Skip to main content
SpringerLink
Log in
Book cover

SUMO Regulation of Cellular Processes pp 283–298Cite as

Sumoylation and Its Contribution to Cancer

  • Chapter
  • First Online:

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

Abstract

Post-translational modifications play an important role in regulating protein activity by altering their functions. Sumoylation is a highly dynamic process which is tightly regulated by a fine balance between conjugating and deconjugating enzyme activities. It affects intracellular localization and their interaction with their binding partners, thereby changing gene expression. Consequently, these changes in turn affect signaling mechanisms that regulate many cellular functions, such as cell growth, proliferation, apoptosis , DNA repair , and cell survival. It is becoming apparent that deregulation in the SUMO pathway contributes to oncogenic transformation by affecting sumoylation/desumoylation of many oncoproteins and tumor suppressors. Loss of balance between sumoylation and desumoylation has been reported in a number of studies in a variety of disease types including cancer. This chapter summarizes the mechanisms and functions of the deregulated SUMO pathway affecting oncogenes and tumor suppressor genes.

Jason S. Lee and Hee June Choi authors contributed equally to this work.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Anckar J, Sistonen L (2007) SUMO: getting it on. Biochem Soc Trans 35:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK, Rosenfeld MG (2002) Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110:55–67

    Article  CAS  PubMed  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 

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

    Article  CAS  PubMed  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 

  • Bode AM, Dong Z (2004) Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 4:793–805

    Article  CAS  PubMed  Google Scholar 

  • Boggio R, Colombo R, Hay RT, Draetta GF, Chiocca S (2004) A mechanism for inhibiting the SUMO pathway. Mol Cell 16:549–561

    Article  CAS  PubMed  Google Scholar 

  • Bossis G, Melchior F (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol Cell 21:349–357

    Article  CAS  PubMed  Google Scholar 

  • Bossis G, Malnou CE, Farras R, Andermarcher E, Hipskind R, Rodriguez M, Schmidt D, Muller S, Jariel-Encontre I, Piechaczyk M (2005) Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol Cell Biol 25:6964–6979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks CL, Gu W (2006) p53 ubiquitination: Mdm2 and beyond. Mol Cell 21:307–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buschmann T, Fuchs SY, Lee CG, Pan ZQ, Ronai Z (2000) SUMO-1 modification of Mdm2 prevents its self-ubiquitination and increases Mdm2 ability to ubiquitinate p53. Cell 101:753–762

    Article  CAS  PubMed  Google Scholar 

  • Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell 131:309–323

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarti SR, Sood R, Ganguly S, Bohlander S, Shen Z, Nucifora G (1999) Modulation of TEL transcription activity by interaction with the ubiquitin-conjugating enzyme UBC9. Proc Natl Acad Sci U S A 96:7467–7472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakrabarti SR, Sood R, Nandi S, Nucifora G (2000) Posttranslational modification of TEL and TEL/AML1 by SUMO-1 and cell-cycle-dependent assembly into nuclear bodies. Proc Natl Acad Sci U S A 97:13281–13285

    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 

  • Cheng J, Bawa T, Lee P, Gong L, Yeh ET (2006) Role of desumoylation in the development of prostate cancer. Neoplasia 8:667–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Ke Y, Ding X, Wang F, Wang H, Wang W, Ahmed K, Liu Z, Xu Y, Aikhionbare F, Yan H, Liu J, Xue Y, Yu J, Powell M, Liang S, Wu Q, Reddy SE, Hu R, Huang H, Jin C, Yao X (2008) Functional characterization of TIP60 sumoylation in UV-irradiated DNA damage response. Oncogene 27:931–941

    Article  CAS  PubMed  Google Scholar 

  • Dai MS, Jin Y, Gallegos JR, Lu H (2006) Balance of Yin and Yang: ubiquitylation-mediated regulation of p53 and c-Myc. Neoplasia 8:630–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S, Shuai K, Grosschedl R, van Deursen JM (2008) Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133:103–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Depaux A, Regnier-Ricard F, Germani A, Varin-Blank N (2007) A crosstalk between hSiah2 and Pias E3-ligases modulates Pias-dependent activation. Oncogene 26:6665–6676

    Article  CAS  PubMed  Google Scholar 

  • Desterro JM, Rodriguez MS, Hay RT (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2:233–239

    Article  CAS  PubMed  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 

  • Faus H, Haendler B (2006) Post-translational modifications of steroid receptors. Biomed Pharmacother 60:520–528

    Article  CAS  PubMed  Google Scholar 

  • Fenrick R, Wang L, Nip J, Amann JM, Rooney RJ, Walker-Daniels J, Crawford HC, Hulboy DL, Kinch MS, Matrisian LM, Hiebert SW (2000) TEL, a putative tumor suppressor, modulates cell growth and cell morphology of ras-transformed cells while repressing the transcription of stromelysin-1. Mol Cell Biol 20:5828–5839

    Article  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 

  • Gambacorta M, Flenghi L, Fagioli M, Pileri S, Leoncini L, Bigerna B, Pacini R, Tanci LN, Pasqualucci L, Ascani S, Mencarelli A, Liso A, Pelicci PG, Falini B (1996) Heterogeneous nuclear expression of the promyelocytic leukemia (PML) protein in normal and neoplastic human tissues. Am J Pathol 149:2023–2035

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8:947–956

    Article  CAS  PubMed  Google Scholar 

  • Geletu M, Balkhi MY, Peer Zada AA, Christopeit M, Pulikkan JA, Trivedi AK, Tenen DG, Behre G (2007) Target proteins of C/EBPalphap30 in AML: C/EBPalphap30 enhances sumoylation of C/EBPalphap42 via up-regulation of Ubc9. Blood 110:3301–3309

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Karin M (2002) Missing pieces in the NF-kappaB puzzle. Cell 109:S81–S96

    Article  CAS  PubMed  Google Scholar 

  • Golub TR, Barker GF, Stegmaier K, Gilliland DG (1997) The TEL gene contributes to the pathogenesis of myeloid and lymphoid leukemias by diverse molecular genetic mechanisms. Curr Top Microbiol Immunol 220:67–79

    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 

  • Gregoire S, Tremblay AM, Xiao L, Yang Q, Ma K, Nie J, Mao Z, Wu Z, Giguere V, Yang XJ (2006) Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J Biol Chem 281:4423–4433

    Article  CAS  PubMed  Google Scholar 

  • Gresko E, Moller A, Roscic A, Schmitz ML (2005) Covalent modification of human homeodomain interacting protein kinase 2 by SUMO-1 at lysine 25 affects its stability. Biochem Biophys Res Commun 329:1293–1299

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez GJ, Ronai Z (2006) Ubiquitin and SUMO systems in the regulation of mitotic checkpoints. Trends Biochem Sci 31:324–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardeland U, Steinacher R, Jiricny J, Schar P (2002) Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J 21:1456–1464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A, Sistonen L (2006) PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci U S A 103:45–50

    Article  CAS  PubMed  Google Scholar 

  • Hilgarth RS, Hong Y, Park-Sarge OK, Sarge KD (2003) Insights into the regulation of heat shock transcription factor 1 SUMO-1 modification. Biochem Biophys Res Commun 303:196–200

    Article  CAS  PubMed  Google Scholar 

  • Hirvonen-Santti SJ, Rannikko A, Santti H, Savolainen S, Nyberg M, Janne OA, Palvimo JJ (2003) Down-regulation of estrogen receptor beta and transcriptional coregulator SNURF/RNF4 in testicular germ cell cancer. Eur Urol 44:742–747

    Article  CAS  PubMed  Google Scholar 

  • Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141

    Article  CAS  PubMed  Google Scholar 

  • Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell 115:565–576

    Article  CAS  PubMed  Google Scholar 

  • Ihara M, Yamamoto H, Kikuchi A (2005) SUMO-1 modification of PIASy, an E3 ligase, is necessary for PIASy-dependent activation of Tcf-4. Mol Cell Biol 25:3506–3518

    Article  CAS  PubMed  PubMed Central  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 

  • Jacques C, Baris O, Prunier-Mirebeau D, Savagner F, Rodien P, Rohmer V, Franc B, Guyetant S, Malthiery Y, Reynier P (2005) Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J Clin Endocrinol Metab 90:2314–2320

    Article  CAS  PubMed  Google Scholar 

  • Jang MS, Ryu SW, Kim E (2002) Modification of Daxx by small ubiquitin-related modifier-1. Biochem Biophys Res Commun 295:495–500

    Article  CAS  PubMed  Google Scholar 

  • Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382

    Article  CAS  PubMed  Google Scholar 

  • Kamitani T, Kito K, Nguyen HP, Wada H, Fukuda-Kamitani T, Yeh ET (1998) Identification of three major sentrinization sites in PML. J Biol Chem 273:26675–26682

    Article  CAS  PubMed  Google Scholar 

  • Karin M (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441:431–436

    Article  CAS  PubMed  Google Scholar 

  • Kim YH, Choi CY, Kim Y (1999) Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc Natl Acad Sci U S A 96:12350–12355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Kim B, Cai L, Choi HJ, Ohgi KA, Tran C, Chen C, Chung CH, Huber O, Rose DW, Sawyers CL, Rosenfeld MG, Baek SH (2005) Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 434:921–926

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Choi HJ, Kim B, Kim MH, Lee JM, Kim IS, Lee MH, Choi SJ, Kim KI, Kim SI, Chung CH, Baek SH (2006) Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat Cell Biol 8:631–639

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Lee JM, Nam HJ, Choi HJ, Yang JW, Lee JS, Kim MH, Kim SI, Chung CH, Kim KI, Baek SH (2007) SUMOylation of pontin chromatin-remodeling complex reveals a signal integration code in prostate cancer cells. Proc Natl Acad Sci U S A 104:20793–20798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knipscheer P, Flotho A, Klug H, Olsen JV, van Dijk WJ, Fish A, Johnson ES, Mann M, Sixma TK, Pichler A (2008) Ubc9 sumoylation regulates SUMO target discrimination. Mol Cell 31:371–382

    Article  CAS  PubMed  Google Scholar 

  • Koken MH, Linares-Cruz G, Quignon F, Viron A, Chelbi-Alix MK, Sobczak-Thepot J, Juhlin L, Degos L, Calvo F, de The H (1995) The PML growth-suppressor has an altered expression in human oncogenesis. Oncogene 10:1315–1324

    CAS  PubMed  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and −2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    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 

  • Lallemand-Breitenbach V, Zhu J, Puvion F, Koken M, Honore N, Doubeikovsky A, Duprez E, Pandolfi PP, Puvion E, Freemont P, de The H (2001) Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J Exp Med 193:1361–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lallemand-Breitenbach V, Zhu J, Kogan S, Chen Z, de The H (2005) Opinion: how patients have benefited from mouse models of acute promyelocytic leukaemia. Nat Rev Cancer 5:821–827

    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 JS, Thorgeirsson SS (2004) Genome-scale profiling of gene expression in hepatocellular carcinoma: classification, survival prediction, and identification of therapeutic targets. Gastroenterology 127:S51–S55

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S, Hallenbeck JM (2007a) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metab 27:950–962

    Article  CAS  PubMed  Google Scholar 

  • Lee HE, Jee CD, Kim MA, Lee HS, Lee YM, Lee BL, Kim WH (2007b) Loss of promyelocytic leukemia protein in human gastric cancers. Cancer Lett 247:103–109

    Article  CAS  PubMed  Google Scholar 

  • Lee YK, Thomas SN, Yang AJ, Ann DK (2007c) Doxorubicin down-regulates Kruppel-associated box domain-associated protein 1 sumoylation that relieves its transcription repression on p21WAF1/CIP1 in breast cancer MCF-7 cells. J Biol Chem 282:1595–1606

    Article  CAS  PubMed  Google Scholar 

  • Lehembre F, Muller S, Pandolfi PP, Dejean A (2001) Regulation of Pax3 transcriptional activity by SUMO-1-modified PML. Oncogene 20:1–9

    Article  CAS  PubMed  Google Scholar 

  • Li H, Leo C, Zhu J, Wu X, O'Neil J, Park EJ, Chen JD (2000) Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol Cell Biol 20:1784–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Peet GW, Balzarano D, Li X, Massa P, Barton RW, Marcu KB (2001) Novel NEMO/IkappaB kinase and NF-kappa B target genes at the pre-B to immature B cell transition. J Biol Chem 276:18579–18590

    Article  CAS  PubMed  Google Scholar 

  • Lin JY, Ohshima T, Shimotohno K (2004) Association of Ubc9, an E2 ligase for SUMO conjugation, with p53 is regulated by phosphorylation of p53. FEBS Lett 573:15–18

    Article  CAS  PubMed  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 

  • Liu B, Yang Y, Chernishof V, Loo RR, Jang H, Tahk S, Yang R, Mink S, Shultz D, Bellone CJ, Loo JA, Shuai K (2007) Proinflammatory stimuli induce IKKalpha-mediated phosphorylation of PIAS1 to restrict inflammation and immunity. Cell 129:903–914

    Article  CAS  PubMed  Google Scholar 

  • Mabb AM, Miyamoto S (2007) SUMO and NF-kappaB ties. Cell Mol Life Sci 64:1979–1996

    Article  CAS  PubMed  Google Scholar 

  • Mao Y, Sun M, Desai SD, Liu LF (2000) SUMO-1 conjugation to topoisomerase I: a possible repair response to topoisomerase-mediated DNA damage. Proc Natl Acad Sci U S A 97:4046–4051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDoniels-Silvers AL, Nimri CF, Stoner GD, Lubet RA, You M (2002) Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clin Cancer Res 8:1127–1138

    CAS  PubMed  Google Scholar 

  • Meinecke I, Cinski A, Baier A, Peters MA, Dankbar B, Wille A, Drynda A, Mendoza H, Gay RE, Hay RT, Ink B, Gay S, Pap T (2007) Modification of nuclear PML protein by SUMO-1 regulates Fas-induced apoptosis in rheumatoid arthritis synovial fibroblasts. Proc Natl Acad Sci U S A 104:5073–5078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minty A, Dumont X, Kaghad M, Caput D (2000) Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J Biol Chem 275:36316–36323

    Article  CAS  PubMed  Google Scholar 

  • Mo YY, Yu Y, Shen Z, Beck WT (2002) Nucleolar delocalization of human topoisomerase I in response to topotecan correlates with sumoylation of the protein. J Biol Chem 277:2958–2964

    Article  CAS  PubMed  Google Scholar 

  • Mo YY, Yu Y, Ee PL, Beck WT (2004) Overexpression of a dominant-negative mutant Ubc9 is associated with increased sensitivity to anticancer drugs. Cancer Res 64:2793–2798

    Article  CAS  PubMed  Google Scholar 

  • Mo YY, Yu Y, Theodosiou E, Rachel Ee PL, Beck WT (2005) A role for Ubc9 in tumorigenesis. Oncogene 24:2677–2683

    Article  CAS  PubMed  Google Scholar 

  • Moilanen AM, Poukka H, Karvonen U, Hakli M, Janne OA, Palvimo JJ (1998) Identification of a novel RING finger protein as a coregulator in steroid receptor-mediated gene transcription. Mol Cell Biol 18:5128–5139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moschos SJ, Mo YY (2006) Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J Mol Histol 37:309–319

    Article  CAS  PubMed  Google Scholar 

  • Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103–118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muller S, Matunis MJ, Dejean A (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J 17:61–70

    Article  CAS  PubMed  PubMed Central  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 

  • Negorev D, Maul GG (2001) Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 20:7234–7242

    Article  CAS  PubMed  Google Scholar 

  • Nelson V, Davis GE, Maxwell SA (2001) A putative protein inhibitor of activated STAT (PIASy) interacts with p53 and inhibits p53-mediated transactivation but not apoptosis. Apoptosis 6:221–234

    Article  CAS  PubMed  Google Scholar 

  • Park J, Seo T, Kim H, Choe J (2005) Sumoylation of the novel protein hRIP{beta} is involved in replication protein A deposition in PML nuclear bodies. Mol Cell Biol 25:8202–8214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul RH, Laidlaw DH, Tate DF, Lee S, Hoth KF, Gunstad J, Zhang S, Lawrence J, Flanigan T (2007) Neuropsychological and neuroimaging outcome of HIV-associated progressive multifocal leukoencephalopathy in the era of antiretroviral therapy. J Integr Neurosci 6:191–203

    Article  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 

  • Pero R, Lembo F, Di Vizio D, Boccia A, Chieffi P, Fedele M, Pierantoni GM, Rossi P, Iuliano R, Santoro M, Viglietto G, Bruni CB, Fusco A, Chiariotti L (2001) RNF4 is a growth inhibitor expressed in germ cells but not in human testicular tumors. Am J Pathol 159:1225–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poukka H, Karvonen U, Janne OA, Palvimo JJ (2000) Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc Natl Acad Sci U S A 97:14145–14150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prudden J, Pebernard S, Raffa G, Slavin DA, Perry JJ, Tainer JA, McGowan CH, Boddy MN (2007) SUMO-targeted ubiquitin ligases in genome stability. EMBO J 26:4089–4101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu J, Liu GH, Wu K, Han P, Wang P, Li J, Zhang X, Chen C (2007) Nitric oxide destabilizes Pias3 and regulates sumoylation. PLoS ONE 2:e1085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rizos H, Woodruff S, Kefford RF (2005) p14ARF interacts with the SUMO-conjugating enzyme Ubc9 and promotes the sumoylation of its binding partners. Cell Cycle 4:597–603

    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 

  • Rodriguez MS, Dargemont C, Hay RT (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276:12654–12659

    Article  CAS  PubMed  Google Scholar 

  • Rompaey LV, Potter M, Adams C, Grosveld G (2000) Tel induces a G1 arrest and suppresses Ras-induced transformation. Oncogene 19:5244–5250

    Article  CAS  PubMed  Google Scholar 

  • Roscic A, Moller A, Calzado MA, Renner F, Wimmer VC, Gresko E, Ludi KS, Schmitz ML (2006) Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol Cell 24:77–89

    Article  CAS  PubMed  Google Scholar 

  • Rowley JD (1999) The role of chromosome translocations in leukemogenesis. Semin Hematol 36:59–72

    CAS  PubMed  Google Scholar 

  • Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275:6252–6258

    Article  CAS  PubMed  Google Scholar 

  • Schmidt D, Muller S (2002) Members 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 

  • Shalizi A, Gaudilliere B, Yuan Z, Stegmuller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311:1012–1017

    Article  CAS  PubMed  Google Scholar 

  • Shen ZX, Shi ZZ, Fang J, Gu BW, Li JM, Zhu YM, Shi JY, Zheng PZ, Yan H, Liu YF, Chen Y, Shen Y, Wu W, Tang W, Waxman S, De The H, Wang ZY, Chen SJ, Chen Z (2004) All-trans retinoic acid/As2O3 combination yields a high quality remission and survival in newly diagnosed acute promyelocytic leukemia. Proc Natl Acad Sci U S A 101:5328–5335

    Article  CAS  PubMed  PubMed Central  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 

  • Shinbo Y, Niki T, Taira T, Ooe H, Takahashi-Niki K, Maita C, Seino C, Iguchi-Ariga SM, Ariga H (2006) Proper SUMO-1 conjugation is essential to DJ-1 to exert its full ac. Cell Death Differ 13(1):96–108

    Article  CAS  PubMed  Google Scholar 

  • Stankovic-Valentin N, Deltour S, Seeler J, Pinte S, Vergoten G, Guerardel C, Dejean A, Leprince D (2007) An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol Cell Biol 27:2661–2675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sternsdorf T, Jensen K, Will H (1997) Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1. J Cell Biol 139:1621–1634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sternsdorf T, Jensen K, Reich B, Will H (1999) The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization, and modification by small ubiquitin-like modifiers. J Biol Chem 274:12555–12566

    Article  CAS  PubMed  Google Scholar 

  • Swaminathan S, Kiendl F, Korner R, Lupetti R, Hengst L, Melchior F (2004) RanGAP1*SUMO1 is phosphorylated at the onset of mitosis and remains associated with RanBP2 upon NPC disassembly. J Cell Biol 164:965–971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tagawa H, Miura I, Suzuki R, Suzuki H, Hosokawa Y, Seto M (2002) Molecular cytogenetic analysis of the breakpoint region at 6q21-22 in T-cell lymphoma/leukemia cell lines. Genes Chromosom Cancer 34:175–185

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Toh EA, Kikuchi Y (2003) Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. J Biochem 133:415–422

    Article  CAS  PubMed  Google Scholar 

  • Ueda M, Ota J, Yamashita Y, Choi YL, Ohki R, Wada T, Koinuma K, Kano Y, Ozawa K, Mano H (2003) DNA microarray analysis of stage progression mechanism in myelodysplastic syndrome. Br J Haematol 123:288–296

    Article  CAS  PubMed  Google Scholar 

  • Ulrich HD (2007) PCNASUMO and Srs2: a model SUMO substrate-effector pair. Biochem Soc Trans 35:1385–1388

    Article  CAS  PubMed  Google Scholar 

  • Uzunova K, Gottsche K, Miteva M, Weisshaar SR, Glanemann C, Schnellhardt M, Niessen M, Scheel H, Hofmann K, Johnson ES, Praefcke GJ, Dohmen RJ (2007) Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282:34167–34175

    Article  CAS  PubMed  Google Scholar 

  • Van Rompaey L, Dou W, Buijs A, Grosveld G (1999) Tel, a frequent target of leukemic translocations, induces cellular aggregation and influences expression of extracellular matrix components. Neoplasia 1:526–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veltman IM, Vreede LA, Cheng J, Looijenga LH, Janssen B, Schoenmakers EF, Yeh ET, van Kessel AG (2005) Fusion of the SUMO/Sentrin-specific protease 1 gene SENP1 and the embryonic polarity-related mesoderm development gene MESDC2 in a patient with an infantile teratoma and a constitutional t(12;15)(q13;q25). Hum Mol Genet 14:1955–1963

    Article  CAS  PubMed  Google Scholar 

  • Villalva C, Trempat P, Greenland C, Thomas C, Girard JP, Moebius F, Delsol G, Brousset P (2002) Isolation of differentially expressed genes in NPM-ALK-positive anaplastic large cell lymphoma. Br J Haematol 118:791–798

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Banerjee S (2004) Differential PIAS3 expression in human malignancy. Oncol Rep 11:1319–1324

    CAS  PubMed  Google Scholar 

  • Wood LD, Irvin BJ, Nucifora G, Luce KS, Hiebert SW (2003) Small ubiquitin-like modifier conjugation regulates nuclear export of TEL, a putative tumor suppressor. Proc Natl Acad Sci U S A 100:3257–3262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto H, Ihara M, Matsuura Y, Kikuchi A (2003) Sumoylation is involved in beta-catenin-dependent activation of Tcf-4. EMBO J 22:2047–2059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Sharrocks AD (2006) PIASxalpha differentially regulates the amplitudes of transcriptional responses following activation of the ERK and p38 MAPK pathways. Mol Cell 22:477–487

    Article  CAS  PubMed  Google Scholar 

  • Yang SH, Jaffray E, Hay RT, Sharrocks AD (2003) Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity. Mol Cell 12:63–74

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Chin W, Chow LT, Chan AS, Yim AP, Leung SF, Mok TS, Chang KS, Johnson PJ, Chan JY (2000) Lack of expression for the suppressor PML in human small cell lung carcinoma. Int J Cancer 85:599–605

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Roberts TM, Yang J, Desai R, Brown GW (2006) Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair 5:336–346

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Sternsdorf T, Bolger TA, Evans RM, Yao TP (2005) Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol Cell Biol 25:8456–8464

    Article  CAS  PubMed  PubMed Central  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 

  • Zhu J, Koken MH, Quignon F, Chelbi-Alix MK, Degos L, Wang ZY, Chen Z, de The H (1997) Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc Natl Acad Sci U S A 94:3978–3983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Chen Z, Lallemand-Breitenbach V, de The H (2002) How acute promyelocytic leukaemia revived arsenic. Nat Rev Cancer 2:705–713

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Seoul National University, Seoul, 151-742, South Korea

    Jason S. Lee, Hee June Choi & Sung Hee Baek

Authors
  1. Jason S. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hee June Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sung Hee Baek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sung Hee Baek .

Editor information

Editors and Affiliations

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

    Van G. Wilson

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Lee, J.S., Choi, H.J., Baek, S.H. (2017). Sumoylation and Its Contribution to Cancer. 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_17

Download citation

Publish with us

Policies and ethics

Search

Navigation