Oxidative DNA damage induces the ATM-mediated transcriptional suppression of the Wnt inhibitor WIF-1 in systemic sclerosis and fibrosis

Science Signaling

Volumn 7, Issue 341, 2014, Pages

  Svegliati, Silvia ^a   Marrone, Giusi ^b   Pezone, Antonio ^b   Spadoni, Tatiana ^a   Grieco, Antonella ^a   Moroncini, Gianluca ^a,c   Grieco, Domenico ^b   Vinciguerra, Maria ^d   Agnese, Savina ^b   Jüngel, Astrid ^e   Distler, Oliver ^e   Musti, Anna Maria ^f   Gabrielli, Armando ^a,c   Avvedimento, Enrico V ^b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c OSPEDALI RIUNITI   (Italy)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f UNIVERSITY OF CALABRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ATM PROTEIN; AZACITIDINE; BETA CATENIN; BLEOMYCIN; COLLAGEN; HISTONE DEACETYLASE 3; HYDROGEN PEROXIDE; IMMUNOGLOBULIN; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; PROTEIN C JUN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TRICHOSTATIN A; UNCLASSIFIED DRUG; WNT INHIBITOR FACTOR 1; WNT PROTEIN; ANTINEOPLASTIC ANTIBIOTIC; ATM PROTEIN, HUMAN; COLLAGEN TYPE 1; COLLAGEN TYPE I, ALPHA 1 CHAIN; HYDROXAMIC ACID; IMMUNOGLOBULIN G; OXYGEN; PROTEIN SYNTHESIS INHIBITOR; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; WIF1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER PATIENT; CELL LYSATE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DEACETYLATION; DNA DAMAGE; DNA DAMAGE CHECKPOINT; EXPERIMENTAL FIBROSIS; FEMALE; FIBROBLAST; FIBROSIS; GENE EXPRESSION; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MCF 7 CELL LINE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SKIN BIOPSY; SYSTEMIC SCLEROSIS; ULTRAVIOLET RADIATION; WESTERN BLOTTING; BIOPSY; CHEMISTRY; DNA METHYLATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIBIOTICS, ANTINEOPLASTIC; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BIOPSY; BLEOMYCIN; COLLAGEN TYPE I; DNA DAMAGE; DNA METHYLATION; FIBROBLASTS; FIBROSIS; GENE SILENCING; HUMANS; HYDROXAMIC ACIDS; IMMUNOGLOBULIN G; OXIDATIVE STRESS; OXYGEN; PROTEIN SYNTHESIS INHIBITORS; REACTIVE OXYGEN SPECIES; REPRESSOR PROTEINS; SCLERODERMA, SYSTEMIC; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84907576727     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004592     Document Type: Article

References (58)

1. J. C. Gross, V. Chaudhary, K. Bartscherer, M. Boutros, Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 10, 1036-1045 (2012).
2. L. Ling, V. Nurcomb, S. M. Cool, Wnt signaling controls the fate of mesenchymal stem cells. Gene 433, 1-7 (2009).
3. C. M. Cruciat, C. Niehrs, Secreted and transmembrane Wnt inhibitors and activators. Cold Spring Harb. Perspect. Biol. 5, a015081 (2013).
4. Y. Kawano, R. Kypta, Secreted antagonists of the Wnt signaling pathway. J. Cell Sci. 1, 2627-2634 (2003).
5. J. C. Hsieh, L. Kodjabachian, M. L. Rebbert, A. Rattner, P. M. Smallwood, C. H. Samos, R. Nusse, I. B. Dawid, J. Nathans, A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 398, 431-436 (1999).
6. C.Wissmann, P. J.Wild, S. Kaiser, S. Roepcke, R. Stoehr, M.Woenckhaus, G. Kristiansen, J. Hsieh, F. Hofstaedter, A. Hartmann, R. Knuechel, A. Rosenthal, C. Pilarsky, WIF1, a component of the Wnt pathway, is down-regulated in prostate, breast, lung, and bladder cancer. J. Pathol. 201, 204-212 (2003).
7. J. Mazieres, B. He, L. You, Z. Xu, A. Y. Lee, I. Mikami, N. Reguart, R. Rosell, F. McCormick, D. M. Jablons, Wnt inhibitory factor-1 is silenced by promoter hypermethylation in human lung cancer. Cancer Res. 64, 4717-4720 (2004).
8. A. S. Brack, M. J. Conboy, S. Roy, M. Lee, C. J. Kuo, C. Keller, T. A. Rando, Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810 (2007).
9. C. Beyer, A. Schramm, A. Akhmetshina, C. Dees, T. Kireva, K. Gelse, S. Sonnylal, B. de Crombrugghe, M. M. Taketo, O. Distler, G. Schett, J. H. Distler, b-Catenin is a central mediator of pro-fibrotic Wnt signaling in systemic sclerosis. Ann. Rheum. Dis. 71, 761-767 (2012).
10. S. Svegliati, R. Cancello, P. Sambo, M. Luchetti, P. Paroncini, G. Orlandini, G. Discepoli, R. Paternò, M. Santillo, C. Cuozzo, S. Cassano, E. V. Avvedimento, A. Gabrielli, Plateletderived growth factor and reactive oxygen species (ROS) regulate Ras protein levels in primary human fibroblasts via ERK1/2. Amplification of ROS and Ras in systemic sclerosis fibroblasts. J. Biol. Chem. 280, 36474-36482 (2005).
11. S. S. Baroni, M. Santillo, F. Bevilacqua, M. Luchetti, T. Spadoni, M. Mancini, P. Fraticelli, P. sambo, A. Funaro, A. Kazlauskas, E. V. Avvedimento, A. Gabrielli, Stimulatory autoantibodies to the PDGF receptor in systemic sclerosis. N. Engl. J. Med. 354, 2667-2676 (2006).
12. Y. Ying, Q. Tao, Epigenetic disruption of the WNT/b-catenin signaling pathway in human cancers. Epigenetics 4, 307-312 (2009).
13. J. Wei, F. Fang, A. P. Lam, J. L. Sargent, E. Hamburg, M. E. Hinchcliff, C. J. Gottardi, R. Atit, M. L. Whitfield, J. Varga, Wnt/b-catenin signaling is hyperactivated in systemic sclerosis and induces Smad-dependent fibrotic responses in mesenchymal cells. Arthritis Rheum. 64, 2734-2745 (2012).
14. L. Ai, Q.Tao, S. Zhong, C. R.Fields,W. Kim,M.W.Lee, Y. Cui, K. D. Brown, K.D. Robertson, Inactivation of Wnt inhibitory factor-1 (WIF1) expression by epigenetic silencing is a common event in breast cancer. Carcinogenesis 27, 1341-1348 (2006).
15. R.Gherzi,M. Trabucchi,M. Ponassi, T. Ruggiero, G. Corte, C. Moroni, C. Y. Chen, K. S. Khabar, J. S. Andersen, P. Briata, The RNA-binding protein KSRP promotes decay of b-catenin mRNA and is inactivated by PI3K-AKT signaling. PLOS Biol. 5, e5 (2006).
16. M. Königshoff, N. Balsara, E. M. Pfaff, M. Kramer, I. Chrobak, W. Seeger, O. Eickelberg, Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLOS One 3, e2142 (2008).
17. A. Akhmetshina, K. Palumbo, C. Dees, C. Bergmann, P. Venalis, P. Zerr, A. Horn, T. Kireva, C. Beyer, J. Zwerina, H. Schneider, A. Sadowski, M. Riener, O. A. MacDougald, O. Distler, G. Sheet, J. Distler, Activation of canonical Wnt signaling is required for TGF-b-mediated fibrosis. Nat. Commun. 3, 735 (2012).
18. J. H. Cheng, H. She, Y. Han, J. Wang, S. Xiong, K. Asahina, H. Tsukamoto, Wnt antagonism inhibits hepatic stellate cell activation and liver fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G39-G49 (2008).
19. S. Damiano, R. Fusco, A. Morano, M. De Mizio, R. Paternò, A. De Rosa, R. Spinelli, S. Amente, R. Frunzio, P. Mondola, F. Miot, P. Laccetti, M. Santillo, E. V. Avvedimento, Reactive oxygen species regulate the levels of dual oxidase (Duox1-2) in human neuroblastoma cells. PLOS One 7, e34405 (2012).
20. Z. Guo, S. Kozlov, M. F. Lavin, M. D. Person, T. T. Paul, ATM activation by oxidative stress. Science 330, 517-521 (2010).
21. J. Chen, J. Stubbe, Bleomycins: Towards better therapeutics. Nat. Rev. Cancer 5, 102-112 (2005).
22. A. Shibata, O. Barton, A. T. Noon, K. Dahm, D. Deckbar, A. A. Goodarzi, M. Löbrich, P. A. Jeggo, Role of ATM and the damage response mediator proteins 53BP1 and MDC1 in the maintenance of G2/M checkpoint arrest. Mol. Cell. Biol. 30, 3371-3383 (2010).
23. S. Bhattacharyya, J. Wei, W. G. Tourtellotte, M. Hinchcliff, C. G. Gottardi, J. Varga, Fibrosis in systemic sclerosis: Common and unique pathobiology. Fibrogenesis Tissue Repair 5 (Suppl. 1), S18 (2012).
24. H. Noh, E. Y. Oh, J. Y. Seo, M. R. Yu, Y. O. Kim, H. Ha, H. B. Lee, Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-b1-induced renal injury. Am. J. Physiol. Renal Physiol. 297, F729-F739 (2009).
25. H. Zhu, L. Shan, P. W. Schiller, A. Mai, T. Peng, Histone deacetylase-3 activation promotes tumor necrosis factor-a (TNF-a) expression in cardiomyocytes during lipopolysaccharide stimulation. J. Biol. Chem. 285, 9429-9436 (2010).
26. N. Koshikawa, J. Hayashi, A. Nakagawara, K. Takenaga, Reactive oxygen speciesgenerating mitochondrial DNA mutation up-regulates hypoxia-inducible factor-1a gene transcription via phosphatidylinositol 3-kinase-Akt/protein kinase C/histone deacetylase pathway. J. Biol. Chem. 284, 33185-33194 (2009).
27. L. C. Huber, J. Distler, F. Moritz, H. Hemmatazad, T. Hauser, B. A. Michel, R. E. Gay, M. Matucci-Cerinic, S. Gay, O. Distler, A. Jüngel, Trichostatin A prevents the accumulation of extracellular matrix in a mouse model of bleomycin-induced skin fibrosis. Arthritis Rheum. 56, 2755-2764 (2007).
28. F. Pacifico, C. Mauro, C. Barone, E. Crescenzi, S. Mellone, M. Monaco, G. Chiappetta, G. Terrazzano, D. Liguoro, P. Vito, E. Consiglio, S. Formisano, A. Leonardi, Oncogenic and anti apoptotic activity of NF-kB in human thyroid carcinomas. J. Biol. Chem. 279, 54610-54619 (2004).
29. M. Bahassi el, S. Karyala, C. R. Tomlinson, M. A. Sartor, M. Medvedovic, R. F. Hennigan, Critical regulation of genes for tumor cell migration by AP-1. Clin. Exp. Metastasis 21, 293-304 (2004).
30. F. Talotta, T. Mega, G. Bossis, L. Casalino, J. Basbous, I. Jariel-Encontre, M. Piechaczyk, P. Verde, Heterodimerization with Fra-1 cooperates with the ERK pathway to stabilize c-Jun in response to the RAS oncoprotein. Oncogene 29, 4732-4740 (2010).
31. T. Hai, C. D. Wolfgang, D. K. Marsee, A. E. Allen, U. Sivaprasad, ATF3 and stress responses. Gene Expr. 7, 321-335 (1999).
32. K. Y. Chung, A. Agarwal, I. Uitto, A. Mauviel, An AP-1 binding sequence is essential for regulation of the human a2(I) collagen (COL1A2) promoter activity by transforming growth factor-b. J. Biol. Chem. 271, 3272-3278 (1996).
33. A. K. Ghosh, Factors involved in the regulation of type I collagen gene expression: Implication in fibrosis. Exp. Biol. Med. 227, 301-314 (2002).
34. S. Morton, R. J. Davis, A. McLaren, P. Cohen, A reinvestigation of the multisite phosphorylation of the transcription factor c-Jun. EMBO J. 22, 3876-3886 (2003).
35. M. Vinciguerra, I. Esposito, S. Salzano, A. Madeo, G. Nagel, M. Maggiolini, A. Gallo, A. M. Musti, Negative charged threonine 95 of c-Jun is essential for c-Jun N-terminal kinase-dependent phosphorylation of threonine 91/93 and stress-induced c-Jun biological activity. Int. J. Biochem. Cell Biol. 40, 307-316 (2008).
36. C. E. Reddy, L. Albaniro, P. De Marco, D. Aiello, M. Maggiolini, A. Napoli, A. M. Musti, Multisite phosphorylation of c-Jun at threonine 91/93/95 triggers the onset of c-Jun pro/apoptotic activity in cerebellar granule neurons. Cell Death Dis. 4, e852 (2013).
37. Y. Tanaka, A. Nakamura, M. S. Morioka, S. Inoue, M. Tamamori-Adachi, K. Yamada, K. Taketani, J. Kawauchi, M. Tanaka-Okamoto, J. Miyoshi, H. Tanaka, S. Kitajima, Systems analysis of ATF3 in stress response and cancer reveals opposing effects on pro-apoptotic genes in p53 pathway. PLOS One 6, e26848 (2011).
38. M. Cebrat, L. Strzadala, P. Kisielow, Wnt inhibitory factor-1: A candidate for a new player in tumorigenesis of intestinal epithelial cells. Cancer Lett. 206, 107-113 (2004).
39. J. W. Wen, J. T. Hwang, G. M. Kelly, Reactive oxygen species and Wnt signalling crosstalk patterns mouse extraembryonic endoderm. Cell. Signal. 24, 2337-2348 (2012).
40. Z. Guo, R. Deshpande, T. Paull, ATM activation in the presence of oxidative stress. Cell Cycle 9, 4805-4811 (2010).
41. C. Cosentino, D. Grieco, V. Costanzo, ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J. 30, 546-555 (2011).
42. A. Gabrielli, E. V. Avvedimento, T. Krieg, Scleroderma. N. Engl. J. Med. 360, 1989-2003 (2009).
43. L. A. Rowe, N. Degtyareva, P. W. Doetsch, DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae. Free Radic. Biol. Med. 45, 1167-1177 (2008).
44. D. Lallemand, G. Spyrou, M. Yaniv, C. M. Pfarr, Variations in Jun and Fos protein expression and AP-1 activity in cycling, resting and stimulated fibroblasts. Oncogene 14, 819-830 (1997).
45. Y. Chinenov, T. Kerppola, Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20, 2438-2452 (2001).
46. L. Shu, K. C. Shen, Y. Wang, S. C. Brooks, Y. A. Wang, Impaired hepatocyte survival and liver regeneration in Atm-deficient mice. Hum. Mol. Genet. 14, 3019-3025 (2005).
47. G. Liang, C. D. Wolfgang, B. P. Chen, T. H. Chen, T. Hai, ATF3 gene. Genomic organization promoter, and regulation. J. Biol. Chem. 271, 1695-1701 (1996).
48. K. Toualbi, M. C. Güller, J. L. Mauriz, C. Labalette, M. A. Buendia, A. Mauviel, D. Bernuau, Physical and functional cooperation between AP-1 and b-catenin for the regulation of TCF-dependent genes. Oncogene 26, 3492-3502 (2007).
49. A. L. Delmas, B. M. Riggs, C. E. Pardo, L. M. Duer, R. P. Darst, E. G. Izumchenko, M. Monroe, A. Hakam, M. P. Kladde, E. M. Siegel, K. D. Brown, WIF1 is a frequent target for epigenetic silencing in squamous cell carcinoma of the cervix. Carcinogenesis 32, 1625-1633 (2011).
50. M. Kansara, M. Tsang, L. Kodjabachian, N. A. Sims, M. K. Trivett, M. Ehrich, A. Dobrovic, J. slavin, P. F. Choong, P. J. Simmons, I. B. Dawid, D. M. Thomas, Wnt inhibitory factor 1 is epigenetically silenced inhuman osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice. J. Clin. Invest. 119, 837-851 (2009).
51. E. V. Avvedimento, S. Obici, M. Sanchez, A. Gallo, A. Musti, M. E. Gottesman, Reactivation of thyroglobulin gene expression in transformed thyroid cells by 5-azacytidine. Cell 58, 1135-1142 (1989).
52. B. L. Vaes, K. J. Dechering, E. P. van Someren, J. M. Hendriks, C. J. van de Ven, A. Feijen, C. L. Mummery, M. J. Reinders, W. Olijve, E. J. van Zoelen, W. T. Steegenga, Microarray analysis reveals expression regulation of Wnt antagonists in differentiating osteoblasts. Bone 36, 803-811 (2005).
53. M. Bocchino, S. Agnese, E. Fagone, S. Svegliati, D. Grieco, C. Vancheri, A. Gabrielli, A. Sanduzzi, E. V. Avvedimento, Reactive oxygen species are required for maintenance and differentiation of primary lung fibroblasts in idiopathic pulmonary fibrosis. PLOS One 5, e14003 (2010).
54. D. Y. Zhang, Y. Pan, C. Zhang, B. X. Yan, S. S. Yu, D. L.Wu, M. M. Shi, K. Shi, X. X. Cai, S. S. Zhou, J. B. Wang, J. P. Pan, L. H. Zhang, Wnt/b-catenin signaling induces the aging of mesenchymal stem cells through promoting the ROS production. Mol. Cell. Biochem. 374, 13-20 (2013).
55. A. Milano, S. A. Pendergrass, J. L. Sargent, L. K. George, T. H. McCalmont, M. K. Connolly, M. L. Whitfield, Molecular subsets in the gene expression signatures of scleroderma skin. PLOS One 3, e2696 (2008).
56. D.Wu,P.Wong, W. Li,C. F. Vogel, F. Matsumura,Suppression of WIF-1 through promoter hypermethylation causes accelerated proliferation of the aryl hydrocarbon receptor (AHR) overexpressing MCF10AT1 breast cancer cells. Toxicology 285, 97-103 (2011).
57. J. Behari, The Wnt/b-catenin signaling pathway in liver biology and disease. Expert Rev. Gastroenterol. Hepatol. 4, 745-759 (2010).
58. M. Bonifazi, I. Tramacere, G. Pomponio, B. Gabrielli, E. V. Avvedimento, C. La Vecchia, E. Negri, A. Gabrielli, Systemic sclerosis (scleroderma) and cancer risk: Systematic review and meta-analysis of observational studies. Rheumatology 52, 143-154 (2013).