Constitutive expression of cathepsin K in the human intervertebral disc: New insight into disc extracellular matrix remodeling via cathepsin K and receptor activator of nuclear factor-κB ligand

Arthritis Research and Therapy

Volumn 13, Issue 4, 2011, Pages

  Gruber, Helen E ^a   Ingram, Jane A ^a   Hoelscher, Gretchen L ^a   Zinchenko, Natalia ^a   Norton, H James ^a   Hanley Jr, Edward N ^a  

^a CAROLINAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN K; OSTEOCLAST DIFFERENTIATION FACTOR; TNFSF11 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IN VIVO STUDY; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DEGENERATION; MALE; PROTEIN FUNCTION; DNA MICROARRAY; GENE EXPRESSION PROFILING; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADULT; AGED; CATHEPSIN K; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RANK LIGAND; YOUNG ADULT;

EID: 80052137674     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3454     Document Type: Article

References (52)

1. Tezuka K, Tezuka Y, Maejima A, Sato T, Nemoto K, Kamioka H, Hakeda Y, Kamegawa M. Molecular cloning of a possible cysteine proteinase predominantly expressed in osteoclasts. J Biol Chem 1994, 269:1106-1109.
2. Li A, Hou WS, Escalante-Torres CR, Gelb BD, Brömme D. Collagenase activity of cathepsin K depends on complex formation with chondroitin sulfate. J Biol Chem 2002, 277:28669-28676. 10.1074/jbc.M204004200, 12039963.
3. Yasuda Y, Kaleta J, Brömme D. The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics. Adv Drug Deliv Rev 2005, 57:973-993. 10.1016/j.addr.2004.12.013, 15876399.
4. Hummell KM, Petrow PK, Franz JK, Muller-Ladner U, Aicher WK, Gay RE, Bromme D, Gay S. Cysteine proteinase cathepsin K mRNA is expressed in synovium of patients with rheumatoid arthritis and is detected at sites of synovial bone descruction. J Rheumatol 1998, 25:1887-1894.
5. Hou W-S, Li W, Keyszer G, Weber E, Levy R, Klein MJ, Gravallese EM, Goldring SR, Brömme D. Comparison of cathepsins K and S expression within the rheumatoid and osteoarthritic synovium. Arthritis Rheum 2002, 46:663-674. 10.1002/art.10114, 11920402.
6. Konttinen YT, Mandelin J, Li T-F, Salo J, Lassus J, Liljeström M, Hukkanen M, Tagai M, Virtanen I, Santavirta S. Acidic cysteine endoproteinase cathepsin K in the degeneration of the superficial articular hyaline cartilage in osteoarthritis. Arthritis Rheum 2002, 46:953-960. 10.1002/art.10185, 11953972.
7. Salminen-Mankonen HJ, Morko J, Vuorio E. Role of cathepsin K in normal joints and in the development of arthritis. Curr Drug Targets 2007, 8:315-323. 10.2174/138945007779940188, 17305509.
8. Dejica VM, Mort JS, Laverty S, Percival MD, Antoniou J, Zukor DJ, Poole AR. Cleavage of type II collagen by cathepsin K in human osteoarthritic cartilage. Amer J Pathol 2008, 173:161-169.
9. Ruettger A, Schueler S, Mollenhauer JA, Weideranders B. Cathepsins B, K, and L are regulated by a defined collagen type II peptide via activation of classical protein kinase C and p38 MAP kinase in articular chondrocytes. J Biol Chem 2008, 283:1043-1051.
10. Morko J, Kiviranta R, Joronen K, Säämänen A-M, Vuorio E, Salminen-Mankonen H. Spontaneous development of synovitis and cartilage degeneration in transgenic mice overexpressin cathepsin K. Arthritis Rheum 2005, 52:3713-3717. 10.1002/art.21423, 16329095.
11. Morko JP, Söderström M, Säämänen AM, Salminen HJ, Vuorio EI. Up regulation of cathepsin K expression in articular chondrocytes in a transgenic mouse model for osteoarthritis. Ann Rheum Dis 2004, 63:649-655. 10.1136/ard.2002.004671, 1755014, 15140771.
12. Dombs MD, Yutzey KE. VEGF and RANKL regulation of NFATc1 in heart valve development. Circ Res 2009, 105:565-574. 10.1161/CIRCRESAHA.109.196469, 2749238, 19661463.
13. Ariga K, Yonenobu K, Nakase T, Kaneko M, Okuda S, Uchiyama Y, Yoshikawa H. Localization of cathepsins D, K, and L in degenerated human intervertebral discs. Spine 2001, 26:2666-2672. 10.1097/00007632-200112150-00007, 11740352.
14. Neidhart M, Baraliakos X, Seemayer C, Zelder D, Gay RE, Michel BA, Boehm H, Gay S, Braun J. Expression of cathepsin K and matrix metalloproteinase 1 indicate persistent osteodestructive activity in long-standing ankylosing spondylitis. Ann Rheum Dis 2009, 68:1334-1339. 10.1136/ard.2008.092494, 18678577.
15. Mwale F, Wang HT, Zukor DJ, Huk OL, Petit A, Antoniou J. Effect of a type II collagen fragment on the expression of genes of the extracellular matrix in cells of the intervertebral disc. Open Orthop J 2008, 2:1-9. 10.2174/1874325000802010001, 2685046, 19461923.
16. Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IKY, Bishop PB. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 1990, 15:411-415. 10.1097/00007632-199005000-00012, 2363069.
17. Gruber HE, Mougeot J-L, Hoelscher GL, Ingram JA, Hanley EN. Microarray analysis of laser capture microdissected annulus cells from the human intervertebral disc. Spine 2007, 32:1181-1187. 10.1097/BRS.0b013e318053ec89, 17495774.
18. Auuerbach JD, Johnnessen W, Borthakur A, Wheaton AJ, Dolinskas CA, Balderston RA, Reddy R, Elliott DM. In vivo quantification of human lumbar disc degeneration using T(1rho)-weighted magnetic resonance imaging. Eur Spine J 2006, 15:S338-S344. 10.1007/s00586-006-0083-2, 2335378, 16552534.
19. Millward-Sadler SJ, Costello PW, Freemont AJ, Hoyland JA. Regulation of catabolic gene expression in normal and degenerate human intervertebral disc cells: implications for the pathogenesis of intervertebral disc degeneration. Arthritis Res Ther 2009, 11:R65. 10.1186/ar2693, 2714110, 19435506.
20. Gruber HE, Ingram JA, Hoelscher GL, Zinchenko N, Norton HJ, Hanley EN. Matrix metalloproetinase 28, a novel matrix metalloproteinase, is constitutively expressed in human intervertebral disc tissue and is present in matrix of more degenerated discs. Arthritis Res Ther 2009, 11:R184. 10.1186/ar2876, 3003526, 20003223.
21. Gruber HE, Ingram JA, Hanley EN. Immunolocalization of MMP-19 in the human intervertebral disc: implications for disc aging and degeneration. Biotech Histochem 2005, 80:157-162. 10.1080/10520290500387607, 16298901.
22. Crean JKG, Roberts S, Jaffray DC, Eisenstein SM, Duance VC. Matrix metalloproteinases in the human intervertebral disc: role in disc degeneration and scoliosis. Spine 1997, 22:2877-2884. 10.1097/00007632-199712150-00010, 9431623.
23. Kozaci LD, Guner A, Oktay G, Guner G. Alterations in biochemical components of extracellular matrix in intervertebral disc herniation: role of MMP-2 and TIMP-2 in type II collagen loss. Cell Biochem Funct 2006, 24:431-436. 10.1002/cbf.1250, 16142692.
24. Shen B, Melrose J, Ghosh P, Taylor TKF. Induction of matrix metalloproteinase-2 and -3 activity in ovine nucleus pulposus cells grown in three-dimensional agarose gel culture by interleukin-1β: a potential pathway of disc degeneration. Eur Spine J 2003, 12:66-75.
25. Nemoto O, Yamagishi M, Yamada H, Kikuchi T, Takaishi H. Matrix metalloproteinase-3 production by human degenerated intervertebral disc. J Spinal Disord 1997, 10:493-498.
26. Roberts S, Caterson B, Menage J, Evans EH, Jaffray DC, Eisenstein SM. Matrix metalloproteinases and aggrecanase - their role in disorders of the human intervertebral disc. Spine 2000, 25:3005-3013. 10.1097/00007632-200012010-00007, 11145811.
27. Momohara S, Okamoto H, Komiya K, Ikari K, Tadkuchi M, Tomatsu T, Kamatani N. Matrix metalloproteinase 28/epilysin expression in cartilage from patients with rheumatoid arthritis and osteoarthritis: comment on the article by Kevorkian et al. Arthritis Rheum 2004, 50:4074-4080. 10.1002/art.20799, 15593191.
28. Le Maitre CL, Freemont AJ, Hoyland JA. Localization of degradative enzymes and their inhibitors in the degenerate human intervertebral disc. J Pathol 2004, 204:47-54. 10.1002/path.1608, 15307137.
29. Weiler C, Nerlich AG, Zipperer J, Bachmeier BE, Boos N. 2002 SSE Award Competition in Basic Science: expression of major matrix metalloproteinases is associated with disc degradation and resorption. Eur Spine J 2002, 11:308-320. 10.1007/s00586-002-0472-0, 12193991.
30. MacLean JJ, Lee CR, Alini M, Iatridis JC. The effects of short-term load duration on anabolic and catabolic gene expression in the rat tail intervertebral disc. J Orthop Res 2005, 23:1120-1127. 10.1016/j.orthres.2005.01.020, 16140193.
31. Richardson SM, Doyle P, Minogue BM, Gnanalinghan K, Hoyland JA. Increased expression of matrix metalloproteinase 10, nerve growth factor and substance P in the painful degenerate intervertebral disc. Arthritis Res Ther 2009, 11:R126. 10.1186/ar2793, 2745810, 19695094.
32. Singh K, Masuda K, Thonar EJMA, An HS, Cs-Szabo G. Age-related changes in the extracellular matrix of nucleus pulposus and anulus fibrosus of human intervertebral disc. Spine 2008, 34:10-16.
33. Cs-Szabo G, Juan DRS, Turumella V, Masuda K, Thonar EJMA, An HS. Changes in mRNA and protein levels of proteoglycans of the anulus fibrosus and nucleus pulposus during intervertebral disc degeneration. Spine 2002, 27:2212-2219. 10.1097/00007632-200210150-00006, 12394896.
34. Freemont AJ. The cellular pathobiology of the degenerate intervertebral disc and discogenic back pain. Rheumatology (Oxford) 2009, 48:5-10.
35. Le Maitre CL, Pockert A, Buttle DJ, Freemont AJ, Hoyland JA. Matrix synthesis and degradation in human intervertebral disc degeneration. Biochem Soc Trans 2007, 35:652-655. 10.1042/BST0350652, 17635113.
36. Hadjipavlou AG, Tzermaidianos MN, Bogduk N, Zindrick MR. The pathophysiology of disc degeneration. A critical review. J Bone Joint Surg Br 2008, 90:1261-1270. 10.1302/0301-620X.90B10.20910, 18827232, 18827232.
37. Purmessur D, Freemont AJ, Hoyland JA. Expression and regulation of neurotrophins in the nondegenerate and degenerate human intervertebral disc. Arthritis Res Ther 2008, 10:R99. 10.1186/ar2487, 2575613, 18727839.
38. Pockert AJ, Richardson SM, Le Maitre CL, Lyon M, Deakin JA, Buttle DJ, Freemont AJ, Hoyland JA. Modified expression of the ADAMTS enzymes and tissue inhibitor of metalloproteinases 3 during human intervertebral disc degeneration. Arthritis Rheum 2009, 60:482-491. 10.1002/art.24291, 19180493.
39. Roberts S, Evans EH, Kletsas D, Jaffray DC, Eisenstein SM. Senescence in human intervertebral discs. Eur Spine J 2006, 15:S312-S316. 10.1007/s00586-006-0126-8, 2335374, 16773379.
40. LeMaitre CL, Freemont AJ, Hoyland JA. The role of interleukin-1 in the pathogenesis of human intervertebral disc degeneration. Arthritis Res Ther 2005, 7:R732-R745. 10.1186/ar1732, 1175026, 15987475.
41. Heathfield SK, Le Maitre CL, Hoyland JA. Caveolin-1 expression and stress-induced premature senescence in human intervertebral disc degeneration. Arthritis Res Ther 2008, 10:R87. 10.1186/ar2468, 2575636, 18681962.
42. Kang JD, Georgescu HI, McIntyre-Larkin L, Stefanovic-Racic M, Donaldson WF, Evans CH. Herniated lumbar intervertebral discs spontaneously produce matrix metalloproteinases, nitric oxide, interleukin-6, and prostaglandin E2. Spine 1996, 21:271-277. 10.1097/00007632-199602010-00003, 8742201.
43. LeMaitre CL, Hoyland JA, Freemont AJ. Catabolic cytokine expression in degenerate and herniated human intervertebral discs: IL-1ß and TNFa expression profile. Arthritis Res Ther 2007, 9:R77. 10.1186/ar2275, 2206382, 17688691.
44. Rand N, Reichert F, Floman Y, Rotshenker S. Murine nucleus pulposus-derived cells secrete interleukins- 1-β, -6, and -10 and granulocyte-macrophage colony-stimulating factor in cell culture. Spine 1997, 22:2598-2601. 10.1097/00007632-199711150-00002, 9399443.
45. Huang KY, Chen W-Y, Lee C-L, Yan J-J, Chang M-S. IL-20 may contribute to the pathogenesis of human intervertebral disc herniation. Spine 2008, 33:2034-2040. 10.1097/BRS.0b013e31817eb872, 18758357.
46. Hoyland JA, Le Maitre C, Freemont AJ. Investigation of the role of IL-1 and TNF in matrix degradation in the intervertebral disc. Rheumatol 2008, 47:809-814.
47. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D. The molecular triad OPG/RANK/RANKL: involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 2004, 15:457-475. 10.1016/j.cytogfr.2004.06.004, 15561602.
48. Leibbrandt A, Penninger JM. RANK/RANKL: regulators of immune responses and bone physiology. Ann N Y Acad Sci 2008, 1143:123-150. 10.1196/annals.1443.016, 19076348.
49. Mackiewicz A, Salo J, Konttinen YT, Holm AK, Indayl A, Pajarinen J, Holm S. Receptor activator of nuclear factor kappa B ligand in an experimental intervertebral disc degeneration. Clin Exp Rheumatol 2009, 27:299-306.
50. McGonigle JS, Giachelli CM, Scatena M. Osteoprotegerin and RANKL differentially regulate angiogenesis and endothelial cell function. Angiogenesis 2009, 12:35-46. 10.1007/s10456-008-9127-z, 19105036, 19105036.
51. Stroup GB, Lark MW, Veber DF, Bhattacharyya A, Blake S, Dare LC, Erhard KF, Hoffman SF, James IE, Marquis RW, Ru Y, Vasko-Moser JA, Tomaszet T, Gowen M. Potent and selective inhibition of human cathepsin K leads to inhibition of bone resorption in vivo in a nonhuman primate. J Bone Mineral Res 2001, 16:1739-1746.
52. Lecaille F, Choe Y, Brandt W, Li Z, Craik CS, Brömme D. Selective inhibition of the collagenolytic activity of human cathepsin K by altering its S2 subsite specificity. Biochemistry 2002, 41:8447-8454. 10.1021/bi025638x, 12081494.