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Published 11 September 2006. doi:10.1083/jcb.200603129
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 174, Number 6, 773-778
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Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling



Keisuke Kamimura1,2, Takashi Koyama1, Hiroko Habuchi2, Ryu Ueda3, Masayuki Masu4, Koji Kimata2, and Hiroshi Nakato1

1 Department of Genetics, Cell Biology, and Development, The University of Minnesota, Minneapolis, MN 55455
2 Institute for Molecular Science of Medicine, Aichi Medical University, Aichi 480-1195, Japan
3 Invertebrate Genetics Laboratory, Genetic Strain Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan
4 Department of Molecular Neurobiology, Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Ibaraki 305-8577, Japan

Correspondence to Hiroshi Nakato: nakat003{at}umn.edu

Specific sulfation sequence of heparan sulfate (HS) contributes to the selective interaction between HS and various proteins in vitro. To clarify the in vivo importance of HS fine structures, we characterized the functions of the Drosophila HS 2-O and 6-O sulfotransferase (Hs2st and Hs6st) genes in FGF-mediated tracheal formation. We found that mutations in Hs2st or Hs6st had unexpectedly little effect on tracheal morphogenesis. Structural analysis of mutant HS revealed not only a loss of corresponding sulfation, but also a compensatory increase of sulfation at other positions, which maintains the level of HS total charge. The restricted phenotypes of Hsst mutants are ascribed to this compensation because FGF signaling is strongly disrupted by Hs2st; Hs6st double mutation, or by overexpression of 6-O sulfatase, an extracellular enzyme which removes 6-O sulfate groups without increasing 2-O sulfation. These findings suggest that the overall sulfation level is more important than strictly defined HS fine structures for FGF signaling in some developmental contexts.

Abbreviations used in this paper: bnl, branchless; btl, breathless; HS, heparan sulfate; HSPG, heparan sulfate proteoglycan; Hs2st, heparan sulfate 2-O sulfotransferase; Hs6st, heparan sulfate 6-O sulfotransferase; sfl; sulfateless; trh, trachealess.


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