Chondroitin-6-sulfate attenuates inflammatory responses in murine macrophages via suppression of NF-κB nuclear translocation

Acta Biomaterialia

Volumn 10, Issue 6, 2014, Pages 2684-2692

  Tan, Guak Kim ^a,b   Tabata, Yasuhiko ^a  

^a KYOTO UNIVERSITY   (Japan)

^b SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

Anti inflammatory effects; Chondroitin 6 sulfate; Glycosaminoglycans; Inflammation; Macrophages

Indexed keywords

GLYCOPROTEINS; HYALURONIC ACID; MACROPHAGES; NITRIC OXIDE; SULFUR COMPOUNDS;

ANTI-INFLAMMATORY EFFECTS; CHONDROITIN; CHONDROITIN-6-SULPHATE; GLYCOSAMINOGLYCANS; INFLAMMATORY MEDIATORS; INFLAMMATORY RESPONSE; LIPOPOLYSACCHARIDES; MURINE MACROPHAGES; NUCLEAR TRANSLOCATIONS; SULPHATES;

PATHOLOGY;

ARGINASE; CHONDROITIN 6 SULFATE; GAMMA INTERFERON; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; HYALURONIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; CHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMOBILIZATION; IMMUNOMODULATION; INCUBATION TIME; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WOUND HEALING; ANIMAL; BAGG ALBINO MOUSE; CELL NUCLEUS; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

MURINAE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CHONDROITIN SULFATES; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; NF-KAPPA B;

EID: 84899647711     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.02.025     Document Type: Article

References (64)

1. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008;454:428-35.
2. Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 2011;13:e23.
3. Glauser MP, Zanetti G, Baumgartner JD, Cohen J. Septic shock: pathogenesis. Lancet 1991;338:732-6.
4. Ishihara K, Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002;13:357-68.
5. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004;25:677-86.
6. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 1999;274:10689-92.
7. Biswas SK, Lewis CE. NF-kappaB as a central regulator of macrophage function in tumors. J Leukoc Biol 2010;88:877-84.
8. Modolell M, Corraliza IM, Link F, Soler G, Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 1995;25:1101-4.
9. Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 1992;176:287-92.
10. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010;32:593-604.
11. Porcheray F, Viaud S, Rimaniol AC, Leone C, Samah B, Dereuddre-Bosquet N, et al. Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol 2005;142:481-9.
12. Esko JDKK, Lindahl U. Proteoglycans and Sulfated Glycosaminoglycans. New York: Cold Spring Harbor Laboratory Press; 2009.
13. Marshall LJ, Ramdin LS, Brooks T. PC DP, Shute JK. Plasminogen activator inhibitor-1 supports IL-8-mediated neutrophil transendothelial migration by inhibition of the constitutive shedding of endothelial IL-8/heparan sulfate/ syndecan-1 complexes. J Immunol 2003;171:2057-65.
14. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002;195:99-111.
15. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-9.
16. Flanagan TC, Wilkins B, Black A, Jockenhoevel S, Smith TJ, Pandit AS. A collagen-glycosaminoglycan co-culture model for heart valve tissue engineering applications. Biomaterials 2006;27:2233-46.
17. Zhong S, Teo WE, Zhu X, Beuerman R, Ramakrishna S, Yung LY. Formation of collagen-glycosaminoglycan blended nanofibrous scaffolds and their biological properties. Biomacromolecules 2005;6:2998-3004.
18. van Susante JLC, Pieper J, Buma P, van Kuppevelt TH, van Beuningen H, van Der Kraan PM, et al. Linkage of chondroitin-sulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials 2001;22:2359-69.
19. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: hostassociated molecular patterns for initiation and modulation of inflammation. FASEB J 2006;20:9-22.
20. Kahan A, Uebelhart D, De Vathaire F, Delmas PD, Reginster JY. 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 2009;60:524-33.
21. Michel BA, Stucki G, Frey D, De Vathaire F, Vignon E, Bruehlmann P, et al. Chondroitins 4 and 6 sulfate in osteoarthritis of the knee: a randomized, controlled trial. Arthritis Rheum 2005;52:779-86.
22. Jomphe C, Gabriac M, Hale TM, Heroux L, Trudeau LE, Deblois D, et al. Chondroitin sulfate inhibits the nuclear translocation of nuclear factor-kappaB in interleukin-1beta-stimulated chondrocytes. Basic Clin Pharmacol Toxicol 2008;102:59-65.
23. Alvarez-Soria ML, Santilana J, Calvo E, Egido J, Herrero-Beaumont G. Differential anticatabolic profile of glucosamine sulfate versus other antiosteoarthritic drugs on human osteoarthritic chondrocytes and synovial fibroblast in culture. Osteoarthritis and Cartilage 2005;13:S153 [Abstract].
24. Wrenshall LE, Stevens RB, Cerra FB, Platt JL. Modulation of macrophage and B cell function by glycosaminoglycans. J Leukoc Biol 1999;66:391-400.
25. Bassleer CT, Combal JP, Bougaret S, Malaise M. Effects of chondroitin sulfate and interleukin-1 beta on human articular chondrocytes cultivated in clusters. Osteoarthritis Cartilage 1998;6:196-204.
26. Chen WC, Yao CL, Chu IM, Wei YH. Compare the effects of chondrogenesis by culture of human mesenchymal stem cells with various type of the chondroitin sulfate C. J Biosci Bioeng 2011;111:226-31.
27. Tan GK, Dinnes DL, Butler LN, Cooper-White JJ. Interactions between meniscal cells and a self assembled biomimetic surface composed of hyaluronic acid, chitosan and meniscal extracellular matrix molecules. Biomaterials 2010;31:6104-18.
28. Fernandez-Botran R, Yan J, Justus DE. Binding of interferon gamma by glycosaminoglycans: a strategy for localization and/or inhibition of its activity. Cytokine 1999;11:313-25.
29. Keuren JF, Wielders SJ, Willems GM, Morra M, Cahalan L, Cahalan P, et al. Thrombogenicity of polysaccharide-coated surfaces. Biomaterials 2003;24:1917-24.
30. Ando I, Tsukumo Y, Wakabayashi T, Akashi S, Miyake K, Kataoka T, et al. Safflower polysaccharides activate the transcription factor NF-kappa B via Toll-like receptor 4 and induce cytokine production by macrophages. Int Immunopharmacol 2002;2:1155-62.
31. Corraliza IM, Campo ML, Soler G, Modolell M. Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 1994;174:231-5.
32. Kolb H, Kolb-Bachofen V. Nitric oxide in autoimmune disease: cytotoxic or regulatory mediator? Immunol Today 1998;19:556-61.
33. Wrenshall LE, Carlson A, Cerra FB, Platt JL. Modulation of cytolytic T cell responses by heparan sulfate. Transplantation 1994;57:1087-94.
34. Bussini S, Meda L, Scarpini E, Clementi E, Conti G, Tiriticco M, et al. Heparan sulfate proteoglycan induces the production of NO and TNF-alpha by murine microglia. Immun Ageing 2005;2:11.
35. Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, et al. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 1998;4:691-7.
36. Noble PW. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol 2002;21:25-9.
37. Holmer E, Kurachi K, Soderstrom G. The molecular-weight dependence of the rate-enhancing effect of heparin on the inhibition of thrombin, factor Xa, factor IXa, factor XIa, factor XIIa and kallikrein by antithrombin. Biochem J 1981;193:395-400.
38. Ogamo A, Nagai A, Nagasawa K. Binding of heparin fractions and other polysulfated polysaccharides to plasma fibronectin: effects of molecular size and degree of sulfation of polysaccharides. Biochim Biophys Acta 1985;841:30-41.
39. Nikitovic D, Zafiropoulos A, Tzanakakis GN, Karamanos NK, Tsatsakis AM. Effects of glycosaminoglycans on cell proliferation of normal osteoblasts and human osteosarcoma cells depend on their type and fine chemical compositions. Anticancer Res 2005;25:2851-6.
40. Campo GM, Avenoso A, Campo S, D'Ascola A, Traina P, Calatroni A. Chondroitin-4-sulphate inhibits NF-kB translocation and caspase activation in collagen-induced arthritis in mice. Osteoarthritis Cartilage 2008;16:1474-83.
41. Wang K, Luo Y. Defined surface immobilization of glycosaminoglycan molecules for probing and modulation of cell-material interactions. Biomacromolecules 2013;14:2373-82.
42. Jin M, Iwamoto T, Yamada K, Satsu H, Totsuka M, Shimizu M. Effects of chondroitin sulfate and its oligosaccharides on toll-like receptor-mediated IL-6 secretion by macrophage-like J774.1 cells. Biosci Biotechnol Biochem 2011;75:1283-9.
43. Means TK, Pavlovich RP, Roca D, Vermeulen MW, Fenton MJ. Activation of TNFalpha transcription utilizes distinct MAP kinase pathways in different macrophage populations. J Leukoc Biol 2000;67:885-93.
44. Neta R, Sayers TJ, Oppenheim JJ. Relationship of TNF to interleukins. Immunol Ser 1992;56:499-566.
45. Matsuno H, Yudoh K, Katayama R, Nakazawa F, Uzuki M, Sawai T, et al. The role of TNF-alpha in the pathogenesis of inflammation and joint destruction in rheumatoid arthritis (RA): a study using a human RA/SCID mouse chimera. Rheumatology (Oxford) 2002;41:329-37.
46. Vassalli P. The pathophysiology of tumor necrosis factor. Annu Rev Immunol 1992;10:411-52.
47. Rudolph SJ, Weinberg DI, McCabe RP. Long-term durability of Crohn's disease treatment with infliximab. Dig Dis Sci 2008;53:1033-41.
48. Feldmann M, Maini RN. Anti-TNF-alpha therapy of rheumatoid arthritis: what have we learned? Ann Rev Immunol 2001;19:163-96.
49. Fitzgerald O, Chandran V. Update on biomarkers in psoriatic arthritis: a report from the GRAPPA 2010 annual meeting. J Rheumatol 2012;39:427-30.
50. Kaneko S, Satoh T, Chiba J, Ju C, Inoue K, Kagawa J. Interleukin-6 and interleukin-8 levels in serum and synovial fluid of patients with osteoarthritis. Cytokines Cell Mol Ther 2000;6:71-9.
51. Richette P, Poitou C, Garnero P, Vicaut E, Bouillot JL, Lacorte JM, et al. Benefits of massive weight loss on symptoms, systemic inflammation and cartilage turnover in obese patients with knee osteoarthritis. Ann Rheum Dis 2011;70:139-44.
52. Larsson PT, Hallerstam S, Rosfors S, Wallen NH. Circulating markers of inflammation are related to carotid artery atherosclerosis. Int Angiol 2005;24:43-51.
53. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001;286:327-34.
54. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991;147:3815-22.
55. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991;174:1209-20.
56. Chmiel JF, Konstan MW, Knesebeck JE, Hilliard JB, Bonfield TL, Dawson DV, et al. IL-10 attenuates excessive inflammation in chronic Pseudomonas infection in mice. Am J Respir Crit Care Med 1999;160:2040-7.
57. Liechty KW, Kim HB, Adzick NS, Crombleholme TM. Fetal wound repair results in scar formation in interleukin-10-deficient mice in a syngeneic murine model of scarless fetal wound repair. J Pediatr Surg 2000;35:866-72. discussion 72-73.
58. Saadane A, Soltys J, Berger M. Role of IL-10 deficiency in excessive nuclear factor-kappaB activation and lung inflammation in cystic fibrosis transmembrane conductance regulator knockout mice. J Allergy Clin Immunol 2005;115:405-11.
59. El Gazzar M. HMGB1 modulates inflammatory responses in LPS-activated macrophages. Inflamm Res 2007;56:162-7.
60. Jin M, Iwamoto T, Yamada K, Satsu H, Totsuka M, Shimizu M. Disaccharide derived from chondroitin sulfate A suppressed CpG-induced IL-6 secretion in macrophage-like J774.1 cells. Cytokine 2010;51:53-9.
61. Mori M, Gotoh T. Regulation of nitric oxide production by arginine metabolic enzymes. Biochem Biophys Res Commun 2000;275:715-9.
62. Campo GM, Avenoso A, Campo S, Traina P, D'Ascola A, Calatroni A. Glycosaminoglycans reduced inflammatory response by modulating toll-like receptor-4 in LPS-stimulated chondrocytes. Arch Biochem Biophys 2009;491:7-15.
63. Rolls A, Cahalon L, Bakalash S, Avidan H, Lider O, Schwartz M. A sulfated disaccharide derived from chondroitin sulfate proteoglycan protects against inflammation-associated neurodegeneration. FASEB J 2006;20:547-9.
64. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol 2005;175:342-9.