Oxidative stress inhibits the proliferation, induces premature senescence and promotes a catabolic phenotype in human nucleus pulposus intervertebral disc cells

European Cells and Materials

Volumn 30, Issue , 2015, Pages 89-103

  Dimozi, A ^a   Mavrogonatou, E ^a   Sklirou, A ^a   Kletsas, Dimitris ^a  

^a INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

Akt; ATM; H2O2; Intervertebral disc nucleus pulposus cells; MAPKs; NF B; Nrf2; Oxidative stress; ROS; Senescence

Indexed keywords

6 N CARBOXYMETHYLLYSINE; ACETYLCYSTEINE; AGGRECAN; AGGRECANASE 2; ATM PROTEIN; BETA GALACTOSIDASE; CHECKPOINT KINASE 2; GELATINASE A; GELATINASE B; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERSTITIAL COLLAGENASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MOLECULAR MARKER; PROTEIN; PROTEIN KINASE B; PROTEIN P21; PROTEOGLYCAN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TRANSCRIPTION FACTOR NRF2;

AGE; AGING; ARTICLE; CARTILAGE CELL; CELL AGING; CELL CYCLE G1 PHASE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; HUMAN; HUMAN CELL; INTERVERTEBRAL DISK DEGENERATION; NUCLEUS PULPOSUS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; TELOMERE; UPREGULATION; CELL CULTURE; CYTOLOGY; INTERVERTEBRAL DISK; METABOLISM; PHENOTYPE; PHYSIOLOGY;

AGGRECANS; CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; HUMANS; HYDROGEN PEROXIDE; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; OXIDATIVE STRESS; PHENOTYPE; UP-REGULATION;

EID: 84940916544     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v030a07     Document Type: Article

References (66)

1. Awai-Kasaoka N, Inoue T, Kameda T, Fujimoto T, Inoue-Mochita M, Tanihara H (2013) Oxidative stress response signaling pathways in trabecular meshwork cells and their effects on cell viability. Mol Vis 19: 1332-1340.
2. Bak MJ, Jun M, Jeong WS (2012) Procyanidins from wild grape (Vitis amurensis) seeds regulate ARE-mediated enzyme expression via Nrf2 coupled with p38 and PI3K/ Akt pathway in HepG2 cells. Int J Mol Sci 13: 801-818.
3. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, Fugger K, Johansson F, Sehested M, Andersen CL, Dyrskjot L, Orntoft T, Lukas J, Kittas C, Helleday T, Halazonetis TD, Bartek J, Gorgoulis VG (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
4. 2: senescence-like growth arrest or apoptosis? Cell Growth Differ 8: 589-598.
5. Bubici C, Papa S, Pham CG, Zazzeroni F, Franzoso G (2006) The NF-kappaB-mediated control of ROS and JNK signaling. Histol Histopathol 21: 69-80.
6. Campisi J, d’Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740.
7. Chen QM, Prowse KR, Tu VC, Purdom S, Linskens MH (2001) Uncoupling the senescent phenotype from telomere shortening in hydrogen peroxide-treated fibroblasts. Exp Cell Res 265: 294-303.
8. de Bittencourt Pasquali MA, Gelain DP, Zeidan- Chulia F, Pires AS, Gasparotto J, Terra SR, Moreira JC (2013) Vitamin A (retinol) downregulates the receptor for advanced glycation endproducts (RAGE) by oxidant-dependent activation of p38 MAPK and NF-kB in human lung cancer A549 cells. Cell Signal 25: 939-954.
9. Deshpande NN, Sorescu D, Seshiah P, Ushio-Fukai M, Akers M, Yin Q, Griendling KK (2002) Mechanism of hydrogen peroxide-induced cell cycle arrest in vascular smooth muscle. Antioxid Redox Signal 4: 845-854.
10. Freemont AJ (2009) The cellular pathobiology of the degenerate intervertebral disc and discogenic back pain. Rheumatology (Oxford) 48: 5-10.
11. Gruber HE, Ingram JA, Norton HJ, Hanley EN, Jr. (2007) Senescence in cells of the aging and degenerating intervertebral disc: immunolocalization of senescence-associated beta-galactosidase in human and sand rat discs. Spine (Phila Pa 1976) 32: 321-327.
12. Guo Z, Deshpande R, Paull TT (2010a) ATM activation in the presence of oxidative stress. Cell Cycle 9: 4805-4811.
13. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT (2010b) ATM activation by oxidative stress. Science 330: 517-521.
14. Han J, Sun P (2007) The pathways to tumor suppression via route p38. Trends Biochem Sci 32: 364-371.
15. Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
16. Hou G, Lu H, Chen M, Yao H, Zhao H (2014) Oxidative stress participates in age-related changes in rat lumbar intervertebral discs. Arch Gerontol Geriatr 59: 665-669.
17. Huang BK, Sikes HD (2014) Quantifying intracellular hydrogen peroxide perturbations in terms of concentration. Redox Biol 2: 955-962.
18. Johnson WEB, Roberts S (2003) Human intervertebral disc cell morphology and cytoskeletal composition: a preliminary study of regional variations in health and disease. J Anat 203: 605-612.
19. Kaneko T, Tahara S, Taguchi T, Kondo H (2001) Accumulation of oxidative DNA damage, 8-oxo-2’- deoxyguanosine, and change of repair systems during in vitro cellular aging of cultured human skin fibroblasts. Mutat Res 487: 19-30.
20. Katz JN (2006) Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J Bone Joint Surg Am 88 Suppl 2: 21-24.
21. Kim KW, Chung HN, Ha KY, Lee JS, Kim YY (2009) Senescence mechanisms of nucleus pulposus chondrocytes in human intervertebral discs. Spine J 9: 658-666.
22. Kletsas D (2009) Senescent cells in the intervertebral disc: numbers and mechanisms. Spine J 9: 677-678.
23. Konstantonis D, Papadopoulou A, Makou M, Eliades T, Basdra EK, Kletsas D (2013) Senescent human periodontal ligament fibroblasts after replicative exhaustion or ionizing radiation have a decreased capacity towards osteoblastic differentiation. Biogerontology 14: 741-751.
24. Le Maitre CL, Freemont AJ, Hoyland JA (2004) Localization of degradative enzymes and their inhibitors in the degenerate human intervertebral disc. J Pathol 204: 47-54.
25. Le Maitre CL, Freemont AJ, Hoyland JA (2006) Human disc degeneration is associated with increased MMP 7 expression. Biotech Histochem 81: 125-131.
26. Le Maitre CL, Freemont AJ, Hoyland JA (2007a) Accelerated cellular senescence in degenerate intervertebral discs: a possible role in the pathogenesis of intervertebral disc degeneration. Arthritis Res Ther 9: R45.
27. Le Maitre CL, Pockert A, Buttle DJ, Freemont AJ, Hoyland JA (2007b) Matrix synthesis and degradation in human intervertebral disc degeneration. Biochem Soc Trans 35: 652-655.
28. Li B, Wang X, Rasheed N, Hu Y, Boast S, Ishii T, Nakayama K, Nakayama KI, Goff SP (2004) Distinct roles of c-Abl and Atm in oxidative stress response are mediated by protein kinase C delta. Genes Dev 18: 1824-1837.
29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
30. Lu T, Finkel T (2008) Free radicals and senescence. Exp Cell Res 314: 1918-1922.
31. Luoma K, Riihimaki H, Luukkonen R, Raininko R, Viikari-Juntura E, Lamminen A (2000) Low back pain in relation to lumbar disc degeneration. Spine (Phila Pa 1976) 25: 487-492.
32. Mavrogonatou E, Angelopoulou MT, Kletsas D (2014) The catabolic effect of TNFalpha on bovine nucleus pulposus intervertebral disc cells and the restraining role of glucosamine sulfate in the TNFalpha-mediated up-regulation of MMP-3. J Orthop Res 32: 1701-1707.
33. Mavrogonatou E, Eliades T, Eliades G, Kletsas D (2010) The effect of triethylene glycol dimethacrylate on p53-dependent G2 arrest in human gingival fibroblasts. Biomaterials 31: 8530-8538.
34. Mavrogonatou E, Kletsas D (2009) High osmolality activates the G1 and G2 cell cycle checkpoints and affects the DNA integrity of nucleus pulposus intervertebral disc cells triggering an enhanced DNA repair response. DNA Repair (Amst) 8: 930-943.
35. Mavrogonatou E, Kletsas D (2010) Effect of varying osmotic conditions on the response of bovine nucleus pulposus cells to growth factors and the activation of the ERK and Akt pathways. J Orthop Res 28: 1276-1282.
36. Mavrogonatou E, Kletsas D (2012) Differential response of nucleus pulposus intervertebral disc cells to high salt, sorbitol, and urea. J Cell Physiol 227: 1179-1187.
37. Nasto LA, Robinson AR, Ngo K, Clauson CL, Dong Q, St Croix C, Sowa G, Pola E, Robbins PD, Kang J, Niedernhofer LJ, Wipf P, Vo NV (2013) Mitochondrial-derived reactive oxygen species (ROS) play a causal role in aging-related intervertebral disc degeneration. J Orthop Res 31: 1150-1157.
38. Nerlich AG, Bachmeier BE, Schleicher E, Rohrbach H, Paesold G, Boos N (2007) 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 1096: 239-248.
39. Nerlich AG, Schleicher ED, Boos N (1997) 1997 Volvo Award winner in basic science studies. Immunohistologic markers for age-related changes of human lumbar intervertebral discs. Spine (Phila Pa 1976) 22: 2781-2795.
40. Owuor ED, Kong AN (2002) Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol 64: 765-770.
41. Papadopoulou A, Kletsas D (2011) Human lung fibroblasts prematurely senescent after exposure to ionizing radiation enhance the growth of malignant lung epithelial cells in vitro and in vivo. Int J Oncol 39: 989-999.
42. Park JY, Kang KA, Kim KC, Cha JW, Kim EH, Hyun JW (2013) Morin Induces Heme Oxygenase-1 via ERK-Nrf2 Signaling Pathway. J Cancer Prev 18: 249-256.
43. 2 inhibits the growth of human pulmonary fibroblast cells by inducing cell death, GSH depletion and G1 phase arrest. Mol Med Rep 7: 1235-1240.
44. Passos JF, von Zglinicki T (2006) Oxygen free radicals in cell senescence: are they signal transducers? Free Radic Res 40: 1277-1283.
45. Pedruzzi LM, Stockler-Pinto MB, Leite M, Jr., Mafra D (2012) Nrf2-keap1 system versus NF-kappaB: the good and the evil in chronic kidney disease? Biochimie 94: 2461-2466.
46. Pockert AJ, Richardson SM, Le Maitre CL, Lyon M, Deakin JA, Buttle DJ, Freemont AJ, Hoyland JA (2009) Modified expression of the ADAMTS enzymes and tissue inhibitor of metalloproteinases 3 during human intervertebral disc degeneration. Arthritis Rheum 60: 482-491.
47. Pratsinis H, Constantinou V, Pavlakis K, Sapkas G, Kletsas D (2012) Exogenous and autocrine growth factors stimulate human intervertebral disc cell proliferation via the ERK and Akt pathways. J Orthop Res 30: 958-964.
48. Pratsinis H, Kletsas D (2007) PDGF, bFGF and IGF-I stimulate the proliferation of intervertebral disc cells in vitro via the activation of the ERK and Akt signaling pathways. Eur Spine J 16: 1858-1866.
49. Roberts S, Caterson B, Menage J, Evans EH, Jaffray DC, Eisenstein SM (2000) Matrix metalloproteinases and aggrecanase: their role in disorders of the human intervertebral disc. Spine (Phila Pa 1976) 25: 3005-3013.
50. Roberts S, Evans EH, Kletsas D, Jaffray DC, Eisenstein SM (2006a) Senescence in human intervertebral discs. Eur Spine J 15 Suppl 3: S312-316.
51. Roberts S, Evans H, Trivedi J, Menage J (2006b) Histology and pathology of the human intervertebral disc. J Bone Joint Surg Am 88 Suppl 2: 10-14.
52. Roninson IB (2002) Tumor senescence as a determinant of drug response in vivo. Drug Resist Updat 5: 204-208.
53. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
54. Singh K, Masuda K, Thonar EJ, An HS, Cs-Szabo G (2009) Age-related changes in the extracellular matrix of nucleus pulposus and anulus fibrosus of human intervertebral disc. Spine (Phila Pa 1976) 34: 10-16.
55. Sivan SS, Hayes AJ, Wachtel E, Caterson B, Merkher Y, Maroudas A, Brown S, Roberts S (2014) Biochemical composition and turnover of the extracellular matrix of the normal and degenerate intervertebral disc. Eur Spine J 23 Suppl 3: S344-353.
56. Sivan SS, Tsitron E, Wachtel E, Roughley P, Sakkee N, van der Ham F, Degroot J, Maroudas A (2006) Age-related accumulation of pentosidine in aggrecan and collagen from normal and degenerate human intervertebral discs. Biochem J 399: 29-35.
57. Studer RK, Gilbertson LG, Georgescu H, Sowa G, Vo N, Kang JD (2008) p38 MAPK inhibition modulates rabbit nucleus pulposus cell response to IL-1. J Orthop Res 26: 991-998.
58. Sykiotis GP, Habeos IG, Samuelson AV, Bohmann D (2011) The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care 14: 41-48.
59. Toussaint O, Medrano EE, von Zglinicki T (2000) Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol 35: 927-945.
60. Urban JP, Roberts S (2003) Degeneration of the intervertebral disc. Arthritis Res Ther 5: 120-130.
61. Urban JP, Smith S, Fairbank JC (2004) Nutrition of the intervertebral disc. Spine (Phila Pa 1976) 29: 2700-2709.
62. Vo N, Niedernhofer LJ, Nasto LA, Jacobs L, Robbins PD, Kang J, Evans CH (2013) An overview of underlying causes and animal models for the study of age-related degenerative disorders of the spine and synovial joints. J Orthop Res 31: 831-837.
63. von Zglinicki T, Pilger R, Sitte N (2000) Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic Biol Med 28: 64-74.
64. Wu ZH, Shi Y, Tibbetts RS, Miyamoto S (2006) Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli. Science 311: 1141-1146.
65. Wuertz K, Vo N, Kletsas D, Boos N (2012) Inflammatory and catabolic signalling in intervertebral discs: the roles of NF-kappaB and MAP kinases. Eur Cell Mater 23: 103-120.
66. 2-induced premature senescence of human fibroblasts. Biogerontology 10: 291-298.