Activation of p38 MAP kinase and stress signalling in fibroblasts from the progeroid Rothmund-Thomson syndrome

Age

Volumn 35, Issue 5, 2013, Pages 1767-1783

  Davis, Terence ^a   Tivey, Hannah S E ^a   Brook, Amy J C ^a   Grimstead, Julia W ^a   Rokicki, Michal J ^a   Kipling, David ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Ageing; Cellular senescence; Progeroid syndrome; Stress associated MAP kinases; Telomerase; Tumour suppressor p53

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P53; SHORT HAIRPIN RNA; TELOMERASE;

ADULT; ARTICLE; CELL AGING; CELL DIVISION; CELL GROWTH; CELL STRUCTURE; CELL SURVIVAL; CELLULAR STRESS SIGNAL; CHILD; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR CLONING; OXIDATIVE STRESS; PRESCHOOL CHILD; PROTEIN EXPRESSION; RECQL4 GENE; ROTHMUND THOMSON SYNDROME; SCHOOL CHILD; SENESCENCE; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; YOUNG ADULT;

ADOLESCENT; AGING; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; ENZYME ACTIVATION; ENZYME INHIBITORS; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMIDAZOLES; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PYRIDINES; RNA; ROTHMUND-THOMSON SYNDROME; YOUNG ADULT;

EID: 84892572956     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9476-9     Document Type: Article

References (68)

1. Abe T, Yoshimura A, Hosono Y, Tada S, Seki M, Enomoto T (2011) The N-terminal region of RECQL4 lacking the helicase domain is both essential and sufficient for the viability of vertebrate cells. Role of the N-terminal region of RECQL4 in cells. Biochim Biophys Acta 1813(3):473-479. doi:10.1016/j.bbamcr. 2011.01.001
2. Bachrati CZ, Hickson ID (2003) RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem J 374(Pt 3):577-606
3. Bagley MC, Davis T, Murziani PGS, Widdowson CS, Kipling D (2010) Use of p38 MAPK inhibitors for the treatment of Werner syndrome. Pharmaceuticals 3:1842-1872
4. Bond JA, Haughton MF, Rowson JM, Smith PJ, Gire V, Wynford-Thomas D, Wyllie FS (1999) Control of replicative life span in human cells: barriers to clonal expansion intermediate between M1 senescence and M2 crisis. Mol Cell Biol 19(4):3103-3114
5. Bridger JM, Kill IR (2004) Aging of Hutchinson-Gilford progeria syndrome fibroblasts is characterised by hyperproliferation and increased apoptosis. Exp Gerontol 39(5):717-724. doi:10.1016/j.exger.2004.02.002
6. Burks LM, Yin J, Plon SE (2007) Nuclear import and retention domains in the amino terminus of RECQL4. Gene 391(1- 2):26-38
7. Cabral RE, Queille S, Bodemer C, de Prost Y, Neto JB, Sarasin A, Daya-Grosjean L (2008) Identification of new RECQL4 mutations in Caucasian Rothmund-Thomson patients and analysis of sensitivity to a wide range of genotoxic agents. Mutat Res 643(1-2):41-47
8. Chen JH, Stoeber K, Kingsbury S, Ozanne SE, Williams GH, Hales CN (2004) Loss of proliferative capacity and induction of senescence in oxidatively stressed human fibroblasts. J Biol Chem 279(47):49439-49446. doi:10.1074/ jbc.M409153200
9. Davis T, Kipling D (2006) Werner Syndrome as an example of inflamm-aging: possible therapeutic opportunities for a progeroid syndrome? Rejuvenation Res 9 (3):402-407
10. Davis T, Kipling D (2009) Assessing the role of stress signalling via p38 MAP kinase in the premature senescence of Ataxia Telangiectasia and Werner syndrome fibroblasts. Biogerontology 10(3):253-266
11. Davis T, Singhrao SK, Wyllie FS, Haughton MF, Smith PJ, Wiltshire M, Wynford-Thomas D, Jones CJ, Faragher RGA, Kipling D (2003) Telomere-based proliferative lifespan barriers in Werner-syndrome fibroblasts involve both p53-dependent and p53-independent mechanisms. J Cell Sci 116(7):1349-1357
12. Davis T, Baird DM, Haughton MF, Jones CJ, Kipling D (2005a) Prevention of accelerated cell aging in Werner syndrome using a p38 mitogen-activated protein kinase inhibitor. J Gerontol A Biol Sci Med Sci 60(11):1386-1393
13. Davis T, Skinner JW, Faragher RGA, Jones CJ, Kipling D (2005b) Replicative senescence in sheep fibroblasts is a p53 dependent process. Exp Gerontol 40(1-2):17-26
14. Davis T, Wyllie FS, Rokicki MJ, Bagley MC, Kipling D (2007) The role of cellular senescence in Werner syndrome: toward therapeutic intervention in human premature aging. Ann N Y Acad Sci 1100:455-469
15. Davis T, Tivey HSE, Kipling D (2009) Telomere dynamics and biology in human progeroid syndromes. In: Mancini L (ed) Telomeres: function, shortening and lengthening. Novascience, New York, pp 1-75
16. Deng Q, Liao R, Wu BL, Sun P (2004) High intensity ras signaling induces premature senescence by activating p38 pathway in primary human fibroblasts. J Biol Chem 279 (2):1050-1059. doi:10.1074/jbc.M308644200
17. Der Kaloustian VM, McGill JJ, Vekemans M, Kopelman HR (1990) Clonal lines of aneuploid cells in Rothmund-Thomson syndrome. Am J Med Genet 37(3):336-339
18. Dulic V, Beney GE, Frebourg G, Drullinger LF, Stein GH (2000) Uncoupling between phenotypic senescence and cell cycle arrest in aging p21-deficient fibroblasts. Mol Cell Biol 20(18):6741-6754
19. Faragher RG, Kill IR, Hunter JA, Pope FM, Tannock C, Shall S (1993) The gene responsible for Werner syndrome may be a cell division "counting" gene. Proc Natl Acad Sci USA 90(24):12030-12034
20. Faragher RG, Sheerin AN, Ostler EL (2009) Can we intervene in human ageing? Expert Rev Mol Med 11:e27. doi:10.1017/S1462399409001197
21. Freund A, Patil CK, Campisi J (2011) p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J 30 (8):1536-1548. doi:10.1038/emboj.2011.69
22. Ghosh AK, Rossi ML, Singh DK, Dunn C, Ramamoorthy M, Croteau DL, Liu Y, Bohr VA (2012) RECQL4, the protein mutated in Rothmund-Thomson syndrome, functions in telomere maintenance. J Biol Chem 287(1):196-209. doi:10.1074/jbc.M111.295063
23. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110(Pt 3):357-368
24. Haq R, Brenton JD, Takahashi M, Finan D, Finkielsztein A, Damaraju S, Rottapel R, Zanke B (2002) Constitutive p38HOG mitogen-activated protein kinase activation induces permanent cell cycle arrest and senescence. Cancer Res 62(17):5076-5082
25. Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621
26. Hofer AC, Tran RT, Aziz OZ, Wright W, Novelli G, Shay J, Lewis M (2005) Shared phenotypes among segmental progeroid syndromes suggest underlying pathways of aging. J Gerontol A Biol Sci Med Sci 60(1):10-20
27. Hoki Y, Araki R, Fujimori A, Ohhata T, Koseki H, Fukumura R, Nakamura M, Takahashi H, Noda Y, Kito S, Abe M (2003) Growth retardation and skin abnormalities of the Recql4- deficient mouse. Hum Mol Genet 12(18):2293-2299. doi:10.1093/hmg/ddg254
28. Huot J, Houle F, Marceau F, Landry J (1997) Oxidative stressinduced actin reorganization mediated by the p38 mitogenactivated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80(3):383-392
29. Ichikawa K, Noda T, Furuichi Y (2002) Preparation of the gene targeted knockout mice for human premature aging diseases, Werner syndrome, and Rothmund-Thomson syndrome caused by the mutation of DNA helicases. Nippon Yakurigaku Zasshi 119(4):219-226
30. Iwasa H, Han J, Ishikawa F (2003) Mitogen-activated protein kinase p38 defines the common senescence-signalling pathway. Genes Cells 8(2):131-144
31. Jin W, Liu H, Zhang Y, Otta SK, Plon SE, Wang LL (2008) Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum Genet 123(6):643-653
32. Kashino G, Kodama S, Nakayama Y, Suzuki K, Fukase K, Goto M, Watanabe M (2003) Relief of oxidative stress by ascorbic acid delays cellular senescence of normal human and Werner syndrome fibroblast cells. Free Radic Biol Med 35 (4):438-443
33. Kerr B, Ashcroft GS, Scott D, Horan MA, Ferguson MW, Donnai D (1996) Rothmund-Thomson syndrome: two case reports show heterogeneous cutaneous abnormalities, an association with genetically programmed ageing changes, and increased chromosomal radiosensitivity. J Med Genet 33(11):928-934
34. Kipling D, Davis T, Ostler EL, Faragher RG (2004) What can progeroid syndromes tell us about human aging? Science 305(5689):1426-1431
35. Kitao S, Ohsugi I, Ichikawa K, Goto M, Furuichi Y, Shimamoto A (1998) Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54(3):443-452
36. Larizza L, Roversi G, Volpi L (2010) Rothmund-Thomson syndrome. Orphanet J Rare Dis 5:2. doi:10.1186/1750-1172-5-2
37. Lindor NM, Devries EM, Michels VV, Schad CR, Jalal SM, Donovan KM, Smithson WA, Kvols LK, Thibodeau SN, Dewald GW (1996) Rothmund-Thomson syndrome in siblings: evidence for acquired in vivo mosaicism. Clin Genet 49(3):124-129
38. Liu Y (2010) Rothmund-Thomson syndrome helicase, RECQ4: on the crossroad between DNA replication and repair. DNA Repair (Amst) 9(3):325-330. doi:10.1016/ j.dnarep.2010.01.006
39. Mann MB, Hodges CA, Barnes E, Vogel H, Hassold TJ, Luo G (2005) Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund- Thomson syndrome. Hum Mol Genet 14(6):813-825
40. Martin GM, Oshima J, Gray MD, Poot M (1999) What geriatricians should know about the Werner syndrome. J Am Geriatr Soc 47(9):1136-1144
41. Matsuno K, Kumano M, Kubota Y, Hashimoto Y, Takisawa H (2006) The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase alpha in the initiation of DNA replication. Mol Cell Biol 26(13):4843-4852
42. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, Piqani B, Eisenhaure TM, Luo B, Grenier JK, Carpenter AE, Foo SY, Stewart SA, Stockwell BR, Hacohen N, Hahn WC, Lander ES, Sabatini DM, Root DE (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124(6):1283-1298. doi:10.1016/j.cell.2006.01.040
43. Morgenstern JP, Land H (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18(12):3587-3596
44. Navarro CL, Cau P, Levy N (2006) Molecular bases of progeroid syndromes. Hum Mol Genet 15(2):R151-R161
45. Orstavik KH, McFadden N, Hagelsteen J, Ormerod E, van der Hagen CB (1994) Instability of lymphocyte chromosomes in a girl with Rothmund-Thomson syndrome. J Med Genet 31(7):570-572
46. Ostler EL, Wallis CV, Sheerin AN, Faragher RG (2002) A model for the phenotypic presentation of Werner's syndrome. Exp Gerontol 37(2-3):285-292
47. Ouyang KJ, Woo LL, Ellis NA (2008) Homologous recombination and maintenance of genome integrity: cancer and aging through the prism of human RecQ helicases. Mech Ageing Dev 129(7-8):425-440. doi:10.1016/j.mad.2008.03.003
48. Rao H, Uhlmann F, Nasmyth K, Varshavsky A (2001) Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability. Nature 410(6831):955-959. doi:10.1038/35073627
49. Rothmund A (1868) Uber cataracte in verbindung mit einer eigenthuemlichen hautdgeneration. Albrecht von Graefes Arch Klin Exp Ophthal 14:159-182
50. Sangrithi MN, Bernal JA, Madine M, Philpott A, Lee J, Dunphy WG, Venkitaraman AR (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund- Thomson syndrome. Cell 121(6):887-898
51. Shinya A, Nishigori C, Moriwaki S, Takebe H, Kubota M, Ogino A, Imamura S (1993) A case of Rothmund- Thomson syndrome with reduced DNA repair capacity. Arch Dermatol 129(3):332-336
52. Shiryaev A, Dumitriu G, Moens U (2011) Distinct roles of MK2 and MK5 in cAMP/PKA- and stress/p38MAPK-induced heat shock protein 27 phosphorylation. J Mol Signal 6 (1):4. doi:10.1186/1750-2187-6-4
53. Smith PJ, Paterson MC (1982) Enhanced radiosensitivity and defectiveDNArepair in cultured fibroblasts derived from Rothmund Thomson syndrome patients. Mutat Res 94(1):213-228
54. Tchirkov A, Lansdorp PM (2003) Role of oxidative stress in telomere shortening in cultured fibroblasts from normal individuals and patients with ataxia-telangiectasia. Hum Mol Genet 12(3):227-232
55. Thomson MS (1936) Poikiloderma congenitale. Br J Dermatol 48:221-234
56. Tollefsbol T, Cohen H (1984) Werner's syndrome: an underdiagnosed disorder resembling premature aging. Age 7:75-88
57. 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(8):927-945
58. VarugheseM, Leavey P, Smith P, Sneath R, Breatnach F, O'Meara A (1992) Osteogenic sarcoma and Rothmund-Thomson syndrome. J Cancer Res Clin Oncol 118(5):389-390
59. Vasseur F, Delaporte E, Zabot MT, Sturque MN, Barrut D, Savary JB, Thomas L, Thomas P (1999) Excision repair defect in Rothmund-Thomson syndrome. Acta Derm Venereol 79(2):150-152
60. Wang LL, Gannavarapu A, Kozinetz CA, Levy ML, Lewis RA, Chintagumpala MM, Ruiz-Maldanado R, Contreras-Ruiz J, Cunniff C, Erickson RP, Lev D, Rogers M, Zackai EH, Plon SE (2003) Association between osteosarcoma and deleterious mutations in the RECQL4 gene in Rothmund- Thomson syndrome. J Natl Cancer Inst 95(9):669-674
61. Wang W, Chen JX, Liao R, Deng Q, Zhou JJ, Huang S, Sun P (2002) Sequential activation of theMEK-extracellular signalregulated kinase andMKK3/6-p38 mitogen-activated protein kinase pathways mediates oncogenic ras-induced premature senescence. Mol Cell Biol 22(10):3389-3403
62. Webley K, Bond JA, Jones CJ, Blaydes JP, Craig A, Hupp T, Wynford-Thomas D (2000) Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage. Mol Cell Biol 20 (8):2803-2808
63. Werner SR, Prahalad AK, Yang J, Hock JM (2006) RECQL4- deficient cells are hypersensitive to oxidative stress/damage: insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem Biophys Res Commun 345(1):403-409
64. Xu X, Liu Y (2009) Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J 28(5):568-577. doi:10.1038/emboj.2009.13
65. Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y (2009) MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J 28(19):3005-3014. doi:10.1038/emboj.2009.235
66. Yin J, Kwon YT, Varshavsky A, Wang W (2004) RECQL4, mutated in the Rothmund-Thomson and RAPADILINO syndromes, interacts with ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Hum Mol Genet 13 (20):2421-2430
67. Yokote K, Hara K, Mori S, Kadowaki T, Saito Y, Goto M (2004) Dysadipocytokinemia in werner syndrome and its recovery by treatment with pioglitazone. Diabetes Care 27 (10):2562-2563
68. Zdanov S, Debacq-Chainiaux F, Toussaint O (2007) Knocking down p53 with siRNA does not affect the overexpression of p21WAF-1 after exposure of IMR-90 hTERT fibroblasts to a sublethal concentration of H2O2 leading to premature senescence. Ann N Y Acad Sci 1100:316-322. doi:10.1196/annals.1395.034