Integrins and the Development of Three-Dimensional Structure in the Drosophila Compound Eye

Longley, Robert L.; Ready, Donald F.

doi:10.1006/dbio.1995.1292

Cited by 151 publications

(188 citation statements)

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“…The embryo and follicle cells are systems in which epithelial polarization is being established (38,39), whereas pupal PRCs undergo a 90°remodeling of already established polarized membranes (17,40). We speculate that this remodeling process requires additional mechanisms for its precise regulation and may be why LKB1 acts on additional downstream targets to regulate polarity in the eye.…”

Section: Discussionmentioning

confidence: 95%

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LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye

Amin

Khan

Johnston

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The serine-threonine kinase LKB1 regulates cell polarity from Caenorhabditis elegans to man. Loss of lkb1 leads to a cancer predisposition, known as Peutz-Jeghers Syndrome. Biochemical analysis indicates that LKB1 can phosphorylate and activate a family of AMPK-like kinases, however, the precise contribution of these kinases to the establishment and maintenance of cell polarity is still unclear. Recent studies propose that LKB1 acts primarily through the AMP kinase to establish and/or maintain cell polarity. To determine whether this simple model of how LKB1 regulates cell polarity has relevance to complex tissues, we examined lkb1 mutants in the Drosophila eye. We show that adherens junctions expand and apical, junctional, and basolateral domains mix in lkb1 mutants. Surprisingly, we find LKB1 does not act primarily through AMPK to regulate cell polarity in the retina. Unlike lkb1 mutants, ampk retinas do not show elongated rhabdomeres or expansion of apical and junctional markers into the basolateral domain. In addition, nutrient deprivation does not reveal a more dramatic polarity phenotype in lkb1 photoreceptors. These data suggest that AMPK is not the primary target of LKB1 during eye development. Instead, we find that a number of other AMPK-like kinase, such as SIK, NUAK, Par-1, KP78a, and KP78b show phenotypes similar to weak lkb1 loss of function in the eye. These data suggest that in complex tissues, LKB1 acts on an array of targets to regulate cell polarity.AMPK ͉ SIK ͉ NUAK ͉ Par-1 ͉ KP78

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Section: Discussionmentioning

confidence: 95%

“…Cells undergo a 90°r otation that turns the apices of the photoreceptor cells (PRCs) toward each other; a process that depends on the adherens junction (AJ) (17). Between 37% and 55% pupal development (pd), the PRC apical surfaces expand, dramatically increasing in depth perpendicular to the plane of the epithelium.…”

mentioning

confidence: 99%

LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye

Amin

Khan

Johnston

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…Apparently, Baz is not required for the apical-basal polarity in larval photoreceptors. However, from late larval to early pupal stage the apical surfaces of R1-R8 turn 90°toward the center of ommatidium, and the apparent apical-basal axis of photoreceptor becomes perpendicular to the distal-proximal axis (2). It is possible that such morphological changes involve respecification of apical-basal polarity in pupal photoreceptors that may require Baz.…”

Section: Sdt Remains Colocalized With Dlt and Crb At Stalk Membranementioning

confidence: 99%

“…How these cells elaborate their different membrane domains is not well understood. In Drosophila, photoreceptors have clearly recognizable apical-basal polarity demarcated by zonula adherens (ZA) (2). Is this polarity established by the same protein complexes that specify epithelial polarity?…”

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confidence: 99%

Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture

Hong

Ackerman

Jan

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Photoreceptors form during Drosophila pupal development and acquire elaborate membrane structures, including the rhabdomeres and stalk membranes. Here, we show that the development of these cellular structures involves two distinct processes: the establishment of apical-basal polarity that requires Bazooka (Baz), and the regionalization of apical membrane into stalk membranes and rhabdomeres that requires Stardust (Sdt). In the absence of Baz, the apical-basal polarity is compromised in early pupal photoreceptors, and no identifiable apical membrane domain is formed. Sdt, in contrast, plays a more limited role in apical-basal polarity but is essential for the proper localization of transmembrane protein Crumbs (Crb), known to be required in the biogenesis of stalk membrane. Loss of Sdt causes strong defects in stalk membrane and rhabdomere resembling crb mutant phenotype. Thus, proteins required for establishing the early embryonic epithelial polarity are used later for the morphogenesis of photoreceptors, with Baz and Sdt functioning in different aspects of the formation of the apical-basal cellular architecture. D ifferent cell types exhibit different degrees of complexity in their morphogenesis. Epithelial cells are polarized to have distinct apical versus basolateral domains. Cascades of protein complexes have been found to specify this polarity (1). Many cells that are derived from epithelial cells have more complex morphology to carry out important functions, such as photoreceptors for vision. How these cells elaborate their different membrane domains is not well understood. In Drosophila, photoreceptors have clearly recognizable apical-basal polarity demarcated by zonula adherens (ZA) (2). Is this polarity established by the same protein complexes that specify epithelial polarity? How might this apical-basal polarity specification influence other structural specializations, e.g., the elaboration of rhabdomere perpendicular to the apical-basal axis? And, what are the mechanisms for regionalizing specific membrane domains in conjunction with the polarity?One approach to address these questions in Drosophila is to test whether similar organizations of genetic pathways in simple and relatively well studied embryonic epithelial polarity also underlie the development of polarity in more specialized cell types like photoreceptors. Drosophila embryonic epithelium represents one of the simplest polarized cell types, and its apical-basal polarity is controlled largely in concert by three protein complexes (1). Baz(DmPar-3)͞DmPar-6͞DaPKC (atypical protein kinase C) plays the earliest and essential role in initiating the apical-basal polarity, whereas Sdt͞Crb͞Dlt (Discs lost) maintains the ZA formation and polarity by counteracting the activity of Dlg (Discs large)͞Lgl (Lethal giant larvae)͞Scrib (Scribble) (3, 4). Except for DaPKC, Crumbs (Crb), and Lgl, all of these proteins contain one or more PDZ domains important for mediating protein-protein interactions (1). The first insight that at least some of these protei...

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“…In Drosophila eye development, the apical domain of photoreceptor cell membrane goes through dramatic reorganization during pupal stage. In the early pupal stage, the light-sensitive membranous structure called rhabdomere begins to develop from the apical surface of cell membrane and grows extensively along the elongating photoreceptors (Kumar and Ready, 1995;Longley and Ready, 1995). During this time, Dpatj colocalizes with Crb-Sdt to the rhabdomere stalk membrane formed between the emerging rhabdomere and adherens junction (AJ).…”

Section: Introductionmentioning

confidence: 99%

Domain-specific early and late function of Dpatj inDrosophilaphotoreceptor cells

Nam

Choi

2006

Dev. Dyn.

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The formation and maintenance of cell polarity is essential for epithelial morphogenesis. Dpatj (Drosophila homolog of mammalian Patj) is a multi-PDZ domain protein that localizes to the apical cell membrane and forms a protein complex with cell polarity proteins, Crumbs (Crb) and Stardust (Sdt). Whereas Crb and Sdt are known to be required for the organization of adherens junctions (AJs) and rhabdomeres in differentiating photoreceptors, the in vivo function of Dpatj as a member of the Crb complex in developing eye has been unclear due to the lack of loss-of-function mutations specifically affecting the dpatj gene.

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Integrins and the Development of Three-Dimensional Structure in the Drosophila Compound Eye

Cited by 151 publications

References 0 publications

LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye

LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye

Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture

Domain-specific early and late function of Dpatj inDrosophilaphotoreceptor cells

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