Sulforaphane represses matrix-degrading proteases and protects cartilage from destruction in vitro and in vivo

Arthritis and Rheumatism

Volumn 65, Issue 12, 2013, Pages 3130-3140

  Davidson, Rose K ^a   Jupp, Orla ^a   De Ferrars, Rachel ^a   Kay, Colin D ^a   Culley, Kirsty L ^a   Norton, Rosemary ^a   Driscoll, Clare ^b,c   Vincent, Tonia L ^b,c   Donell, Simon T ^d   Bao, Yongping ^a   Clark, Ian M ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; HISTONE DEACETYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEOGLYCAN; STRESS ACTIVATED PROTEIN KINASE; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL VIABILITY; CHONDROPROTECTION; CONTROLLED STUDY; DNA BINDING; DRUG EFFICACY; ENZYME ACTIVITY; EXPLANT; FIBROBLAST; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; KNEE MENISCUS; MALE; MOUSE; NONHUMAN; NOSE CARTILAGE; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNOVIOCYTE; WESTERN BLOTTING;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CARTILAGE, ARTICULAR; CATTLE; CHONDROCYTES; HUMANS; ISOTHIOCYANATES; MATRIX METALLOPROTEINASES; MICE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OSTEOARTHRITIS; SIGNAL TRANSDUCTION;

EID: 84889011679     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.38133     Document Type: Article

References (51)

1. Troeberg L, Nagase H,. Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim Biophys Acta 2012; 1824: 133-45.
2. McAlindon TE, Jacques P, Zhang Y, Hannan MT, Aliabadi P, Weissman B, et al. Do antioxidant micronutrients protect against the development and progression of knee osteoarthritis? Arthritis Rheum 1996; 39: 648-56.
3. Wang Y, Hodge A, Wluka A, English D, Giles G, O'Sullivan R, et al. Effect of antioxidants on knee cartilage and bone in healthy, middle-aged subjects: a cross-sectional study. Arthritis Res Ther 2007; 9: R66.
4. Williams FM, Skinner J, Spector TD, Cassidy A, Clark IM, Davidson RM, et al. Dietary garlic and hip osteoarthritis: evidence of a protective effect and putative mechanism of action. BMC Musculoskelet Disord 2010; 11: 280.
5. Juge N, Mithen RF, Traka M,. Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci 2007; 64: 1105-27.
6. Dinkova-Kostova AT, Kostov RV,. Glucosinolates and isothiocyanates in health and disease. Trends Mol Med 2012; 18: 337-47.
7. Brandenburg LO, Kipp M, Lucius R, Pufe T, Wruck CJ,. Sulforaphane suppresses LPS-induced inflammation in primary rat microglia. Inflamm Res 2010; 59: 443-50.
8. Zakkar M, Van der Heiden K, Luong LA, Chaudhury H, Cuhlmann S, Hamdulay SS, et al. Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler Thromb Vasc Biol 2009; 29: 1851-7.
9. 2 production in osteoarthritic chondrocytes. Biochem Pharmacol 2009; 77: 1806-13.
10. Kim HA, Yeo Y, Kim WU, Kim S,. Phase 2 enzyme inducer sulphoraphane blocks matrix metalloproteinase production in articular chondrocytes. Rheumatology (Oxford) 2009; 48: 932-8.
11. Kim HA, Yeo Y, Jung HA, Jung YO, Park SJ, Kim SJ,. Phase 2 enzyme inducer sulphoraphane blocks prostaglandin and nitric oxide synthesis in human articular chondrocytes and inhibits cartilage matrix degradation. Rheumatology 2012; 51: 1006-16.
12. Kong JS, Yoo SA, Kim HS, Kim HA, Yea K, Ryu SH, et al. Inhibition of synovial hyperplasia, rheumatoid T cell activation, and experimental arthritis in mice by sulforaphane, a naturally occurring isothiocyanate. Arthritis Rheum 2010; 62: 159-70.
13. Gibbs A, Schwartzman J, Deng V, Alumkal J,. Sulforaphane destabilizes the androgen receptor in prostate cancer cells by inactivating histone deacetylase 6. Proc Natl Acad Sci U S A 2009; 106: 16663-8.
14. Young D, Lakey R, Pennington C, Jones D, Kevorkian L, Edwards D, et al. Histone deacetylase inhibitors modulate metalloproteinase gene expression in chondrocytes and block cartilage resorption. Arthritis Res Ther 2005; 7: R503-12.
15. Chen WP, Bao JP, Hu PF, Feng J, Wu LD,. Alleviation of osteoarthritis by trichostatin A, a histone deacetylase inhibitor, in experimental osteoarthritis. Mol Biol Rep 2010; 37: 3967-72.
16. Culley KL, Hui W, Barter MJ, Davidson RK, Swingler TE, Destrument AP, et al. Class I histone deacetylase inhibition modulates metalloproteinase expression and blocks cytokine-induced cartilage degradation. Arthritis Rheum 2013; 65: 1822-30.
17. Nian H, Delage B, Ho E, Dashwood RH,. Modulation of histone deacetylase activity by dietary isothiocyanates and allyl sulfides: studies with sulforaphane and garlic organosulfur compounds. Environ Mol Mutagen 2009; 50: 213-21.
18. Nuttall RK, Pennington CJ, Taplin J, Wheal A, Yong VW, Forsyth PA, et al. Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells. Mol Cancer Res 2003; 1: 333-45.
19. Porter S, Scott SD, Sassoon EM, Williams MR, Jones JL, Girling AC, et al. Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin Cancer Res 2004; 10: 2429-40.
20. Billington CJ,. Cartilage proteoglycan release assay. Methods Mol Biol 2001; 151: 451-6.
21. Shingleton WD, Ellis AJ, Rowan AD, Cawston TE,. Retinoic acid combines with interleukin-1 to promote the degradation of collagen from bovine nasal cartilage: matrix metalloproteinases-1 and -13 are involved in cartilage collagen breakdown. J Cell Biochem 2000; 79: 519-31.
22. Glasson SS, Askew R, Sheppard B, Carito B, Blanchet T, Ma HL, et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis [published erratum appears in Nature 2007;446:102]. Nature 2005; 434: 644-8.
23. Chia SL, Sawaji Y, Burleigh A, McLean C, Inglis J, Saklatvala J, et al. Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis. Arthritis Rheum 2009; 60: 2019-27.
24. Caterson B, Flannery CR, Hughes CE, Little CB,. Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol 2000; 19: 333-44.
25. Loeser RF, Goldring SR, Scanzello CR, Goldring MB,. Osteoarthritis: a disease of the joint as an organ [review]. Arthritis Rheum 2012; 64: 1697-707.
26. Facchini A, Stanic I, Cetrullo S, Borzi RM, Filardo G, Flamigni F,. Sulforaphane protects human chondrocytes against cell death induced by various stimuli. J Cell Physiol 2011; 226: 1771-9.
27. Gasper AV, Al-Janobi A, Smith JA, Bacon JR, Fortun P, Atherton C, et al. Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli. Am J Clin Nutr 2005; 82: 1283-91.
28. Dashwood RH, Ho E,. Dietary histone deacetylase inhibitors: from cells to mice to man. Semin Cancer Biol 2007; 17: 363-9.
29. Guillen MI, Megias J, Gomar F, Alcaraz MJ,. Haem oxygenase-1 regulates catabolic and anabolic processes in osteoarthritic chondrocytes. J Pathol 2008; 214: 515-22.
30. Ruiz-Romero C, Calamia V, Mateos J, Carreira V, Martinez-Gomariz M, Fernandez M, et al. Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics: a decrease in mitochondrial superoxide dismutase points to a redox imbalance. Mol Cell Proteomics 2009; 8: 172-89.
31. Henrotin Y, Kurz B, Aigner T,. Oxygen and reactive oxygen species in cartilage degradation: friends or foes? Osteoarthritis Cartilage 2005; 13: 643-54.
32. Regan EA, Bowler RP, Crapo JD,. Joint fluid antioxidants are decreased in osteoarthritic joints compared to joints with macroscopically intact cartilage and subacute injury. Osteoarthritis Cartilage 2008; 16: 515-21.
33. Aini H, Ochi H, Iwata M, Okawa A, Koga D, Okazaki M, et al. Procyanidin b3 prevents articular cartilage degeneration and heterotopic cartilage formation in a mouse surgical osteoarthritis model. PLoS One 2012; 7: e37728.
34. Xu C, Shen G, Chen C, Gelinas C, Kong AN,. Suppression of NF-κB and NF-κB-regulated gene expression by sulforaphane and PEITC through IκBα, IKK pathway in human prostate cancer PC-3 cells. Oncogene 2005; 24: 4486-95.
35. Moon DO, Kim MO, Kang SH, Choi YH, Kim GY,. Sulforaphane suppresses TNF-α-mediated activation of NF-κB and induces apoptosis through activation of reactive oxygen species-dependent caspase-3. Cancer Lett 2009; 274: 132-42.
36. Kim JY, Park HJ, Um SH, Sohn EH, Kim BO, Moon EY, et al. Sulforaphane suppresses vascular adhesion molecule-1 expression in TNF-α-stimulated mouse vascular smooth muscle cells: involvement of the MAPK, NF-κB and AP-1 signaling pathways [published erratum appears in Vascul Pharmacol 2013;58:157]. Vascul Pharmacol 2012; 56: 131-41.
37. Heiss E, Herhaus C, Klimo K, Bartsch H, Gerhauser C,. Nuclear factor κB is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms. J Biol Chem 2001; 276: 32008-15.
38. Heiss E, Gerhauser C,. Time-dependent modulation of thioredoxin reductase activity might contribute to sulforaphane-mediated inhibition of NF-κB binding to DNA. Antioxid Redox Signal 2005; 7: 1601-11.
39. Kim SJ, Kang SY, Shin HH, Choi HS,. Sulforaphane inhibits osteoclastogenesis by inhibiting nuclear factor-κB. Mol Cells 2005; 20: 364-70.
40. Reddy NM, Kleeberger SR, Yamamoto M, Kensler TW, Scollick C, Biswal S, et al. Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol Genomics 2007; 32: 74-81.
41. Zhang Y,. Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000; 21: 1175-82.
42. Zhang Y,. Molecular mechanism of rapid cellular accumulation of anticarcinogenic isothiocyanates. Carcinogenesis 2001; 22: 425-31.
43. Sakon S, Xue X, Takekawa M, Sasazuki T, Okazaki T, Kojima Y, et al. NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 2003; 22: 3898-909.
44. Keum YS, Yu S, Chang PP, Yuan X, Kim JH, Xu C, et al. Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res 2006; 66: 8804-13.
45. Hu R, Khor TO, Shen G, Jeong WS, Hebbar V, Chen C, et al. Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 2006; 27: 2038-46.
46. Lefebvre V, Li P, de Crombrugghe B,. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 1998; 17: 5718-33.
47. Leung KK, Ng LJ, Ho KK, Tam PP, Cheah KS,. Different cis-regulatory DNA elements mediate developmental stage- and tissue-specific expression of the human COL2A1 gene in transgenic mice. J Cell Biology 1998; 141: 1291-300.
48. Lefebvre V, Behringer RR, de Crombrugghe B,. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis Cartilage 2001; 9 Suppl 1: S69-75.
49. Caron MM, Emans PJ, Surtel DA, Cremers A, Voncken JW, Welting TJ, et al. Activation of NF-κB/p65 facilitates early chondrogenic differentiation during endochondral ossification. PLoS One 2012; 7: e33467.
50. Yoshida T, Hashimura M, Kuwata T, Matsumoto T, Suzuki E, Tazo Y, et al. Transcriptional regulation of the α-1 type II collagen gene by nuclear factor κB/p65 and Sox9 in the chondrocytic phenotype of uterine carcinosarcomas. Hum Pathol 2013. E-pub ahead of print.
51. Saito T, Fukai A, Mabuchi A, Ikeda T, Yano F, Ohba S, et al. Transcriptional regulation of endochondral ossification by HIF-2α during skeletal growth and osteoarthritis development. Nat Med 2010; 16: 678-86.