Exploiting enzyme specificities in digestions of chondroitin sulfates A and C: Production of well-defined hexasaccharides

Glycobiology

Volumn 22, Issue 6, 2012, Pages 826-838

  Pomin, Vitor H ^a   Park, Younghee ^a   Huang, Rongrong ^a   Heiss, Christian ^a   Sharp, Joshua S ^a   Azadi, Parastoo ^a   Prestegard, James H ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Chondroitin sulfate; Chondroitinase; Enzymatic specificity; Hyaluronidase; Oligosaccharides

Indexed keywords

CHONDROITIN 4 SULFATE; CHONDROITIN 6 SULFATE; DISACCHARIDE; HYALURONIDASE; HYDROLASE; LYASE; OLIGOSACCHARIDE;

ANION EXCHANGE; ARTICLE; ASSAY; DIGESTION; ENZYME ISOLATION; ENZYME SPECIFICITY; GEL PERMEATION CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

ANIMALS; CHONDROITIN LYASES; CHONDROITIN SULFATES; HYALURONOGLUCOSAMINIDASE; MALE; OLIGOSACCHARIDES; PSORIASIS; SHEEP; SUBSTRATE SPECIFICITY; TESTIS;

BACTERIA (MICROORGANISMS);

EID: 84860375872     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws055     Document Type: Article

References (62)

1. Achur RN, Kakizaki I, Goel S, Kojima K, Madhunapantula SV, Goyal A, Ohta M, Kumar S, Takagaki K, Gowda DC. 2008. Structural interactions in chondroitin 4-sulfate mediated adherence of Plasmodium falciparum infected erythrocytes in human placenta during pregnancy-associated malaria. Biochemistry. 47: 12635-12643.
2. Aguiar JAK, Lima CR, Berto AGA, Michelacci YM. 2003. An improved methodology to produce Flavobacterium heparinum chondroitinases, important instruments for diagnosis of diseases. Biotechnol Appl Biochem. 37: 115-127.
3. Beaulieu JF, Vachon PH, Chartrand S. 1991. Immunolocalization of extracellular-matrix components during organogenesis in the human small-intestine. Anat Embryol. 183: 363-369.
4. Ben-Zaken O, Tzaban S, Tal Y, Horonchik L, Esko JD, Vlodavsky I, Taraboulos A. 2003. Cellular heparan sulfate participates in the metabolism of prions. J Biol Chem. 278: 40041-40049.
5. Caterson B, Griffin J, Mahmoodian F, Sorrell JM. 1990. Monoclonalantibodies against chondroitin sulfate isomers-their use as probe for investigating proteoglycan metabolism. Biochem Soc Trans. 18: 820-823.
6. Cattaruzza S, Perris R. 2005. Proteoglycan control of cell movement during wound healing and cancer spreading. Matrix Biol. 24: 400-417.
7. Cohn RH, Cassiman JJ, Bernfield MR. 1976. Relationship of transformation, cell density, and growth-control to cellular distribution of newly synthesized glycosaminoglycan. J Cell Biol. 71: 280-294.
8. de Aguiar C, Lobao-Soares B, Alvarez-Silva M, Trentin AG. 2005. Glycosaminoglycans modulate C6 glioma cell adhesion to extracellular matrix components and alter cell proliferation and cell migration. BMC Cell Biol. 6.
9. De Mattos DA, Stelling MP, Tovar AMF, Mourao PAS. 2008. Heparan sulfates from arteries and veins differ in their antithrombin-mediated anticoagulant activity. J Thromb Haemost. 6: 1987-1990.
10. Deepa SS, Yamada S, Fukui S, Sugahara K. 2007. Structural determination of novel sulfated octasaccharides isolated from chondroitin sulfate of shark cartilage and their application for characterizing monoclonal antibody epitopes. Glycobiology. 17: 631-645.
11. Dodgson KS, Lloyd AG. 1958. Degradation of cartilage chondroitin sulphate by the chondroitinase of Proteus vulgaris. Biochem J. 68: 88-94.
12. Domowicz M, Mangoura D, Schwartz NB. 2000. Cell specific-chondroitin sulfate proteoglycan expression during CNS morphogenesis in the chick embryo. Int J Dev Neurosci. 18: 629-641.
13. Doodes PD, Cao YX, Hamel KM, Wang YM, Rodeghero RL, Kobezda T, Finnegan A. 2009. CCR5 is involved in resolution of inflammation in proteoglycan-induced arthritis. Arthritis Rheum. 60: 2945-2953.
14. Ernst S, Langer R, Cooney CL, Sasisekharan R. 1995. Enzymatic degradation of glycosaminoglycans. Crit Rev Biochem Mol Biol. 30: 387-444.
15. Gandhi NS, Mancera RL. 2008. The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des. 72: 455-482.
16. Gorio A, Lesma E, Vergani L, DiGiulio AM. 1997. Glycosaminoglycan supplementation promotes nerve regeneration and muscle reinnervation. Eur J Neurosci. 9: 1748-1753.
17. Gu K, Linhardt RJ, Laliberté M, Gu k, Zimmerman J. 1995. Purification, characterization and specificities of chondroitin lyases and glycuronidase from Flavobacterium heparinum. Biochem J. 312: 569-577.
18. Hamai A, Hashimoto N, Mochizuki H, Kato F, Makigushi Y, Horie K, Suzuki S. 1997. Two distinct chondroitin sulfate ABC lyases: An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J Biol Chem. 272: 9123-9130.
19. Handel TM, Johnson Z, Crown SE, Lau EK, Sweeney M, Proudfoot AE. 2005. Regulation of protein function by glycosaminoglycans-as exemplified by chemokines. Ann Rev Biochem. 74: 385-410.
20. Hardingham TE, Fosang AJ, Hey NJ, Hazell PK, Kee WJ, Ewins RJF. 1994. The sulfation pattern in chondroitin sulfate chains investigated by chondroitinase ABC and ACIL digestion and reactivity with monoclonal antibodies. Carbohydr Res. 255: 241-254.
21. He L, Giri TK, Vicente CP, Tollefsen DM. 2008. Vascular dermatan sulfate regulates the antithrombotic activity of heparin cofactor II. Blood. 111: 4118-4125.
22. Horonchik L, Tzaban S, Ben-Zaken O, Yedidia Y, Rouvinski A, Papy-Garcia D, Barritault D, Vlodavsky I, Taraboulos A. 2005. Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem. 280: 17062-17067.
23. Imberty A, Lortat-Jacob H, Perez S. 2007. Structural view of glycosaminoglycan-protein interactions. Carbohydr Res. 342: 430-439.
24. Inatani M, Haruta M, Honjo M, Oohira A, Kido N, Takahashi M, Honda Y, Tanihara H. 2001. Upregulated expression of N-syndecan, a transmembrane heparan sulfate proteoglycan, in differentiated neural stem cells. Brain Res. 920: 217-221.
25. Jandik KA, Gu KA, Linhardt RJ. 1994. Action pattern of polysaccharide lyases on glycosaminoglycans. Glycobiology. 4: 289-296.
26. Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, Carrell RW. 1997. The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci USA. 94: 14683-14688.
27. Kaplan CD, O'Neill SK, Koreny T, Czipri M, Finnegan A. 2002. Development of inflammation in proteoglycan-induced arthritis is dependent on Fc gamma R regulation of the cytokine/chemokine environment. J Immunol. 169: 5851-5859.
28. Khorlin AY, Vikha IV, Milishnikov AN. 1973. Subunit structure of testicular hyaluronidase. FEBS Lett. 31: 107-110.
29. Koninger J, Giese NA, Bartel M, di Mola FF, Berberat PO, di Sebastiano P, Giese T, Buchler MW, Friess H. 2006. The ECM proteoglycan decorin links desmoplasia and inflammation in chronic pancreatitis. J Clin Pathol. 59: 21-27.
30. Knudson W, Gundlach MW, Schimid TM, Conrad HE. 1984. Selective hydrolysis of chondroitin sulfates by hyaluronidase. Biochemistry. 23: 368-375.
31. Lindahl U, Hook M. 1978. Glycosaminoglycans and their binding to biological macromolecules. Ann Rev Biochem. 47: 385-417.
32. Lunin VV, Li YG, Linhardt RJ, Miyazono H, Kyogashima M, Kaneko T, Bell AW, Cygler M. 2004. High-resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: An enzyme-substrate complex defines the catalytic mechanism. J Mol Biol. 337: 367-386.
33. Michel G, Pojasek K, Li YG, Sulea T, Linhardt RJ, Raman R, Prabhakar V, Sasisekharan R, Cygler M. 2004. The structure of chondroitin B lyase complexed with glycosaminoglycan oligosaccharides unravels a calcium-dependent catalytic machinery. J Biol Chem. 279: 32882-32896.
34. Michelacci YM, Dietrich CP. 1976. Chondroitinase C from Flavobacterium heparinum. J Biol Chem. 251: 1154-1158.
35. Mucci A, Schenetti L, Volpi N. 2000. H-1 and C-13 nuclear magnetic resonance identification and characterization of components of chondroitin sulfates of various origin. Carbohydr Polym. 41: 37-45.
36. Muramatsu T, Muramatsu H. 2008. Glycosaminoglycan-binding cytokines as tumor markers. Proteomics. 8: 3350-3359.
37. Muthusamy A, Achur RN, Valiyaveettil M, Madhunapantula SV, Kakizaki I, Bhavanandan VP, Gowda CD. 2004. Structural characterization of the bovine tracheal chondroitin sulfate chains and binding of Plasmodium falciparum-infected erythrocytes. Glycobiology. 14: 635-645.
38. Nadanaka S, Sugahara K. 1997. The unusual tetrasaccharide sequence GlcA β1-3GalNAc(4-sulfate)β1-4GlcA(2-sulfate)β1-3GalNAc(6-sulfate) found in the hexasaccharides prepared by testicular hyaluronidase digestion of shark cartilage chondroitin sulfate D. Glycobiology. 7: 253-263.
39. Oettl M, Hoechstetter J, Asen I, Bernhardt G, Buschauer A. 2003. Comparative characterization of bovine testicular hyaluronidase and a hyaluronate lyase from Streptococcus agalactiae in pharmaceutical preparations. Eur J Pharm Sci. 18: 267-277.
40. Ototani N, Yosizawa Z. 1979. Purification of chondroitinase-B and chondroitinase-C using glycosaminoglycan-bound AH-Sepharose-4B. Carbohydr Res. 70: 295-306.
41. Perris R, Perissinotto D, Pettway Z, BronnerFraser M, Morgelin M, Kimata K. 1996. Inhibitory effects of PG-H/aggrecan and PG-M/versican on avian neural crest cell migration. FASEB J. 10: 293-301.
42. Pettway Z, Domowicz M, Schwartz NB, BronnerFraser M. 1996. Age-dependent inhibition of neural crest migration by the notochord correlates with alterations in the S103L chondroitin sulfate proteoglycan. Exp Cell Res. 225: 195-206.
43. Pomin VH, Sharp JS, Li XY, Wang LC, Prestegard JH. 2010. Characterization of glycosaminoglycans by N-15 NMR spectroscopy and in vivo isotopic labeling. Anal Chem. 82: 4078-4088.
44. Pothacharoen P, Kalayanamitra K, Deepa SS, Fukui S, Hattori T, Fukushima N, Hardingham T, Kongtawelert P, Sugahara K. 2007. Two related but distinct chondroitin sulfate mimetope octasaccharide sequences recognized by monoclonal antibody WF6. J Biol Chem. 282: 35232-35246.
45. Raman R, Sasisekharan V, Sasisekharan R. 2005. Structural insights into biological roles of protein-glycosaminoglycan interactions. Chem Biol. 12: 267-277.
46. Richard B, Swanson R, Olson ST. 2009. The signature 3-O-sulfo group of the anticoagulant heparin sequence is critical for heparin binding to antithrombin but is not required for allosteric activation. J Biol Chem. 284: 27054-27064.
47. Rigden DJ, Jedrzejas MJ. 2003. Structures of Streptococcus pneumoniae hyaluronate lyase in complex with chondroitin and chondroitin sulfate disaccharides-insights into specificity and mechanism of action. J Biol Chem. 278: 50596-50606.
48. Sasisekharan R, Raman R, Prabhakar V. 2006. Glycomics approach to structure-function relationships of glycosaminoglycans. Ann Rev Biomed Eng. 8: 181-231.
49. Shaya D, Hahn BS, Bjerkan TM, Kim WS, Park NY, Sim JS, Kim YS, Cygler M. 2008. Composite active site of chondroitin lyase ABC accepting both epimers of uronic acid. Glycobiology. 18: 270-277.
50. Singh K, Gittis AG, Nguyen P, Gowda DC, Miller LH, Garboczi DN. 2008. Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A. Nat Struct Mol Biol. 15: 932-938.
51. Sorrell JM, Carrino DA, Caplan AI. 1993. Structural domains in chondroitin sulfate identified by anti-chondroitin sulfate monoclonal- antibodies-immunosequencing of chondroitin sulfates. Matrix. 13: 351-361.
52. Stern R, Jedrzejas MJ. 2006. Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem Rev. 106: 818-839.
53. Sugahara K, Mikami T, Uyama T, Mizugushi S, Nomura K, Kitagawa H. 2003. Recent advances in structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol. 13: 612-620.
54. Takagaki K, Munakata H, Majima M, Endo M. 1999. Enzymatic reconstruction of a hybrid glycosaminoglycan containing 6-sulfated, 4-sulfated, and unsulfated N-acetylgalactosamine. Biochem Biophys Res Commun. 258: 741-744.
55. Takagaki K, Nakamura T, Izumi J, Saitoh H, Endo M, Kojima K, Kato I, Majima M. 1994. Characterization of hydrolysis and transglycosylation by testicular hyaluronidase using ion-spray mass-spectrometry. Biochemistry. 33: 6503-6507.
56. Thesleff I, Jalkanen M, Vainio S, Bernfield M. 1988. Cell-surface proteoglycan expression correlates with epithelial mesenchymal interaction during tooth morphogenesis. Dev Biol. 129: 565-572.
57. Tully SE, Mabon R, Gama CI, Tsai SM, Liu XW, Hsieh-Wilson LC. 2004. A chondroitin sulfate small molecule that stimulates neuronal growth. J Am Chem Soc. 126: 7736-7737.
58. vanPutten JPM, Hayes SF, Duensing TD. 1997. Natural proteoglycan receptor analogs determine the dynamics of Opa adhesin-mediated gonococcal infection of Chang epithelial cells. Infect Immun. 65: 5028-5034.
59. Volpi N. 1994. Fractionation of heparin, dermatan sulfate, and chondroitin sulfate sequential precipitation-a method to purify a single glycosaminoglycan species from a mixture. Anal Biochem. 218: 382-391.
60. Warner RG, Hundt C, Weiss S, Turnbull JE. 2002. Identification of the heparan sulfate binding sites in the cellular prion protein. J Biol Chem. 277: 18421-18430.
61. Xie HX, Nie P, Chang MX, Liu Y, Yao WJ. 2005. Gene cloning and functional analysis of glycosaminoglycan-degrading enzyme chondroitin AC lyase from Flavobacterium columnare G(4). Arch Microbiol. 184: 49-55.
62. Zhang ZQ, Park Y, Kemp MM, Zhao WJ, Im AR, Shaya D, Cygler M, Kim YS, Linhardt RJ. 2009. Liquid chromatography-mass spectrometry to study chondroitin lyase action pattern. Anal Biochem. 385: 57-64.