Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila

Jason Burgess, Lauren M. Del Bel, Cheng I J Ma, Barbara Barylko, Gordon Polevoy, Janet Rollins, Joseph P. Albanesi, Helmut Krämer, Julie A. Brill

Research output: Contribution to journalArticle

Abstract

Type II phosphatidylinositol 4-kinase (PI4KII) produces the lipid phosphatidylinositol 4-phosphate (PI4P), a key regulator of membrane trafficking. Here, we generated genetic models of the sole Drosophila melanogaster PI4KII gene. A specific requirement for PI4KII emerged in larval salivary glands. In PI4KII mutants, mucin-containing glue granules failed to reach normal size, with glue protein aberrantly accumulating in enlarged Rab7-positive late endosomes. Presence of PI4KII at the Golgi and on dynamic tubular endosomes indicated two distinct foci for its function. First, consistent with the established role of PI4P in the Golgi, PI4KII is required for sorting of glue granule cargo and the granule-associated SNARE Snap24. Second, PI4KII also has an unforeseen function in late endosomes, where it is required for normal retromer dynamics and for formation of tubular endosomes that are likely to be involved in retrieving Snap24 and Lysosomal enzyme receptor protein (Lerp) from late endosomes to the trans-Golgi network. Our genetic analysis of PI4KII in flies thus reveals a novel role for PI4KII in regulating the fidelity of granule protein trafficking in secretory tissues.

Original languageEnglish (US)
Pages (from-to)3040-3050
Number of pages11
JournalJournal of Cell Science
Volume125
Issue number16
StatePublished - Aug 15 2012

Fingerprint

1-Phosphatidylinositol 4-Kinase
Endosomes
Secretory Vesicles
Adhesives
trans-Golgi Network
SNARE Proteins
Genetic Models
Mucins
Protein Transport
Salivary Glands
Drosophila melanogaster
Diptera
Proteins
Drosophila inturned protein
Lipids
Membranes
Enzymes
Genes

Keywords

  • LERP
  • Mucin granule
  • PI 4-kinase
  • Ptdins(4)P
  • Regulated secretion
  • Salivary gland
  • Snap-24

ASJC Scopus subject areas

  • Cell Biology

Cite this

Burgess, J., Del Bel, L. M., Ma, C. I. J., Barylko, B., Polevoy, G., Rollins, J., ... Brill, J. A. (2012). Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. Journal of Cell Science, 125(16), 3040-3050.

Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. / Burgess, Jason; Del Bel, Lauren M.; Ma, Cheng I J; Barylko, Barbara; Polevoy, Gordon; Rollins, Janet; Albanesi, Joseph P.; Krämer, Helmut; Brill, Julie A.

In: Journal of Cell Science, Vol. 125, No. 16, 15.08.2012, p. 3040-3050.

Research output: Contribution to journalArticle

Burgess, J, Del Bel, LM, Ma, CIJ, Barylko, B, Polevoy, G, Rollins, J, Albanesi, JP, Krämer, H & Brill, JA 2012, 'Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila', Journal of Cell Science, vol. 125, no. 16, pp. 3040-3050.
Burgess J, Del Bel LM, Ma CIJ, Barylko B, Polevoy G, Rollins J et al. Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. Journal of Cell Science. 2012 Aug 15;125(16):3040-3050.
Burgess, Jason ; Del Bel, Lauren M. ; Ma, Cheng I J ; Barylko, Barbara ; Polevoy, Gordon ; Rollins, Janet ; Albanesi, Joseph P. ; Krämer, Helmut ; Brill, Julie A. / Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. In: Journal of Cell Science. 2012 ; Vol. 125, No. 16. pp. 3040-3050.
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