Identification of novel chondroitin proteoglycans in Caenorhabditis elegans: Embryonic cell division depends on CPG-1 and CPG-2

Journal of Cell Biology

Volumn 173, Issue 6, 2006, Pages 985-994

  Olson, Sara K ^a,b   Bishop, Joseph R ^a   Yates, John R ^d   Oegema, Karen ^a,c   Esko, Jeffrey D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; PROTEIN CPG 1; PROTEIN CPG 2; PROTEOCHONDROITIN; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; CELL DIVISION; COELENTERATE; CONTROLLED STUDY; CYTOKINESIS; DROSOPHILA MELANOGASTER; EMBRYO CELL; EMBRYO DEVELOPMENT; MASS SPECTROMETRY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIVISION; CHITIN; GLYCOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PROTEOCHONDROITIN SULFATES; PROTEOMICS; RNA INTERFERENCE; SEQUENCE ANALYSIS, PROTEIN;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; HYDRA VULGARIS; INVERTEBRATA; VERTEBRATA;

EID: 33745238969     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200603003     Document Type: Article

References (51)

1. Audhya, A., F. Hyndman, I.X. McLeod, A.S. Maddox, J.R. Yates III, A. Desai, and K. Oegema. 2005. A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J. Cell Biol. 171:267-279.
2. Bame, K.J., and J.D. Esko. 1989. Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264:8059-8065.
3. Beintema, J.J. 1994. Structural features of plant chitinases and chitin-binding proteins. FEBS Lett. 350:159-163.
4. Bellin, R., I. Capila, J. Lincecum, P.W. Park, O. Reizes, and M.R. Bernfield. 2002. Unlocking the secrets of syndecans: transgenic organisms as a potential key. Glycoconj. J. 19:295-304.
5. Berninsone, P., H.Y. Hwang, I. Zemtseva, H.R. Horvitz, and C.B. Hirschberg. 2001. SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetylgalactosamine, and UDP-galactose. Proc. Natl. Acad. Sci. USA. 98:3738-3743.
6. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
7. Bulik, D.A., and P.W. Robbins. 2002. The Caenorhabditis elegans sqv genes and functions of proteoglycans in development. Biochim Biophys Acta. 1573:247-257.
8. Bulik, D.A., G. Wei, H. Toyoda, A. Kinoshita-Toyoda, W.R. Waldrip, J.D. Esko, P.W. Robbins, and S.B. Selleck. 2000. sqv-3 -7, and -8, a set of genes affecting morphogenesis in Caenorhabditis elegans, encode enzymes required for glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA. 97:10838-10843.
9. Esko, J.D. 1993. Special considerations for proteoglycans and glycosaminoglycans and their purification. In Current Protocols in Molecular Biology. F. Ausubel, R. Brent, B. Kingston, D. Moore, J. Seidman, J. Smith, K. Struhl, A. Varki, and J. Coligan, editors. Greene Publishing and Wiley-Interscience, New York. 17.2.1-17.2.9.
10. Esko, J.D., and A. Manzi. 1996. Measurement of uronic acids. In Current Protocols in Molecular Biology. F. Ausubel, R. Brent, B. Kingston, D. Moore, J. Seidman, J. Smith, K. Struhl, A. Varki, and J. Coligan, editors. Greene Publishing and Wiley-Interscience, New York. 17.9.8-17.9.11.
11. Esko, J.D., and L. Zhang. 1996. Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6:663-670.
12. Esko, J.D., and S.B. Selleck. 2002. Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71:435-471.
13. Ghiselli, G., and R.V. Iozzo. 2000. Overexpression of bamacan/SMC3 causes transformation. J. Biol. Chem. 275:20235-20238.
14. Goldberg, M., D. Septier, O. Rapoport, R.V. Iozzo, M.F. Young, and L.G. Ameye. 2005. Targeted disruption of two small leucine-rich proteoglycans, biglycan and decorin, excerpts divergent effects on enamel and dentin formation. Calcif. Tissue Int. 77:297-310.
15. Grobe, K., and J.D. Esko. 2002. Regulated translation of heparan sulfate N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes by structured 5′-untranslated regions and internal ribosome entry sites. J. Biol. Chem. 277:30699-30706.
16. Habuchi, O. 2000. Diversity and functions of glycosaminoglycan sulfotransferases. Biochim. Biophys. Acta. 1474:115-127.
17. Hassell, J., Y. Yamada, and E. Arikawa-Hirasawa. 2002. Role of perlecan in skeletal development and diseases. Glycoconj. J. 19:263-267.
18. Herman, T., E. Hartwieg, and H.R. Horvitz. 1999. sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination. Proc. Natl. Acad. Sci. USA. 96:968-973.
19. Hwang, H.Y., and H.R. Horvitz. 2002a. The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated. Proc. Natl. Acad. Sci. USA. 99:14224-14229.
20. Hwang, H.Y., and H.R. Horvitz. 2002b. The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 transporter may act in the Golgi apparatus to affect Caenorhabditis elegans vulval morphogenesis and embryonic development. Proc. Natl. Acad. Sci. USA. 99:14218-14223.
21. Hwang, H.Y., S.K. Olson, J.R. Brown, J.D. Esko, and H.R. Horvitz. 2003a. The Caenorhabditis elegans genes sqv-2 and sqv-6, which are required for vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase. J. Biol. Chem. 278:11735-11738.
22. Hwang, H.Y., S.K. Olson, J.D. Esko, and H.R. Horvitz. 2003b. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature. 423:439-443.
23. Iozzo, R.V. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67:609-652.
24. Izumikawa, T., H. Kitagawa, S. Mizuguchi, K.H. Nomura, K. Nomura, J. Tamura, K. Gengyo-Ando, S. Mitani, and K. Sugahara. 2004. Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division. J. Biol. Chem. 279:53755-53761.
25. Jones, A.R., R. Francis, and T. Schedl. 1996. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180:165-183.
26. Kamath, R.S., M. Martinez-Campos, P. Zipperlen, A.G. Fraser, and J. Ahringer. 2001. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2:RESEARCH0002.1-RESEARCH0002.10.
27. Lee, M.H., and T. Schedl. 2001. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15:2408-2420.
28. Lee, M.H., and T. Schedl. 2004. Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev. 18:1047-1059.
29. MacCoss, M.J., W.H. McDonald, A. Saraf, R. Sadygov, J.M. Clark, J.J. Tasto, K.L. Gould, D. Wolters, M. Washburn, A. Weiss, et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. USA. 99:7900-7905.
30. Maddox, A.S., B. Habermann, A. Desai, and K. Oegema. 2005. Distinct roles for two C. elegans anillins in the gonad and early embryo. Development. 132:2837-2848.
31. Marneros, A.G., and B.R. Olsen. 2005. Physiological role of collagen XVIII and endostatin. FASEB J. 19:716-728.
32. Merzendorfer, H., and L. Zimoch. 2003. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J. Exp. Biol. 206:4393-4412.
33. Mizuguchi, S., T. Uyama, H. Kitagawa, K.H. Nomura, K. Dejima, K. Gengyo-Ando, S. Mitani, K. Sugahara, and K. Nomura. 2003. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature. 423:443-448.
34. Niisato, K., A. Fujikawa, S. Komai, T. Shintani, E. Watanabe, G. Sakaguchi, G. Katsuura, T. Manabe, and M. Noda. 2005. Age-dependent enhancement of hippocampal long-term potentiation and impairment of spatial learning through the Rho-associated kinase pathway in protein tyrosine phosphatase receptor type Z-deficient mice. J. Neurosci. 25:1081-1088.
35. Olson, S.K., and J.D. Esko. 2004. Proteoglycans. In Encyclopedia of Biological Chemistry. Vol. 3. W. Lennarz and M.D. Lane, editors. Elsevier, Oxford. 549-555.
36. Ozerdem, U., and W.B. Stallcup. 2004. Pathological angiogenesis is reduced by targeting pericytes via the NG2 proteoglycan. Angiogenesis. 7:269-276.
37. Reinke, V., H.E. Smith, J. Nance, J. Wang, C. Van Doren, R. Begley, S.J. Jones, E.B. Davis, S. Scherer, S. Ward, and S.K. Kim. 2000. A global profile of germline gene expression in C. elegans. Mol. Cell. 6:605-616.
38. Schwartz, N.B., and M. Domowicz. 2002. Chondrodysplasias due to proteoglycan defects. Glycobiology. 12:57R-68R.
39. Schwartz, N.B., and M. Domowicz. 2004. Proteoglycans in brain development. Glycoconj. J. 21:329-341.
40. Sugahara, K., T. Mikami, T. Uyama, S. Mizuguchi, K. Nomura, and H. Kitagawa. 2003. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13:612-620.
41. Toyoda, H., A. Kinoshita-Toyoda, and S.B. Selleck. 2000. Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J. Biol. Chem. 275:2269-2275.
42. Venegas, A., J.C. Goldstein, K. Beauregard, A. Oles, N. Abdulhayoglu, and J.A. Fuhrman. 1996. Expression of recombinant microfilarial chitinase and analysis of domain function. Mol. Biochem. Parasitol. 78:149-159.
43. Washburn, M.P., D. Wolters, and J.R. Yates III. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19:242-247.
44. Washburn, M.P., R. Ulaszek, C. Deciu, D.M. Schieltz, and J.R. Yates III. 2002. Analysis of quantitative proteomic data generated via multidimensional protein identification technology. Anal. Chem. 74:1650-1657.
45. Wells, L., K. Vosseller, R.N. Cole, J.M. Cronshaw, M.J. Matunis, and G.W. Hart. 2002. Mapping sites of O-GlcNAc modification using affinity tags for serine and threonine post-translational modifications. Mol. Cell. Proteomics. 1:791-804.
46. Wolters, D.A., M.P. Washburn, and J.R. Yates III. 2001. An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 73:5683-5690.
47. Wright, H.T., G. Sandrasegaram, and C.S. Wright. 1991. Evolution of a family of N-acetylglucosamine binding proteins containing the disulfide-rich domain of wheat germ agglutinin. J. Mol. Evol. 33:283-294.
48. Wu, R.R., and J.R. Couchman. 1997. cDNA cloning of the basement membrane chondroitin sulfate proteoglycan core protein, bamacan: a five domain structure including coiled-coil motifs. J. Cell Biol. 136:433-444.
49. Yamada, S., I. Van Die, D.H. Van den Eijnden, A. Yokota, H. Kitagawa, and K. Sugahara. 1999. Demonstration of glycosaminoglycans in Caenorhabditis elegans. FEBS Lett. 459:327-331.
50. Yamada, S., Y. Okada, M. Ueno, S.S. Deepa, S. Nishimura, M. Fujita, I. Van Die, Y. Hirabayashi, and K. Sugahara. 2002. Determination of the glycosaminoglycan-protein linkage region oligosaccharide structures of proteoglycans from Drosophila melanogaster and Caenorhabditis elegans. J. Biol. Chem. 277:31877-31886.
51. Zelensky, A.N., and J.E. Gready. 2003. Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD). Proteins. 52:466-477.