Epithelial Tube Morphology Is Determined by the Polarized Growth and Delivery of Apical Membrane

Myat, Monn Monn; Andrew, Deborah J.

doi:10.1016/s0092-8674(02)01140-6

Cited by 122 publications

(184 citation statements)

References 40 publications

(5 reference statements)

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“…The function of Sdt͞Crb͞Dlt in pupal photoreceptor is not at the level of maintaining the apical-basal polarity as in embryonic epithelia, but for specifying and controlling the growth of special membrane domains such as stalk membrane. Consistent with this hypothesis, Crb is also required in the growth of apical membrane of salivary tubes (17). Overall, while protein-protein interactions in Sdt͞Crb͞Dlt complex are preserved in pupal photoreceptors, the function of the complex apparently changes and adapts to the process of developing specific cellular architecture.…”

Section: Discussionmentioning

confidence: 60%

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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Section: Discussionmentioning

confidence: 60%

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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“…An alternative explanation might reside in the function of the gene that could be compensated by other molecules. We favor the latter alternative, first because classical mutants affecting tube formation also show variable phenotypes, thereby reflecting the view that different processes and various environments interplay with each other in tube development (28). Second, in the mfat1 knock-out mouse, only some mutants showed distinctive morphological defects as holo-prosencephaly (14).…”

Section: Silencing Of Fat-like Transcript Impairs Tubular Tissue Formmentioning

confidence: 92%

The fat-like Gene of Drosophila Is the True Orthologue of Vertebrate Fat Cadherins and Is Involved in the Formation of Tubular Organs

Castillejo-López¹,

Arias²,

Baumgärtner³

2004

Journal of Biological Chemistry

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Fat cadherins constitute a subclass of the large cadherin family characterized by the presence of 34 cadherin motifs. To date, three mammalian Fat cadherins have been described; however, only limited information is known about the function of these molecules. In this paper, we describe the second fat cadherin in Drosophila, fat-like (ftl). We show that ftl is the true orthologue of vertebrate fat-like genes, whereas the previously characterized tumor suppressor cadherin, fat, is more distantly related as compared with ftl. Ftl is a large molecule of 4705 amino acids. It is expressed apically in luminal tissues such as trachea, salivary glands, proventriculus, and hindgut. Silencing of ftl results in the collapse of tracheal epithelia giving rise to breaks, deletions, and sac-like structures. Other tubular organs such as proventriculus, salivary glands, and hindgut are also malformed or missing. These data suggest that Ftl is required for morphogenesis and maintenance of tubular structures of ectodermal origin and underline its similarity in function to a reported lethal mouse knock-out of fat1 where glomerular epithelial processes collapse. Based on our results, we propose a model where Ftl acts as a spacer to keep tubular epithelia apart rather than the previously described adhesive properties of the cadherin superfamily.

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“…Morphogenesis of the salivary gland requires coordinated cell shape changes, cell intercalations and direct cell migration of the ~135 ectodermal salivary gland precursor cells. 15,16 Salivary gland cells require extensive changes in adhesion properties to internalize and form a tube that then extends posteriorly by extensive cell-cell and cell-matrix interactions. Flies with defects in genes encoding various adhesion molecules, such as integrins or DE-cadherin exhibit defects in tube elongation and abnormal cellular shape.…”

Section: Introductionmentioning

confidence: 99%

“…Flies with defects in genes encoding various adhesion molecules, such as integrins or DE-cadherin exhibit defects in tube elongation and abnormal cellular shape. [15][16][17][18][19][20][21] Defects in adhesion result in small, poorly organized salivary glands. 22 We posited that similar phenotypes might be apparent if Garz pathway, inhibits trafficking of adhesion molecules DE-cadherin (DE-cad) and Flamingo to the cell surface, disrupts the localization of the tumor suppressor Discs large (Dlg) involved in polarity determination and causes a dramatic disorganization of the salivary gland.…”

Section: Introductionmentioning

confidence: 99%

The Garz Sec7 domain guanine nucleotide exchange factor for Arf regulates salivary gland development in Drosophila

Szul¹,

Burgess

Jeon

et al. 2011

Cellular Logistics

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Epithelial Tube Morphology Is Determined by the Polarized Growth and Delivery of Apical Membrane

Cited by 122 publications

References 40 publications

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

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

The fat-like Gene of Drosophila Is the True Orthologue of Vertebrate Fat Cadherins and Is Involved in the Formation of Tubular Organs

The Garz Sec7 domain guanine nucleotide exchange factor for Arf regulates salivary gland development in Drosophila

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