Depletion of gangliosides enhances cartilage degradation in mice

Osteoarthritis and Cartilage

Volumn 22, Issue 2, 2014, Pages 313-322

  Sasazawa, F ^a   Onodera, T ^a   Yamashita, T ^b   Seito, N ^a   Tsukuda, Y ^a   Fujitani, N ^c   Shinohara, Y ^c   Iwasaki, N ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AZABU UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Gangliosides; Glycosphingolipids; Interleukin 1 ; Mice; Osteoarthritis

Indexed keywords

AGGRECANASE 2; COLLAGENASE 3; GANGLIOSIDE; GANGLIOSIDE GM3; GLYCOSPHINGOLIPID; INTERLEUKIN 1ALPHA;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARTILAGE CELL; CARTILAGE DEGENERATION; IN VIVO STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; UPREGULATION;

GANGLIOSIDES; GLYCOSPHINGOLIPIDS; INTERLEUKIN-1Α; MICE; OSTEOARTHRITIS;

ADAM PROTEINS; AGING; ANIMALS; APOPTOSIS; ARTHRITIS, EXPERIMENTAL; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; DISEASE PROGRESSION; GANGLIOSIDES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTERLEUKIN-1ALPHA; MALE; MATRIX METALLOPROTEINASE 3; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOARTHRITIS; TISSUE CULTURE TECHNIQUES;

EID: 84893778823     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2013.11.015     Document Type: Article

References (49)

1. van der Kraan P.M. Osteoarthritis year 2012 in review: biology. Osteoarthritis Cartilage 2012, 20:1447-1450.
2. Kannu P., Bateman J.F., Belluoccio D., Fosang A.J., Savarirayan R. Employing molecular genetics of chondrodysplasias to inform the study of osteoarthritis. Arthritis Rheum 2009, 60:325-334.
3. Qvist P., Bay-Jensen A.C., Christiansen C., Dam E.B., Pastoureau P., Karsdal M.A. The disease modifying osteoarthritis drug (DMOAD): is it in the horizon?. Pharmacol Res 2008, 58:1-7.
4. Hakomori S. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. JBiol Chem 1990, 265:18713-18716.
5. Regina Todeschini A., Hakomori S.I. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim Biophys Acta 2008, 1780:421-433.
6. Seito N., Yamashita T., Tsukuda Y., Matsui Y., Urita A., Onodera T., et al. Interruption of glycosphingolipid synthesis enhances osteoarthritis development in mice. Arthritis Rheum 2012, 64:2579-2588.
7. Yamashita T., Wada R., Sasaki T., Deng C., Bierfreund U., Sandhoff K., et al. Avital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci U S A 1999, 96:9142-9147.
8. Yamashita T., Wada R., Proia R.L. Early developmental expression of the gene encoding glucosylceramide synthase, the enzyme controlling the first committed step of glycosphingolipid synthesis. Biochim Biophys Acta 2002, 1573:236-240.
9. Hakomori S.I. Structure and function of glycosphingolipids and sphingolipids: recollections and future trends. Biochim Biophys Acta 2008, 1780:325-346.
10. David M.J., Portoukalian J., Rebbaa A., Vignon E., Carret J.P., Richard M. Characterization of gangliosides from normal and osteoarthritic human articular cartilage. Arthritis Rheum 1993, 36:938-942.
11. David M.J., Hellio M.P., Portoukalian J., Richard M., Caton J., Vignon E. Gangliosides from normal and osteoarthritic joints. JRheumatol Suppl 1995, 43:133-135.
12. Tsukuda Y., Iwasaki N., Seito N., Kanayama M., Fujitani N., Shinohara Y., et al. Ganglioside GM3 has an essential role in the pathogenesis and progression of rheumatoid arthritis. PLoS One 2012, 7:e40136.
13. Yamashita T., Hashiramoto A., Haluzik M., Mizukami H., Beck S., Norton A., et al. Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc Natl Acad Sci U S A 2003, 100:3445-3449.
14. Obernier J.A., Baldwin R.L. Establishing an appropriate period of acclimatization following transportation of laboratory animals. ILAR J 2006, 47:364-369.
15. Matsui Y., Iwasaki N., Kon S., Takahashi D., Morimoto J., Denhardt D.T., et al. Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum 2009, 60:2362-2371.
16. Stoop R., van der Kraan P.M., Buma P., Hollander A.P., Billinghurst R.C., Poole A.R., et al. Type II collagen degradation in spontaneous osteoarthritis in C57Bl/6 and BALB/c mice. Arthritis Rheum 1999, 42:2381-2389.
17. Kamekura S., Hoshi K., Shimoaka T., Chung U., Chikuda H., Yamada T., et al. Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthritis Cartilage 2005, 13:632-641.
18. Clements K.M., Price J.S., Chambers M.G., Visco D.M., Poole A.R., Mason R.M. Gene deletion of either interleukin-1beta, interleukin-1beta-converting enzyme, inducible nitric oxide synthase, or stromelysin 1 accelerates the development of knee osteoarthritis in mice after surgical transection of the medial collateral ligament and partial medial meniscectomy. Arthritis Rheum 2003, 48:3452-3463.
19. Mankin H.J., Dorfman H., Lippiello L., Zarins A. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. JBone Joint Surg Am 1971, 53:523-537.
20. Mankin H.J. Biochemical and metabolic abnormalities in osteoarthritic human cartilage. Fed Proc 1973, 32:1478-1480.
21. Glasson S.S., Askew R., Sheppard B., Carito B., Blanchet T., Ma H.L., et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005, 434:644-648.
22. Stanton H., Golub S.B., Rogerson F.M., Last K., Little C.B., Fosang A.J. Investigating ADAMTS-mediated aggrecanolysis in mouse cartilage. Nat Protoc 2011, 6:388-404.
23. Hashimoto S., Takahashi K., Ochs R.L., Coutts R.D., Amiel D., Lotz M. Nitric oxide production and apoptosis in cells of the meniscus during experimental osteoarthritis. Arthritis Rheum 1999, 42:2123-2131.
24. Gosset M., Berenbaum F., Thirion S., Jacques C. Primary culture and phenotyping of murine chondrocytes. Nat Protoc 2008, 3:1253-1260.
25. Salvat C., Pigenet A., Humbert L., Berenbaum F., Thirion S. Immature murine articular chondrocytes in primary culture: a new tool for investigating cartilage. Osteoarthritis Cartilage 2005, 13:243-249.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
27. Urita A., Matsuhashi T., Onodera T., Nakagawa H., Hato M., Amano M., et al. Alterations of high-mannose type N-glycosylation in human and mouse osteoarthritis cartilage. Arthritis Rheum 2011, 63:3428-3438.
28. Fujitani N., Takegawa Y., Ishibashi Y., Araki K., Furukawa J., Mitsutake S., et al. Qualitative and quantitative cellular glycomics of glycosphingolipids based on rhodococcal endoglycosylceramidase-assisted glycan cleavage, glycoblotting-assisted sample preparation, and matrix-assisted laser desorption ionization tandem time-of-flight mass spectrometry analysis. JBiol Chem 2011, 286:41669-41679.
29. Ito M., Yamagata T. Purification and characterization of glycosphingolipid-specific endoglycosidases (endoglycoceramidases) from a mutant strain of Rhodococcus sp. Evidence for three molecular species of endoglycoceramidase with different specificities. JBiol Chem 1989, 264:9510-9519.
30. Sokolove J., Lepus C.M. Role of inflammation in the pathogenesis of osteoarthritis: latest findings and interpretations. Ther Adv Musculoskelet Dis 2013, 5:77-94.
31. Scanzello C.R., Goldring S.R. The role of synovitis in osteoarthritis pathogenesis. Bone 2012, 51:249-257.
32. Ohmi Y., Tajima O., Ohkawa Y., Yamauchi Y., Sugiura Y., Furukawa K. Gangliosides are essential in the protection of inflammation and neurodegeneration via maintenance of lipid rafts: elucidation by a series of ganglioside-deficient mutant mice. JNeurochem 2011, 116:926-935.
33. Lim S.T., Esfahani K., Avdoshina V., Mocchetti I. Exogenous gangliosides increase the release of brain-derived neurotrophic factor. Neuropharmacology 2011, 60:1160-1167.
34. Liang S., Wang M., Tapping R.I., Stepensky V., Nawar H.F., Triantafilou M., et al. Ganglioside GD1a is an essential coreceptor for Toll-like receptor 2 signaling in response to the B subunit of type IIb enterotoxin. JBiol Chem 2007, 282:7532-7542.
35. Nagafuku M., Okuyama K., Onimaru Y., Suzuki A., Odagiri Y., Yamashita T., et al. CD4 and CD8 T cells require different membrane gangliosides for activation. Proc Natl Acad Sci U S A 2012, 109:E336-E342.
36. Zhu Y., Gumlaw N., Karman J., Zhao H., Zhang J., Jiang J.L., et al. Lowering glycosphingolipid levels in CD4+ T cells attenuates T cell receptor signaling, cytokine production, and differentiation to the Th17 lineage. JBiol Chem 2011, 286:14787-14794.
37. Ziolkowska M., Koc A., Luszczykiewicz G., Ksiezopolska-Pietrzak K., Klimczak E., Chwalinska-Sadowska H., et al. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers invitro IL-17 production via cyclosporin A-sensitive mechanism. JImmunol 2000, 164:2832-2838.
38. Zamli Z., Sharif M. Chondrocyte apoptosis: a cause or consequence of osteoarthritis?. Int J Rheum Dis 2011, 14:159-166.
39. Troeberg L., Nagase H. Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim Biophys Acta 2012, 1824:133-145.
40. Ferrari G., Anderson B.L., Stephens R.M., Kaplan D.R., Greene L.A. Prevention of apoptotic neuronal death by GM1 ganglioside. Involvement of Trk neurotrophin receptors. JBiol Chem 1995, 270:3074-3080.
41. Fighera M.R., Royes L.F., Furian A.F., Oliveira M.S., Fiorenza N.G., Frussa-Filho R., et al. GM1 ganglioside prevents seizures, Na+, K+-ATPase activity inhibition and oxidative stress induced by glutaric acid and pentylenetetrazole. Neurobiol Dis 2006, 22:611-623.
42. Sokolova T.V., Zakharova I.O., Furaev V.V., Rychkova M.P., Avrova N.F. Neuroprotective effect of ganglioside GM1 on the cytotoxic action of hydrogen peroxide and amyloid beta-peptide in PC12 cells. Neurochem Res 2007, 32:1302-1313.
43. Cavallini L., Venerando R., Miotto G., Alexandre A. Ganglioside GM1 protection from apoptosis of rat heart fibroblasts. Arch Biochem Biophys 1999, 370:156-162.
44. Sergent O., Pereira M., Belhomme C., Chevanne M., Huc L., Lagadic-Gossmann D. Role for membrane fluidity in ethanol-induced oxidative stress of primary rat hepatocytes. JPharmacol Exp Ther 2005, 313:104-111.
45. Liang Y.J., Kuo H.H., Lin C.H., Chen Y.Y., Yang B.C., Cheng Y.Y., et al. Switching of the core structures of glycosphingolipids from globo- and lacto- to ganglio-series upon human embryonic stem cell differentiation. Proc Natl Acad Sci U S A 2010, 107:22564-22569.
46. Kuan C.T., Chang J., Mansson J.E., Li J., Pegram C., Fredman P., et al. Multiple phenotypic changes in mice after knockout of the B3gnt5 gene, encoding Lc3 synthase - a key enzyme in lacto-neolacto ganglioside synthesis. BMC Dev Biol 2010, 10:114.
47. Ogasawara N., Katagiri Y.U., Kiyokawa N., Kaneko T., Sato B., Nakajima H., et al. Accelerated biosynthesis of neolacto-series glycosphingolipids in differentiated mouse embryonal carcinoma F9 cells detected by using dodecyl N-acetylglucosaminide as a saccharide primer. JBiochem 2011, 149:321-330.
48. Hellio Le Graverand-Gastineau M.P. OA clinical trials: current targets and trials for OA. Choosing molecular targets: what have we learned and where we are headed?. Osteoarthritis Cartilage 2009, 17:1393-1401.
49. Nagahori N., Yamashita T., Amano M., Nishimura S. Effect of ganglioside GM3 synthase gene knockout on the glycoprotein N-glycan profile of mouse embryonic fibroblast. Chembiochem 2013, 14:73-82.