Caveolin-1 expression and stress-induced premature senescence in human intervertebral disc degeneration

Arthritis Research and Therapy

Volumn 10, Issue 4, 2008, Pages

  Heathfield, Sarah Kathleen ^a   Le Maitre, Christine Lyn ^b   Hoyland, Judith Alison ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b SHEFFIELD HALLAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; BIOLOGICAL MARKER;

ADULT; AGED; AGING; ARTICLE; CONTROLLED STUDY; CORRELATION FUNCTION; DISEASE ASSOCIATION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERVERTEBRAL DISK DEGENERATION; NUCLEUS PULPOSUS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; STRESS INDUCED PREMATURE SENESCENCE; INTERVERTEBRAL DISK; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PREMATURE AGING; SPINE DISEASE;

ADULT; AGED; AGING, PREMATURE; BIOLOGICAL MARKERS; CAVEOLIN 1; CYCLIN-DEPENDENT KINASE INHIBITOR P16; HUMANS; INTERVERTEBRAL DISK; MIDDLE AGED; SPINAL DISEASES; STRESS, PHYSIOLOGICAL;

EID: 50549099313     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2468     Document Type: Article

References (66)

1. Burton AK Balague F Cardon G Eriksen HR Henrotin Y Lahad A Leclerc A Muller G Beek van der AJ Chapter 2. European guidelines for prevention in low back pain: November 2004 Eur Spine J 2006, 15(Suppl 2):S136-168. 10.1007/s00586-006-1070-3 16550446
2. Maniadakis N Gray A The economic burden of back pain in the UK Pain 2000, 84:95-103. 10.1016/S0304-3959(99)00187-6 10601677
3. Peterson CK Bolton JE Wood AR A cross-sectional study correlating lumbar spine degeneration with disability and pain Spine 2000, 25:218-223. 10.1097/00007632-200001150-00013 10685487
4. Luoma K Riihimaki H Luukkonen R Raininko R Viikari-Juntura E Lamminen A Low back pain in relation to lumbar disc degeneration Spine 2000, 25:487-492. 10.1097/00007632-200002150-00016 10707396
5. Roughley PJ Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix Spine 2004, 29:2691-2699. 10.1097/01.brs.0000146101.53784.b1 15564918
6. Adams MA Roughley PJ What is intervertebral disc degeneration, and what causes it? Spine 2006, 31:2151-2161. 10.1097/01.brs.0000231761.73859.2c 16915105
7. Sambrook PN MacGregor AJ Spector TD Genetic influences on cervical and lumbar disc degeneration: A magnetic resonance imaging study in twins Arthritis Rheum 1999, 42:366-372. 10.1002/ 1529-0131(199902)42:2<366::AID-ANR20>3.0.CO;2-6 10025932
8. MacGregor AJ Andrew T Sambrook PN Spector TD Structural, psychological, and genetic influences on low back and neck pain: A study of adult female twins Arthritis Rheum 2004, 51:160-167. 10.1002/art.20236 15077255
9. Miller JA Schmatz C Schultz AB Lumbar disc degeneration: Correlation with age, sex, and spine level in 600 autopsy specimens Spine 1988, 13:173-178. 10.1097/00007632-198802000-00008 3406837
10. Boos N Weissbach S Rohrbach H Weiler C Spratt KF Nerlich AG Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science Spine 2002, 27:2631-2644. 10.1097/ 00007632-200212010-00002 12461389
11. Anderson DG Tannoury C Molecular pathogenic factors in symptomatic disc degeneration Spine J 2005, 5(Suppl 6):260S-266S. 16291122 10.1016/ j.spinee.2005.02.010
12. Freemont AJ Watkins A Le Maitre C Jeziorska M Hoyland JA Current understanding of cellular and molecular events in intervertebral disc degeneration: Implications for therapy J Pathol 2002, 196:374-379. 10.1002/path.1050 11920731
13. Minamino T Komuro I Vascular cell senescence: Contribution to atherosclerosis Circ Res 2007, 100:15-26. 10.1161/ 01.RES.0000256837.40544.4a 17204661
14. Price JS Waters JG Darrah C Pennington C Edwards DR Donell ST Clark IM The role of chondrocyte senescence in osteoarthritis Aging Cell 2002, 1:57-65. 10.1046/j.1474-9728.2002.00008.x 12882354
15. Martin JA Buckwalter JA Roles of articular cartilage aging and chondrocyte senescence in the pathogenesis of osteoarthritis Iowa Orthop J 2001, 21:1-7. 1888191 11813939
16. Roberts S Evans EH Kletsas D Jaffray DC Eisenstein SM Senescence in human intervertebral discs Eur Spine J 2006 ,15(Suppl 15):312-316. 16773379 10.1007/s00586-006-0126-8
17. Gruber HE Ingram JA Norton HJ Hanley EN Jr Senescence in cells of the aging and degenerating intervertebral disc: Immunolocalization of senescence-associated beta-galactosidase in human and sand rat discs Spine 2007, 32:321-327. 10.1097/01.brs.0000253960.57051.de 17268263
18. Le Maitre CL Freemont AJ Hoyland JA Accelerated cellular senescence in degenerate intervertebral discs: A possible role in the pathogenesis of intervertebral disc degeneration Arthritis Res Ther 2007, 9:R45. 2206356 17498290 10.1186/ar2198
19. Dai SM Shan ZZ Nakamura H Masuko-Hongo K Kato T Nishioka K Yudoh K Catabolic stress induces features of chondrocyte senescence through overexpression of caveolin 1: Possible involvement of caveolin 1-induced down-regulation of articular chondrocytes in the pathogenesis of osteoarthritis Arthritis Rheum 2006, 54:818-831. 10.1002/art.21639 16508959
20. Frippiat C Chen QM Zdanov S Magalhaes JP Remacle J Toussaint O Subcytotoxic H2O2 stress triggers a release of transforming growth factor-beta 1, which induces biomarkers of cellular senescence of human diploid fibroblasts J Biol Chem 2001, 276:2531-2537. 10.1074/ jbc.M006809200 11060295
21. Dumont P Balbeur L Remacle J Toussaint O Appearance of biomarkers of in vitro ageing after successive stimulation of WI-38 fibroblasts with IL-1alpha and TNF-alpha: Senescence associated beta-galactosidase activity and morphotype transition J Anat 2000, 197(Pt 4):529-537. 1468167 11197525 10.1046/j.1469-7580.2000.19740529.x
22. Dumont P Burton M Chen QM Gonos ES Frippiat C Mazarati JB Eliaers F Remacle J Toussaint O Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast Free Radic Biol Med 2000, 28:361-373. 10.1016/S0891-5849(99)00249-X 10699747
23. Mendez MV Raffetto JD Phillips T Menzoian JO Park HY The proliferative capacity of neonatal skin fibroblasts is reduced after exposure to venous ulcer wound fluid: A potential mechanism for senescence in venous ulcers J Vasc Surg 1999, 30:734-743. 10.1016/S0741-5214(99)70113-8 10514213
24. Chen Q Ames BN Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells Proc Natl Acad Sci USA 1994, 91:4130-4134. 43738 8183882 10.1073/pnas.91.10.4130
25. Parton RG Simons K The multiple faces of caveolae Nat Rev Mol Cell Biol 2007, 8:185-194. 10.1038/nrm2122 17318224
26. Smart EJ Graf GA McNiven MA Sessa WC Engelman JA Scherer PE Okamoto T Lisanti MP Caveolins, liquid-ordered domains, and signal transduction Mol Cell Biol 1999, 19:7289-7304. 84723 10523618
27. Liu P Rudick M Anderson RG Multiple functions of caveolin-1 J Biol Chem 2002, 277:41295-41298. 10.1074/jbc.R200020200 12189159
28. Okamoto T Schlegel A Scherer PE Lisanti MP Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane J Biol Chem 1998, 273:5419-5422. 10.1074/jbc.273.10.5419 9488658
29. Park WY Park JS Cho KA Kim DI Ko YG Seo JS Park SC Up-regulation of caveolin attenuates epidermal growth factor signaling in senescent cells J Biol Chem 2000, 275:20847-20852. 10.1074/jbc.M908162199 10781609
30. Wheaton K Sampsel K Boisvert FM Davy A Robbins S Riabowol K Loss of functional caveolae during senescence of human fibroblasts J Cell Physiol 2001, 187:226-235. 10.1002/jcp.1071 11268002
31. Volonte D Zhang K Lisanti MP Galbiati F Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts Mol Biol Cell 2002, 13:2502-2517. 117330 12134086 10.1091/mbc.01-11-0529
32. Linge A Weinhold K Blasche R Kasper M Barth K Downregulation of caveolin-1 affects bleomycin-induced growth arrest and cellular senescence in A549 cells Int J Biochem Cell Biol 2007, 39:1964-1974. 10.1016/j.biocel.2007.05.018 17662641
33. Voghel G Thorin-Trescases N Farhat N Nguyen A Villeneuve L Mamarbachi AM Fortier A Perrault LP Carrier M Thorin E Cellular senescence in endothelial cells from atherosclerotic patients is accelerated by oxidative stress associated with cardiovascular risk factors Mech Ageing Dev 2007, 128:662-671. 10.1016/j.mad.2007.09.006 18022214
34. Nerlich AG Bachmeier BE Schleicher E Rohrbach H Paesold G Boos N Immunomorphological analysis of RAGE receptor expression and NF-kappaB activation in tissue samples from normal and degenerated intervertebral discs of various ages Ann N Y Acad Sci 2007, 1096:239-248. 10.1196/ annals.1397.090 17405935
35. Nerlich AG Schleicher ED Boos N 1997 Volvo Award winner in basic science studies. Immunohistologic markers for age-related changes of human lumbar intervertebral discs Spine 1997, 22:2781-2795. 10.1097/ 00007632-199712150-00001 9431614
36. Schleicher ED Wagner E Nerlich AG Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging J Clin Invest 1997, 99:457-468. 507819 9022079 10.1172/JCI119180
37. Le Maitre CL Freemont AJ Hoyland JA The role of interleukin-1 in the pathogenesis of human intervertebral disc degeneration Arthritis Res Ther 2005, 7:R732-745. 1175026 15987475 10.1186/ar1732
38. Le Maitre CL Hoyland JA Freemont AJ Catabolic cytokine expression in degenerate and herniated human intervertebral discs: IL-1beta and TNFalpha expression profile Arthritis Res Ther 2007, 9:R77. 2206382 17688691 10.1186/ar2275
39. Sive JI Baird P Jeziorsk M Watkins A Hoyland JA Freemont AJ Expression of chondrocyte markers by cells of normal and degenerate intervertebral discs Mol Pathol 2002, 55:91-97. 1187156 11950957 10.1136/mp.55.2.91
40. 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
41. Toussaint O Dumont P Dierick JF Pascal T Frippiat C Chainiaux F Sluse F Eliaers F Remacle J Stress-induced premature senescence. Essence of life, evolution, stress, and aging Ann N Y Acad Sci 2000, 908:85-98. 10911950
42. Campisi J Kim SH Lim CS Rubio M Cellular senescence, cancer and aging: the telomere connection Exp Gerontol 2001, 36:1619-1637. 10.1016/ S0531-5565(01)00160-7 11672984
43. Martin JA Buckwalter JA Aging, articular cartilage chondrocyte senescence and osteoarthritis Biogerontology 2002, 3:257-264. 10.1023/ A:1020185404126 12237562
44. Hayflick L The limited in vitro lifetime of human diploid cell strains Exp Cell Res 1965, 37:614-636. 10.1016/0014-4827(65)90211-9 14315085
45. Oh CW Bump EA Kim JS Janigro D Mayberg MR Induction of a senescence-like phenotype in bovine aortic endothelial cells by ionizing radiation Radiat Res 2001, 156:232-240. 10.1667/ 0033-7587(2001)156[0232:IOASLP]2.0.CO;2 11500132
46. Chainiaux F Magalhaes JP Eliaers F Remacle J Toussaint O UVB-induced premature senescence of human diploid skin fibroblasts Int J Biochem Cell Biol 2002, 34:1331-1339. 10.1016/S1357-2725(02)00022-5 12200029
47. Medrano EE Im S Yang F Abdel-Malek ZA Ultraviolet B light induces G1 arrest in human melanocytes by prolonged inhibition of retinoblastoma protein phosphorylation associated with long-term expression of the p21Waf-1/SDI-1/Cip-1 protein Cancer Res 1995, 55:4047-4052. 7664278
48. Wang X Wong SC Pan J Tsao SW Fung KH Kwong DL Sham JS Nicholls JM Evidence of cisplatin-induced senescent-like growth arrest in nasopharyngeal carcinoma cells Cancer Res 1998, 58:5019-5022. 9823301
49. Rodemann HP Differential degradation of intracellular proteins in human skin fibroblasts of mitotic and mitomycin-C (MMC)-induced postmitotic differentiation states in vitro Differentiation 1989, 42:37-43. 10.1111/ j.1432-0436.1989.tb00605.x 2620784
50. Robles SJ Buehler PW Negrusz A Adami GR Permanent cell cycle arrest in asynchronously proliferating normal human fibroblasts treated with doxorubicin or etoposide but not camptothecin Biochem Pharmacol 1999, 58:675-685. 10.1016/S0006-2952(99)00127-6 10413306
51. Serrano M Lin AW McCurrach ME Beach D Lowe SW Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a Cell 1997, 88:593-602. 10.1016/S0092-8674(00)81902-9 9054499
52. Cho KA Park SC Caveolin-1 as a prime modulator of aging: A new modality for phenotypic restoration? Mech Ageing Dev 2005, 126:105-110. 10.1016/ j.mad.2004.09.029 15610768
53. Sherr CJ Roberts JM CDK inhibitors: Positive and negative regulators of G1-phase progression Genes Dev 1999, 13:1501-1512. 10.1101/ gad.13.12.1501 10385618
54. Huschtscha LI Reddel RR p16(INK4a) and the control of cellular proliferative life span Carcinogenesis 1999, 20:921-926. 10.1093/carcin/ 20.6.921 10357768
55. Satyanarayana A Rudolph KL p16 and ARF: Activation of teenage proteins in old age J Clin Invest 2004, 114:1237-1240. 524239 15520854
56. Beausejour CM Krtolica A Galimi F Narita M Lowe SW Yaswen P Campisi J Reversal of human cellular senescence: Roles of the p53 and p16 pathways Embo J 2003, 22:4212-4222. 175806 12912919 10.1093/emboj/cdg417
57. Krishnamurthy J Torrice C Ramsey MR Kovalev GI Al-Regaiey K Su L Sharpless NE Ink4a/Arf expression is a biomarker of aging J Clin Invest 2004, 114:1299-1307. 524230 15520862
58. Zhou HW Lou SQ Zhang K Recovery of function in osteoarthritic chondrocytes induced by p16INK4a-specific siRNA in vitro Rheumatology (Oxford) 2004, 43:555-568. 10.1093/rheumatology/keh127 15026580
59. Robles SJ Adami GR Agents that cause DNA double strand breaks lead to p16INK4a enrichment and the premature senescence of normal fibroblasts Oncogene 1998, 16:1113-1123. 10.1038/sj.onc.1201862 9528853
60. Park JI Jeong JS Han JY Kim DI Gao YH Park SC Rodgers GP Kim IH Hydroxyurea induces a senescence-like change of K562 human erythroleukemia cell J Cancer Res Clin Oncol 2000, 126:455-460. 10.1007/ s004320050013 10961388
61. Le Maitre CL Hoyland JA Freemont AJ Interleukin-1 receptor antagonist delivered directly and by gene therapy inhibits matrix degradation in the intact degenerate human intervertebral disc: An in situ zymographic and gene therapy study Arthritis Res Ther 2007, 9:R83. 2206387 17760968 10.1186/ar2282
62. 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
63. Lisanti MP Scherer PE Vidugiriene J Tang Z Hermanowski-Vosatka A Tu YH Cook RF Sargiacomo M Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: Implications for human disease J Cell Biol 1994, 126:111-126. 2120102 7517942 10.1083/jcb.126.1.111
64. Kislinger T Fu C Huber B Qu W Taguchi A Du Yan S Hofmann M Yan SF Pischetsrieder M Stern D Schmidt AM N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression J Biol Chem 1999, 274:31740-31749. 10.1074/jbc.274.44.31740 10531386
65. Schwab W Gavlik JM Beichler T Funk RH Albrecht S Magdolen V Luther T Kasper M Shakibaei M Expression of the urokinase-type plasminogen activator receptor in human articular chondrocytes: Association with caveolin and beta 1-integrin Histochem Cell Biol 2001, 115:317-323. 11405060
66. Nicholl SM Roztocil E Davies MG Plasminogen activator system and vascular disease Curr Vasc Pharmacol 2006, 4:101-116. 10.2174/ 157016106776359880 16611153