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The Role of Sumoylation in Senescence

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Book cover SUMO Regulation of Cellular Processes

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 963))

Abstract

Cellular senescence is a program initiated by many stress signals including aberrant activation of oncogenes, DNA damage, oxidative lesions and telomere attrition. Once engaged senescence irreversibly limits cellular proliferation and potently prevents tumor formation in vivo. The precise mechanisms driving the onset of senescence are still not completely defined, although the pRb and p53 tumor suppressor pathways converge with the SUMO cascade to regulate cellular senescence. Sumoylation translocates p53 to PML nuclear bodies where it can co-operate with many sumoylated co-factors in a program that activates pRb and favors senescence. Once activated pRb integrates various proteins, many of them sumoylated, into a repressor complex that inhibits the transcription of proliferation-promoting genes and initiates chromatin condensation. Sumoylation is required for heterochromatin formation during senescence and may act as a scaffold to stabilize the pRb repressor complex. Thus, SUMO is a critical component of a tumor-suppressor network that limits aberrant cell proliferation and tumorigenesis.

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References

  • Adams PD (2007) Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 397:84–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayaydin F, Dasso M (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 15:5208–5218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker DJ, Perez-Terzic C, Jin F, Pitel K, Niederlander NJ, Jeganathan K, Yamada S, Reyes S, Rowe L, Hiddinga HJ, Eberhardt NL, Terzic A, van Deursen JM (2008) Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency. Nat Cell Biol 10:825–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Porath I, Weinberg RA (2005) The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37:961–976

    Article  CAS  PubMed  Google Scholar 

  • Benanti JA, Williams DK, Robinson KL, Ozer HL, Galloway DA (2002) Induction of extracellular matrix-remodeling genes by the senescence-associated protein APA-1. Mol Cell Biol 22:7385–7397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernardi R, Pandolfi PP (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8:1006–1016

    Article  CAS  PubMed  Google Scholar 

  • Binda O, Roy JS, Branton PE (2006) RBP1 family proteins exhibit SUMOylation-dependent transcriptional repression and induce cell growth inhibition reminiscent of senescence. Mol Cell Biol 26:1917–1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bischof O, Dejean A (2007) SUMO is growing senescent. Cell Cycle 6:677–681

    Article  CAS  PubMed  Google Scholar 

  • Bischof O, Kirsh O, Pearson M, Itahana K, Pelicci PG, Dejean A (2002) Deconstructing PML-induced premature senescence. EMBO J 21:3358–3369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bischof O, Schwamborn K, Martin N, Werner A, Sustmann C, Grosschedl R, Dejean A (2006) The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol Cell 22:783–794

    Article  CAS  PubMed  Google Scholar 

  • Blackburn EH (2001) Switching and signaling at the telomere. Cell 106:661–673

    Article  CAS  PubMed  Google Scholar 

  • Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352

    Article  CAS  PubMed  Google Scholar 

  • Brooks CL, Li M, Gu W (2004) Monoubiquitination: The Signal for p53 Nuclear Export? Cell Cycle 3:436–438

    CAS  PubMed  Google Scholar 

  • Bruce SA, Deamond SF, Ts’o PO (1986) In vitro senescence of Syrian hamster mesenchymal cells of fetal to aged adult origin. Inverse relationship between in vivo donor age and in vitro proliferative capacity. Mech Ageing Dev 34:151–173

    Article  CAS  PubMed  Google Scholar 

  • Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel RR (1997) Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3:1271–1274

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Carter S, Vousden KH (2008) p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53. Cell Cycle 7:2519–2528

    Article  CAS  PubMed  Google Scholar 

  • Chang E, Harley CB (1995) Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci U S A 92:11190–11194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Chen J (2003) MDM2-ARF complex regulates p53 sumoylation. Oncogene 22:5348–5357

    Article  CAS  PubMed  Google Scholar 

  • Collado M, Serrano M (2005) The senescent side of tumor suppression. Cell Cycle 4:1722–1724

    Article  CAS  PubMed  Google Scholar 

  • Collado M, Serrano M (2006) The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 6:472–476

    Article  CAS  PubMed  Google Scholar 

  • Cotter MA, Florell SR, Leachman SA, Grossman D (2007) Absence of senescence-associated beta-galactosidase activity in human melanocytic nevi in vivo. J Invest Dermatol 127:2469–2471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cotter MA, Florell SR, Leachman SA, Grossman D (2008) Response to Gray-Schopfer et al. and Michaloglou et al. J Invest Dermatol 128:1583–1584

    Article  CAS  Google Scholar 

  • David G, Neptune MA, DePinho RA (2002) SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J Biol Chem 277:23658–23663

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Di Ventura B, Funaya C, Antony C, Knop M, Serrano L (2008) Reconstitution of Mdm2-dependent post-translational modifications of p53 in yeast. PLoS ONE 3:e1507

    Article  PubMed  PubMed Central  Google Scholar 

  • Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92:9363–9367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duprez E, Saurin AJ, Desterro JM, Lallemand-Breitenbach V, Howe K, Boddy MN, Solomon E, de The H, Hay RT, Freemont PS (1999) SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J Cell Sci 112:381–393

    CAS  PubMed  Google Scholar 

  • Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW (2000) PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 14:2015–2027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fogal V, Gostissa M, Sandy P, Zacchi P, Sternsdorf T, Jensen K, Pandolfi PP, Will H, Schneider C, Del Sal G (2000) Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J 19:6185–6195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalo S, Blasco MA (2005) Role of Rb family in the epigenetic definition of chromatin. Cell Cycle 4:752–755

    Article  CAS  PubMed  Google Scholar 

  • Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, Del Sal G (1999) Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 18:6462–6471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haferkamp S, Becker TM, Scurr LL, Kefford RF, Rizos H (2008) p16INK4a-induced senescence is disabled by melanoma-associated mutations. Aging Cell 7:733–745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345:458–460

    Article  CAS  PubMed  Google Scholar 

  • Haupt Y, Maya R, Kaza A, Oren M (1997) Mdm2 promotes the rapid degradation of p53. Nature 387:296–299

    Article  CAS  PubMed  Google Scholar 

  • Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585–621

    Article  CAS  PubMed  Google Scholar 

  • Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, Kamitani T, Yeh ET, Strauss JF 3rd, Maul GG (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 147:221–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang H, Kim ET, Lee HR, Park JJ, Go YY, Choi CY, Ahn JH (2006) Inhibition of SUMO-independent PML oligomerization by the human cytomegalovirus IE1 protein. J Gen Virol 87:2181–2190

    Article  CAS  PubMed  Google Scholar 

  • Kurz DJ, Decary S, Hong Y, Erusalimsky JD (2000) Senescence-associated (beta)-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J Cell Sci 113:3613–3622

    CAS  PubMed  Google Scholar 

  • Kuwata T, Kitagawa M, Kasuga T (1993) Proliferative activity of primary cutaneous melanocytic tumours. Virchows Arch A Pathol Anat Histopathol 423:359–364

    Article  CAS  PubMed  Google Scholar 

  • Kwek SS, Derry J, Tyner AL, Shen Z, Gudkov AV (2001) Functional analysis and intracellular localization of p53 modified by SUMO-1. Oncogene 20:2587–2599

    Article  CAS  PubMed  Google Scholar 

  • Ledl A, Schmidt D, Muller S (2005) Viral oncoproteins E1A and E7 and cellular LxCxE proteins repress SUMO modification of the retinoblastoma tumor suppressor. Oncogene 24:3810–3818

    Article  CAS  PubMed  Google Scholar 

  • Lee BY, Han JA, Im JS, Morrone A, Johung K, Goodwin EC, Kleijer WJ, DiMaio D, Hwang ES (2006) Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 5:187–195

    Article  CAS  PubMed  Google Scholar 

  • Li T, Santockyte R, Shen RF, Tekle E, Wang G, Yang DC, Chock PB (2006) Expression of SUMO-2/3 Induced Senescence through p53- and pRB-mediated Pathways. J Biol Chem 281:36221–36227

    Article  CAS  PubMed  Google Scholar 

  • Li B, Zhou J, Liu P, Hu J, Jin H, Shimono Y, Takahashi M, Xu G (2007) Polycomb protein Cbx4 promotes SUMO modification of de novo DNA methyltransferase Dnmt3a. Biochem J 405:369–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin DY, Huang YS, Jeng JC, Kuo HY, Chang CC, Chao TT, Ho CC, Chen YC, Lin TP, Fang HI, Hung CC, Suen CS, Hwang MJ, Chang KS, Maul GG, Shih HM (2006) Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol Cell 24:341–354

    Article  CAS  PubMed  Google Scholar 

  • Ling Y, Sankpal UT, Robertson AK, McNally JG, Karpova T, Robertson KD (2004) Modification of de novo DNA methyltransferase 3a (Dnmt3a) by SUMO-1 modulates its interaction with histone deacetylases (HDACs) and its capacity to repress transcription. Nucleic Acids Res 32:598–610 . Print 2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maldonado JL, Timmerman L, Fridlyand J, Bastian BC (2004) Mechanisms of cell-cycle arrest in Spitz nevi with constitutive activation of the MAP-kinase pathway. Am J Pathol 164:1783–1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauri F, McNamee LM, Lunardi A, Chiacchiera F, Del Sal G, Brodsky MH, Collavin L (2008) Modification of Drosophila p53 by SUMO modulates its transactivation and pro-apoptotic functions. J Biol Chem 283:20848–20856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michaloglou C, Soengas MS, Mooi WJ, Peeper DS (2008) Comment on “Absence of senescence-associated beta-galactosidase activity in human melanocytic nevi in vivo”. J. Invest. Dermatol. 128:1582–1583 ; author reply 1583–1584

    Article  CAS  PubMed  Google Scholar 

  • Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, Majoor DM, Shay JW, Mooi WJ, Peeper DS (2005) BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436:720–724

    Article  CAS  PubMed  Google Scholar 

  • Mooi WJ, Peeper DS (2006) Oncogene-induced cell senescence–halting on the road to cancer. N Engl J Med 355:1037–1046

    Article  CAS  PubMed  Google Scholar 

  • Morris EJ, Dyson NJ (2001) Retinoblastoma protein partners. Adv Cancer Res 82:1–54

    Article  CAS  PubMed  Google Scholar 

  • Muller S, Berger M, Lehembre F, Seeler JS, Haupt Y, Dejean A (2000) c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 275:13321–13329

    Article  CAS  PubMed  Google Scholar 

  • Narita M, Nunez S, Heard E, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW (2003) Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703–716

    Article  CAS  PubMed  Google Scholar 

  • Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S, Higashimoto Y, Appella E, Minucci S, Pandolfi PP, Pelicci PG (2000) PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406:207–210

    Article  CAS  PubMed  Google Scholar 

  • Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, Moses TY, Hostetter G, Wagner U, Kakareka J, Salem G, Pohida T, Heenan P, Duray P, Kallioniemi O, Hayward NK, Trent JM, Meltzer PS (2003) High frequency of BRAF mutations in nevi. Nat Genet 33:19–20

    Article  CAS  PubMed  Google Scholar 

  • Potts PR, Yu H (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol 14:581–590

    Article  CAS  PubMed  Google Scholar 

  • Price JS, Waters JG, Darrah C, Pennington C, Edwards DR, Donell ST, Clark IM (2002) The role of chondrocyte senescence in osteoarthritis. Aging Cell 1:57–65

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MS, Desterro JM, Lain S, Midgley CA, Lane DP, Hay RT (1999) SUMO-1 modification activates the transcriptional response of p53. EMBO J 18:6455–6461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roninson IB (2003) Tumor cell senescence in cancer treatment. Cancer Res 63:2705–2715

    CAS  PubMed  Google Scholar 

  • Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22:6068–6077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15:3088–3103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saitoh N, Uchimura Y, Tachibana T, Sugahara S, Saitoh H, Nakao M (2006) In situ SUMOylation analysis reveals a modulatory role of RanBP2 in the nuclear rim and PML bodies. Exp Cell Res 312:1418–1430

    Article  CAS  PubMed  Google Scholar 

  • Schmidt D, Müller S (2002) Member of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci U S A 99:2872–2877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt CA, Fridman JS, Yang M, Lee S, Baranov E, Hoffman RM, Lowe SW (2002) A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 109:335–346

    Article  CAS  PubMed  Google Scholar 

  • Schneider EL, Mitsui Y (1976) The relationship between in vitro cellular aging and in vivo human age. Proc Natl Acad Sci U S A 73:3584–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekiyama N, Ikegami T, Yamane T, Ikeguchi M, Uchimura Y, Baba D, Ariyoshi M, Tochio H, Saitoh H, Shirakawa M (2008) Structure of the sumo-interacting motif of MCAF1 bound to sumo-3. J Biol Chem 7:7

    Google Scholar 

  • Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ (2000) Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 257:162–171

    Article  CAS  PubMed  Google Scholar 

  • Shay JW (1997) Telomerase in human development and cancer. J Cell Physiol 173:266–270

    Article  CAS  PubMed  Google Scholar 

  • Shen TH, Lin HK, Scaglioni PP, Yung TM, Pandolfi PP (2006) The mechanisms of PML-nuclear body formation. Mol Cell 24:331–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherr CJ (1996) Cancer cell cycles. Science 274:1672–1677

    Article  CAS  PubMed  Google Scholar 

  • Sherr CJ, McCormick F (2002) The RB and p53 pathways in cancer. Cancer Cell 2:103–112

    Article  CAS  PubMed  Google Scholar 

  • Shin JA, Choi ES, Kim HS, Ho JC, Watts FZ, Park SD, Jang YK (2005) SUMO modification is involved in the maintenance of heterochromatin stability in fission yeast. Mol Cell 19:817–828

    Article  CAS  PubMed  Google Scholar 

  • Stielow B, Sapetschnig A, Wink C, Kruger I, Suske G (2008) SUMO-modified Sp3 represses transcription by provoking local heterochromatic gene silencing. EMBO Rep 9:899–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugrue MM, Shin DY, Lee SW, Aaronson SA (1997) Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc Natl Acad Sci U S A 94:9648–9653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi K, Yoshida N, Murakami N, Kawata K, Ishizaki H, Tanaka-Okamoto M, Miyoshi J, Zinn AR, Shime H, Inoue N (2007) Dynamic regulation of p53 subnuclear localization and senescence by MORC3. Mol Biol Cell 18:1701–1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Nishide J, Okazaki K, Kato H, Niwa O, Nakagawa T, Matsuda H, Kawamukai M, Murakami Y (1999) Characterization of a fission yeast SUMO-1 homologue, pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol Cell Biol 19:8660–8672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Qu LK, Zhang J, Wang W, Michaelson JS, Degenhardt YY, El-Deiry WS, Yang X (2006) Critical role for Daxx in regulating Mdm2. Nat Cell Biol 8:855–862

    Article  CAS  PubMed  Google Scholar 

  • te Poele RH, Okorokov AL, Jardine L, Cummings J, Joel SP (2002) DNA damage is able to induce senescence in tumor cells in vitro and in vivo. Cancer Res 62:1876–1883

    Google Scholar 

  • Trimarchi JM, Lees JA (2002) Sibling rivalry in the E2f family. Nat Rev Mol Cell Biol 3:11–20

    Article  CAS  PubMed  Google Scholar 

  • Uchimura Y, Ichimura T, Uwada J, Tachibana T, Sugahara S, Nakao M, Saitoh H (2006) Involvement of SUMO modification in MBD1- and MCAF1-mediated heterochromatin formation. J Biol Chem 281:23180–23190

    Article  CAS  PubMed  Google Scholar 

  • Xhemalce B, Riising EM, Baumann P, Dejean A, Arcangioli B, Seeler JS (2007) Role of SUMO in the dynamics of telomere maintenance in fission yeast. Proc Natl Acad Sci U S A 104:893–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Sharrocks AD (2004) SUMO promotes HDAC-mediated transcriptional repression. Mol Cell 13:611–617

    Article  CAS  PubMed  Google Scholar 

  • Yates KE, Korbel GA, Shtutman M, Roninson IB, Dimaio D (2008) Repression of the SUMO-specific protease 1 induces p53-dependent premature senescence in normal human fibroblasts. Aging Cell 24:24

    Google Scholar 

  • Ye X, Zerlanko B, Zhang R, Somaiah N, Lipinski M, Salomoni P, Adams PD (2007) Definition of pRB- and p53-dependent and -independent steps in HIRA/ASF1a-mediated formation of senescence-associated heterochromatin foci. Mol Cell Biol 27:2452–2465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR (1999) Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res 59:4175–4179

    CAS  PubMed  Google Scholar 

  • Zhang R, Chen W, Adams PD (2007) Molecular dissection of formation of senescence-associated heterochromatin foci. Mol Cell Biol 27:2343–2358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Poustovoitov MV, Ye X, Santos HA, Chen W, Daganzo SM, Erzberger JP, Serebriiskii IG, Canutescu AA, Dunbrack RL, Pehrson JR, Berger JM, Kaufman PD, Adams PD (2005) Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell 8:19–30

    Article  CAS  PubMed  Google Scholar 

  • Zhong S, Muller S, Ronchetti S, Freemont PS, Dejean A, Pandolfi PP (2000) Role of SUMO-1-modified PML in nuclear body formation. Blood 95:2748–2752

    CAS  PubMed  Google Scholar 

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Acknowledgements

Our work is supported by the National Health and Medical Research Council of Australia (NHMRC), the Cancer Council of New South Wales and an infrastructure grant to Westmead Millennium Institute by the Health Department of NSW through Sydney West Area Health Service.

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Authors and Affiliations

  1. Faculty of Medicine and Health Sciences, Macquarie University, NSW, Sydney, 2109, Australia

    Lyndee L. Scurr & Helen Rizos

  2. UKR - Universitätsklinikum Regensburg, Klinik und Poliklinik für Dermatologie, Franz-Josef-Strauss-Allee 11, D-93053, Regensburg, Germany

    Sebastian Haferkamp

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Correspondence to Helen Rizos .

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  1. Department of Microbial Pathogenesis and Immunology, College of Medicine, Texas A&M Health Science Center, Bryan, Texas, USA

    Van G. Wilson

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Scurr, L.L., Haferkamp, S., Rizos, H. (2017). The Role of Sumoylation in Senescence. In: Wilson, V. (eds) SUMO Regulation of Cellular Processes. Advances in Experimental Medicine and Biology, vol 963. Springer, Cham. https://doi.org/10.1007/978-3-319-50044-7_13

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