Identification of human hyaluronidase-4 as a novel chondroitin sulfate hydrolase that preferentially cleaves the galactosaminidic linkage in the trisulfated tetrasaccharide sequence

Glycobiology

Volumn 20, Issue 3, 2009, Pages 300-309

  Kaneiwa, Tomoyuki ^a   Mizumoto, Shuji ^a   Sugahara, Kazuyuki ^a   Yamada, Shuhei ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Chondroitin sulfate; Glycosaminoglycan; Hyaluronan; Hyaluronidase; Sulfated oligosaccharide

Indexed keywords

BETA N ACETYLGALACTOSAMINIDASE; CHONDROITIN SULFATE HYDROLASE; GLUCURONIC ACID; HYALURONIDASE; HYALURONIDASE 4; HYDROLASE; N ACETYLGALACTOSAMINE; TETRASACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; HUMAN; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; TEMPERATURE;

AMINO ACID SEQUENCE; CARBOHYDRATE SEQUENCE; CHONDROITIN SULFATES; CLONING, MOLECULAR; GALACTOSAMINE; HUMANS; HYALURONOGLUCOSAMINIDASE; HYDROLASES; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; CHONDRICHTHYES; MAMMALIA;

EID: 77949909575     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp174     Document Type: Article

References (39)

1. Benchetrit LC, Pahuja SL, Gray ED, Edstrom RD. 1977. A sensitive method for the assay of hyaluronidase activity. Anal Biochem. 79:431-437.
2. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. 2002. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:636-640.
3. Csoka AB, Frost GI, Stern R. 2001. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol. 20:499-508.
4. Csóka AB, Scherer SW, Stern R. 1999. Expression analysis of six paralogous human hyaluronidase genes clustered on chromosomes 3p21 and 7q31. Genomics. 60:356-361.
5. 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.
6. Duterme C, Mertens-Strijthagen J, Tammi MI, Flamion B. 2009. Two novel functions of hyaluronidase-2 (Hyal2): Formation of the glycocalyx and control of CD44-ERM interactions. J Biol Chem. doi:10.1074/jbc.M109.044362.
7. Esko JD, Selleck SB. 2002. Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 71:435-471.
8. Harada H, Takahashi M. 2007. CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and -2. J Biol Chem. 282:5597-5607.
9. Hopwood JJ. 1989. Enzymes that degrade heparin and heparan sulphate. In: Lane DA, Lindahl U, editors. Heparin. London: Edward Arnold, p. 191-227.
10. Iozzo RV. 1998. Matrix proteoglycans: From molecular design to cellular function. Annu Rev Biochem. 67:609-652.
11. Jedrzejas MJ, Stern R. 2005. Structures of vertebrate hyaluronidases and their unique enzymatic mechanism of hydrolysis. Proteins. 61:227-238.
12. Kaneiwa T, Yamada S, Mizumoto S, Montaño AM, Mitani S, Sugahara K. 2008. Identification of a novel chondroitin hydrolase in Caenorhabditis elegans. J Biol Chem. 283:14971-14979.
13. Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K, Miyasaka M. 2002. Oversulfated chondroitin/dermatan sulfates containing GlcA(1/IdoA(1-3GalNAc(4,6-O-disulfate) interact with L-and P-selectin and chemokines. J Biol Chem. 277:12921-12930.
14. Kinoshita A, Sugahara K. 1999. Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with the fluorophore 2-aminobenzamide by high-performance liquid chromatography: Application to disaccharide composition analysis and exosequencing of oligosaccharides. Anal Biochem. 269:367-378.
15. Kresse H, Glössl J. 1987. Glycosaminoglycan degradation. Adv Enzymol Relat Areas Mol Biol. 60:217-311.
16. Lepperdinger G, Strobl B, Kreil G. 1998. HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J Biol Chem. 273:22466-22470.
17. 1H-nuclear magnetic resonance spectroscopy. Glycoconj J. 25:603-610.
18. Lokeshwar VB, Schroeder GL, Carey RI, Soloway MS, Iida N. 2002. Regulation of hyaluronidase activity by alternative mRNA splicing. J Biol Chem. 277:33654-33663.
19. Nadanaka S, Sugahara K. 1997. The unusual tetrasaccharide sequence GlcA beta 1-3GalNAc(4-sulfate)beta 1-4GlcA(2-sulfate)beta 1-3GalNAc(6-sulfate) found in the hexasaccharides prepared by testicular hyaluronidase digestion of shark cartilage chondroitin sulfate D. Glycobiology. 7:253-263.
20. Okada Y, Yamada S, Toyoshima M, Dong J, Nakajima M, Sugahara K. 2002. Structural recognition by recombinant human heparanase that plays critical roles in tumor metastasis: Hierarchical sulfate groups with differential effects and the essential target disulfated trisaccharide sequence. J Biol Chem. 277:42488-42495.
21. Prabhakar V, Sasisekharan R. 2006. The biosynthesis and catabolism of galactosaminoglycans. Adv Pharmacol. 53:69-115.
22. Pavão MS, Vilela-Silva AC, Mourão PA. 2006. Biosynthesis of chondroitin sulfate: From the early, precursor discoveries to nowadays, genetics approaches. Adv Pharmacol. 53:117-140.
23. Rai SK, Duh FM, Vigdorovich V, Danilkovitch-Miagkova A, Lerman MI, Miller AD. 2001. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc Natl Acad Sci USA. 98:4443-4448.
24. Rauch U, Kappler L. 2006. Chondroitin/dermatan sulfates in the central nervous system: Their structures and functions in health and disease. Adv Pharmacol. 53:337-356.
25. Rodén L. 1980. Structure and metabolism of connective tissue proteoglycans. In: Lennarz WJ, editor. The Biochemistry of Glycoproteins and Proteoglycans. New York: Plenum Publishing Corp. p. 267-371.
26. Stenstad T, Magnus JH, Husby G. 1994. Characterization of proteoglycans associated with mouse splenic AA amyloidosis. Biochem J. 303:663-670.
27. Stern R, Jedrzejas MJ. 2006. Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem Rev. 106:818-839.
28. Sugahara K, Kitagawa H. 2000. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr Opin Struct Biol. 10:518-527.
29. Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H. 2003. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol. 13:612-620.
30. Sugahara K, Shigeno K, Masuda M, Fujii N, Kurosaka A, Takeda K. 1994a. Structural studies on the chondroitinase ABC-resistant sulfated tetrasaccharides isolated from various chondroitin sulfate isomers. Carbohydr Res. 255:145-163.
31. Sugahara K, Takemura Y, Sugiura M, Kohno Y, Yoshida K, Takeda K, Khoo K-H, Morris HR, Dell A. 1994b. Chondroitinase ABC-resistant sulfated trisaccharides isolated from digests of chondroitin/dermatan sulfate chains. Carbohydr Res. 255:165-182.
32. Sugahara K, Tanaka Y, Yamada S, Seno N, Kitagawa H, Haslam SM, Morris HR, Dell A. 1996. Novel sulfated oligosaccharides containing 3-O-sulfated glucuronic acid from king crab cartilage chondroitin sulfate K: Unexpected degradation by chondroitinase ABC. J Biol Chem. 271:26745-26754.
33. Sugahara K, Yamada S. 2000. Structure and function of oversulfated chondroitin sulfate variants: Unique sulfation patterns and neuroregulatory activities. Trends Glycosci Glycotechnol. 12:321-349.
34. Uyama T, Kitagawa H, Sugahara K. 2007. Biosynthesis of glycosaminoglycans and proteoglycans. In: Kamerling JP, editor. Comprehensive Glycoscience. Vol. 3. Amsterdam: Elsevier. p. 79-104.
35. Van Den Hoven MJ, Rops AL, Vlodavsky I, Levidiotis V, Berden JH, Van Der Vlag J. 2007. Heparanase in glomerular diseases. Kidney Int. 72:543-548.
36. Volpi N, Maccari F. 2003. Purification and characterization of hyaluronic acid from the mollusc bivalve Mytilus galloprovincialis. Biochimie. 85:619-625.
37. Yamada S, Van Die I, Van Den Eijnden DH, Yokota A, Kitagawa H, Sugahara K. 1999. Demonstration of glycosaminoglycans in Caenorhabditis elegans. FEBS Lett. 459:327-331.
38. Yamada S, Morimoto H, Fujisawa T, Sugahara K. 2007. Glycosaminoglycans in Hydra magnipapillata (Hydrozoa, Cnidaria): Demonstration of chondroitin in the developing nematocyst, the sting organelle, and structural characterization of glycosaminoglycans. Glycobiology. 17:886-894.
39. Zhang L, Bharadwaj AG, Casper A, Barkley J, Barycki JJ, Simpson MA. 2009. Hyaluronidase activity of human Hyal1 requires active site acidic and tyrosine residues. J Biol Chem. 284:9433-9442.