A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles

Patrizia Adamczyk, Claudia Zenkert, Prakash G. Balasubramanian, Shuhei Yamada, Saori Murakoshi, Kazuyuki Sugahara*, Jung Shan Hwang, Takashi Gojobori, Thomas W. Holstein, Suat Özbek

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

Abstract

Membrane tubulation is generally associated with rearrangements of the cytoskeleton and other cytoplasmic factors. Little is known about the contribution of extracellular matrix components to this process. Here, we demonstrate an essential role of proteoglycans in the tubulation of the cnidarian nematocyst vesicle. The morphogenesis of this extrusive organelle takes place inside a giant post-Golgi vesicle, which topologically represents extracellular space. This process includes the formation of a complex collagenous capsule structure that elongates into a long tubule, which invaginates after its completion. We show that a non-sulfated chondroitin appears as a scaffold in early morphogenesis of all nematocyst types in Hydra and Nematostella. It accompanies the tubulation of the vesicle membrane forming a provisional tubule structure, which after invagination matures by collagen incorporation. Inhibition of chondroitin synthesis by β-xylosides arrests nematocyst morphogenesis at different stages of tubule outgrowth resulting in retention of tubule material and a depletion of mature capsules in the tentacles of hydra. Our data suggest a conserved role of proteoglycans in the stabilization of a membrane protrusion as an essential step in organelle morphogenesis.

Original languageEnglish (US)
Pages (from-to)25613-25623
Number of pages11
JournalJournal of Biological Chemistry
Volume285
Issue number33
DOIs
StatePublished - Aug 13 2010

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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