The modulation of the oxidative stress response in chondrocytes by Wip1 and its effect on senescence and dedifferentiation during in vitro expansion

Biomaterials

Volumn 34, Issue 9, 2013, Pages 2380-2388

  Cha, Byung Hyun ^a   Lee, Ji Seon ^b   Kim, Sung Won ^c   Cha, Hyuk Jin ^b   Lee, Soo Hong ^a  

^a CHA University   (South Korea)

^b Sogang University   (South Korea)

^c The Catholic University of Korea   (South Korea)

Author keywords

Cartilage tissue development; Chondrocyte; Dedifferentiation; Oxidative stress modulator; Senescence; Wip 1

Indexed keywords

CARTILAGE TISSUES; CHONDROCYTES; DEDIFFERENTIATION; SENESCENCE; WIP-1;

CARTILAGE; EXPANSION; MAMMALS; MODULATION; OXIDATIVE STRESS; TISSUE;

BODY FLUIDS;

MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOPROTEIN PHOSPHATASE; UNCLASSIFIED DRUG; WIP 1 POTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARTILAGE; CARTILAGE CELL; CARTILAGE TRANSPLANTATION; CELL AGING; CELL DEDIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL REGENERATION; CHONDROGENESIS; CHONDROPATHY; CONTROLLED STUDY; FEMALE; GENE DELIVERY SYSTEM; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; WILD TYPE;

ANIMALS; CARTILAGE; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; FEMALE; GENE TRANSFER TECHNIQUES; HUMANS; KNEE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, NUDE; MITOCHONDRIA; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PHOSPHOPROTEIN PHOSPHATASES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

MUS;

EID: 84872607641     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.12.009     Document Type: Article

References (48)

1. Browne J.E., Anderson A.F., Arciero R., Mandelbaum B., Moseley J.B., Micheli L.J., et al. Clinical outcome of autologous chondrocyte implantation at 5 years in US subjects. Clin Orthop Relat Res 2005, 237-245.
2. McNickle A.G., L'Heureux D.R., Yanke A.B., Cole B.J. Outcomes of autologous chondrocyte implantation in a diverse patient population. Am J Sports Med 2009, 37:1344-1350.
3. Choi E.-H., Park K.-S., Han I.B., S-W.K. Co-culture condition of adipose derived stromal cells and nucleus pulposus cells for regeneration of intervertebral disc. Tiss Eng Reg Med 2009, 6:461-466.
4. Benya P.D., Shaffer J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 1982, 30:215-224.
5. Schulze-Tanzil G. Activation and dedifferentiation of chondrocytes: implications in cartilage injury and repair. Ann Anat 2009, 191:325-338.
6. Serrano M., Blasco M.A. Putting the stress on senescence. Curr Opin Cell Biol 2001, 13:748-753.
7. Lee J.S., Lee M.O., Moon B.H., Shim S.H., Fornace A.J., Cha H.J. Senescent growth arrest in mesenchymal stem cells is bypassed by Wip1-mediated downregulation of intrinsic stress signaling pathways. Stem Cells 2009, 27:1963-1975.
8. Brandl A., Hartmann A., Bechmann V., Graf B., Nerlich M., Angele P. Oxidative stress induces senescence in chondrocytes. J Orthop Res 2011, 29:1114-1120.
9. Carlo M.D., Loeser R.F. Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis Rheum 2003, 48:3419-3430.
10. Hong E.H., Lee S.J., Kim J.S., Lee K.H., Um H.D., Kim J.H., et al. Ionizing radiation induces cellular senescence of articular chondrocytes via negative regulation of SIRT1 by p38 kinase. J Biol Chem 2010, 285:1283-1295.
11. Morita K., Miyamoto T., Fujita N., Kubota Y., Ito K., Takubo K., et al. Reactive oxygen species induce chondrocyte hypertrophy in endochondral ossification. J Exp Med 2007, 204:1613-1623.
12. Domm C., Schunke M., Christesen K., Kurz B. Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 2002, 10:13-22.
13. Parrinello S., Samper E., Krtolica A., Goldstein J., Melov S., Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 2003, 5:741-747.
14. Grayson W.L., Zhao F., Bunnell B., Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 2007, 358:948-953.
15. Yudoh K., Nguyen T., Nakamura H., Hongo-Masuko K., Kato T., Nishioka K. Potential involvement of oxidative stress in cartilage senescence and development of osteoarthritis: oxidative stress induces chondrocyte telomere instability and downregulation of chondrocyte function. Arthritis Res Ther 2005, 7:R380-R391.
16. Lo Y.Y., Conquer J.A., Grinstein S., Cruz T.F. Interleukin-1 beta induction of c-fos and collagenase expression in articular chondrocytes: involvement of reactive oxygen species. J Cell Biochem 1998, 69:19-29.
17. Campisi J., d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007, 8:729-740.
18. Itahana K., Zou Y., Itahana Y., Martinez J.L., Beausejour C., Jacobs J.J., et al. Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol 2003, 23:389-401.
19. Takekawa M., Adachi M., Nakahata A., Nakayama I., Itoh F., Tsukuda H., et al. p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. Embo J 2000, 19:6517-6526.
20. Bulavin D.V., Phillips C., Nannenga B., Timofeev O., Donehower L.A., Anderson C.W., et al. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet 2004, 36:343-350.
21. Lu X., Nannenga B., Donehower L.A. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev 2005, 19:1162-1174.
22. Shreeram S., Demidov O., Hee W., Yamaguchi H., Onishi N., Kek C., et al. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol Cell 2006, 23:757-764.
23. Cha H., Lowe J.M., Li H., Lee J.S., Belova G.I., Bulavin D.V., et al. Wip1 directly dephosphorylates gamma-H2AX and attenuates the DNA damage response. Cancer Res 2010, 70:4112-4122.
24. Lowe J., Cha H., Lee M.O., Mazur S.J., Appella E., Fornace A.J. Regulation of the Wip1 phosphatase and its effects on the stress response. Front Biosci 2012, 17:1480-1498.
25. Lee S.J., Kang S.W., Do H.J., Han I., Shin D.A., Kim J.H., et al. Enhancement of bone regeneration by gene delivery of BMP2/Runx2 bicistronic vector into adipose-derived stromal cells. Biomaterials 2010, 31:5652-5659.
26. Cawthon R.M. Telomere measurement by quantitative PCR. Nucleic Acids Res 2002, 30:e47.
27. Bruder S.P., Jaiswal N., Haynesworth S.E. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 1997, 64:278-294.
28. Wagner W., Bork S., Lepperdinger G., Joussen S., Ma N., Strunk D., et al. How to track cellular aging of mesenchymal stromal cells?. Aging (Albany NY) 2010, 2:224-230.
29. Zaucke F., Dinser R., Maurer P., Paulsson M. Cartilage oligomeric matrix protein (COMP) and collagen IX are sensitive markers for the differentiation state of articular primary chondrocytes. Biochem J 2001, 358:17-24.
30. Goessler U.R., Bugert P., Bieback K., Baisch A., Sadick H., Verse T., et al. Expression of collagen and fiber-associated proteins in human septal cartilage during in vitro dedifferentiation. Int J Mol Med 2004, 14:1015-1022.
31. Lin Z., Fitzgerald J.B., Xu J., Willers C., Wood D., Grodzinsky A.J., et al. Gene expression profiles of human chondrocytes during passaged monolayer cultivation. J Orthop Res 2008, 26:1230-1237.
32. Han M.K., Song E.K., Guo Y., Ou X., Mantel C., Broxmeyer H.E. SIRT1 regulates apoptosis and nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell Stem Cell 2008, 2:241-251.
33. Le Guezennec X., Bulavin D.V. WIP1 phosphatase at the crossroads of cancer and aging. Trends Biochem Sci 2010, 35:109-114.
34. Salmon A.B., Richardson A., Perez V.I. Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging?. Free Radic Biol Med 2010, 48:642-655.
35. Shao L., Li H., Pazhanisamy S.K., Meng A., Wang Y., Zhou D. Reactive oxygen species and hematopoietic stem cell senescence. Int J Hematol 2011, 94:24-32.
36. Cristofalo V., Lorenzini A., Allen R., Torres C., Tresini M. Replicative senescence: a critical review. Mech Ageing Dev 2004, 125:827-848.
37. Millis A.J., McCue H.M., Kumar S., Baglioni C. Metalloproteinase and TIMP-1 gene expression during replicative senescence. Exp Gerontol 1992, 27:425-428.
38. Hwang E.S., Yoon G., Kang H.T. A comparative analysis of the cell biology of senescence and aging. Cell Mol Life Sci 2009, 66:2503-2524.
39. Tolstonog G.V., Shoeman R.L., Traub U., Traub P. Role of the intermediate filament protein vimentin in delaying senescence and in the spontaneous immortalization of mouse embryo fibroblasts. DNA Cell Biol 2001, 20:509-529.
40. Guan J.L. Role of focal adhesion kinase in integrin signaling. Int J Biochem Cell Biol 1997, 29:1085-1096.
41. Cho K.A., Ryu S.J., Oh Y.S., Park J.H., Lee J.W., Kim H.P., et al. Morphological adjustment of senescent cells by modulating caveolin-1 status. J Biol Chem 2004, 279:42270-42278.
42. Wu C., Dedhar S. Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 2001, 155:505-510.
43. Rice K.M., Desai D.H., Kinnard R.S., Harris R., Wright G.L., Blough E.R. Load-induced focal adhesion mechanotransduction is altered with aging in the Fischer 344/NNiaHSd x Brown Norway/BiNia rat aorta. Biogerontology 2007, 8:257-267.
44. Campisi J., Kim S.H., Lim C.S., Rubio M. Cellular senescence, cancer and aging: the telomere connection. Exp Gerontol 2001, 36:1619-1637.
45. Fujimoto H., Onishi N., Kato N., Takekawa M., Xu X.Z., Kosugi A., et al. Regulation of the antioncogenic Chk2 kinase by the oncogenic Wip1 phosphatase. Cell Death Differ 2006, 13:1170-1180.
46. Wong E., Le Guezennec X., Demidov O., Marshall N., Wang S., Krishnamurthy J., et al. p38MAPK controls expression of multiple cell cycle inhibitors and islet proliferation with advancing age. Dev Cell 2009, 17:142-149.
47. Zhu Y., Zhang C., Lu L., Demidov O., Sun L., Yang L., et al. Wip1 regulates the generation of new neural cells in the adult olfactory bulb through p53-dependent cell cycle control. Stem Cells 2009, 27:1433-1442.
48. Demidov O.N., Timofeev O., Lwin H.N., Kek C., Appella E., Bulavin D.V. Wip1 phosphatase regulates p53-dependent apoptosis of stem cells and tumorigenesis in the mouse intestine. Cell Stem Cell 2007, 1:180-190.