Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye

Mosley-Bishop, Kathleen L.; Li, Qinghong; Patterson, Kristin D.; Fischer, Janice A.

doi:10.1016/s0960-9822(99)80501-6

Cited by 150 publications

(173 citation statements)

References 26 publications

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“…Nuclear migrations are a second distinguishing cellular feature of the morphogenetic furrow (Ready et al, 1976;Fischer-Vize and Mosley, 1994). The basal migration of nuclei within the furrow and their subsequent apical rise in post-mitotic cells is dependent upon microtubule motors such as Dynein and associated proteins (Fan and Ready, 1997;Mosley-Bishop et al, 1999;Swan et al, 1999;Houalla et al, 2005). We have used this feature to further analyze the cellular behavior of cells lacking emc.…”

Section: Emc Functions As An Inhibitor Of Apical Surface Constrictionmentioning

confidence: 99%

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Spratford

Kumar

2013

Development

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The compound eye of Drosophila melanogaster is configured by a differentiating wave, the morphogenetic furrow, that sweeps across the eye imaginal disc and transforms thousands of undifferentiated cells into a precisely ordered repetitive array of 800 ommatidia. The initiation of the furrow at the posterior margin of the epithelium and its subsequent movement across the eye field is controlled by the activity of the Hedgehog (Hh) signaling pathway. Differentiating photoreceptors that lie behind the furrow produce and secrete the Hh morphogen, which is captured by cells within the furrow itself. This leads to the stabilization of the full-length form of the zinc-finger transcription factor Cubitus interruptus (Ci155), the main effector of Hh signaling. Ci155 functions as a transcriptional activator of a number of downstream targets, including decapentaplegic (dpp), a TGFβ homolog. In this report, we describe a mechanism that is in place within the fly retina to limit Hh pathway activity within and ahead of the furrow. We demonstrate that the helix-loop-helix (HLH) protein Extramacrochaetae (Emc) regulates Ci155 levels. Loss of emc leads to an increase in Ci155 levels, nuclear migration, apical cell constriction and an acceleration of the furrow. We find that these roles are distinct from the bHLH protein Hairy (H), which we show restricts atonal (ato) expression ahead of the furrow. Secondary furrow initiation along the dorsal and ventral margins is blocked by the activity of the Wingless (Wg) pathway. We also show that Emc regulates and cooperates with Wg signaling to inhibit lateral furrow initiation.

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Section: Emc Functions As An Inhibitor Of Apical Surface Constrictionmentioning

confidence: 99%

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Spratford

Kumar

2013

Development

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“…In Drosophila, the glued phenotype of photoreceptor nuclei is shared by klarsicht mutants (Mosley-Bishop et al, 1999). The klarsicht gene was found to encode a protein with a Cterminal domain shared with ANC-1 of C. elegans and Syne/Nesprin proteins of vertebrates (Starr and Fischer, 2005;Wilhelmsen et al, 2006).…”

Section: Linking the Nucleus To The Cytoskeletonmentioning

confidence: 99%

Nuclear migration during retinal development

2008

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In this review we focus on the mechanisms, regulation, and cellular consequences of nuclear migration in the developing retina. In the nervous system, nuclear migration is prominent during both proliferative and post-mitotic phases of development. Interkinetic nuclear migration is the process where the nucleus oscillates from the apical to basal surfaces in proliferative neuroepithelia. Proliferative nuclear movement occurs in step with the cell cycle, with M-phase being confined to the apical surface and G1-, S-, and G2-phases occurring at more basal locations. Later, following cell cycle exit, some neuron precursors migrate by nuclear translocation. In this mode of cellular migration, nuclear movement is the driving force for motility. Following discussion of the key components and important regulators for each of these processes, we present an emerging model where interkinetic nuclear migration functions to distinguish cell fates among retinal neuroepithelia. Keywordsinterkinetic nuclear migration; nuclear translocation; nucleokinesis; neurogenesis; dynein; cell cycle; cell behavior OverviewNeuronal development is regulated by a complex array of intrinsic and extrinsic signals that act on progenitor neuroepithelial cells to ensure the correct cell type is generated in the right numbers and at the appropriate time of development (Donovan et al., 2005;Cayouette et al., 2006). In addition, multiple signaling cues are integrated in post-mitotic neuronal precursors to facilitate directed cell migration and correct laminar positioning (Malicki et al., 2004). This spatial and temporal regulation of neuronal cell-type fate commitment and histogenesis is dependent on the regulation of the mitotic cell cycle, and in particular at the level of cell cycle exit (Ohnuma and Harris, 2003). Recent data suggest that nuclear migration is a critical process for several aspects of neuronal development, including that of the neural retina. The focus of this review is on interkinetic nuclear migration and nuclear translocation during retinogenesis, although much of what we know is from observations in other regions of the developing nervous system. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript Interkinetic nuclear migrationInterkinetic nuclear migration is the proliferative cell behavior where the nuclei of neuroepithelial cells migrate in an apical-basal manner and in phase with the cell cycle (Frade 2002). Neuroepithelial cell divisions are confined to apical locations while S-phase occu...

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“…Four apical cone cells Klar and C. elegans Anc-1 (homologous to vertebrate secrete the lens. The eye develops during the larval and Syne-1 and Drosophila Msp-300) are known to contain pupal stages in a cellular monolayer called the eye disc KASH domains (Mosley-Bishop et al 1999;Starr and (Wolff and Ready 1993). A wave of morphogenesis, Han 2002).…”

mentioning

confidence: 99%

Drosophila Klarsicht Has Distinct Subcellular Localization Domains for Nuclear Envelope and Microtubule Localization in the Eye

et al. 2004

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The Drosophila klarsicht (klar) gene is required for developmentally regulated migrations of photoreceptor cell nuclei in the eye. klar encodes a large ‫052ف(‬ kD) protein with only one recognizable amino acid sequence motif, a KASH (K lar, Anc-1, S yne-1 h omology) domain, at its C terminus. It has been proposed that Klar facilitates nuclear migration by linking the nucleus to the microtubule organizing center (MTOC). Here we perform genetic and immunohistochemical experiments that provide a critical test of this model. We analyze mutants in the endogenous klar gene and also flies that express deleted forms of Klar protein from transgenes. We find that the KASH domain of Klar is critical for perinuclear localization and for function. In addition, we find that the N-terminal portion of Klar is also important for function and contains a domain that localizes the protein to microtubules apical to the nucleus. These results provide strong support for a model in which Klar links the nucleus to the MTOC.

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Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye

Cited by 150 publications

References 26 publications

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Nuclear migration during retinal development

Drosophila Klarsicht Has Distinct Subcellular Localization Domains for Nuclear Envelope and Microtubule Localization in the Eye

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