The actomyosin machinery is required for Drosophila retinal lumen formation

PLoS Genet. 2014 Sep 18;10(9):e1004608. doi: 10.1371/journal.pgen.1004608. eCollection 2014 Sep.

Abstract

Multicellular tubes consist of polarized cells wrapped around a central lumen and are essential structures underlying many developmental and physiological functions. In Drosophila compound eyes, each ommatidium forms a luminal matrix, the inter-rhabdomeral space, to shape and separate the key phototransduction organelles, the rhabdomeres, for proper visual perception. In an enhancer screen to define mechanisms of retina lumen formation, we identified Actin5C as a key molecule. Our results demonstrate that the disruption of lumen formation upon the reduction of Actin5C is not linked to any discernible defect in microvillus formation, the rhabdomere terminal web (RTW), or the overall morphogenesis and basal extension of the rhabdomere. Second, the failure of proper lumen formation is not the result of previously identified processes of retinal lumen formation: Prominin localization, expansion of the apical membrane, or secretion of the luminal matrix. Rather, the phenotype observed with Actin5C is phenocopied upon the decrease of the individual components of non-muscle myosin II (MyoII) and its upstream activators. In photoreceptor cells MyoII localizes to the base of the rhabdomeres, overlapping with the actin filaments of the RTW. Consistent with the well-established roll of actomyosin-mediated cellular contraction, reduction of MyoII results in reduced distance between apical membranes as measured by a decrease in lumen diameter. Together, our results indicate the actomyosin machinery coordinates with the localization of apical membrane components and the secretion of an extracellular matrix to overcome apical membrane adhesion to initiate and expand the retinal lumen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AC133 Antigen
  • Actins / genetics
  • Actins / metabolism
  • Actomyosin / metabolism*
  • Animals
  • Antigens, CD / metabolism
  • Cell Membrane / metabolism
  • Drosophila / embryology
  • Drosophila / genetics
  • Drosophila / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Extracellular Matrix / metabolism
  • Eye Proteins / metabolism
  • Female
  • Glycoproteins / metabolism
  • Male
  • Membrane Proteins / metabolism
  • Morphogenesis* / genetics
  • Myosin Type II / deficiency
  • Myosin Type II / genetics
  • Peptides / metabolism
  • Protein Transport
  • Retina / embryology
  • Retina / metabolism*

Substances

  • AC133 Antigen
  • Actins
  • Antigens, CD
  • Drosophila Proteins
  • Eye Proteins
  • Glycoproteins
  • Membrane Proteins
  • Peptides
  • crb protein, Drosophila
  • eys protein, Drosophila
  • Actomyosin
  • Myosin Type II

Grants and funding

This work was funded from the American Cancer Society (RSG-10-041-01-DDC) to ACZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.