Partially acetylated chitooligosaccharides bind to YKL-40 and stimulate growth of human osteoarthritic chondrocytes

Biochemical and Biophysical Research Communications

Volumn 434, Issue 2, 2013, Pages 298-304

  Einarsson, Jon M ^a   Bahrke, Sven ^b   Sigurdsson, Bjarni Thor ^c   Ng, Chuen How ^a   Petersen, Petur Henry ^c   Sigurjonsson, Olafur E ^d,e   Jonsson, Halldor ^d   Gislason, Johannes ^a   Thormodsson, Finnbogi R ^a,c   Peter, Martin G ^b  

^a Genis hf ^*  (Iceland)

^b UNIVERSITY OF POTSDAM   (Germany)

^c UNIVERSITY OF ICELAND   (Iceland)

^d LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^e REYKJAVIK UNIVERSITY   (Iceland)

Author keywords

Cell culture; Chitolectin; Chitooligosaccharides; Chondrocytes; High affinity binding; Rheumatoid arthritis; YKL 40

Indexed keywords

CHITINASE 3 LIKE PROTEIN 1; CHITOSAN; CHITOSE OLIGOSACCHARIDE; N ACETYLGLUCOSAMINE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARTILAGE CELL; CELL COUNT; CELL GROWTH; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRAFILTRATION;

ACETYLATION; ACETYLGLUCOSAMINE; ADIPOKINES; CELL COUNT; CELL SURVIVAL; CELLS, CULTURED; CHITIN; CHONDROCYTES; CHROMATOGRAPHY, GEL; COLLAGEN TYPE II; CULTURE MEDIA; HUMANS; LECTINS; OLIGOSACCHARIDES; OSTEOARTHRITIS; POLYMERIZATION; PRIMARY CELL CULTURE; PROTEIN BINDING; TRISACCHARIDES;

EID: 84877058497     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.02.122     Document Type: Article

References (43)

1. Denuziere A., Ferrier D., Damour O., et al. Domard, chitosan-chondroitin sulfate and chitosan-hyaluronate polyelectrolyte complexes: biological properties. Biomaterials 1998, 19:1275-1285.
2. Muzzarelli R.A.A. Chitins and chitosans for the repair of wounded skin, nerve, cartilage and bone. Carbohydr. Polym. 2009, 76:167-182.
3. Suzuki K., Mikami T., Okawa Y., et al. Antitumor effect of hexa-N-acetylchitohexaose and chitohexaose. Carbohydr. Res. 1986, 151:403-408.
4. Kim S.K., Rajapakse N. Enzymatic production and biological activities of chitosan oligosaccharides (COS): a review. Carbohydr. Polym. 2005, 62:357-368.
5. Yin H., Du Y.G., Zhang J.Z. Low molecular weight and oligomeric chitosans and their bioactivities. Curr. Top. Med. Chem. 2009, 9:1546-1559.
6. Li X.B., Roseman S. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc. Natl. Acad. Sci. USA 2004, 101:627-631.
7. Meibom K.L., Li X.B.B., Nielsen A.T., et al. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 2004, 101:2524-2529.
8. Vander P., Vårum K.M., Domard A., et al. Comparison of the ability of partially N-acetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol. 1998, 118:1353-1359.
9. Petutschnig E.K., Jones A.M.E., Serazetdinova L., et al. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 2010, 285:28902-28911.
10. Hakala B.E., White C., Recklies A.D. Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J. Biol. Chem. 1993, 268:25803-25810.
11. Renkema G.H., Boot R.G., Au F.L., et al. Chitotriosidase, a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologs of family 18 glycosyl hydrolases secreted by human macrophages. Eur. J. Biochem. 1998, 251:504-509.
12. Houston D.R., Recklies A.D., Krupa J.C., et al. Structure and ligand-induced conformational change of the 39-kDa glycoprotein from human articular chondrocytes. J. Biol. Chem. 2003, 278:30206-30212.
13. Fusetti F., Pijning T., Kalk K.H., et al. Crystal structure and carbohydrate-binding properties of the human cartilage glycoprotein-39. J. Biol. Chem. 2003, 278:37753-37760.
14. Bigg H.F., Wait R., Rowan A.D., et al. The mammalian chitinase-like lectin, YKL-40, binds specifically to type I collagen and modulates the rate of type I collagen fibril formation. J. Biol. Chem. 2006, 281:21082-21095.
15. Volck B., Price P.A., Johansen J.S., et al. YKL-40, a mammalian member of the chitinase family, is a matrix protein of specific granules in human neutrophils. Proc. Assoc. Am. Phys. 1998, 110:351-360.
16. Volck B., Ostergaard K., Johansen J.S., et al. The distribution of YKL-40 in osteoarthritic and normal human articular cartilage. Scand. J. Rheumatol. 1999, 28:171-179.
17. Volck B., Johansen J.S., Stoltenberg M., et al. Studies on YKL-40 in knee joints of patients with rheumatoid arthritis and osteoarthritis. Involvement of YKL-40 in the joint pathology. Osteoarthritis Cartilage 2001, 9:203-214.
18. Connor J., Dodds R., Emery J., et al. Human cartilage glycoprotein 39 (HC gp-39) mRNA expression in adult and fetal chondrocytes, osteoblasts and osteocytes by in-situ hybridization. Osteoarthritis Cartilage 2000, 8:87-95.
19. Johansen J.S., Kirwan J.R., Price P.A., et al. Serum YKL-40 concentrations in patients with early rheumatoid arthritis: relation to joint destruction. Scand. J. Rheumatol. 2001, 30:297-304.
20. Vignon E. Is glycoprotein YKL40 a new marker for joint disorders?. Joint Bone Spine 2001, 68:454-456.
21. Huang K., Wu L.D. YKL-40: a potential biomarker for osteoarthritis. J. Int. Med. Res. 2009, 37:18-24.
22. Recklies A.D., White C., Ling H. The chitinase 3-like protein human cartilage glycoprotein 39 (HC-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase- and protein kinase beta-mediated signalling pathways. Biochem. J. 2002, 365:119-126.
23. De Ceuninck F., Gaufillier S., Bonnaud A., et al. YKL-40 (cartilage gp-39) induces proliferative events in cultured chondrocytes and synoviocytes and increases glycosaminoglycan synthesis in chondrocytes. Biochem. Biophys. Res. Commun. 2001, 285:926-931.
24. Badariotti F., Kypriotou M., Lelong C., et al. The phylogenetically conserved molluscan chitinase-like protein 1 (Cg-Clp1), homologue of human HC-gp39, stimulates proliferation and regulates synthesis of extracellular matrix components of mammalian chondrocytes. J. Biol. Chem. 2006, 281:29583-29596.
25. Fusetti F., von Moeller H., Houston D., et al. Structure of human chitotriosidase - implications for specific inhibitor design and function of mammalian chitinase-like lectins. J. Biol. Chem. 2002, 277:25537-25544.
26. Zaheer-ul-Haq P., Dalal N.N., Aronson, et al. Family 18 chitolectins: comparison of MGP40 and HUMGP39. Biochem. Biophys. Res. Commun. 2007, 359:221-226.
27. S. Bahrke, Mass spectrometric analysis of chitooligosaccharides and their interaction with proteins. PhD Thesis, University of Potsdam, Germany. 2007. http://opus.kobv.de/ubp/volltexte/2008/2017/.
28. Haebel S., Bahrke S., Peter M.G. Quantitative sequencing of complex mixtures of heterochitooligosaccharides by vMALDI-Linear ion trap mass spectrometry. Anal. Chem. 2007, 79:5557-5566.
29. van Aalten D.M.F., Komander D., Synstad B., et al. Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc. Natl. Acad. Sci. USA 2001, 98:8979-8984.
30. Fukamizo T., Sasaki C., Schelp E., et al. Kinetic properties of chitinase-1 from the fungal pathogen Coccidioides immitis. Biochemistry 2001, 40:2448-2454.
31. Sasaki C., Yokoyama A., Itoh Y., et al. Comparative study of the reaction mechanism of family 18 chitinases from plants and microbes. J. Biochem. 2002, 131:557-564.
32. Taira T., Fujiwara M., Dennhart N., et al. Transglycosylation reaction catalyzed by a class V chitinase from cycad, Cycas revoluta: a study involving site-directed mutagenesis, HPLC, and real-time ESI-MS. Biochim. Biophys. Acta 1804, 2010:668-675.
33. Ohnuma T., Fukamizo T. Chitin/chitosan oligosaccharides: effective substrates for functional analysis of chitinases/chitosanases. Chitin, chitosan, oligosaccharides and their derivatives 2010, 295-324. CRC Press, Boca Raton, FL, USA. S.-K. Kim (Ed.).
34. Tsuruha J.-I., Masuko-Hongo K., Kato T., et al. Autoimmunity against YKL-39, a human cartilage derived protein, in patients with osteoarthritis. J. Rheumatol. 2002, 29:1459-1466.
35. Du H., Masuko-Hongo K., Nakamura H., et al. The prevalence of autoantibodies against cartilage intermediate layer protein, YKL-39, osteopontin, and cyclic citrullinated peptide in patients with early-stage knee osteoarthritis: evidence of a variety of autoimmune processes. Rheumatol. Int. 2005, 26:35-41.
36. Knorr T., Obermayr F., Bartnik E., et al. YKL-39 (chitinase 3-like protein 2), but not YKL-40 (chitinase 3-like protein 1), is up regulated in osteoarthritic chondrocytes. Ann. Rheum. Dis. 2003, 62:995-998.
37. Steck E., Breit S., Breusch S.J., et al. Enhanced expression of the human chitinase 3-like 2 gene (YKL-39) but not chitinase 3-like 1 gene (YKL-40) in osteoarthritic cartilage. Biochem. Biophys. Res. Commun. 2002, 299:109-115.
38. Boot R.G., Blommaart E.F.C., Swart E., et al. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 2001, 276:6770-6778.
39. Hu B., Trinh K., Figueira W.F., et al. Isolation and sequence of a novel human chondrocyte protein related to mammalian members of the chitinase protein family. J. Biol. Chem. 1996, 271:19415-19420.
40. Schimpl M., Rush C.L., Betou M., et al. Human YKL-39 is a pseudo-chitinase with retained chitooligosaccharide-binding properties. Biochem. J. 2012, 446:149-157.
41. Letzel M.C., Synstad B., Eijsink V.G.H., et al. Libraries of chito-oligosaccharides of mixed acetylation patterns and their interactions with chitinases. Adv. Chitin Sci. 2000, 4:545-552.
42. Cederkvist F., Zamfir A.D., Bahrke S., et al. Identification of a high-affinity-binding oligosaccharide by (+) nanoelectrospray quadrupole time-of-flight tandem mass spectrometry of a noncovalent enzyme-ligand complex. Angew. Chem., Int. Ed. 2006, 45:2429-2434.
43. Cederkvist F.H., Parmer M.P., Varum K.M., et al. Inhibition of a family 18 chitinase by chitooligosaccharides. Carbohydr. Polym. 2008, 74:41-49.