Altered telomere homeostasis and resistance to skin carcinogenesis in suv39h1 transgenic mice

Cell Cycle

Volumn 14, Issue 9, 2015, Pages 1438-1446

  Petti, Eleonora ^a   Jordi, Fabian ^b   Buemi, Valentina ^a   Dinami, Roberto ^a   Benetti, Roberta ^a,d   Blasco, Maria A ^b   Schoeftner, Stefan ^a,c  

^a Laboratorio Nazionale CIB LNCIB   (Italy)

^b Structural Biology and Biocomputing Programme   (Spain)

^c UNIVERSITY OF TRIESTE   (Italy)

^d UNIVERSITY OF UDINE   (Italy)

Author keywords

Carcinogenesis; Chromatin; Suv39h HMTase; Telomere length; Telomeres

Indexed keywords

DIMETHYLBENZ[A]ANTHRACENE; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1BETA; HISTONE H3; HISTONE METHYLTRANSFERASE; MICROSATELLITE DNA; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN SUV39H1; UNCLASSIFIED DRUG; 7,12 DIMETHYLBENZ[A]ANTHRACENE; CBX1 PROTEIN, MOUSE; HISTONE; METHYLTRANSFERASE; NONHISTONE PROTEIN; RAS PROTEIN; REPRESSOR PROTEIN; SUV39H1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLONOGENESIS; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; EMBRYO; EPIDERMAL STEM CELL; FIBROBLAST; GENE MUTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE H RAS; SKIN CARCINOGENESIS; TELOMERE HOMEOSTASIS; TELOMERE LENGTH; TELOMERE SHORTENING; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CBA MOUSE; CELL TRANSFORMATION; CHEMICALLY INDUCED; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENZYMOLOGY; EPIDERMIS; FEMALE; GENETICS; MALE; METABOLISM; METHYLATION; MUTATION; PATHOLOGY; SKIN NEOPLASMS; TELOMERE; TUMOR CELL LINE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; EPIDERMIS; FEMALE; HISTONES; HUMANS; MALE; METHYLATION; METHYLTRANSFERASES; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MUTATION; RAS PROTEINS; REPRESSOR PROTEINS; SKIN NEOPLASMS; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

EID: 84983542837     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1021517     Document Type: Article

References (34)

1. Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, et al. Regulation of chromatin structure by sitespecific histone H3 methyltransferases. Nature 2000; 406:593-9; PMID:10949293; http://dx.doi.org/10.1038/35020506
2. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001; 410:116-20; PMID:11242053; http://dx.doi.org/10.1038/35065132
3. Fodor BD, Shukeir N, Reuter G, Jenuwein T. Mammalian Su(var) genes in chromatin control. Annu Rev Cell Dev Biol 2010; 26:471-501; PMID:19575672; http://dx.doi.org/10.1146/annurev.cellbio.042308.113225
4. Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 2001; 107:323-37; PMID:11701123; http://dx.doi.org/10.1016/S0092-8674(01)00542-6
5. Bulut-Karslioglu A, De La Rosa-Velázquez IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J, Galán C, Winter GE, Engist B, Gerle B, et al. Suv39h-Dependent H3K9me3 Marks Intact Retrotransposons and Silences LINE Elements in Mouse Embryonic Stem Cells. Mol Cell 2014; 55:277-90; PMID:24981170; http://dx.doi.org/10.1016/j.molcel.2014.05.029
6. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 2005; 6:611-22; PMID:16136653; http://dx.doi.org/10.1038/nrg1656
7. García-Cao M, O’Sullivan R, Peters AHFM, Jenuwein T, Blasco MA. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 2004; 36:94-9; PMID:14702045; http://dx.doi.org/10.1038/ng1278
8. Benetti R, García-Cao M, Blasco MA. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet 2007; 39:243-50; PMID:17237781; http://dx.doi.org/10.1038/ng1952
9. Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet 2007; 8:299-309; PMID:17363977; http://dx.doi.org/10.1038/nrg2047
10. Chan SRWL, Blackburn EH. Telomeres and telomerase. Philos Trans R Soc Lond B Biol Sci 2004; 359:109-21; PMID:15065663; http://dx.doi.org/10.1098/rstb.2003.1370
11. d’Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003; 426:194-8; PMID:14608368; http://dx.doi.org/10.1038/nature02118
12. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O’Carroll D, Firestein R, Cleary M, Jenuwein T, Herrera RE, et al. Rb targets histone H3 methylation and HP1 to promoters. Nature 2001; 412:561-5; PMID:11484059; http://dx.doi.org/10.1038/35087620
13. Narita M, Ñunez S, Heard E, Narita M, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW. Rbmediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113:703-16; PMID:12809602; http://dx.doi.org/10.1016/S0092-8674(03)00401-X
14. Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AHFM, Schlegelberger B, Stein H, Dörken B, Jenuwein T, Schmitt CA. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 2005; 436:660-5; PMID:16079837; http://dx.doi.org/10.1038/nature03841
15. Reimann M, Lee S, Loddenkemper C, Dörr JR, Tabor V, Aichele P, Stein H, Dörken B, Jenuwein T, Schmitt CA. Tumor stroma-derived TGF-beta limits myc-driven lymphomagenesis via Suv39h1- dependent senescence. Cancer Cell 2010; 17:262-72; PMID:20227040; http://dx.doi.org/10.1016/j. ccr.2009.12.043
16. Lee AC, Fenster BE, Ito H, Takeda K, Bae NS, Hirai T, Yu ZX, Ferrans VJ, Howard BH, Finkel T. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J Biol Chem 1999; 274:7936-40; PMID:10075689; http://dx.doi.org/10.1074/jbc.274.12.7936
17. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, Benguría A, Zaballos A, Flores JM, Barbacid M, et al. Tumour biology: senescence in premalignant tumours. Nature 2005; 436:642; PMID:16079833; http://dx.doi.org/10.1038/436642a
18. Michaloglou C, Vredeveld LCW, Soengas MS, Denoyelle C, Kuilman T, van der Horst CMAM, Majoor DM, Shay JW, Mooi WJ, Peeper DS. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005; 436:720-4; PMID:16079850; http://dx.doi.org/10.1038/ nature03890
19. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre’ M, Nuciforo PG, Bensimon A, et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-42; PMID:17136094; http://dx.doi.org/10.1038/nature05327
20. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou L-VF, Kolettas E, Niforou K, Zoumpourlis VC, et al. Oncogeneinduced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444:633-7; PMID:17136093; http://dx.doi. org/10.1038/nature05268
21. Zinyk DL, Mercer EH, Harris E, Anderson DJ, Joyner AL. Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr Biol 1998; 8:665-8; PMID:9635195; http://dx. doi.org/10.1016/S0960-9822(98)70255-6
22. Melcher M, Schmid M, Aagaard L, Selenko P, Laible G, Jenuwein T. Structure-function analysis of SUV39H1 reveals a dominant role in heterochromatin organization, chromosome segregation, and mitotic progression. Mol Cell Biol 2000; 20:3728-41; PMID:10779362; http://dx.doi.org/10.1128/ MCB.20.10.3728-3741.2000
23. Czvitkovich S, Sauer S, Peters AH, Deiner E, Wolf A, Laible G, Opravil S, Beug H, Jenuwein T. Over-expression of the SUV39H1 histone methyltransferase induces altered proliferation and differentiation in transgenic mice. Mech Dev 2001; 107:141-53; PMID:11520670; http://dx.doi.org/10.1016/S0925-4773(01)00464-6
24. 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; PMID:9054499; http://dx.doi. org/10.1016/S0092-8674(00)81902-9
25. Balmain A, Ramsden M, Bowden GT, Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature 307:658-60; PMID:6694757; http://dx.doi.org/10.1038/307658a0
26. GarcGarcía-Cao I, GarcGarcía-Cao M, Martín-Caballero J, Criado LM, Klatt P, Flores JM, Weill J-C, Blasco MA, Serrano M. "Super p53" mice exhibit enhanced DNA damage response, are tumor resistant and age normally. EMBO J 2002; 21:6225-35; PMID:12426394; http://dx.doi.org/10.1093/emboj/ cdf595
27. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991; 108:193-9; PMID:1660837; http://dx.doi.org/10.1016/0378-1119(91)90434-D
28. Muñoz P, Blanco R, Flores JM, Blasco MA. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat Genet 2005; 37:1063-71; PMID:16142233; http://dx.doi.org/10.1038/ng1633
29. Flores I, Canela A, Vera E, Tejera A, Cotsarelis G, Blasco MA. The longest telomeres: a general signature of adult stem cell compartments. Genes Dev 2008; 22:654-67; PMID:18283121; http://dx.doi.org/10.1101/gad.451008
30. Samper E, Goytisolo FA, Slijepcevic P, van Buul PP, Blasco MA. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep 2000; 1:244-52; PMID:11256607; http://dx.doi.org/10.1093/embo-reports/kvd051
31. Dinami R, Ercolani C, Petti E, Piazza S, Ciani Y, Sestito R, Sacconi A, Biagioni F, le Sage C, Agami R, et al. miR-155 drives telomere fragility in human breast cancer by targeting TRF1. Cancer Res 2014;; PMID:24876105
32. Blanco R, Muñoz P, Flores JM, Klatt P, Blasco MA. Telomerase abrogation dramatically accelerates TRF2- induced epithelial carcinogenesis. Genes Dev 2007; 21:206-20; PMID:17234886; http://dx.doi.org/10.1101/gad.406207
33. Schuler M, Maurer U, Goldstein JC, Breitenbücher F, Hoffarth S, Waterhouse NJ, Green DR. p53 triggers apoptosis in oncogene-expressing fibroblasts by the induction of Noxa and mitochondrial Bax translocation. Cell Death Differ 2003; 10:451-60; PMID:12719722; http://dx.doi.org/10.1038/sj. cdd.4401180
34. Efeyan A, Murga M, Martinez-Pastor B, Ortega-Molina A, Soria R, Collado M, Fernandez-Capetillo O, Serrano M. Limited role of murine ATM in oncogene- induced senescence and p53-dependent tumor suppression. PLoS One 2009; 4:e5475; PMID:19421407; http://dx.doi.org/10.1371/journal. pone.0005475