Elsevier

Differentiation

Volume 74, Issue 7, September 2006, Pages 326-348
Differentiation

ORIGINAL ARTICLE
From fate to function: the Drosophila trachea and salivary gland as models for tubulogenesis

https://doi.org/10.1111/j.1432-0436.2006.00095.xGet rights and content

Abstract

Tube formation is a ubiquitous process required to sustain life in multicellular organisms. The tubular organs of adult mammals include the lungs, vasculature, digestive and excretory systems, as well as secretory organs such as the pancreas, salivary, prostate, and mammary glands. Other tissues, including the embryonic heart and neural tube, have requisite stages of tubular organization early in development. To learn the molecular and cellular basis of how epithelial cells are organized into tubular organs of various shapes and sizes, investigators have focused on the Drosophila trachea and salivary gland as model genetic systems for branched and unbranched tubes, respectively. Both organs begin as polarized epithelial placodes, which through coordinated cell shape changes, cell rearrangement, and cell migration form elongated tubes. Here, we discuss what has been discovered regarding the details of cell fate specification and tube formation in the two organs; these discoveries reveal significant conservation in the cellular and molecular events of tubulogenesis.

References (125)

  • N. Hacohen et al.

    Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways

    Cell

    (1998)
  • K.D. Henderson et al.

    Regulation and function of Scr, exd, and hth in the Drosophila salivary gland

    Dev Biol

    (2000)
  • K.D. Henderson et al.

    Cell fate specification in the Drosophila salivary gland: the integration of homeotic gene function with the Dpp signaling cascade

    Dev Biol

    (1999)
  • J. Jarecki et al.

    Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF

    Cell

    (1999)
  • J. Jin et al.

    Regulation of Drosophila tracheal system development by protein kinase B

    Dev Cell

    (2001)
  • C. Klambt

    EGF receptor signalling: roles of Star and Rhomboid revealed

    Curr Biol

    (2002)
  • T. Kolesnikov et al.

    Netrin and Slit guide salivary gland migration

    Dev Biol

    (2005)
  • R.P. Kuhnlein et al.

    Regulation of Drosophila spalt gene expression

    Mech Dev

    (1997)
  • J.R. Lee et al.

    Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila

    Cell

    (2001)
  • J. Mata et al.

    Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating String/Cdc25 proteolysis

    Cell

    (2000)
  • K.L. Mosley-Bishop et al.

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

    Curr Biol

    (1999)
  • M.M. Myat et al.

    Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane

    Cell

    (2002)
  • M.M. Myat et al.

    A molecular link between FGF and Dpp signaling in branch-specific migration of the Drosophila trachea

    Dev Biol

    (2005)
  • T. Ohshiro et al.

    Ligand-dependent activation of breathless FGF receptor gene in Drosophila developing trachea

    Mech Dev

    (2002)
  • M. Reichman-Fried et al.

    Breathless, a Drosophila FGF receptor homolog, is required for the onset of tracheal cell migration and tracheole formation

    Mech Dev

    (1995)
  • C. Ribeiro et al.

    In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis

    Dev Cell

    (2002)
  • C. Ribeiro et al.

    Genetic control of cell intercalation during tracheal morphogenesis in Drosophila

    Curr Biol

    (2004)
  • E. Ruberte et al.

    An absolute requirement for both the type II and type I receptors, Punt and Thick veins, for Dpp signaling in vivo

    Cell

    (1995)
  • T.C. Seher et al.

    Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation

    Curr Biol

    (2000)
  • P. Seshaiah et al.

    Pasilla, the Drosophila homologue of the human Nova-1 and Nova-2 proteins, is required for normal secretion in the salivary gland

    Dev Biol

    (2001)
  • P. Steneberg et al.

    Dpp and Notch specify the fusion cell fate in the dorsal branches of the Drosophila trachea

    Mech Dev

    (1999)
  • D. Sutherland et al.

    Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching

    Cell

    (1996)
  • H. Tanaka et al.

    Formin3 is required for assembly of the F-actin structure that mediates tracheal fusion in Drosophila

    Dev Biol

    (2004)
  • E.W. Abrams et al.

    CrebA regulates secretory activity in the Drosophila salivary gland and epidermis

    Development

    (2005)
  • E.W. Abrams et al.

    Fork head and Sage maintain a uniform and patent salivary gland lumen through regulation of two downstream target genes, PH4αSG1 and PH4αSG2

    Development

    (2006)
  • M. Affolter et al.

    The Drosophila SRF homolog is expressed in a subset of tracheal cells and maps within a genomic region required for tracheal development

    Development

    (1994)
  • M. Affolter et al.

    Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis

    Development

    (1994)
  • M.G. Anderson et al.

    Function of the Drosophila POU domain transcription factor Drifter as an upstream regulator of breathless receptor tyrosine kinase expression in developing trachea

    Development

    (1996)
  • M.G. Anderson et al.

    Drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia

    Genes Dev

    (1995)
  • D.J. Andrew et al.

    The Drosophila dCreb-A gene is required for dorsal/ventral patterning of the larval cuticle

    Development

    (1997)
  • D.J. Andrew et al.

    Setting limits on homeotic gene function: restraint of sex combs reduced activity by teashirt and other homeotic genes

    Embo J

    (1994)
  • G.J. Beitel et al.

    Genetic control of epithelial tube size in the Drosophila tracheal system

    Development

    (2000)
  • M. Boube et al.

    Specific tracheal migration is mediated by complementary expression of cell surface proteins

    Genes Dev

    (2001)
  • P.L. Bradley et al.

    Organ formation in Drosophila: specification and morphogenesis of the salivary gland

    Bioessays

    (2001)
  • G. Bronner et al.

    Sp1/egr-like zinc-finger protein required for endoderm specification and germ-layer formation in Drosophila

    Nature

    (1994)
  • J.F. de Celis et al.

    Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster

    Development

    (1995)
  • V. Chandrasekaran et al.

    Senseless is necessary for the survival of embryonic salivary glands in Drosophila

    Development

    (2003)
  • V. Chandrasekaran et al.

    Tec29 controls actin remodeling and endoreplication during invagination of the Drosophila embryonic salivary glands

    Development

    (2005)
  • C.K. Chen et al.

    The transcription factors Knirps and Knirps related control cell migration and branch morphogenesis during Drosophila tracheal development

    Development

    (1998)
  • C. Chiang et al.

    Control of Drosophila tracheal branching by the novel homeodomain gene unplugged, a regulatory target for genes of the Bithorax complex

    Development

    (1995)

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