Preparation of chondroitin sulfate libraries containing disulfated disaccharide units and inhibition of thrombin by these chondroitin sulfates

Glycoconjugate Journal

Volumn 27, Issue 5, 2010, Pages 479-489

  Numakura, Mario ^a,b   Kusakabe, Noriko ^a   Ishige, Kazuya ^b   Ohtake Niimi, Shiori ^a   Habuchi, Hiroko ^c   Habuchi, Osami ^a  

^a AICHI UNIVERSITY OF EDUCATION   (Japan)

^b YAMASA CORPORATION   (Japan)

^c AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Chondroitin sulfate; Disulfated disaccharide; Inhibition of thrombin; Sulfotransferase

Indexed keywords

CHONDROITIN SULFATE; DISACCHARIDE; FIBRINOGEN; N ACETYLGALACTOSAMINE 4 SULFATE 6 O SULFOTRANSFERASE; SULFOTRANSFERASE; THROMBIN; UNCLASSIFIED DRUG; URONOSYL 2 O SULFOTRANSFERASE;

ARTICLE; CATALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME MECHANISM; IN VITRO STUDY; INHIBITION KINETICS; MOLECULAR LIBRARY; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; STRUCTURE ACTIVITY RELATION; SULFATION;

ANIMALS; ANTITHROMBINS; CHONDROITIN SULFATES; DISACCHARIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR X; FIBRINOGEN; HUMANS; SMALL MOLECULE LIBRARIES; SULFOTRANSFERASES; THROMBIN;

EID: 77955569887     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-010-9293-2     Document Type: Article

References (36)

1. Y Kawai N Seno K Anno 1966 Chondroitin polysulfate of squid cartilage J. Biochem. 60 317 321 1:CAS:528:DyaF28XltV2gurc%3D 5970999
2. S Suzuki H Saito T Yamagata K Anno N Seno Y Kawai T Furuhashi 1968 Formation of three types of disulfated disaccharides from chondroitin sulfates by chondroitinase digestion J. Biol. Chem. 243 1543 1550 1:CAS:528: DyaF1cXosVGgug%3D%3D 5647269
3. RL Stevens R Adachi 2007 Protease-proteoglycan complexes of mouse and human mast cells and importance of their beta-tryptase-heparin complexes in inflammation and innate immunity Immunol. Rev. 217 155 167 10.1111/j.1600-065X. 2007.00525.x 1:CAS:528:DC%2BD2sXnt1Gmurs%3D 17498058 (Pubitemid 46718158)
4. AM Clement K Sugahara A Faissner 1999 Chondroitin sulfate E promotes neurite outgrowth of rat embryonic day 18 hippocampal neurons Neurosci. Lett. 269 125 128 10.1016/S0304-3940(99)00432-2 1:CAS:528:DyaK1MXktVGqtbY%3D 10454148 (Pubitemid 29317716)
5. SE Tully R Mabon CI Gama SM Tsai X Liu LC Hsieh-Wilson 2004 A chondroitin sulfate small molecule that stimulates neuronal growth J. Am. Chem. Soc. 126 7736 7737 10.1021/ja0484045 1:CAS:528:DC%2BD2cXksVKhsr4%3D 15212495 (Pubitemid 38812740)
6. H Kawashima M Hirose J Hirose D Nagakubo AHK Plaas M Miyasaka 2000 Binding of a Large Chondroitin Sulfate/Dermatan Sulfate Proteoglycan, Versican, to L-selectin, P-selectin, and CD44 J. Biol. Chem. 275 35448 35456 10.1074/jbc.M003387200 1:CAS:528:DC%2BD3cXotFeiurg%3D 10950950
7. J Hirose H Kawashima O Yoshie K Tashiro M Miyasaka 2001 Versican interacts with chemokines and modulates cellular responses J. Biol. Chem. 276 5228 5234 10.1074/jbc.M007542200 1:CAS:528:DC%2BD3MXhtlyjs7s%3D 11083865
8. C Ueoka N Kaneda I Okazaki S Nadanaka T Muramatsu K Sugahara 2000 Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural ans functional implications of the over-sulfated chondroitin sulfate J. Biol. Chem. 275 37407 37413 10.1074/jbc.M002538200 1:CAS:528:DC%2BD3cXoslWgs7Y%3D 10978312 (Pubitemid 32004844)
9. SS Deepa Y Umehara S Higashiyama N Itoh K Sugahara 2002 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 J. Biol. Chem. 277 43707 43716 10.1074/jbc.M207105200 1:CAS:528:DC%2BD38Xos1alurw%3D 12221095 (Pubitemid 36157787)
10. M Asada M Shinomiya M Suzuki E Honda R Sugimoto M Ikekita T Imamura 2009 Glycosaminoglycan affinity of the complete fibroblast growth factor family Biochim. Biophys. Acta. 1790 40 48 1:CAS:528:DC%2BD1cXhsVKrtLbP 18835578
11. K Bergefall E Trybala M Johansson T Uyama S Naito S Yamada H Kitagawa K Sugahara T Bergström 2005 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 J. Biol. Chem. 280 32193 32199 10.1074/jbc.M503645200 1:CAS:528:DC%2BD2MXpvVyqsrY%3D 16027159 (Pubitemid 41361826)
12. T Uyama M Ishida T Izumikawa E Trybala F Tufaro T Bergström K Sugahara H Kitagawa 2006 Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity J. Biol. Chem. 281 38668 38674 10.1074/jbc.M609320200 1:CAS:528:DC%2BD28Xht12msr3I 17040900 (Pubitemid 46041992)
13. F Li GB Ten Dam S Murugan S Yamada T Hashiguchi S Mizumoto K Oguri M Okayama TH van Kuppevelt K Sugahara 2008 Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells J. Biol. Chem. 283 34294 34304 10.1074/jbc.M806015200 1:CAS:528:DC%2BD1cXhsVelu7vM 18930920
14. Basappa S Murugan KN Sugahara CM Lee GB ten Dam TH van Kuppevelt M Miyasaka S Yamada K Sugahara 2009 Involvement of chondroitin sulfate E in the liver tumor focal formation of murine osteosarcoma cells Glycobiology 19 735 742 10.1093/glycob/cwp041 1:CAS:528:DC%2BD1MXms1Cjtr4%3D 19293233
15. M Ishii N Maeda 2008 Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex J. Biol. Chem. 283 32610 32620 10.1074/jbc.M806331200 1:CAS:528:DC%2BD1cXhtlOjtLrE 18819920
16. HJ Ra S Harju-Baker F Zhang RJ Linhardt CL Wilson WC Parks 2009 Control of promatrilysin (MMP7) activation and substrate-specific activity by sulfated glycosaminoglycans J. Biol. Chem. 284 27924 27932 10.1074/jbc.M109.035147 1:CAS:528:DC%2BD1MXht1Sqsb%2FJ 19654318
17. AM Clement S Nadanaka K Masayama C Mandl K Sugahara A Faissner 1998 The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D Motifs, and is sufficient to promote neurite outgrowth J. Biol. Chem. 273 28444 18453 10.1074/jbc.273.43.28444 1:CAS:528:DyaK1cXntVClsb0%3D 9774473 (Pubitemid 28496150)
18. N Maeda J He Y Yajima T Mikami K Sugahara T Yabe 2003 Heterogeneity of the Chondroitin Sulfate Portion of Phosphacan/6B4 Proteoglycan Regulates Its Binding Affinity for Pleiotrophin/Heparin Binding Growth-associated Molecule J. Biol. Chem. 278 35805 25811 10.1074/jbc.M305530200 1:CAS:528: DC%2BD3sXntVajtrs%3D 12840014 (Pubitemid 37102358)
19. O Habuchi K Sugiura N Kawai 1977 Glucose branches in chondroitin sulfates from squid cartilage J. Biol. Chem. 252 4570 4576 1:CAS:528:DyaE2sXkvFOksLs%3D 873906
20. A Kinoshita S Yamada SM Haslam HR Morris A Dell K Sugahara 1997 Novel tetrasaccharides isolated from squid cartilage chondroitin sulfate E contain unusual sulfated disaccharide units GlcA(3-O-sulfate)beta1-3GalNAc(6-O-sulfate) or GlcA(3-O-sulfate)beta1-3GalNAc J. Biol. Chem. 272 19656 19665 10.1074/jbc.272.32.19656 1:CAS:528:DyaK2sXltlGksr0%3D 9242620 (Pubitemid 27340053)
21. Y Ito O Habuchi 2000 Purification and characterization of N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase from the squid cartilage J. Biol. Chem. 275 34728 34736 10.1074/jbc.M909633199 1:CAS:528: DC%2BD3cXotFWltbw%3D 10871629
22. S Ohtake Y Ito M Fukuta O Habuchi 2001 Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene J. Biol. Chem. 276 43894 43900 10.1074/jbc.M104922200 1:CAS:528:DC%2BD3MXos12ntL0%3D 11572857
23. T Yamaguchi S Ohtake K Kimata O Habuchi 2007 Molecular cloning of squid N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase and synthesis of a unique chondroitin sulfate containing E-D hybrid tetrasaccharide structure by the recombinant enzyme Glycobiology 17 1365 1376 10.1093/glycob/cwm103 1:CAS:528:DC%2BD2sXhtlejsrbN 17893095 (Pubitemid 350131313)
24. O Habuchi R Moroi S Ohtake 2002 Emzymatic synthesis of chondroitin sulfate E by N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase purified from the squid cartilage Anal. Biochem. 310 129 136 10.1016/S0003-2697(02)00277-4 1:CAS:528:DC%2BD38XotlKis70%3D 12423630 (Pubitemid 35388253)
25. M Kobayashi G Sugumaran J Liu NW Shworak JE Silbert RD Rosenberg 1999 Molecular cloning and characterization of a human uronyl 2-sulfotransferase that sulfates iduronyl and glucuronyl residues in dermatan/chondroitin sulfate J. Biol. Chem. 274 10474 10480 10.1074/jbc.274.15.10474 1:CAS:528: DyaK1MXis1Gju7g%3D 10187838 (Pubitemid 29180925)
26. S Ohtake K Kimata O Habuchi 2005 Recognition of sulfation pattern of chondroitin sulfate by uronosyl 2-O-sulfotransferase J. Biol. Chem. 280 39115 39123 10.1074/jbc.M508816200 1:CAS:528:DC%2BD2MXht1emsrvK 16192264 (Pubitemid 41713862)
27. 35S]sulfate with a predetermined specific activity Anal. Biochem. 148 303 310 10.1016/0003-2697(85) 90233-7 1:CAS:528:DyaL2MXltF2gsL8%3D 4061812 (Pubitemid 15045385)
28. O Habuchi Y Matsui Y Kotoya Y Aoyama Y Yasuda M Noda 1993 Purification of chondroitin 6-sulfotransferase secreted from cultured chick embryo chondrocytes J. Biol. Chem. 268 21968 21974 1:CAS:528:DyaK3sXlsFCmt7g%3D 8408053
29. H Toyoda A Kinoshita-Toyoda SB 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 10.1074/jbc.275.4.2269 1:CAS:528:DC%2BD3cXpvFerug%3D%3D 10644674 (Pubitemid 30081981)
30. BL Henry BH Monien PE Bock UR Desai 2007 A novel allosteric pathway of thrombin inhibition. EXOSITE II MEDIATED POTENT INHIBITION OF THROMBIN BY CHEMO-ENZYMATIC, SULFATED DEHYDROPOLYMERS OF 4-HYDROXYCINNAMIC ACIDS J. Biol. Chem. 282 31891 31899 10.1074/jbc.M704257200 1:CAS:528:DC%2BD2sXht1WlsrfP 17804413 (Pubitemid 350106430)
31. V Vigdorovich D Miller RK Strong 2007 Ability of hyaluronidase 2 to degrade extracellular hyaluronan is not required for its function as a receptor for jaagsiekte sheep retrovirus J. Virol. 81 3124 3129 10.1128/JVI.02177-06 1:CAS:528:DC%2BD2sXjslWrur0%3D 17229709 (Pubitemid 46456621)
32. CT Esmon 1993 Cell mediated events that control blood coagulations and vascular injury Annu. Rev. Cell Biol. 9 1 26 10.1146/annurev.cb.09.110193.000245 1:CAS:528:DyaK2cXltFamsg%3D%3D 8280458
33. Conrad, H.E.: Heparin-biding proteins. Academic, London (1998)
34. M-C Bourin U Lindahl 1990 Functional role of the polysaccharide component of rabbit thrombomodulin proteoglycan Effects on inactivation of thrombin by antithrombin, cleavage of fibrinogen by thrombin and thrombin-catalysed activation of Factor V Biochem. J. 270 419 425 1:CAS:528:DyaK3cXlt12rsLg%3D 2169242
35. M-C Bourin E Lundgren-Akerlund U Lindahl 1990 Isolation and characterization of the glycosaminoglycan component of rabbit thrombomodulin proteoglycan J. Biol. Chem. 265 15424 15431 1:CAS:528:DyaK3cXlvVKrurc%3D 2168413
36. MS Pereira B Mulloy PAS Mourão 1999 Structure and anticoagulant activity of sulfated fucans: COMPARISON BETWEEN THE REGULAR, REPETITIVE AND LINEAR FUCANS FROM ECHINODERMS WITH THE MORE HETEROGENEOUS AND BRANCHED POLYMERS FROM BROWN ALGAE J. Biol. Chem. 274 7656 7667 10.1074/jbc.274.12.7656 1:CAS:528:DyaK1MXitFSktrY%3D 10075653 (Pubitemid 29144226)