Skip to main content

Advertisement

SpringerLink
Log in

Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Chondroitin sulfate (CS) and dermatan sulfate (DS) interact with various extracellular molecules such as growth factors, cytokines/chemokines, neurotrophic factors, morphogens, and viral proteins, thereby playing roles in a variety of biological processes including cell adhesion, proliferation, tissue morphogenesis, neurite outgrowth, infections, and inflammation/leukocyte trafficking. CS/DS are modified with sulfate groups at C-2 of uronic acid residues as well as C-4 and/or C-6 of N-acetyl-D-galactosamine residues, yielding enormous structural diversity, which enables the binding with numerous proteins. We have demonstrated that highly sulfated CS-E from squid cartilage, for example, interacts with heparin-binding proteins including midkine, pleiotrophin, and fibroblast growth factors expressed in brain with high affinity (Kd values in the nM range). Here, we analyzed the binding of CS and DS, which have a relatively low degree of sulfation and have been widely used as a nutraceutical and a drug for osteoarthritis etc., with a number of heparin-binding neurotrophic factors/cytokines using surface plasmon resonance (SPR) and structurally characterized the CS/DS chains. SPR showed that relatively low sulfated CS-A, DS, and CS-C also bound with significant affinity to midkine, pleiotrophin, hepatocyte growth factor, monokine-induced by interferon-γ, and stromal cell derived factor-1β, although the binding was less intense than that with highly sulfated CS-D and CS-E. These findings suggest that even low sulfated CS and/or DS chains may contain binding domains, which include fine sugar sequences with specific sulfation patterns, and that sugar sequences, conformations and electrostatic potential are more important than the simple degree of sulfation represented by disaccharide composition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CS:

Chondroitin sulfate

DS:

Dermatan sulfate

FGF:

Fibroblast growth factor

GAG:

Glycosaminoglycan

HIV:

Human immunodeficiency virus

HGF:

Hepatocyte growth factor

MIG:

Monokine-induced by interferon-γ

MK:

Midkine

PG:

Proteoglycan

PTN:

Pleiotrophin

RANTES:

Regulated upon activation normal T cell express sequence

SDB-1β:

Stromal cell derived factor-1β

SPR:

Surface plasmon resonance

References

  1. Mizumoto, S., Uyama, T., Mikami, T., Kitagawa, H., Sugahara, K.: Biosynthetic pathways for differential expression of functional chondroitin sulfate and heparan sulfate. In: Yarema, K.J. (ed.) Handbook of Carbohydrate Engineering, pp. 289–324. CRC Press, Boca Raton (2005)

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. 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, 612–620 (2003)

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  5. Kawashima, H., Atarashi, K., Hirose, M., Hirose, J., Yamada, S., Sugahara, K., Miyasaka, M.: Oversulfated chondroitin/dermatan sulfates containing GlcAβ1/IdoAα1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 277, 12921–12930 (2002)

    Article  PubMed  CAS  Google Scholar 

  6. Thiele, H., Sakano, M., Kitagawa, H., Sugahara, K., Rajab, A., Hohne, W., Leschik, G., Nurnberg, P., Mundlos, S.: Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc. Natl. Acad. Sci. U. S. A. 101, 10155–10160 (2004)

    Article  PubMed  CAS  Google Scholar 

  7. Bao, X., Muramatsu, T., Sugahara, K.: Demonstration of the pleiotrophin-binding oligosaccharide sequences isolated from chondroitin sulfate/dermatan sulfate hybrid chains of embryonic pig brains. J. Biol. Chem. 280, 35318–35328 (2005)

    Article  PubMed  CAS  Google Scholar 

  8. Uyama, T., Ishida, M., Izumikawa, T., Trybala, E., Tufaro, F., Bergström, T., Sugahara, K., Kitagawa, H.: Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity. J. Biol. Chem. 281, 38668–38674 (2006)

    Article  PubMed  CAS  Google Scholar 

  9. Li, F., ten Dam, G.B., Murugan, S., Yamada, S., Hashiguchi, T., Mizumoto, S., Oguri, K., Okayama, M., van Kuppevelt, T.H., Sugahara, K.: Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells. J. Biol. Chem. 283, 34294–34304 (2008)

    Article  PubMed  CAS  Google Scholar 

  10. Mizumoto, S., Takahashi, J., Sugahara, K.: Receptor for advanced glycation end products (RAGE) functions as a receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or the sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells. J. Biol. Chem. 287, 18985–18994 (2012)

    Article  PubMed  CAS  Google Scholar 

  11. Miyake, N., Kosho, T., Mizumoto, S., Furuichi, T., Hatamochi, A., Nagashima, Y., Arai, E., Takahashi, K., Kawamura, R., Wakui, K., Takahashi, J., Kato, H., Yasui, H., Ishida, T., Ohashi, H., Nishimura, G., Shiina, M., Saitsu, H., Tsurusaki, Y., Doi, H., Fukushima, Y., Ikegawa, S., Yamada, S., Sugahara, K., Matsumoto, N.: Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum. Mutat. 31, 966–974 (2010)

    Article  PubMed  CAS  Google Scholar 

  12. Deepa, S.S., Umehara, Y., Higashiyama, S., Itoh, N., Sugahara, K.: Specific interactions of oversulfated chondroitin sulfate E with various heparin- binding growth factors: implications as a physiological binding partner. J. Biol. Chem. 277, 43707–43716 (2002)

    Article  PubMed  CAS  Google Scholar 

  13. Maeda, N., Fukazawa, N., Hata, T.: The binding of chondroitin sulfate to pleiotrophin/heparin-binding growth-associated molecule is regulated by chain length and oversulfated structures. J. Biol. Chem. 281, 4894–4902 (2006)

    Article  PubMed  CAS  Google Scholar 

  14. Toida, T., Sakai, S., Akiyama, H., Linhardt, R.J.: Immunological activity of chondroitin sulfate. In: Volpi, N. (ed.) Advances in Pharmacology, vol. 53, pp. 403–415. Elsevier, San Diego (2006)

    Google Scholar 

  15. Uebelhart, D., Knols, K., de Bruin, E.D., Verbruggen, G.: Treatment of knee osteoarthritis with oral chondroitin sulfate. In: Volpi, N. (ed.) Advances in Pharmacology, vol. 53, pp. 523–539. Elsevier, San Diego (2006)

    Google Scholar 

  16. Johnson, Z., Proudfoot, A.E., Handel, T.M.: Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 16, 625–636 (2005)

    Article  PubMed  CAS  Google Scholar 

  17. Kinoshita, A., Sugahara, K.: Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with the fluorophore 2-aminobenzamide by high-performance liquid chromatography: application to disaccharide composition analysis and exo-sequencing of oligosaccharides. Anal. Biochem. 269, 367–378 (1999)

    Article  PubMed  CAS  Google Scholar 

  18. Conrad, H.E.: Degradation of heparan sulfate by nitrous acid. In: Iozzo, R.V. (ed.) Methods in Molecular Biology “Proteoglycan Protocols”, vol. 171, pp. 347–351. Humana Press, Totowa (2001)

    Google Scholar 

  19. Levy, J.A.: The unexpected pleiotropic activities of RANTES. J. Immunol. 182, 3945–3946 (2009)

    Article  PubMed  CAS  Google Scholar 

  20. Farouk, S.S., Rader, D.J., Reilly, M.P., Mehta, N.N.: CXCL12: a new player in coronary disease identified through human genetics. Trends Cardiovasc. Med. 20, 204–209 (2010)

    Article  PubMed  CAS  Google Scholar 

  21. Müller, M., Carter, S., Hofer, M.J., Campbell, I.L.: The chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity—a tale of conflict and conundrum. Neuropathol. Appl. Neurobiol. 36, 368–387 (2010)

    Article  PubMed  Google Scholar 

  22. Mizumoto, S., Sugahara, K.: Glycosaminoglycan chain analysis and characterization (Glycosylation/Epimerization). In: Rédini, F. (ed.) Methods in Molecular Biology, “Proteoglycans: Methods and Protocols”, vol. 836, pp. 99–115. Humana Press, Springer, New York (2012)

    Google Scholar 

  23. Bao, X., Nishimura, S., Mikami, T., Yamada, S., Itoh, N., Sugahara, K.: Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of L-iduronic acid than those from the adult pig brain, exhibit neuritogenic and growth factor-binding activities. J. Biol. Chem. 279, 9765–9776 (2004)

    Article  PubMed  CAS  Google Scholar 

  24. Bitter, T., Muir, H.: A modified uronic acid carbazole reaction. Anal. Biochem. 4, 330–334 (1962)

    Article  PubMed  CAS  Google Scholar 

  25. Imada, K., Oka, H., Kawasaki, D., Miura, N., Sato, T., Ito, A.: Anti-arthritic action mechanisms of natural chondroitin sulfate in human articular chondrocytes and synovial fibroblasts. Biol. Pharm. Bull. 33, 410–414 (2010)

    Article  PubMed  CAS  Google Scholar 

  26. ten Dam, G.B., van de Westerlo, E.M., Purushothaman, A., Stan, R.V., Bulten, J., Sweep, F.C., Massuger, L.F., Sugahara, K., van Kuppevelt, T.H.: Antibody GD3G7 selected against embryonic glycosaminoglycans defines chondroitin sulfate-E domains highly up-regulated in ovarian cancer and involved in VEGF binding. Am. J. Pathol. 171, 1324–1333 (2007)

    Article  PubMed  Google Scholar 

  27. Lyon, M., Deakin, J.A., Rahmoune, H., Fernig, D.G., Nakamura, T., Gallagher, J.T.: Hepatocyte growth factor/scatter factor binds with high affinity to dermatan sulfate. J. Biol. Chem. 273, 271–278 (1998)

    Article  PubMed  CAS  Google Scholar 

  28. Friand, V., Haddad, O., Papy-Garcia, D., Hlawaty, H., Vassy, R., Hamma-Kourbali, Y., Perret, G.Y., Courty, J., Baleux, F., Oudar, O., Gattegno, L., Sutton, A., Charnaux, N.: Glycosaminoglycan mimetics inhibit SDF-1/CXCL12-mediated migration and invasion of human hepatoma cells. Glycobiology 19, 1511–1524 (2009)

    Article  PubMed  CAS  Google Scholar 

  29. Shimazaki, Y., Nagata, I., Ishii, M., Tanaka, M., Marunouchi, T., Hata, T., Maeda, N.: Developmental change and function of chondroitin sulfate deposited around cerebellar Purkinje cells. J. Neurosci. Res. 82, 172–183 (2005)

    Article  PubMed  CAS  Google Scholar 

  30. Ishii, M., Maeda, N.: Spatiotemporal expression of chondroitin sulfate sulfotransferases in the postnatal developing mouse cerebellum. Glycobiology 18, 602–614 (2008)

    Article  PubMed  CAS  Google Scholar 

  31. Conrad, H.E.: Heparin-Binding Proteins. Academic, San Diego (1998)

    Google Scholar 

  32. Zhang, F., McLellan, J.S., Ayala, A.M., Leahy, D.J., Linhardt, R.J.: Kinetic and structural studies on interactions between heparin or heparan sulfate and proteins of the hedgehog signaling pathway. Biochemistry 46, 3933–3941 (2007)

    Article  PubMed  CAS  Google Scholar 

  33. Casu, B.: In: Garg, H.G., Linhardt, R.J., Hales, C.A. (eds.) Structure and Active Domains of Heparin: Chemistry and Biology of Heparin and Heparan Sulfate, pp. 1–28. Elsevier, Oxford (2005)

    Chapter  Google Scholar 

  34. 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  PubMed  CAS  Google Scholar 

  35. Nandini, C.D., Mikami, T., Ohta, M., Itoh, N., Akiyama-Nambu, F., Sugahara, K.: Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish: neuritogenic activity and binding activities toward growth factors and neurotrophic factors. J. Biol. Chem. 279, 50799–50809 (2004)

    Article  PubMed  CAS  Google Scholar 

  36. Li, F., Shetty, A.K., Sugahara, K.: Neuritogenic activity of chondroitin/dermatan sulfate hybrid chains of embryonic pig brain and their mimicry from shark liver: involvement of the pleiotrophin and hepatocyte growth factor signaling pathways. J. Biol. Chem. 282, 2956–2966 (2007)

    Article  PubMed  CAS  Google Scholar 

  37. Hashiguchi, T., Kobayashi, T., Fongmoon, D., Shetty, A.K., Mizumoto, S., Miyamoto, N., Nakamura, T., Yamada, S., Sugahara, K.: Demonstration of the hepatocyte growth factor signaling pathway in the in vitro neuritogenic activity of chondroitin sulfate from ray fish cartilage. Biochim. Biophys. Acta 1810, 406–413 (2011)

    Article  PubMed  CAS  Google Scholar 

  38. Miyata, S., Komatsu, Y., Yoshimura, Y., Taya, C., Kitagawa, H.: Persistent cortical plasticity by upregulation of chondroitin 6-sulfation. Nat. Neurosci. 15, 414–422 (2012)

    Article  PubMed  CAS  Google Scholar 

  39. Fukui, S., Feizi, T., Galustian, C., Lawson, A.M., Chai, W.: Oligosaccharide microarrays for high-throughput detection and specificity assignments of carbohydrate-protein interactions. Nat. Biotechnol. 20, 1011–1017 (2002)

    Article  PubMed  CAS  Google Scholar 

  40. Yamaguchi, K., Tamaki, H., Fukui, S.: Detection of oligosaccharide ligands for hepatocyte growth factor/scatter factor (HGF/SF), keratinocyte growth factor (KGF/FGF-7), RANTES and heparin cofactor II by neoglycolipid microarrays of glycosaminoglycan-derived oligosaccharide fragments. Glycoconj. J. 23, 513–523 (2006)

    Article  PubMed  CAS  Google Scholar 

  41. Li, F., Nandini, C.D., Hattori, T., Bao, X., Murayama, D., Nakamura, T., Fukushima, N., Sugahara, K.: Structure of pleiotrophin- and hepatocyte growth factor-binding sulfated hexasaccharide determined by biochemical and computational approaches. J. Biol. Chem. 285, 27673–27685 (2010)

    Article  PubMed  CAS  Google Scholar 

  42. Maeda, N., He, J., Yajima, Y., Mikami, T., Sugahara, K., Yabe, T.: Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/HB-GAM. J. Biol. Chem. 278, 35805–35811 (2003)

    Article  PubMed  CAS  Google Scholar 

  43. Ito, Y., Hikino, M., Yajima, Y., Mikami, T., Sirko, L., von Holst, A., Faissner, A., Fukui, S., Sugahara, K.: Structural characterization of the epitopes of the monoclonal antibodies 473HD, CS-56 and MO-225 specific for chondroitin sulfate D-type using the oligosaccharide library. Glycobiology 15, 593–603 (2005)

    Article  PubMed  CAS  Google Scholar 

  44. Mitsunaga, C., Mikami, T., Mizumoto, S., Fukuda, J., Sugahara, K.: Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum: Spatiotemporal regulation of the expression of critical disulfated disaccharides by specific sulfotransferases. J. Biol. Chem. 281, 18942–18952 (2006)

    Article  PubMed  CAS  Google Scholar 

  45. Handel, T.M., Johnson, Z., Crown, S.E., Lau, E.K., Proudfoot, A.E.: Regulation of protein function by glycosaminoglycans—as exemplified by chemokines. Annu. Rev. Biochem. 74, 385–410 (2005)

    Article  PubMed  CAS  Google Scholar 

  46. Hileman, R.E., Fromm, J.R., Weiler, J.M., Linhardt, R.J.: Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 20, 156–167 (1998)

    Article  PubMed  CAS  Google Scholar 

  47. Appay, V., Rowland-Jones, S.L.: RANTES: a versatile and controversial chemokine. Trends Immunol 22, 83–87 (2001)

    Article  PubMed  CAS  Google Scholar 

  48. Proudfoot, A.E., Fritchley, S., Borlat, F., Shaw, J.P., Vilbois, F., Zwahlen, C., Trkola, A., Marchant, D., Clapham, P.R., Wells, T.N.: The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity. J. Biol. Chem. 276, 10620–10626 (2001)

    Article  PubMed  CAS  Google Scholar 

  49. Martin, L., Blanpain, C., Garnier, P., Wittamer, V., Parmentier, M., Vita, C.: Structural and functional analysis of the RANTES-glycosaminoglycans interactions. Biochemistry 40, 6303–6318 (2001)

    Article  PubMed  CAS  Google Scholar 

  50. Farber, J.M.: A macrophage mRNA selectively induced by gamma-interferon encodes a member of the platelet factor 4 family of cytokines. Proc. Natl. Acad. Sci. U. S. A. 87, 5238–5242 (1990)

    Article  PubMed  CAS  Google Scholar 

  51. Sgadari, C., Farber, J.M., Angiolillo, A.L., Liao, F., Teruya-Feldstein, J., Burd, P.R., Yao, L., Gupta, G., Kanegane, C., Tosato, G.: Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood 89, 2635–2643 (1997)

    PubMed  CAS  Google Scholar 

  52. Schwartz, G.N., Liao, F., Gress, R.E., Farber, J.M.: Suppressive effects of recombinant human monokine induced by IFN-γ (rHuMig) chemokine on the number of committed and primitive hemopoietic progenitors in liquid cultures of CD34+ human bone marrow cells. J. Immunol. 159, 895–904 (1997)

    PubMed  CAS  Google Scholar 

  53. Oberlin, E., Amara, A., Bachelerie, F., Bessia, C., Virelizier, J.L., Arenzana-Seisdedos, F., Schwartz, O., Heard, J.M., Clark-Lewis, I., Legler, D.F., Loetscher, M., Baggiolini, M., Moser, B.: The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382, 833–835 (1996)

    Article  PubMed  CAS  Google Scholar 

  54. Omata, T., Segawa, Y., Itokazu, Y., Inoue, N., Tanaka, Y.: Effects of chondroitin sulfate-C on bradykinin-induced proteoglycan depletion in rats. Arzneimittelforschung 49, 577–581 (1999)

    PubMed  CAS  Google Scholar 

  55. Beren, J., Hill, S.L., Diener-West, M., Rose, N.R.: Effect of pre-loading oral glucosamine HCl/chondroitin sulfate/manganese ascorbate combination on experimental arthritis in rats. Exp. Biol. Med. 226, 144–151 (2001)

    CAS  Google Scholar 

  56. Kahan, A., Uebelhart, D., De Vathaire, F., Delmas, P.D., Reginster, J.Y.: Long-term effects of chondroitins 4 and 6 sulfate on knee osteoarthritis: the study on osteoarthritis progression prevention, a two-year, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 60, 524–533 (2009)

    Article  PubMed  CAS  Google Scholar 

  57. Clegg, D.O., Reda, D.J., Harris, C.L., Klein, M.A., O’Dell, J.R., Hooper, M.M., Bradley, J.D., Bingham 3rd, C.O., Weisman, M.H., Jackson, C.G., Lane, N.E., Cush, J.J., Moreland, L.W., Schumacher Jr., H.R., Oddis, C.V., Wolfe, F., Molitor, J.A., Yocum, D.E., Schnitzer, T.J., Furst, D.E., Sawitzke, A.D., Shi, H., Brandt, K.D., Moskowitz, R.W., Williams, H.J.: Glucosamine, chondroitin sulfate, and the two in combination for painful knee osteoarthritis. N. Engl. J. Med. 354, 795–808 (2006)

    Article  PubMed  CAS  Google Scholar 

  58. Cho, S.Y., Sim, J.S., Jeong, S.C., Chang, S.Y., Choi, D.W., Toida, T., Kim, Y.S.: Effects of low molecular weight chondroitin sulfate on type II collagen-induced arthritis in DBA/1 J mice. Biol. Pharm. Bull. 27, 47–51 (2004)

    Article  PubMed  CAS  Google Scholar 

  59. Lamari, F.N., Theocharis, A.D., Asimakopoulou, A.P., Malavaki, C.J., Karamanos, N.K.: Metabolism and biochemical/physiological roles of chondroitin sulfates: analysis of endogenous and supplemental chondroitin sulfates in blood circulation. Biomed. Chromatogr. 20, 539–550 (2006)

    Article  PubMed  CAS  Google Scholar 

  60. Jain, A., Gupta, Y., Jain, K.: Perspectives of biodegradable natural polysaccharides for site-specific drug delivery to the colon. J. Pharm. Pharm. Sci. 10, 86–128 (2007)

    PubMed  CAS  Google Scholar 

  61. Theoharides, T.C., Patra, P., Boucher, W., Letourneau, R., Kempuraj, D., Chiang, G., Jeudy, S., Hasse, L., Athanasiou, A.: Chondroitin sulphate inhibits connective tissue mast cells. Br. J. Pharmacol. 131, 1039–1049 (2000)

    Article  PubMed  CAS  Google Scholar 

  62. McCarty, M.F., Russell, A.L., Seed, M.P.: Sulfated glycosaminoglycans and glucosamine may synergize in promoting synovial hyaluronic acid synthesis. Med. Hypotheses 54, 798–802 (2000)

    Article  PubMed  CAS  Google Scholar 

  63. Sakai, S., Akiyama, H., Sato, Y., Yoshioka, Y., Linhardt, R.J., Goda, Y., Maitani, T., Toida, T.: Chondroitin sulfate intake inhibits the IgE-mediated allergic response by down-regulating Th2 responses in mice. J. Biol. Chem. 281, 19872–19880 (2006)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by Grants-in-aid for Scientific Research on Innovative Areas (24110501) (to K.S.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT), Japan–Thailand Research Cooperative Program (to K. S.), Young Scientists (B) 23790066 (to S. M.) from the Japan Society for the Promotion of Science (JSPS), and the endowment from Zeria Pharmaceutical Co., Ltd.

Author information

Author notes

  1. Duriya Fongmoon

    Present address: Department of Medical Services, Ministry of Public Health, The Lampang Cancer Hospital, Lampang, 52000, Thailand

Authors and Affiliations

  1. Laboratory of Proteoglycan Signaling and Therapeutics, Frontier Research Center for Post-Genomic Science and Technology, Hokkaido University Graduate School of Life Science, West-11, North-21, Kita-ku, Sapporo, Hokkaido, 001-0021, Japan

    Shuji Mizumoto, Duriya Fongmoon & Kazuyuki Sugahara

Authors
  1. Shuji Mizumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duriya Fongmoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuyuki Sugahara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazuyuki Sugahara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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, 619–632 (2013). https://doi.org/10.1007/s10719-012-9463-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-012-9463-5

Keywords

Search

Navigation