Chondroitin sulfate E fragments enhance CD44 cleavage and CD44-dependent motility in tumor cells

Cancer Research

Volumn 68, Issue 17, 2008, Pages 7191-7199

  Sugahara, Kazuki N ^a,f   Hirata, Takako ^b   Tanaka, Toshiyuki ^a,g   Ogino, Shinji ^c   Takeda, Mitsuhiro ^c,h   Terasawa, Hiroaki ^c,i   Shimada, Ichio ^c   Tamura, Jun Ichi ^d   Ten Dam, Gerdy B ^e   Van Kuppevelt, Toin H ^e   Miyasaka, Masayuki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d TOTTORI UNIVERSITY   (Japan)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f BURNHAM INSTITUTE   (United States)

^g HYOGO COLLEGE OF MEDICINE   (Japan)

^h NAGOYA UNIVERSITY   (Japan)

ⁱ KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; CHONDROITIN SULFATE E; HERMES ANTIGEN; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; CHONDROITIN SULFATE GLYCOSAMINOGLYCAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; TUMOR CELL; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD44; CELL LINE, TUMOR; CELL MOVEMENT; CHONDROITIN SULFATES; CHROMATOGRAPHY, GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED BALB C; MICE, NUDE; PANCREATIC NEOPLASMS;

EID: 52049106366     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-6198     Document Type: Article

References (47)

1. Smetsers TF, van de Westerlo EM, ten Dam GB, et al. Localization and characterization of melanoma-associated glycosaminoglycans: differential expression of chondroitin and heparan sulfate epitopes in melanoma. Cancer Res 2003;63:2965-70.
2. Smetsers TF, van de Westerlo EM, ten Dam GB, et al. Human single-chain antibodies reactive with native chondroitin sulfate detect chondroitin sulfate alterations in melanoma and psoriasis. J Invest Dermatol 2004;122:707-16.
3. Yamori T, Ota DM, Cleary KR, Irimura T. Increased content of chondroitin sulfate proteoglycan in human colorectal carcinoma metastases compared with the primary tumor as determined by an anti-chondroitin-sulfate monoclonal antibody. J Cell Biochem 1988;36:405-16.
4. Ricciardelli C, Quinn DI, Raymond WA, et al. Elevated levels of peritumoral chondroitin sulfate are predictive of poor prognosis in patients treated by radical prostatectomy for early-stage prostate cancer. Cancer Res 1999;59:2324-8.
5. Denholm EM, Lin YQ, Silver PJ. Anti-tumor activities of chondroitinase AC and chondroitinase B: inhibition of angiogenesis, proliferation and invasion. Eur J Pharmacol 2001;416:213-21.
6. Lee CM, Tanaka T, Murai T, et al. Novel chondroitin sulfate-binding cationic liposomes loaded with cisplatin efficiently suppress the local growth and liver metastasis of tumor cells in vivo. Cancer Res 2002;62:4282-8.
7. Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K. Specific molecular interactions of over-sulfated chondroitin sulfate E with various heparinbinding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 2002;277:43707-16.
8. Ueoka C, Kaneda N, Okazaki I, Nadanaka S, Muramatsu T, Sugahara K. Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural and functional implications of the oversulfated chondroitin sulfate. J Biol Chem 2000;275:37407-13.
9. Kawashima H, Atarashi K, Hirose M, et al. Oversulfated chondroitin/dermatan sulfates containing GlcAβ1/IdoAα1-3GalNAc(4,6-O- disulfate) interact with L- and P-selectin and chemokines. J Biol Chem 2002;277:12921-30.
10. Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol 2003;13:612-20.
11. Sugahara K, Mikami T. Chondroitin/dermatan sulfate in the central nervous system. Curr Opin Struct Biol 2007;17:536-45.
12. ten Dam GB, van de Westerlo EM, Purushothaman A, 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. Am J Pathol 2007;171:1324-33.
13. Lesley J, Hyman R, Kincade PW. CD44 and its interaction with extracellular matrix. Adv Immunol 1993;54:271-335.
14. Bourguignon LY, Singleton PA, Diedrich F, Stern R, Gilad E. CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2and cathepsin B activation and breast tumor cell invasion. J Biol Chem 2004;279:26991-7007.
15. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 2004;4:528-39.
16. Sugahara KN, Hirata T, Hayasaka H, Stern R, Murai T, Miyasaka M. Tumor cells enhance their own CD44 cleavage and motility by generating hyaluronan fragments. J Biol Chem 2006;281:5861-8.
17. Stern R, Asari AA, Sugahara KN. Hyaluronan fragments: an information-rich system. Eur J Cell Biol 2006;85:699-715.
18. Sugahara KN, Hirata T, Murai T, Miyasaka M. Hyaluronan oligosaccharides and tumor progression. Trends Glycosci Glycotech 2004;16:187-97.
19. Sugahara KN, Murai T, Nishinakamura H, Kawashima H, Saya H, Miyasaka M. Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells. J Biol Chem 2003;278:32259-65.
20. Baker JR, Yu H, Morrison K, Averett WF, Pritchard DG. Specificity of the hyaluronate lyase of group-B streptococcus toward unsulphated regions of chondroitin sulphate. Biochem J 1997;327:65-71.
21. Csoka AB, Frost GI, Stern R. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol 2001;20:499-508.
22. Okamoto I, Tsuiki H, Kenyon LC, et al. Proteolytic cleavage of the CD44 adhesion molecule in multiple human tumors. Am J Pathol 2002;160:441-7.
23. Guo YJ, Liu G, Wang X, et al. Potential use of soluble CD44 in serum as indicator of tumor burden and metastasis in patients with gastric or colon cancer. Cancer Res 1994;54:422-6.
24. Okamoto I, Kawano Y, Tsuiki H, et al. CD44 cleavage induced by a membrane-associated metalloprotease plays a critical role in tumor cell migration. Oncogene 1999;18:1435-46.
25. Tamura J, Tokuyoshi M. Synthesis of chondroitin sulfate E hexasaccharide in the repeating region by an effective elongation strategy toward longer chondroitin oligosaccharide. Biosci Biotechnol Biochem 2004;68:2436-43.
26. Tamura J, Nakada Y, Taniguchi K, Yamane M. Synthesis of chondroitin sulfate E octasaccharide in a repeating region involving an acetamide auxiliary. Carbohydr Res 2007;343:39-47.
27. Bardeesy N, DePinho RA. Pancreatic cancer biology and genetics. Nat Rev Cancer 2002;2:897-909.
28. Purushothaman A, Fukuda J, Mizumoto S, 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. J Biol Chem 2007;282:19442-52.
29. Kawashima H, Hirose M, Hirose J, Nagakubo D, Plaas AH, Miyasaka M. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to Lselectin, P-selectin, and CD44. J Biol Chem 2000;275:35448-56.
30. Hamai A, Hashimoto N, Mochizuki H, et al. Two distinct chondroitin sulfate ABC lyases. An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J Biol Chem 1997;272:9123-30.
31. Takeda M, Terasawa H, Sakakura M, et al. Hyaluronan recognition mode of CD44 revealed by crosssaturation and chemical shift perturbation experiments. J Biol Chem 2003;278:43550-5.
32. Takeda M, Terasawa H, Sakakura M, et al. 1H, 13C and 15N backbone resonance assignments of the hyaluronan-binding domain of CD44. J Biomol NMR 2004;29:97-8.
33. Okamoto I, Kawano Y, Murakami D, et al. Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J Cell Biol 2001;155:755-62.
34. Theocharis AD, Tsara ME, Papageorgacopoulou N, Karavias DD, Theocharis DA. Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochim Biophys Acta 2000;1502:201-6.
35. Theocharis AD, Vynios DH, Papageorgakopoulou N, Skandalis SS, Theocharis DA. Altered content composition and structure of glycosaminoglycans and proteoglycans in gastric carcinoma. Int J Biochem Cell Biol 2003;35:376-90.
36. Kajita M, Itoh Y, Chiba T, et al. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 2001;153:893-904.
37. Varki A, Angata T. Siglecs - the Major Sub-family of Itype Lectins. Glycobiology 2006;16:1-27R.
38. Lokeshwar VB, Cerwinka WH, Lokeshwar BL. HYAL1 hyaluronidase: a molecular determinant of bladder tumor growth and invasion. Cancer Res 2005; 65:2243-50.
39. Liu D, Pearlman E, Diaconu E, et al. Expression of hyaluronidase by tumor cells induces angiogenesis in vivo. Proc Natl Acad Sci U S A 1996;93:7832-7.
40. Deepa SS, Kalayanamitra K, Ito Y, et al. Novel sulfated octa- and decasaccharides from squid cartilage chondroitin sulfate E: sequencing and application for determination of the epitope structure of the monoclonal antibody MO-225. Biochemistry 2007;46:2453-65.
41. Knudson W, Chow G, Knudson CB. CD44-mediated uptake and degradation of hyaluronan. Matrix Biol 2002; 21:15-23.
42. Bourguignon LY, Zhu H, Shao L, Chen YW. CD44 interaction with tiam1 promotes Rac1 signaling and hyaluronic acid-mediated breast tumor cell migration. J Biol Chem 2000;275:1829-38.
43. Nagano O, Saya H. Mechanism and biological significance of CD44 cleavage. Cancer Sci 2004;95:930-5.
44. Nagano O, Murakami D, Hartmann D, et al. Cellmatrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca(2+) influx and PKC activation. J Cell Biol 2004;165:893-902.
45. Oliferenko S, Kaverina I, Small JV, Huber LA. Hyaluronic acid (HA) binding to CD44 activates Rac1 and induces lamellipodia outgrowth. J Cell Biol 2000;148:1159-64.
46. Takeda M, Ogino S, Umemoto R, et al. Ligand-induced structural changes of the CD44 hyaluronan-binding domain revealed by NMR. J Biol Chem 2006;281:40089-95.
47. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-8.