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BioMed Research International
Volume 2013 (2013), Article ID 656319, 9 pages
Expression of N-Acetylgalactosamine 4-Sulfate 6-O-Sulfotransferase Involved in Chondroitin Sulfate Synthesis Is Responsible for Pulmonary Metastasis
1Laboratory of Proteoglycan Signaling and Therapeutics, Frontier Research Center for Post-Genomic Science and Technology, Graduate School of Life Science Hokkaido University, West-11, North-21, Kita-ku, Sapporo, Hokkaido 001-0021, Japan
2Department of Pathobiochemistry, Faculty of Pharmacy, Meijo University, 150 Yagotoyama, Tempaku-ku, Nagoya 468-8503, Japan
Received 27 November 2012; Accepted 20 December 2012
Academic Editor: Davide Vigetti
Copyright © 2013 Shuji Mizumoto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- R. V. Iozzo, “Matrix proteoglycans: from molecular design to cellular function,” Annual Review of Biochemistry, vol. 67, pp. 609–652, 1998.
- K. Sugahara and H. Kitagawa, “Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans,” Current Opinion in Structural Biology, vol. 10, no. 5, pp. 518–527, 2000.
- K. Sugahara, T. Mikami, T. Uyama, S. Mizuguchi, K. Nomura, and H. Kitagawa, “Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate,” Current Opinion in Structural Biology, vol. 13, no. 5, pp. 612–620, 2003.
- K. Sugahara and T. Mikami, “Chondroitin/dermatan sulfate in the central nervous system,” Current Opinion in Structural Biology, vol. 17, no. 5, pp. 536–545, 2007.
- M. M. Fuster and J. D. Esko, “The sweet and sour of cancer: glycans as novel therapeutic targets,” Nature Reviews Cancer, vol. 5, no. 7, pp. 526–542, 2005.
- A. E. Faassen, J. A. Schrager, D. J. Klein, T. R. Oegema, J. R. Couchman, and J. B. McCarthy, “A cell surface chondroitin sulfate proteoglycan, immunologically related to CD44, is involved in type I collagen-mediated melanoma cell motility and invasion,” Journal of Cell Biology, vol. 116, no. 2, pp. 521–531, 1992.
- U. Günthert, M. Hofmann, W. Rudy et al., “A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells,” Cell, vol. 65, no. 1, pp. 13–24, 1991.
- J. Iida, A. M. L. Meijne, J. R. Knutson, L. T. Furcht, and J. B. McCarthy, “Cell surface chondroitin sulfate proteoglycans in tumor cell adhesion, motility and invasion,” Seminars in Cancer Biology, vol. 7, no. 3, pp. 155–162, 1996.
- C. A. Cooney, F. Jousheghany, A. Yao-Borengasser et al., “Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells,” Breast Cancer Research, vol. 13, article R58, 2011.
- S. Kim, H. Takahashi, W. W. Lin et al., “Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis,” Nature, vol. 457, no. 7225, pp. 102–106, 2009.
- M. Kusche-Gullberg and L. Kjellén, “Sulfotransferases in glycosaminoglycan biosynthesis,” Current Opinion in Structural Biology, vol. 13, no. 5, pp. 605–611, 2003.
- M. Klüppel, T. N. Wight, C. Chan, A. Hinek, and J. L. Wrana, “Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis,” Development, vol. 132, no. 17, pp. 3989–4003, 2005.
- H. Thiele, M. Sakano, H. Kitagawa et al., “Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 27, pp. 10155–10160, 2004.
- M. H. H. van Roij, S. Mizumoto, S. Yamada et al., “Spondyloepiphyseal dysplasia, omani type: further definition of the phenotype,” American Journal of Medical Genetics A, vol. 146, no. 18, pp. 2376–2384, 2008.
- B. Tuysuz, S. Mizumoto, K. Sugahara, A. Çelebi, S. Mundlos, and S. Turkmen, “Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3,” Clinical Genetics, vol. 75, no. 4, pp. 375–383, 2009.
- S. Nadanaka, A. Clement, K. Masayama, A. Faissner, and K. Sugahara, “Characteristic hexasaccharide sequences in octasaccharides derived from shark cartilage chondroitin sulfate D with a neurite outgrowth promoting activity,” Journal of Biological Chemistry, vol. 273, no. 6, pp. 3296–3307, 1998.
- X. Bao, T. Muramatsu, and K. Sugahara, “Demonstration of the pleiotrophin-binding oligosaccharide sequences isolated from chondroitin sulfate/dermatan sulfate hybrid chains of embryonic pig brains,” Journal of Biological Chemistry, vol. 280, no. 42, pp. 35318–35328, 2005.
- A. Purushothaman, K. Sugahara, and A. Faissner, “Chondroitin sulfate, “wobble motifs” modulate maintenance and differentiation of neural stem cells and their progeny,” Journal of Biological Chemistry, vol. 287, no. 5, pp. 2935–2942, 2012.
- K. Bergefall, E. Trybala, M. Johansson et al., “Chondroitin sulfate characterized by the E-disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2C cells,” Journal of Biological Chemistry, vol. 280, no. 37, pp. 32193–32199, 2005.
- T. Uyama, M. Ishida, T. Izumikawa et al., “Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity,” Journal of Biological Chemistry, vol. 281, no. 50, pp. 38668–38674, 2006.
- A. Purushothaman, J. Fukuda, S. Mizumoto et al., “Functions of chondroitin sulfate/dermatan sulfate chains in brain development: critical roles of E and iE disaccharide units recognized by a single chain antibody GD3G7,” Journal of Biological Chemistry, vol. 282, no. 27, pp. 19442–19452, 2007.
- G. B. ten Dam, E. M. A. van de Westerlo, A. Purushothaman et al., “Antibody GD3G7 selected against embryonic glycosaminoglycans defines chondroitin sulfate-E domains highly up-regulated in ovarian cancer and involved in vascular endothelial growth factor binding,” American Journal of Pathology, vol. 171, no. 4, pp. 1324–1333, 2007.
- K. N. Sugahara, T. Hirata, T. Tanaka et al., “Chondroitin sulfate E fragments enhance CD44 cleavage and CD44-dependent motility in tumor cells,” Cancer Research, vol. 68, no. 17, pp. 7191–7199, 2008.
- S. Ohtake, Y. Ito, M. Fukuta, and O. Habuchi, “Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene,” Journal of Biological Chemistry, vol. 276, no. 47, pp. 43894–43900, 2001.
- S. Ohtake-Niimi, S. Kondo, T. Ito et al., “Mice deficient in N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase are unable to synthesize chondroitin/dermatan sulfate containing N-acetylgalactosamine 4,6-bissulfate residues and exhibit decreased protease activity in bone marrow-derived mast cells,” Journal of Biological Chemistry, vol. 285, no. 27, pp. 20793–20805, 2010.
- Y. Ito, M. Watanabe, T. Nishizawa et al., “The utility of formalin-fixed and paraffin-embedded tissue blocks for quantitative analysis of N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase mRNA expressed by colorectal cancer cells,” Acta Histochemica et Cytochemica, vol. 40, no. 2, pp. 53–59, 2007.
- F. Li, G. B. ten Dam, S. Murugan et al., “Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells,” Journal of Biological Chemistry, vol. 283, no. 49, pp. 34294–34304, 2008.
- S. Mizumoto, J. Takahashi, and K. Sugahara, “Receptor for advanced glycation end products (RAGE) functions as receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells,” Journal of Biological Chemistry, vol. 287, no. 23, pp. 18985–18994, 2012.
- A. Kinoshita and K. Sugahara, “Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liquid chromatography: application to disaccharide composition analysis and exosequencing of oligosaccharides,” Analytical Biochemistry, vol. 269, no. 2, pp. 367–378, 1999.
- S. Mizumoto and K. Sugahara, “Glycosaminoglycan chain analysis and characterization (glycosylation/epimerization),” Methods in Molecular Biology, vol. 836, pp. 99–115, 2012.
- B. Rashidi, M. Yang, P. Jiang et al., “A highly metastatic Lewis lung carcinoma orthotopic green fluorescent protein model,” Clinical and Experimental Metastasis, vol. 18, no. 1, pp. 57–60, 2000.
- I. J. Fidler, “The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited,” Nature Reviews Cancer, vol. 3, no. 6, pp. 453–458, 2003.
- P. S. Steeg, “Tumor metastasis: mechanistic insights and clinical challenges,” Nature Medicine, vol. 12, no. 8, pp. 895–904, 2006.
- S. A. Eccles and D. R. Welch, “Metastasis: recent discoveries and novel treatment strategies,” The Lancet, vol. 369, no. 9574, pp. 1742–1757, 2007.
- P. Friedl and K. Wolf, “Tumour-cell invasion and migration: diversity and escape mechanisms,” Nature Reviews Cancer, vol. 3, no. 5, pp. 362–374, 2003.
- S. S. Deepa, Y. Umehara, S. Higashiyama, N. Itoh, and K. Sugahara, “Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors: implications as a physiological binding partner in the brain and other tissues,” Journal of Biological Chemistry, vol. 277, no. 46, pp. 43707–43716, 2002.
- E. Ruoslahti and E. Engvall, “Complexing of fibronectin glycosaminoglycans and collagen,” Biochimica et Biophysica Acta, vol. 631, no. 2, pp. 350–358, 1980.
- E. G. Hayman, A. Oldberg, G. R. Martin, and E. Ruoslahti, “Codistribution of heparan sulfate proteoglycan, laminin, and fibronectin in the extracellular matrix of normal rat kidney cells and their coordinate absence in transformed cells,” Journal of Cell Biology, vol. 94, no. 1, pp. 28–35, 1982.
- M. P. Hoffman, J. A. Engbring, P. K. Nielsen et al., “Cell type-specific differences in glycosaminoglycans modulate the biological activity of a heparin-binding peptide (RKRLQVQLSIRT) from the G domain of the laminin α1 chain,” Journal of Biological Chemistry, vol. 276, no. 25, pp. 22077–22085, 2001.
- J. Zhang, J. Nakayama, C. Ohyama et al., “Sialyl Lewis X-dependent lung colonization of B16 melanoma cells through a selectin-like endothelial receptor distinct from E- or P-selectin,” Cancer Research, vol. 62, no. 15, pp. 4194–4198, 2002.
- B. Monzavi-Karbassi, J. S. Stanley, L. Hennings et al., “Chondroitin sulfate glycosaminoglycans as major P-selectin ligands on metastatic breast cancer cell lines,” International Journal of Cancer, vol. 120, no. 6, pp. 1179–1191, 2007.
- H. Kawashima, K. Atarashi, M. Hirose et al., “Oversulfated chondroitin/dermatan sulfates containing GlcAβ1/IdoAα1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines,” Journal of Biological Chemistry, vol. 277, no. 15, pp. 12921–12930, 2002.
- C. H. Chou, C. M. Teng, K. Y. Tzen, Y. C. Chang, J. H. Chen, and J. C. H. Cheng, “MMP-9 from sublethally irradiated tumor promotes Lewis lung carcinoma cell invasiveness and pulmonary metastasis,” Oncogene, vol. 31, pp. 458–468, 2011.
- S. Munesue, Y. Yoshitomi, Y. Kusano et al., “A novel function of syndecan-2, suppression of matrix metalloproteinase-2 activation, which causes suppression of metastasis,” Journal of Biological Chemistry, vol. 282, no. 38, pp. 28164–28174, 2007.
- J. Iida, D. Pei, T. Kang et al., “Melanoma chondroitin sulfate proteoglycan regulates matrix metalloproteinase-dependent human melanoma invasion into type I collagen,” Journal of Biological Chemistry, vol. 276, no. 22, pp. 18786–18794, 2001.
- Y. Shintani, S. Takashima, Y. Asano et al., “Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling,” EMBO Journal, vol. 25, no. 13, pp. 3045–3055, 2006.