A Non-sulfated Chondroitin Stabilizes Membrane Tubulation in Cnidarian Organelles*
- Patrizia Adamczyk‡,
- Claudia Zenkert‡,
- Prakash G. Balasubramanian‡,
- Shuhei Yamada§,
- Saori Murakoshi§,
- Kazuyuki Sugahara§,1,
- Jung Shan Hwang¶,
- Takashi Gojobori¶,
- Thomas W. Holstein‡ and
- Suat Özbek‡,2
- From the ‡Institute of Zoology, Department of Molecular Evolution and Genomics, Heidelberg University, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany,
- the §Laboratory of Proteoglycan Signaling and Therapeutics, Faculty of Advanced Life Science, Graduate School of Life Science, Hokkaido University, Sapporo 001-0021, Japan, and
- the ¶Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan
- 1 To whom correspondence may be addressed: Faculty of Advanced Life Science, Hokkaido University, Nishi 11-choume, Kita 21-jo, Kita-ku, Sapporo, Hokkaido 001-0021, Japan. Tel.: 81-11-706-9054; Fax: 81-11-706-9056; E-mail: k-sugar{at}sci.hokudai.ac.jp.
- 2 To whom correspondence may be addressed. Tel.: 496221545638; Fax: 496221545678; E-mail: soezbek{at}zoo.uni-heidelberg.de.
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.
- Chondroitin
- Extracellular Matrix Proteins
- Membrane
- Protein Assembly
- Subcellular Organelles
- Hydra
- Membrane Tubulation
- Nematocyst
- Organelle Morphogenesis
Footnotes
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↵* This work was supported by a grant from the German Science Foundation (Deutsche Forschungsgemeinschaft) (to S. Ö. and T. W. H.) and in part by Grants-in-aid for Scientific Research (B) (20390019) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) (to K. S.).
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3 The abbreviations used are:
- ECM
- extracellular matrix
- TGN
- trans-Golgi network
- GAG
- glycosaminoglycan
- PNN
- perineuronal net
- TEM
- transmission electron microscopy
- CS
- chondroitin sulfate
- PG
- proteoglycan
- BSA
- bovine serum albumin
- PBS
- phosphate-buffered saline
- 2AB
- 2-aminobenzamide.
- © 2010 by The American Society for Biochemistry and Molecular Biology, Inc.
