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Chondroitin sulfate/dermatan sulfate sulfatases from mammals and bacteria

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Abstract

Sulfatases that specifically catalyze the hydrolysis of the sulfate groups on chondroitin sulfate (CS)/dermatan sulfate (DS) poly- and oligosaccharides belong to the formylglycine-dependent family of sulfatases and have been widely found in various mammalian and bacterial organisms. However, only a few types of CS/DS sulfatase have been identified so far. Recently, several novel CS/DS sulfatases have been cloned and characterized. Advanced studies have provided significant insight into the biological function and mechanism of action of CS/DS sulfatases. Moreover, further studies will provide powerful tools for structural and functional studies of CS/DS as well as related applications. This article reviews the recent progress in CS/DS sulfatase research and is expected to initiate further research in this field.

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Abbreviations

CS:

chondroitin sulfate

DS:

dermatan sulfate

PG:

proteoglycan

GAG:

glycosaminoglycan

GlcA:

D-glucuronic acid

GalNAc:

N-acetyl-D-galactosamine

IdoA:

L-iduronic acid

CNS:

central nervous system

FGly:

Cα-formylglycine

SUMF1:

sulfatase modifying factor 1

ARSB:

N-acetylgalactosamine-4-O-sulfatase

GALNS:

N-acetylgalactosamine-6-O-sulfatase

Hep/HS:

heparin/heparan sulfate

MPSs:

mucopolysaccharidoses

M6PR:

mannose-6-phosphate receptor

pNP-S:

p-nitrophenyl sulfate

4MUS:

4-methylumbelliferyl sulfate

References

  1. Mizuguchi S., Uyama T., Kitagawa H., Nomura K.H., Dejima K., Gengyo-Ando K., Mitani S., Sugahara K., Nomura K.: Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature. 423(6938), 443–448 (2003)

    Article  CAS  PubMed  Google Scholar 

  2. Ruoslahti E., Yamaguchi Y.: Proteoglycans as modulators of growth factor activities. Cell. 64(5), 867–869 (1991)

    Article  CAS  PubMed  Google Scholar 

  3. Silbert J.E., Sugumaran G.: Biosynthesis of chondroitin/dermatan sulfate. Iubmb Life. 54(4), 177–186 (2002)

    Article  CAS  PubMed  Google Scholar 

  4. Sugahara K., Kitagawa H.: Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10(5), 518–527 (2000)

    Article  CAS  PubMed  Google Scholar 

  5. Lindahl U., Roden L.: The role of galactose and xylose in the linkage region of heparin to protein. J. Biol. Chem. 240, 2821–2826 (1965)

    CAS  PubMed  Google Scholar 

  6. Nakano T., Betti M., Pietrasik Z.: Extraction, isolation and analysis of chondroitin sulfate glycosaminoglycans. Recent patents on food,. Nutr.Agric. 2(1), 61–74 (2010)

    CAS  Google Scholar 

  7. Sugahara K., Mikami T.: Chondroitin/dermatan sulfate in the central nervous system. Curr. Opin. Struct. Biol. 17(5), 536–545 (2007)

    Article  CAS  PubMed  Google Scholar 

  8. Silbert J.E., Sugumaran G.: Biosynthesis of chondroitin/dermatan sulfate. Iubmb Life. 54(4), 177–186 (2002)

    Article  CAS  PubMed  Google Scholar 

  9. 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. 13(5), 612–620 (2003)

    Article  CAS  PubMed  Google Scholar 

  10. Malavaki C., Mizumoto S., Karamanos N., Sugahara K.: Recent advances in the structural study of functional chondroitin sulfate and dermatan sulfate in health and disease. Connect. Tissue Res. 49(3), 133–139 (2008)

    Article  CAS  PubMed  Google Scholar 

  11. Morgenstern D.A., Asher R.A., Fawcett J.W.: Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137, 313–332 (2002)

    Article  CAS  PubMed  Google Scholar 

  12. Trowbridge J.M., Gallo R.L.: Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology. 12(9), 117R–125R (2002)

    Article  CAS  PubMed  Google Scholar 

  13. Mizumoto S., Fongmoon D., Sugahara K.: Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines. Glycoconj. J. 30(6), 619–632 (2013)

    Article  CAS  PubMed  Google Scholar 

  14. Mizumoto S., Yamada S., Sugahara K.: Molecular interactions between chondroitin–dermatan sulfate and growth factors/receptors/matrix proteins. Curr. Opin. Struct. Biol. 34, 35–42 (2015)

    Article  CAS  PubMed  Google Scholar 

  15. Dhoot G.K., Gustafsson M.K., Ai X., Sun W., Standiford D.M., Emerson C.J.: Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science. 293(5535), 1663–1666 (2001)

    Article  CAS  PubMed  Google Scholar 

  16. Parenti G., Meroni G., Ballabio A.: The sulfatase gene family. Curr. Opin. Genet. Dev. 7(3), 386–391 (1997)

    Article  CAS  PubMed  Google Scholar 

  17. Hanson S.R.: Best, M.D., Wong, C.H.: sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Ed. Eng. 43(43), 5736–5763 (2004)

    Article  CAS  Google Scholar 

  18. Schmidt B., Selmer T., Ingendoh A., von Figura K.: A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell. 82(2), 271–278 (1995)

    Article  CAS  PubMed  Google Scholar 

  19. Dierks T., Schmidt B., Borissenko L.V., Peng J., Preusser A., Mariappan M., von Figura K.: Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme. Cell. 113(4), 435–444 (2003)

    Article  CAS  PubMed  Google Scholar 

  20. Dierks T., Miech C., Hummerjohann J., Schmidt B., Kertesz M.A., von Figura K.: Posttranslational formation of formylglycine in prokaryotic sulfatases by modification of either cysteine or serine. J. Biol. Chem. 273(40), 25560–25564 (1998)

    Article  CAS  PubMed  Google Scholar 

  21. Lukatela G., Krauss N., Theis K., Selmer T., Gieselmann V., von Figura K., Saenger W.: Crystal structure of human arylsulfatase A: the aldehyde function and the metal ion at the active site suggest a novel mechanism for sulfate ester hydrolysis. Biochem.-US. 37(11), 3654–3664 (1998)

    Article  CAS  Google Scholar 

  22. Dierks T., Schmidt B., Borissenko L.V., Peng J., Preusser A., Mariappan M., von Figura K.: Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme. Cell. 113(4), 435–444 (2003)

    Article  CAS  PubMed  Google Scholar 

  23. Cosma M.P., Pepe S., Annunziata I., Newbold R.F., Grompe M., Parenti G., Ballabio A.: The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell. 113(4), 445–456 (2003)

    Article  CAS  PubMed  Google Scholar 

  24. Buono M., Cosma M.P.: Sulfatase activities towards the regulation of cell metabolism and signaling in mammals. Cell. Mol. Life Sci. 67(5), 769–780 (2010)

    Article  CAS  PubMed  Google Scholar 

  25. Szameit C., Miech C., Balleininger M., Schmidt B., von Figura K., Dierks T.: The iron sulfur protein AtsB is required for posttranslational formation of formylglycine in the Klebsiella sulfatase. J. Biol. Chem. 274(22), 15375–15381 (1999)

    Article  CAS  PubMed  Google Scholar 

  26. Szameit C., Miech C., Balleininger M., Schmidt B., von Figura K., Dierks T.: The iron sulfur protein AtsB is required for posttranslational formation of formylglycine in the Klebsiella sulfatase. J. Biol. Chem. 274(22), 15375–15381 (1999)

    Article  CAS  PubMed  Google Scholar 

  27. Bhattacharyya S., Kotlo K., Shukla S., Danziger R.S., Tobacman J.K.: Distinct effects of N-acetylgalactosamine-4-sulfatase and galactose-6-sulfatase expression on chondroitin sulfates. J. Biol. Chem. 283(15), 9523–9530 (2008)

    Article  CAS  PubMed  Google Scholar 

  28. Myette J.R., Shriver Z., Claycamp C., McLean M.W., Venkataraman G., Sasisekharan R.: The heparin/heparan sulfate 2-O-sulfatase from Flavobacterium heparinum: Molecular cloning, recombinant expression, and biochemical characterization. J. Biol. Chem. 278(14), 12157–12166 (2003)

    Article  CAS  PubMed  Google Scholar 

  29. Sugahara K., Kojima T.: Specificity studies of bacterial sulfatases by means of structurally defined sulfated oligosaccharides isolated from shark cartilage chondroitin sulfate D. Eur. J. Biochem. 239(3), 865–870 (1996)

    Article  CAS  PubMed  Google Scholar 

  30. De Sousa J.J., Nader H.B., Dietrich C.P.: Sequential degradation of chondroitin sulfate in molluscs. Desulfation of chondroitin sulfate without prior depolymerization by a novel sulfatase from Anomalocardia brasiliana. J. Biol. Chem. 265(33), 20150–20155 (1990)

    Google Scholar 

  31. Ulmer J.E., Vilen E.M., Namburi R.B., Benjdia A., Beneteau J., Malleron A., Bonnaffe D., Driguez P.A., Descroix K., Lassalle G., Le Narvor C., Sandstrom C., Spillmann D., Berteau O.: Characterization of glycosaminoglycan (GAG) sulfatases from the human gut symbiont bacteroides thetaiotaomicron reveals the first GAG-specific bacterial endosulfatase. J. Biol. Chem. 289(35), 24289–24303 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang W., Han W., Cai X., Zheng X., Sugahara K., Li F.: Cloning and characterization of a novel chondroitin sulfate/dermatan sulfate 4-O-endosulfatase from a marine bacterium. J. Biol. Chem. 290(12), 7823–7832 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Benjdia A., Martens E.C., Gordon J.I., Berteau O.: Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, bacteroides thetaiotaomicron. J. Biol. Chem. 286(29), 25973–25982 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Dierks T., Lecca M.R., Schlotterhose P., Schmidt B., von Figura K.: Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. EMBO J. 18(8), 2084–2091 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Knaust A., Schmidt B., Dierks T., von Bulow R., von Figura K.: Residues critical for formylglycine formation and/or catalytic activity of arylsulfatase A. Biochemistry-US. 37(40), 13941–13946 (1998)

    Article  CAS  Google Scholar 

  36. Bond C.S., Clements P.R., Ashby S.J., Collyer C.A., Harrop S.J., Hopwood J.J., Guss J.M.: Structure of a human lysosomal sulfatase. Structure. 5(2), 277–289 (1997)

    Article  CAS  PubMed  Google Scholar 

  37. Boltes I., Czapinska H., Kahnert A., von Bulow R., Dierks T., Schmidt B., von Figura K., Kertesz M.A., Uson I.: 1.3 A structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. Structure. 9(6), 483–491 (2001)

    Article  CAS  PubMed  Google Scholar 

  38. Yamagata T., Saito H., Habuchi O., Suzuki S.: Purification and properties of bacterial chondroitinases and chondrosulfatases. J. Biol. Chem. 243(7), 1523–1535 (1968)

    CAS  PubMed  Google Scholar 

  39. Raman R., Myette J.R., Shriver Z., Pojasek K., Venkataraman G., Sasisekharan R.: The Heparin/heparan sulfate 2-O-sulfatase from Flavobacterium heparinum: A structural and biochemical study of the enzyme active site and saccharide substrate specificity. J. Biol. Chem. 278(14), 12167–12174 (2003)

    Article  CAS  PubMed  Google Scholar 

  40. Dietrich C.P., Silva M.E., Michelacci Y.M.: Sequential degradation of heparin in Flavobacterium heparinum. Purification and properties of five enzymes involved in heparin degradation. J. Biol. Chem. 248(18), 6408–6415 (1973)

    CAS  PubMed  Google Scholar 

  41. Han W., Wang W., Zhao M., Sugahara K., Li F.: A novel eliminase from a marine bacterium that degrades hyaluronan and chondroitin sulfate. J. Biol. Chem. 289(40), 27886–27898 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Shain H., Homer K.A., Beighton D.: Degradation and utilisation of chondroitin sulphate by Streptococcus intermedius. J. Med. Microbiol. 44(5), 372–380 (1996)

    Article  CAS  PubMed  Google Scholar 

  43. Mougous J.D., Green R.E., Williams S.J., Brenner S.E., Bertozzi C.R.: Sulfotransferases and sulfatases in mycobacteria. Chem. Biol. 9(7), 767–776 (2002)

    Article  CAS  PubMed  Google Scholar 

  44. Jacobs J.A., Stobberingh E.E.: Hydrolytic enzymes of Streptococcus anginosus, Streptococcus constellatus and Streptococcus intermedius in relation to infection. Eur. J. Clin. Microbiol. Infect. Dis. 14(9), 818–820 (1995)

    Article  CAS  PubMed  Google Scholar 

  45. Benjdia A., Berteau O.: Sulfatases and radical SAM enzymes: emerging themes in glycosaminoglycan metabolism and the human microbiota. Biochem. Soc. Trans. 44(1), 109–115 (2016)

    Article  CAS  PubMed  Google Scholar 

  46. Tomatsu S., Fukuda S., Masue M., Sukegawa K., Fukao T., Yamagishi A., Hori T., Iwata H., Ogawa T., Nakashima Y., Et A.: Morquio disease: isolation, characterization and expression of full-length cDNA for human N-acetylgalactosamine-6-sulfate sulfatase. Biochem. Biophys. Res. Commun. 181(2), 677–683 (1991)

    Article  CAS  PubMed  Google Scholar 

  47. Valayannopoulos, V., Wijburg, F.A.: Therapy for the mucopolysaccharidoses. Rheumatology (Oxford), 50 Suppl 5, v49-v59 (2011)

  48. Lim C.T., Horwitz A.L.: Purification and properties of human N-acetylgalactosamine-6-sulfate sulfatase. Biochim. Biophys. Acta. 657(2), 344–355 (1981)

    Article  CAS  PubMed  Google Scholar 

  49. Glossl J., Truppe W., Kresse H.: Purification and properties of N-acetylgalactosamine 6-sulphate sulphatase from human placenta. Biochem. J. 181(1), 37–46 (1979)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Peters C., Schmidt B., Rommerskirch W., Rupp K., Zuhlsdorf M., Vingron M., Meyer H.E., Pohlmann R., von Figura K.: Phylogenetic conservation of arylsulfatases. cDNA cloning and expression of human arylsulfatase B. J. Biol. Chem. 265(6), 3374–3381 (1990)

    CAS  PubMed  Google Scholar 

  51. Sardiello M., Annunziata I., Roma G., Ballabio A.: Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum. Mol. Genet. 14(21), 3203–3217 (2005)

    Article  CAS  PubMed  Google Scholar 

  52. Shaklee P.N., Glaser J.H., Conrad H.E.: A sulfatase specific for glucuronic acid 2-sulfate residues in glycosaminoglycans. J. Biol. Chem. 260(16), 9146–9149 (1985)

    CAS  PubMed  Google Scholar 

  53. Brown W.J., Farquhar M.G.: The mannose-6-phosphate receptor for lysosomal enzymes is concentrated in cis Golgi cisternae. Cell. 36(2), 295–307 (1984)

    Article  CAS  PubMed  Google Scholar 

  54. Doray B., Ghosh P., Griffith J., Geuze H.J., Kornfeld S.: Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science. 297(5587), 1700–1703 (2002)

    Article  CAS  PubMed  Google Scholar 

  55. Yamada S.: Catabolism of chondroitin sulfate. Cell. Mol. Biol. Lett. 20(2), 196–212 (2015)

    Article  CAS  PubMed  Google Scholar 

  56. Glossl J., Kresse H.: Impaired degradation of keratan sulphate by Morquio A fibroblasts. Biochem. J. 203(1), 335–338 (1982)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kunieda T., Simonaro C.M., Yoshida M., Ikadai H., Levan G., Desnick R.J., Schuchman E.H.: Mucopolysaccharidosis type VI in rats: isolation of cDNAs encoding arylsulfatase B, chromosomal localization of the gene, and identification of the mutation. Genomics. 29(3), 582–587 (1995)

    Article  CAS  PubMed  Google Scholar 

  58. Peters C., Schmidt B., Rommerskirch W., Rupp K., Zuhlsdorf M., Vingron M., Meyer H.E., Pohlmann R., von Figura K.: Phylogenetic conservation of arylsulfatases. cDNA cloning and expression of human arylsulfatase B. J. Biol. Chem. 265(6), 3374–3381 (1990)

    CAS  PubMed  Google Scholar 

  59. Rivera-Colon Y., Schutsky E.K., Kita A.Z., Garman S.C.: The structure of human GALNS reveals the molecular basis for mucopolysaccharidosis IV A. J. Mol. Biol. 423(5), 736–751 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Da, S.E., Strufaldi, M.W., Andriolo, R.B., Silva, L.A.: Enzyme replacement therapy with idursulfase for mucopolysaccharidosis type II (Hunter syndrome). Cochrane Database Syst Rev(11), D8185 (2011)

  61. Bhattacharyya S., Feferman L., Tobacman J.K.: Increased expression of colonic Wnt9A through Sp1-mediated transcriptional effects involving arylsulfatase B, chondroitin 4-sulfate, and galectin-3. J. Biol. Chem. 289(25), 17564–17575 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhang X., Bhattacharyya S., Kusumo H., Goodlett C.R., Tobacman J.K., Guizzetti M.: Arylsulfatase B modulates neurite outgrowth via astrocyte chondroitin-4-sulfate: dysregulation by ethanol. Glia. 62(2), 259–271 (2014)

    Article  PubMed  Google Scholar 

  63. Ai X., Kitazawa T., Do A.T., Kusche-Gullberg M., Labosky P.A., Emerson C.J.: SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development. 134(18), 3327–3338 (2007)

    Article  CAS  PubMed  Google Scholar 

  64. Bhattacharyya S., Look D., Tobacman J.K.: Increased arylsulfatase B activity in cystic fibrosis cells following correction of CFTR. Clin. Chim. Acta. 380(1–2), 122–127 (2007)

    Article  CAS  PubMed  Google Scholar 

  65. Draper R.K., Fiskum G.M., Edmond J.: Purification, molecular weight, amino acid, and subunit composition of arylsulfatase A from human liver. Arch. Biochem. Biophys. 177(2), 525–538 (1976)

    Article  CAS  PubMed  Google Scholar 

  66. Yoshida K., Miyauchi S., Kikuchi H., Tawada A., Tokuyasu K.: Analysis of unsaturated disaccharides from glycosaminoglycuronan by high-performance liquid chromatography. Anal. Biochem. 177(2), 327–332 (1989)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This work was financially supported by the National Natural Science Foundation of China (No. 31570071), the Major State Basic Research Development Program of China (No. 2012CB822102), and the Shenzhen strategic emerging industry development special funds (No. JCYJ20140418115815063).

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Authors and Affiliations

  1. National Glycoengineering Research Center, Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, and Shenzhen Research Institute, Shandong University, Jinan, 250100, Peoples, Republic of China

    Shumin Wang & Fuchuan Li

  2. Proteoglycan Signaling and Therapeutics Research Group, Faculty of Advanced Life Science, Hokkaido University Graduate School of Life Science, Sapporo, 001-0021, Japan

    Kazuyuki Sugahara

  3. Department of Pathobiochemistry, Faculty of Pharmacy, Nagoya, Aichi, 468-8503, Japan

    Kazuyuki Sugahara

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  1. Shumin Wang
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Wang, S., Sugahara, K. & Li, F. Chondroitin sulfate/dermatan sulfate sulfatases from mammals and bacteria. Glycoconj J 33, 841–851 (2016). https://doi.org/10.1007/s10719-016-9720-0

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