellular portion of N(TM) (N(ICD)). In the current work, we show that the N(EC) and N(TM) subunits of Drosophila Notch and human Notch1 (hN1) interact noncovalently. N(EC)-N(TM) interaction was disrupted by 0.1% sodium dodecyl sulfate or divalent cation chelators such as EDTA, and stabilized by millimolar Ca(2+). Deletion of the Ca(2+)-binding Lin12-Notch (LN) repeats from the N(EC) subunit resulted in spontaneous shedding of N(EC) into conditioned medium, implying that the LN repeats are important in maintaining the interaction of N(EC) and N(TM). The functional consequences of EDTA-induced N(EC) dissociation were studied by using hN1-expressing NIH 3T3 cells. Treatment of these cells for 10 to 15 min with 0.5 to 10 mM EDTA resulted in the rapid shedding of N(EC), the transient appearance of a polypeptide of the expected size of N(ICD), increased intranuclear anti-Notch1 staining, and the transient activation of an Notch-sensitive reporter gene. EDTA treatment of HeLa cells expressing endogenous Notch1 also stimulated reporter gene activity to a degree equivalent to that resulting from exposure of the cells to the ligand Delta1. These findings indicate that receptor activation can occur as a consequence of N(EC) dissociation, which relieves inhibition of the intrinsically active N(TM) subunit.
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                Author and article information

                Journal
                Curr Genomics
                CG
                Current Genomics
                Bentham Science Publishers Ltd.
                1389-2029
                1875-5488
                August 2008
                : 9
                : 5
                : 312-323
                Affiliations
                [1 ]Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, pr. Lavrentieva 10, Novosibirsk, 630090 Russia
                [2 ]Novosibirsk State University, ul. Pirogova 2, Novosibirsk, 630090, Russia
                Author notes
                [* ]Address correspondence to this author at the Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, pr. Lavrentieva 10, Novosibirsk, 630090, Russia; E-mail: furman@ 123456bionet.nsc.ru
                Article
                CG-9-312
                10.2174/138920208785133271
                2685642
                19471605
                81d57c64-583c-4d60-8d95-d1c57e544369
                ©2008 Bentham Science Publishers Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.5/) which permits unrestrictive use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 April 2008
                : 17 May 2008
                : 25 May 2008
                Categories
                Article

                Genetics
                achaete–scute complex,bristle pattern,signaling pathways,drosophila.,macrochaetes
                Genetics
                achaete–scute complex, bristle pattern, signaling pathways, drosophila., macrochaetes

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