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The “in and out” of glucosamine 6-O-sulfation: the 6th sense of heparan sulfate

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Abstract

The biological properties of Heparan sulfate (HS) polysaccharides essentially rely on their ability to bind and modulate a multitude of protein ligands. These interactions involve internal oligosaccharide sequences defined by their sulfation patterns. Amongst these, the 6-O-sulfation of HS contributes significantly to the polysaccharide structural diversity and is critically involved in the binding of many proteins. HS 6-O-sulfation is catalyzed by 6-O-sulfotransferases (6OSTs) during biosynthesis, and it is further modified by the post-synthetic action of 6-O-endosulfatases (Sulfs), two enzyme families that remain poorly characterized. The aim of the present review is to summarize the contribution of 6-O-sulfates in HS structure/function relationships and to discuss the present knowledge on the complex mechanisms regulating HS 6-O-sulfation.

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References

  1. Sarrazin S., Lamanna W.C., Esko J.D.: Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 3, (2011). doi:10.1101/cshperspect.a004952

  2. Esko, J.D., Kimata, K., Lindahl, U.: Proteoglycans and Sulfated Glycosaminoglycans. In: Varki A, C.R., Esko JD, Freeze H, Hart G, Marth J. (ed.) Essentials of Glycobiology. 2nd edition. Cold Spring Harbor Laboratory Press (2009)

  3. Whitelock J.M., Iozzo R.V.: Heparan sulfate: a complex polymer charged with biological activity. Chem. Rev. 105, 2745–2764 (2005)

    Article  CAS  PubMed  Google Scholar 

  4. Capila I., Linhardt R.J.: Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 41, 391–412 (2002)

    Article  PubMed  Google Scholar 

  5. Lindahl U., Li J.P.: Interactions between heparan sulfate and proteins-design and functional implications. Int. Rev. Cell Mol. Biol. 276, 105–159 (2009)

    Article  PubMed  CAS  Google Scholar 

  6. Imberty A., Lortat-Jacob H., Perez S.: Structural view of glycosaminoglycan-protein interactions. Carbohydr. Res. 342, 430–439 (2007)

    Article  CAS  PubMed  Google Scholar 

  7. Kusche-Gullberg M., Kjellen L.: Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605–611 (2003)

    Article  CAS  PubMed  Google Scholar 

  8. Esko J.D., Lindahl U.: Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169–173 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Li J.-P., Kusche-Gullberg M.: Heparan sulfate: biosynthesis, structure, and function. Int. Rev. Cell Mol. Biol. 325, 215–273 (2016)

    Article  PubMed  Google Scholar 

  10. Esko J.D., Selleck S.B.: ORDER OUT OF CHAOS: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002)

    Article  CAS  PubMed  Google Scholar 

  11. Vives R.R., Seffouh A., Lortat-Jacob H.: Post-synthetic regulation of HS structure: the Yin and Yang of the sulfs in cancer. Front. Oncol. 3, 331 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rosen S.D., Lemjabbar-Alaoui H.: Sulf-2: an extracellular modulator of cell signaling and a cancer target candidate. Expert Opin. Ther. Targets. 14, 935–949 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hammond E., Khurana A., Shridhar V., Dredge K.: The role of Heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front. Oncol. 4, 195 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  14. Carlsson P., Presto J., Spillmann D., Lindahl U., Kjellen L.: Heparin/heparan sulfate biosynthesis: processive formation of N-sulfated domains. J. Biol. Chem. 283, 20008–20014 (2008)

    Article  CAS  PubMed  Google Scholar 

  15. Préchoux A., Halimi C., Simorre J.-P., Lortat-Jacob H., Laguri C.: C5-epimerase and 2-O-sulfotransferase associate in vitro to generate contiguous epimerized and 2-O-sulfated heparan sulfate domains. ACS Chem. Biol. 10, 1064–1071 (2015)

    Article  PubMed  CAS  Google Scholar 

  16. Pye D.A., Vives R.R., Turnbull J.E., Hyde P., Gallagher J.T.: Heparan sulfate oligosaccharides require 6-O-sulfation for promotion of basic fibroblast growth factor mitogenic activity. J. Biol. Chem. 273, 22936–22942 (1998)

    Article  CAS  PubMed  Google Scholar 

  17. Merry C.L., Lyon M., Deakin J.A., Hopwood J.J., Gallagher J.T.: Highly sensitive sequencing of the sulfated domains of heparan sulfate. J. Biol. Chem. 274, 18455–18462 (1999)

    Article  CAS  PubMed  Google Scholar 

  18. Brickman Y.G., Ford M.D., Gallagher J.T., Nurcombe V., Bartlett P.F., Turnbull J.E.: Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273, 4350–4359 (1998)

    Article  CAS  PubMed  Google Scholar 

  19. Allen B.L., Rapraeger A.C.: Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J. Cell Biol. 163, 637–648 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Feyzi E., Saldeen T., Larsson E., Lindahl U., Salmivirta M.: Age-dependent modulation of heparan sulfate structure and function. J. Biol. Chem. 273, 13395–13398 (1998)

    Article  CAS  PubMed  Google Scholar 

  21. Huynh M.B., Morin C., Carpentier G., Garcia-Filipe S., Talhas-Perret S., Barbier-Chassefiere V., van Kuppevelt T.H., Martelly I., Albanese P., Papy-Garcia D.: Age-related changes in rat myocardium involve altered capacities of glycosaminoglycans to potentiate growth factor functions and heparan sulfate-altered sulfation. J. Biol. Chem. 287, 11363–11373 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jayson G.C., Lyon M., Paraskeva C., Turnbull J.E., Deakin J.A., Gallagher J.T.: Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 273, 51–57 (1998)

    Article  CAS  PubMed  Google Scholar 

  23. Safaiyan F., Lindahl U., Salmivirta M.: Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells. Eur. J. Biochem. FEBS. 252, 576–582 (1998)

    Article  CAS  Google Scholar 

  24. Hosono-Fukao T., Ohtake-Niimi S., Hoshino H., Britschgi M., Akatsu H., Hossain M.M., Nishitsuji K., van Kuppevelt T.H., Kimata K., Michikawa M., Wyss-Coray T., Uchimura K.: Heparan sulfate subdomains that are degraded by Sulf accumulate in cerebral amyloid ss plaques of Alzheimer’s disease: evidence from mouse models and patients. Am. J. Pathol. 180, 2056–2067 (2012)

    Article  CAS  PubMed  Google Scholar 

  25. Bruinsma I.B., te Riet L., Gevers T., ten Dam G.B., van Kuppevelt T.H., David G., Küsters B., de Waal R.M.W., Verbeek M.M.: Sulfation of heparan sulfate associated with amyloid-beta plaques in patients with Alzheimer’s disease. Acta Neuropathol. (Berl.). 119(211–220), (2010)

  26. Alhasan A.A., Spielhofer J., Kusche-Gullberg M., Kirby J.A., Ali S.: Role of 6-O-sulfated heparan sulfate in chronic renal fibrosis. J. Biol. Chem. 289, 20295–20306 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang L., Brown J.R., Varki A., Esko J.D.: Heparin’s anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J. Clin. Invest. 110, 127–136 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Reine T.M., Kusche-Gullberg M., Feta A., Jenssen T., Kolset S.O.: Heparan sulfate expression is affected by inflammatory stimuli in primary human endothelial cells. Glycoconj J. 29, 67–76 (2012)

    Article  CAS  PubMed  Google Scholar 

  29. Hassing H.C., Mooij H., Guo S., Monia B.P., Chen K., Kulik W., Dallinga-Thie G.M., Nieuwdorp M., Stroes E.S., Williams K.J.: Inhibition of hepatic sulfatase-2 in vivo: a novel strategy to correct diabetic dyslipidemia. Hepatology. 55, 1746–1753 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wijnhoven T.J.M., Lensen J.F.M., Rops A.L.W.M.M., van der Vlag J., Kolset S.O., Bangstad H.-J., Pfeffer P., van den Hoven M.J.W., Berden J.H.M., van den Heuvel L.P.W.J., van Kuppevelt T.H.: Aberrant heparan sulfate profile in the human diabetic kidney offers new clues for therapeutic glycomimetics. Am. J. Kidney Dis. Off. J. Natl. Kidney Found. 48, 250–261 (2006)

    Article  CAS  Google Scholar 

  31. Petitou M., Casu B., Lindahl U.: 1976–1983, a critical period in the history of heparin: the discovery of the antithrombin binding site. Biochimie. 85, 83–89 (2003)

    Article  CAS  PubMed  Google Scholar 

  32. Zhang L., Beeler D.L., Lawrence R., Lech M., Liu J., Davis J.C., Shriver Z., Sasisekharan R., Rosenberg R.D.: 6-O-sulfotransferase-1 represents a critical enzyme in the anticoagulant heparan sulfate biosynthetic pathway. J. Biol. Chem. 276, 42311–42321 (2001)

    Article  CAS  PubMed  Google Scholar 

  33. Gallagher J.: Fell-Muir lecture: heparan sulphate and the art of cell regulation: a polymer chain conducts the protein orchestra. Int. J. Exp. Pathol. 96, 203–231 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Harmer N.J.: Insights into the role of heparan sulphate in fibroblast growth factor signalling. Biochem. Soc. Trans. 34, 442–445 (2006)

    Article  CAS  PubMed  Google Scholar 

  35. Li Y., Sun C., Yates E.A., Jiang C., Wilkinson M.C., Fernig D.G.: Heparin binding preference and structures in the fibroblast growth factor family parallel their evolutionary diversification. Open Biol. 6, (2016)

  36. Rapraeger A.C., Krufka A., Olwin B.B.: Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science. 252, 1705–1708 (1991)

    Article  CAS  PubMed  Google Scholar 

  37. Yayon A., Klagsbrun M., Esko J.D., Leder P., Ornitz D.M.: Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64, 841–848 (1991)

    Article  CAS  PubMed  Google Scholar 

  38. Faham S., Hileman R.E., Fromm J.R., Linhardt R.J., Rees D.C.: Heparin structure and interactions with basic fibroblast growth factor. Science. 271, 1116–1120 (1996)

    Article  CAS  PubMed  Google Scholar 

  39. DiGabriele A.D., Lax I., Chen D.I., Svahn C.M., Jaye M., Schlessinger J., Hendrickson W.A.: Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature. 393, 812–817 (1998)

    Article  CAS  PubMed  Google Scholar 

  40. Maccarana M., Casu B., Lindahl U.: Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor [published erratum appears in J Biol Chem 1994 Feb 4;269(5):3903]. J Biol Chem. 268, 23898–23905 (1993)

    CAS  PubMed  Google Scholar 

  41. Kreuger J., Salmivirta M., Sturiale L., Gimenez-Gallego G., Lindahl U.: Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J. Biol. Chem. 276, 30744–30752 (2001)

    Article  CAS  PubMed  Google Scholar 

  42. Ashikari-Hada S., Habuchi H., Kariya Y., Itoh N., Reddi A.H., Kimata K.: Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J. Biol. Chem. 279, 12346–12354 (2004)

    Article  CAS  PubMed  Google Scholar 

  43. Ishihara M.: Structural requirements in heparin for binding and activation of FGF-1 and FGF-4 are different from that for FGF-2. Glycobiology. 4, 817–824 (1994)

    Article  CAS  PubMed  Google Scholar 

  44. Turnbull J.E., Fernig D.G., Ke Y., Wilkinson M.C., Gallagher J.T.: Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267, 10337–10341 (1992)

    CAS  PubMed  Google Scholar 

  45. Habuchi H., Suzuki S., Saito T., Tamura T., Harada T., Yoshida K., Kimata K.: Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor. Biochem J. 285, 805–813 (1992)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lundin L., Larsson H., Kreuger J., Kanda S., Lindahl U., Salmivirta M., Claesson-Welsh L.: Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J. Biol. Chem. 275, 24653–24660 (2000)

    Article  CAS  PubMed  Google Scholar 

  47. Sugaya N., Habuchi H., Nagai N., Ashikari-Hada S., Kimata K.: 6-O-sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J. Biol. Chem. 283, 10366–10376 (2008)

    Article  CAS  PubMed  Google Scholar 

  48. Seffouh A., Milz F., Przybylski C., Laguri C., Oosterhof A., Bourcier S., Sadir R., Dutkowski E., Daniel R., van Kuppevelt T.H., Dierks T., Lortat-Jacob H., Vives R.R.: HSulf sulfatases catalyze processive and oriented 6-O-desulfation of heparan sulfate that differentially regulates fibroblast growth factor activity. Faseb J. 27, 2431–2439 (2013)

    Article  CAS  PubMed  Google Scholar 

  49. Xu R., Ori A., Rudd T.R., Uniewicz K.A., Ahmed Y.A., Guimond S.E., Skidmore M.A., Siligardi G., Yates E.A., Fernig D.G.: Diversification of the structural determinants of fibroblast growth factor-heparin interactions implications for binding specificity. J. Biol. Chem. 287, 40061–40073 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Patel V.N., Likar K.M., Zisman-Rozen S., Cowherd S.N., Lassiter K.S., Sher I., Yates E.A., Turnbull J.E., Ron D., Hoffman M.P.: Specific heparan sulfate structures modulate FGF10-mediated submandibular gland epithelial morphogenesis and differentiation. J. Biol. Chem. 283, 9308–9317 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Feyzi E., Lustig F., Fager G., Spillmann D., Lindahl U., Salmivirta M.: Characterization of heparin and heparan sulfate domains binding to the long splice variant of platelet-derived growth factor a chain. J. Biol. Chem. 272, 5518–5524 (1997)

    Article  CAS  PubMed  Google Scholar 

  52. Lyon M., Deakin J.A., Mizuno K., Nakamura T., Gallagher J.T.: Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J. Biol. Chem. 269, 11216–11223 (1994)

    CAS  PubMed  Google Scholar 

  53. Rickard S.M., Mummery R.S., Mulloy B., Rider C.C.: The binding of human glial cell line-derived neurotrophic factor to heparin and heparan sulfate: importance of 2-O-sulfate groups and effect on its interaction with its receptor, GFRalpha1. Glycobiology. 13, 419–426 (2003)

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  55. Cole C.L., Rushton G., Jayson G.C., Avizienyte E.: Ovarian cancer cell heparan sulfate 6-O-sulfotransferases regulate an angiogenic program induced by heparin-binding epidermal growth factor (EGF)-like growth factor/EGF receptor signaling. J. Biol. Chem. 289, 10488–10501 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Robinson C.J., Mulloy B., Gallagher J.T., Stringer S.E.: VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J. Biol. Chem. 281, 1731–1740 (2006)

    Article  CAS  PubMed  Google Scholar 

  57. Ferreras C., Rushton G., Cole C.L., Babur M., Telfer B.A., van Kuppevelt T.H., Gardiner J.M., Williams K.J., Jayson G.C., Avizienyte E.: Endothelial heparan sulfate 6-O-sulfation levels regulate angiogenic responses of endothelial cells to fibroblast growth factor 2 and vascular endothelial growth factor. J. Biol. Chem. 287, 36132–36146 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ono K., Hattori H., Takeshita S., Kurita A., Ishihara M.: Structural features in heparin that interact with VEGF165 and modulate its biological activity. Glycobiology. 9, 705–711 (1999)

    Article  CAS  PubMed  Google Scholar 

  59. Charo I.F., Ransohoff R.M.: The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354, 610–621 (2006)

    Article  CAS  PubMed  Google Scholar 

  60. Zlotnik A., Yoshie O.: The chemokine superfamily revisited. Immunity. 36, 705–716 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Sadir R., Imberty A., Baleux F., Lortat-Jacob H.: Heparan sulfate/heparin oligosccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J. Biol. Chem. 279, 43854–43860 (2004)

    Article  CAS  PubMed  Google Scholar 

  62. Sweeney E.A., Lortat-Jacob H., Priestley G.V., Nakamoto B., Papayannopoulou T.: Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood. 99, 44–51 (2002)

    Article  CAS  PubMed  Google Scholar 

  63. Lortat-Jacob H., Grosdidier A., Imberty A.: Structural diversity of heparan sulfate binding domains in chemokines. Proc Natl Acad Sci U A. 99, 1229–1234 (2002)

    Article  CAS  Google Scholar 

  64. Monneau Y., Arenzana-Seisdedos F., Lortat-Jacob H.: The sweet spot: how GAGs help chemokines guide migrating cells. J. Leukoc. Biol. 99, 935–953 (2016)

    Article  CAS  PubMed  Google Scholar 

  65. Proudfoot A.E.: The biological relevance of chemokine-proteoglycan interactions. Biochem. Soc. Trans. 34, 422–426 (2006)

    Article  CAS  PubMed  Google Scholar 

  66. Sadir R., Baleux F., Grosdidier A., Imberty A., Lortat-Jacob H.: Characterization of the stromal cell-derived factor-1alpha-heparin complex. J. Biol. Chem. 276, 8288–8296 (2001)

    Article  CAS  PubMed  Google Scholar 

  67. Uchimura K., Morimoto-Tomita M., Bistrup A., Li J., Lyon M., Gallagher J., Werb Z., Rosen S.D.: HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem. 7, 2 (2006)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Roy S., El Hadri A., Richard S., Denis F., Holte K., Duffner J., Yu F., Galcheva-Gargova Z., Capila I., Schultes B., Petitou M., Kaundinya G.V.: Synthesis and biological evaluation of a unique heparin mimetic hexasaccharide for structure-activity relationship studies. J. Med. Chem. 57, 4511–4520 (2014)

    Article  CAS  PubMed  Google Scholar 

  69. Zhang S., Condac E., Qiu H., Jiang J., Gutierrez-Sanchez G., Bergmann C., Handel T., Wang L.: Heparin-induced leukocytosis requires 6-O-sulfation and is caused by blockade of selectin- and CXCL12 protein-mediated leukocyte trafficking in mice. J. Biol. Chem. 287, 5542–5553 (2012)

    Article  CAS  PubMed  Google Scholar 

  70. Spillmann D., Witt D., Lindahl U.: Defining the interleukin-8-binding domain of heparan sulfate. J. Biol. Chem. 273, 15487–15493 (1998)

    Article  CAS  PubMed  Google Scholar 

  71. Pichert A., Schlorke D., Franz S., Arnhold J.: Functional aspects of the interaction between interleukin-8 and sulfated glycosaminoglycans. Biomatter. 2, 142–148 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  72. Stringer S.E., Gallagher J.T.: Specific binding of the chemokine platelet factor 4 to heparan sulfate. J. Biol. Chem. 272, 20508–20514 (1997)

    Article  CAS  PubMed  Google Scholar 

  73. Pempe E.H., Burch T.C., Law C.J., Liu J.: Substrate specificity of 6-O-endosulfatase (Sulf-2) and its implications in synthesizing anticoagulant heparan sulfate. Glycobiology. 22, 1353–1362 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Jayson G.C., Hansen S.U., Miller G.J., Cole C.L., Rushton G., Avizienyte E., Gardiner J.M.: Synthetic heparan sulfate dodecasaccharides reveal single sulfation site interconverts CXCL8 and CXCL12 chemokine biology. Chem. Commun. Camb. Engl. 51, 13846–13849 (2015)

    Article  CAS  Google Scholar 

  75. Shaw J.P., Johnson Z., Borlat F., Zwahlen C., Kungl A., Roulin K., Harrenga A., Wells T.N., Proudfoot A.E.: The X-Ray Structure of RANTES; Heparin-Derived Disaccharides Allows the Rational Design of Chemokine Inhibitors. Struct. Camb. 12, 2081–2093 (2004)

    Article  CAS  Google Scholar 

  76. Coulson-Thomas V.J.: The role of heparan sulphate in development: the ectodermal story. Int. J. Exp. Pathol. 97, 213–229 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yan D., Lin X.: Shaping Morphogen Gradients by Proteoglycans. Cold Spring Harb. Perspect. Biol. 1, (2009)

  78. Lyon M., Rushton G., Gallagher J.T.: The interaction of the transforming growth factor-betas with heparin/heparan sulfate is isoform-specific. J. Biol. Chem. 272, 18000–18006 (1997)

    Article  CAS  PubMed  Google Scholar 

  79. Yue X., Li X., Nguyen H.T., Chin D.R., Sullivan D.E., Lasky J.A.: Transforming growth factor-beta1 induces heparan sulfate 6-O-endosulfatase 1 expression in vitro and in vivo. J. Biol. Chem. 283, 20397–20407 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Yue X., Lu J., Auduong L., Sides M.D., Lasky J.A.: Overexpression of Sulf2 in idiopathic pulmonary fibrosis. Glycobiology. 23, 709–719 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Lu J., Auduong L., White E.S., Yue X.: Up-regulation of heparan sulfate 6-O-sulfation in idiopathic pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 50, 106–114 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Ai X., Do A.T., Lozynska O., Kusche-Gullberg M., Lindahl U., Emerson Jr. C.P.: QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162, 341–351 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kleinschmit A., Koyama T., Dejima K., Hayashi Y., Kamimura K., Nakato H.: Drosophila heparan sulfate 6-O endosulfatase regulates wingless morphogen gradient formation. Dev. Biol. 345, 204–214 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Blackhall, F.H., Merry, C.L., Lyon, M., Jayson, G.C., Folkman, J., Javaherian, K., Gallagher, J.T.: Binding of endostatin to endothelial heparan sulphate shows a differential requirement for specific sulphates. Biochem J. Pt, (2003)

  85. Shipp E.L., Hsieh-Wilson L.C.: Profiling the sulfation specificities of glycosaminoglycan interactions with growth factors and chemotactic proteins using microarrays. Chem. Biol. 14, 195–208 (2007)

    Article  CAS  PubMed  Google Scholar 

  86. Kalia M., Chandra V., Rahman S.A., Sehgal D., Jameel S.: Heparan sulfate proteoglycans are required for cellular binding of the hepatitis E virus ORF2 capsid protein and for viral infection. J. Virol. 83, 12714–12724 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pankonin M.S., Gallagher J.T., Loeb J.A.: Specific structural features of heparan sulfate proteoglycans potentiate neuregulin-1 signaling. J. Biol. Chem. 280, 383–388 (2005)

    Article  CAS  PubMed  Google Scholar 

  88. Lindahl B., Westling C., Giménez-Gallego G., Lindahl U., Salmivirta M.: Common binding sites for β-amyloid fibrils and fibroblast growth factor-2 in heparan sulfate from human cerebral cortex. J. Biol. Chem. 274, 30631–30635 (1999)

    Article  CAS  PubMed  Google Scholar 

  89. Scholefield, Z., Yates, E.A., Wayne, G., Amour, A., McDowell, W., Turnbull, J.E.: Heparan sulfate regulates amyloid precursor protein processing by BACE1, the Alzheimer’s {beta}-secretase. J. Cell Biol. (2003)

  90. Habuchi H., Habuchi O., Kimata K.: Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J. Biol. Chem. 270, 4172–4179 (1995)

    Article  CAS  PubMed  Google Scholar 

  91. Habuchi H., Tanaka M., Habuchi O., Yoshida K., Suzuki H., Ban K., Kimata K.: The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J. Biol. Chem. 275, 2859–2868 (2000)

    Article  CAS  PubMed  Google Scholar 

  92. Habuchi H., Miyake G., Nogami K., Kuroiwa A., Matsuda Y., Kusche-Gullberg M., Habuchi O., Tanaka M., Kimata K.: Biosynthesis of heparan sulphate with diverse structures and functions: two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties. Biochem J. 371, 131–142 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Habuchi O.: Diversity and functions of glycosaminoglycan sulfotransferases. Biochim. Biophys. Acta BBA - Gen. Subj. 1474, 115–127 (2000)

    Article  CAS  Google Scholar 

  94. Nagai N., Habuchi H., Esko J.D., Kimata K.: Stem domains of heparan sulfate 6-O-sulfotransferase are required for Golgi localization, oligomer formation and enzyme activity. J. Cell Sci. 117, 3331–3341 (2004)

    Article  CAS  PubMed  Google Scholar 

  95. Nagai N., Habuchi H., Kitazume S., Toyoda H., Hashimoto Y., Kimata K.: Regulation of heparan sulfate 6-O-sulfation by β-secretase activity. J. Biol. Chem. 282, 14942–14951 (2007)

    Article  CAS  PubMed  Google Scholar 

  96. Smeds E., Habuchi H., Do A.T., Hjertson E., Grundberg H., Kimata K., Lindahl U., Kusche-Gullberg M.: Substrate specificities of mouse heparan sulphate glucosaminyl 6-O-sulphotransferases. Biochem J. 372, 371–380 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Do A.-T., Smeds E., Spillmann D., Kusche-Gullberg M.: Overexpression of Heparan Sulfate 6-O-Sulfotransferases in Human Embryonic Kidney 293 Cells Results in Increased N-Acetylglucosaminyl 6-O-Sulfation. J. Biol. Chem. 281, 5348–5356 (2006)

    Article  CAS  PubMed  Google Scholar 

  98. Jemth P., Smeds E., Do A.T., Habuchi H., Kimata K., Lindahl U., Kusche-Gullberg M.: Oligosaccharide library-based assessment of heparan sulfate 6-O-sulfotransferase substrate specificity. J. Biol. Chem. 278, 24371–24376 (2003)

    Article  CAS  PubMed  Google Scholar 

  99. Sedita J., Izvolsky K., Cardoso W.V.: Differential expression of heparan sulfate 6-O-sulfotransferase isoforms in the mouse embryo suggests distinctive roles during organogenesis. Dev. Dyn. Off. Publ. Am. Assoc. Anat. 231, 782–794 (2004)

    CAS  Google Scholar 

  100. Kamimura K., Fujise M., Villa F., Izumi S., Habuchi H., Kimata K., Nakato H.: Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) Gene structure, expression, and function in the formation of the tracheal system. J. Biol. Chem. 276, 17014–17021 (2001)

    Article  CAS  PubMed  Google Scholar 

  101. Bulow H.E., Hobert O.: Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron. 41, 723–736 (2004)

    Article  PubMed  Google Scholar 

  102. Habuchi H., Nagai N., Sugaya N., Atsumi F., Stevens R.L., Kimata K.: Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J. Biol. Chem. 282, 15578–15588 (2007)

    Article  CAS  PubMed  Google Scholar 

  103. Pratt T., Conway C.D., Tian N.M.M.-L., Price D.J., Mason J.O.: Heparan Sulphation patterns generated by specific heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J. Neurosci. 26, 6911–6923 (2006)

    Article  CAS  PubMed  Google Scholar 

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

  105. Morimoto-Tomita M., Uchimura K., Werb Z., Hemmerich S., Rosen S.D.: Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277, 49175–49185 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Frese M.A., Milz F., Dick M., Lamanna W.C., Dierks T.: Characterization of the human sulfatase Sulf1 and its high affinity heparin/heparan sulfate interaction domain. J. Biol. Chem. 284, 28033–28044 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Tang R., Rosen S.D.: Functional consequences of the subdomain organization of the sulfs. J. Biol. Chem. 284, 21505–21514 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Ai X., Do A.T., Kusche-Gullberg M., Lindahl U., Lu K., Emerson Jr. C.P.: Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J. Biol. Chem. 281, 4969–4976 (2006)

    Article  CAS  PubMed  Google Scholar 

  109. Ambasta R.K., Ai X., Emerson Jr. C.P.: Quail Sulf1 function requires asparagine-linked glycosylation. J. Biol. Chem. 282, 34492–34499 (2007)

    Article  CAS  PubMed  Google Scholar 

  110. Milz, F., Harder, A., Neuhaus, P., Breitkreuz-Korff, O., Walhorn, V., Lubke, T., Anselmetti, D., Dierks, T.: Cooperation of binding sites at the hydrophilic domain of cell-surface sulfatase Sulf1 allows for dynamic interaction of the enzyme with its substrate heparan sulfate. Biochim. Biophys. Acta (2013).

  111. Harder A., Möller A.-K., Milz F., Neuhaus P., Walhorn V., Dierks T., Anselmetti D.: Catch bond interaction between cell-surface sulfatase Sulf1 and glycosaminoglycans. Biophys. J. 108, 1709–1717 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  113. Staples G.O., Shi X., Zaia J.: Glycomics analysis of mammalian heparan sulfates modified by the human extracellular sulfatase HSulf2. PLoS One. 6, e16689 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Viviano B.L., Paine-Saunders S., Gasiunas N., Gallagher J., Saunders S.: Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist noggin. J. Biol. Chem. 279, 5604–5611 (2004)

    Article  CAS  PubMed  Google Scholar 

  115. Lai J., Chien J., Staub J., Avula R., Greene E.L., Matthews T.A., Smith D.I., Kaufmann S.H., Roberts L.R., Shridhar V.: Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J. Biol. Chem. 278, 23107–23117 (2003)

    Article  CAS  PubMed  Google Scholar 

  116. Li J., Kleeff J., Abiatari I., Kayed H., Giese N.A., Felix K., Giese T., Buchler M.W., Friess H.: Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol. Cancer. 4, 14 (2005)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Narita K., Staub J., Chien J., Meyer K., Bauer M., Friedl A., Ramakrishnan S., Shridhar V.: HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res. 66, 6025–6032 (2006)

    Article  CAS  PubMed  Google Scholar 

  118. Wang S., Ai X., Freeman S.D., Pownall M.E., Lu Q., Kessler D.S., Emerson Jr. C.P.: QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc Natl Acad Sci U A. 101, 4833–4838 (2004)

    Article  CAS  Google Scholar 

  119. Lai J.P., Chien J.R., Moser D.R., Staub J.K., Aderca I., Montoya D.P., Matthews T.A., Nagorney D.M., Cunningham J.M., Smith D.I., Greene E.L., Shridhar V., Roberts L.R.: hSulf1 sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology. 126, 231–248 (2004)

    Article  CAS  PubMed  Google Scholar 

  120. Dai Y., Yang Y., MacLeod V., Yue X., Rapraeger A.C., Shriver Z., Venkataraman G., Sasisekharan R., Sanderson R.D.: HSulf-1 and HSulf-2 are potent inhibitors of myeloma tumor growth in vivo. J. Biol. Chem. 280, 40066–40073 (2005)

    Article  CAS  PubMed  Google Scholar 

  121. Narita K., Chien J., Mullany S.A., Staub J., Qian X., Lingle W.L., Shridhar V.: Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer. J. Biol. Chem. 282, 14413–14420 (2007)

    Article  CAS  PubMed  Google Scholar 

  122. Langsdorf A., Schumacher V., Shi X., Tran T., Zaia J., Jain S., Taglienti M., Kreidberg J.A., Fine A., Ai X.: Expression regulation and function of heparan sulfate 6-O-endosulfatases in the spermatogonial stem cell niche. Glycobiology. 21, 152–161 (2011)

    Article  CAS  PubMed  Google Scholar 

  123. Otsuki S., Hanson S.R., Miyaki S., Grogan S.P., Kinoshita M., Asahara H., Wong C.H., Lotz M.K.: Extracellular sulfatases support cartilage homeostasis by regulating BMP and FGF signaling pathways. Proc Natl Acad Sci U A. 107, 10202–10207 (2010)

    Article  CAS  Google Scholar 

  124. Danesin C., Agius E., Escalas N., Ai X., Emerson C., Cochard P., Soula C.: Ventral neural progenitors switch toward an oligodendroglial fate in response to increased sonic hedgehog (Shh) activity: involvement of sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J. Neurosci. 26, 5037–5048 (2006)

    Article  CAS  PubMed  Google Scholar 

  125. Ma H.Y., Zhang F., Li J., Mo M.L., Chen Z., Liu L., Zhou H.M., Sheng Q.: HSulf-1 suppresses cell growth and down-regulates hedgehog signaling in human gastric cancer cells. Oncol. Lett. 2, 1291–1295 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Kalus I., Salmen B., Viebahn C., von Figura K., Schmitz D., D’Hooge R., Dierks T.: Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. J. Cell. Mol. Med. 13, 4505–4521 (2009)

    Article  CAS  PubMed  Google Scholar 

  127. Kalus I., Rohn S., Puvirajesinghe T.M., Guimond S.E., Eyckerman-Kolln P.J., Ten Dam G., van Kuppevelt T.H., Turnbull J.E., Dierks T.: Sulf1 and Sulf2 Differentially Modulate Heparan Sulfate Proteoglycan Sulfation during Postnatal Cerebellum Development: Evidence for Neuroprotective and Neurite Outgrowth Promoting Functions. PLoS One. 10, e0139853 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Oustah A.A., Danesin C., Khouri-Farah N., Farreny M.-A., Escalas N., Cochard P., Glise B., Soula C.: Dynamics of Sonic hedgehog signaling in the ventral spinal cord are controlled by intrinsic changes in source cells requiring Sulfatase 1. Development. 141, 1392–1403 (2014)

    Article  PubMed  CAS  Google Scholar 

  129. Zhao W., Sala-Newby G.B., Dhoot G.K.: Sulf1 expression pattern and its role in cartilage and joint development. Dev. Dyn. 235, 3327–3335 (2006)

    Article  CAS  PubMed  Google Scholar 

  130. Holst C.R., Bou-Reslan H., Gore B.B., Wong K., Grant D., Chalasani S., Carano R.A., Frantz G.D., Tessier-Lavigne M., Bolon B., French D.M., Ashkenazi A.: Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS One. 2, e575 (2007)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Freeman S.D., Keino-Masu K., Masu M., Ladher R.K.: Expression of the heparan sulfate 6-O-endosulfatases, Sulf1 and Sulf2, in the avian and mammalian inner ear suggests a role for sulfation during inner ear development. Dev. Dyn. Off. Publ. Am. Assoc. Anat. 244, 168–180 (2015)

    CAS  Google Scholar 

  132. Hayano S., Kurosaka H., Yanagita T., Kalus I., Milz F., Ishihara Y., Islam M.N., Kawanabe N., Saito M., Kamioka H., Adachi T., Dierks T., Yamashiro T.: Roles of heparan sulfate sulfation in dentinogenesis. J. Biol. Chem. 287, 12217–12229 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Ramsbottom S.A., Maguire R.J., Fellgett S.W., Pownall M.E.: Sulf1 influences the Shh morphogen gradient during the dorsal ventral patterning of the neural tube in Xenopus Tropicalis. Dev. Biol. 391, 207–218 (2014)

    Article  CAS  PubMed  Google Scholar 

  134. Winterbottom E.F., Pownall M.E.: Complementary expression of HSPG 6-O-endosulfatases and 6-O-sulfotransferase in the hindbrain of Xenopus laevis. Gene Expr. Patterns GEP. 9, 166–172 (2009)

    Article  CAS  PubMed  Google Scholar 

  135. Meyers J.R., Planamento J., Ebrom P., Krulewitz N., Wade E., Pownall M.E.: Sulf1 modulates BMP signaling and is required for somite morphogenesis and development of the horizontal myoseptum. Dev. Biol. 378, 107–121 (2013)

    Article  CAS  PubMed  Google Scholar 

  136. Nakamura I., Fernandez-Barrena M.G., Ortiz-Ruiz M.C., Almada L.L., Hu C., Elsawa S.F., Mills L.D., Romecin P.A., Gulaid K.H., Moser C.D., Han J.J., Vrabel A., Hanse E.A., Akogyeram N.A., Albrecht J.H., Monga S.P., Sanderson S.O., Prieto J., Roberts L.R., Fernandez-Zapico M.E.: Activation of the transcription factor GLI1 by WNT signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration. J. Biol. Chem. 288, 21389–21398 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Maltseva I., Chan M., Kalus I., Dierks T., Rosen S.D.: The SULFs, Extracellular Sulfatases for Heparan Sulfate, Promote the Migration of Corneal Epithelial Cells during Wound Repair. PLoS One. 8, e69642 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Tran T.H., Shi X., Zaia J., Ai X.: Heparan sulfate 6-O-endosulfatases (sulfs) coordinate the Wnt signaling pathways to regulate myoblast fusion during skeletal muscle regeneration. J. Biol. Chem. 287, 32651–32664 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Schumacher V.A., Schlotzer-Schrehardt U., Karumanchi S.A., Shi X., Zaia J., Jeruschke S., Zhang D., Pavenstadt H., Drenckhan A., Amann K., Ng C., Hartwig S., Ng K.H., Ho J., Kreidberg J.A., Taglienti M., Royer-Pokora B., Ai X.: WT1-dependent sulfatase expression maintains the normal glomerular filtration barrier. J. Am. Soc. Nephrol. 22, 1286–1296 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Takashima Y., Keino-Masu K., Yashiro H., Hara S., Suzuki T., Kuppevelt T.H., van Masu M., Nagata M.: Heparan sulfate 6-O-endosulfatases, Sulf1 and Sulf2, regulate glomerular integrity by modulating growth factor signaling. Am. J. Physiol. - Ren. Physiol. 310, F395–F408 (2016)

    Article  CAS  Google Scholar 

  141. Lai J.-P., Sandhu D.S., Shire A.M., Roberts L.R.: The tumor suppressor function of human sulfatase 1 (SULF1) in carcinogenesis. J. Gastrointest. Cancer. 39, 149–158 (2008)

    Article  CAS  PubMed  Google Scholar 

  142. Lemjabbar-Alaoui H., van Zante A., Singer M.S., Xue Q., Wang Y.Q., Tsay D., He B., Jablons D.M., Rosen S.D.: Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene. 29, 635–646 (2010)

    Article  CAS  PubMed  Google Scholar 

  143. Phillips J.J., Huillard E., Robinson A.E., Ward A., Lum D.H., Polley M.Y., Rosen S.D., Rowitch D.H., Werb Z.: Heparan sulfate sulfatase SULF2 regulates PDGFRalpha signaling and growth in human and mouse malignant glioma. J. Clin. Invest. 122, 911–922 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Khurana A., Jung-Beom D., He X., Kim S.H., Busby R.C., Lorenzon L., Villa M., Baldi A., Molina J., Goetz M.P., Shridhar V.: Matrix detachment and proteasomal inhibitors diminish Sulf-2 expression in breast cancer cell lines and mouse xenografts. Clin Exp Metastasis. 30, 407–415 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Nawroth R., van Zante A., Cervantes S., McManus M., Hebrok M., Rosen S.D.: Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One. 2, e392 (2007)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Khurana A., McKean H., Kim H., Kim S.-H., Mcguire J., Roberts L.R., Goetz M.P., Shridhar V.: Silencing of HSulf-2 expression in MCF10DCIS.com cells attenuate ductal carcinoma in situ progression to invasive ductal carcinoma in vivo. Breast Cancer Res. BCR. 14, R43 (2012)

    Article  CAS  PubMed  Google Scholar 

  147. Abiatari I., Kleeff J., Li J., Felix K., Büchler M.W., Friess H.: Hsulf-1 regulates growth and invasion of pancreatic cancer cells. J. Clin. Pathol. 59, 1052–1058 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Moussay E., Palissot V., Vallar L., Poirel H.A., Wenner T., El Khoury V., Aouali N., Van Moer K., Leners B., Bernardin F., Muller A., Cornillet-Lefebvre P., Delmer A., Duhem C., Ries F., van Dyck E., Berchem G.: Determination of genes and microRNAs involved in the resistance to fludarabine in vivo in chronic lymphocytic leukemia. Mol. Cancer. 9, 115 (2010)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Otsuki S., Taniguchi N., Grogan S.P., D’Lima D., Kinoshita M., Lotz M.: Expression of novel extracellular sulfatases Sulf-1 and Sulf-2 in normal and osteoarthritic articular cartilage. Arthritis Res Ther. 10, R61 (2008)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  150. Tsai T.-T., Ho N.Y.-J., Fang H.-C., Lai P.-L., Niu C.-C., Chen L.-H., Chen W.-J., Pang J.-H.S.: Increased sulfatase 1 gene expression in degenerative intervertebral disc cells. J. Orthop. Res. 33, 312–317 (2015)

    Article  CAS  PubMed  Google Scholar 

  151. Celie J.W., Rutjes N.W., Keuning E.D., Soininen R., Heljasvaara R., Pihlajaniemi T., Drager A.M., Zweegman S., Kessler F.L., Beelen R.H., Florquin S., Aten J.: Van den born, J.: Subendothelial heparan sulfate proteoglycans become major L-selectin and monocyte chemoattractant protein-1 ligands upon renal ischemia/reperfusion. Am. J. Pathol. 170, 1865–1878 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Yue, X., Shan, B., Lasky, J.A.: TGF-β: Titan of Lung Fibrogenesis. Curr. Enzyme Inhib. 6, (2010)

  153. Singer M.S., Phillips J.J., Lemjabbar-Alaoui H., Wang Y.Q., Wu J., Goldman R., Rosen S.D.: SULF2, a heparan sulfate endosulfatase, is present in the blood of healthy individuals and increases in cirrhosis. Clin. Chim. Acta. 440, 72–78 (2015)

    Article  CAS  PubMed  Google Scholar 

  154. Taghizadeh E., Kalantar S.M., Mahdian R., Sheikhha M.H., Farashahi-Yazd E., Ghasemi S., Shahbazi Z.: SULF 1 gene polymorphism, rs6990375 is in significant association with fetus failure in IVF technique. Iran. J. Reprod. Med. 13, 215–220 (2015)

    Google Scholar 

  155. Zahraei M., Sheikhha M.H., Kalantar S.M., Ghasemi N., Jahaninejad T., Rajabi S., Mohammadpour H.: The association of arylendosulfatase 1 (SULF1) gene polymorphism with recurrent miscarriage. J. Assist. Reprod. Genet. 31, 157–161 (2014)

    Article  PubMed  Google Scholar 

  156. Lum D.H., Tan J., Rosen S.D., Werb Z.: Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol. Cell. Biol. 27, 678–688 (2007)

    Article  CAS  PubMed  Google Scholar 

  157. Lamanna W.C., Baldwin R.J., Padva M., Kalus I., Ten Dam G., van Kuppevelt T.H., Gallagher J.T., von Figura K., Dierks T., Merry C.L.: Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem J. 400, 63–73 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Lamanna W.C., Frese M.A., Balleininger M., Dierks T.: Sulf loss influences N-, 2-O-, and 6-O-sulfation of multiple heparan sulfate proteoglycans and modulates fibroblast growth factor signaling. J. Biol. Chem. 283, 27724–27735 (2008)

    Article  CAS  PubMed  Google Scholar 

  159. Nagamine S., Tamba M., Ishimine H., Araki K., Shiomi K., Okada T., Ohto T., Kunita S., Takahashi S., Wismans R.G., van Kuppevelt T.H., Masu M., Keino-Masu K.: Organ-specific sulfation patterns of heparan sulfate generated by extracellular sulfatases Sulf1 and Sulf2 in mice. J. Biol. Chem. 287, 9579–9590 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Lai J.P., Sandhu D.S., Yu C., Han T., Moser C.D., Jackson K.K., Guerrero R.B., Aderca I., Isomoto H., Garrity-Park M.M., Zou H., Shire A.M., Nagorney D.M., Sanderson S.O., Adjei A.A., Lee J.S., Thorgeirsson S.S., Roberts L.R.: Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology. 47, 1211–1222 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Morimoto-Tomita M., Uchimura K., Bistrup A., Lum D.H., Egeblad M., Boudreau N., Werb Z., Rosen S.D.: Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia. 7, 1001–1010 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Presto J., Thuveson M., Carlsson P., Busse M., Wilen M., Eriksson I., Kusche-Gullberg M., Kjellen L.: Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci U A. 105, 4751–4756 (2008)

    Article  CAS  Google Scholar 

  163. Dejima K., Takemura M., Nakato E., Peterson J., Hayashi Y., Kinoshita-Toyoda A., Toyoda H., Nakato H.: Analysis of drosophila glucuronyl C5-epimerase: implications for developmental roles of heparan sulfate sulfation compensation and 2-O-sulfated glucuronic acid. J. Biol. Chem. 288, 34384–34393 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Qin Y., Ke J., Gu X., Fang J., Wang W., Cong Q., Li J., Tan J., Brunzelle J.S., Zhang C., Jiang Y., Melcher K., Li J., Xu H.E., Ding K.: Structural and functional study of D-glucuronyl C5-epimerase. J. Biol. Chem. 290, 4620–4630 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Buresh-Stiemke R.A., Malinowski R.L., Keil K.P., Vezina C.M., Oosterhof A., Van Kuppevelt T.H., Marker P.C.: Distinct expression patterns of Sulf1 and Hs6st1 spatially regulate heparan sulfate sulfation during prostate development. Dev. Dyn. 241, 2005–2013 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Pye D.A., Vives R.R., Hyde P., Gallagher J.T.: Regulation of FGF-1 mitogenic activity by heparan sulfate oligosaccharides is dependent on specific structural features: differential requirements for the modulation of FGF-1 and FGF-2. Glycobiology. 10, 1183–1192 (2000)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work is supported by grants from the Agence Nationale de la Recherche (ANR-12-SVSE-008) and Université Grenoble-Alpes (UGA AGIR program).

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El Masri, R., Seffouh, A., Lortat-Jacob, H. et al. The “in and out” of glucosamine 6-O-sulfation: the 6th sense of heparan sulfate. Glycoconj J 34, 285–298 (2017). https://doi.org/10.1007/s10719-016-9736-5

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