A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles.
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 beta-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.
Adamczyk
Patrizia
P
Department of Molecular Evolution and Genomics, Institute of Zoology, Heidelberg University, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany.
Zenkert
Claudia
C
Balasubramanian
Prakash G
PG
Yamada
Shuhei
S
Murakoshi
Saori
S
Sugahara
Kazuyuki
K
Hwang
Jung Shan
JS
Gojobori
Takashi
T
Holstein
Thomas W
TW
Ozbek
Suat
S
D000818:Animals; D002807:Chondroitin / Q000378:metabolism*; D002850:Chromatography, Gel; D003063:Cnidaria / Q000378:metabolism*; D005455:Fluorescent Antibody Technique; D006025:Glycosaminoglycans / Q000378:metabolism; D006829:Hydra / Q000378:metabolism; D007150:Immunohistochemistry; D007425:Intracellular Membranes / Q000378:metabolism*; D015388:Organelles / Q000378:metabolism*
D006025:Glycosaminoglycans; D002807:Chondroitin