Sumo Control

  • Katharina Maderböck
  • Andrea Pichler
Part of the Subcellular Biochemistry book series (SCBI, volume 54)


Sumoylation, the covalent attachment of SUMO peptide to cellular proteins, is an essential regulator of protein function involved in a wide range of cellular events. Deregulation of the SUMO pathway is implicated in the pathogenesis of several diseases, so it is important to understand how this system is controlled. Sumoylation is a highly dynamic regulatory mechanism, involving an energy dependent enzyme cascade for conjugation and another set of enzymes for deconjugation. In this chapter we will highlight the different mechanisms controlling the SUMO system.


Human Physiology Regulatory Mechanism Protein Function Cellular Protein Cellular Event 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Garcia-Dominguez M, Reyes JC. SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 2009.Google Scholar
  2. 2.
    Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009; 458:461–7.PubMedCrossRefGoogle Scholar
  3. 3.
    Geiss-Friedlander R, Melchior F. Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 2007; 8:947–56.PubMedCrossRefGoogle Scholar
  4. 4.
    Geoffroy MC, Hay RT. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat Rev Mol Cell Biol 2009; 10:564–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Meulmeester E, Melchior F. Cell biology: SUMO. Nature 2008; 452:709–11.PubMedCrossRefGoogle Scholar
  6. 6.
    Guo D, Li M, Zhang Y et al. A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat Genet 2004; 36:837–41.PubMedCrossRefGoogle Scholar
  7. 7.
    Bohren KM, Nadkarni V, Song JH et al. A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 2004; 279:27233–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Evdokimov E, Sharma P, Lockett SJ et al. Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J Cell Sci 2008; 121:4106–13.PubMedCrossRefGoogle Scholar
  9. 9.
    Vertegaal AC, Andersen JS, Ogg SC et al. Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol Cell Proteomics 2006; 5:2298–310.PubMedCrossRefGoogle Scholar
  10. 10.
    Bernier-Villamor V, Sampson DA, Matunis MJ et al. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 2002; 108:345–56.PubMedCrossRefGoogle Scholar
  11. 11.
    Pichler A, Knipscheer P, Oberhofer E et al. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat Struct Mol Biol 2005; 12:264–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Hietakangas V, Anckar J, Blomster HA et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci USA 2006; 103:45–50.PubMedCrossRefGoogle Scholar
  13. 13.
    Yang SH, Galanis A, Witty J et al. An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J 2006; 25:5083–93.PubMedCrossRefGoogle Scholar
  14. 14.
    Minty A, Dumont X, Kaghad M et al. 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 2000; 275:36316–23.PubMedCrossRefGoogle Scholar
  15. 15.
    Song J, Durrin LK, Wilkinson TA et al. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci USA 2004; 101:14373–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Song J, Zhang Z, Hu W et al. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J Biol Chem 2005; 280:40122–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Hannich JT, Lewis A, Kroetz MB et al. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 2005; 280:4102–10.PubMedCrossRefGoogle Scholar
  18. 18.
    Hecker CM, Rabiller M, Haglund K et al. Specification of SUMO1-and SUMO2-interacting motifs. J Biol Chem 2006; 281:16117–27.PubMedCrossRefGoogle Scholar
  19. 19.
    Zhu J, Zhu S, Guzzo CM et al. Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J Biol Chem 2008; 283:29405–15.PubMedCrossRefGoogle Scholar
  20. 20.
    Ouyang J, Shi Y, Valin A et al. Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. Mol Cell 2009; 34:145–54.PubMedCrossRefGoogle Scholar
  21. 21.
    Stehmeier P, Muller S. Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol Cell 2009; 33:400–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Goodson ML, Hong Y, Rogers R et al. Sumo-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor. J Biol Chem 2001; 276:18513–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Knipscheer P, Flotho A, Klug H et al. Ubc9 sumoylation regulates SUMO target discrimination. Mol Cell 2008; 31:371–82.PubMedCrossRefGoogle Scholar
  24. 24.
    Pfander B, Moldovan GL, Sacher M et al. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 2005; 436:428–33.PubMedGoogle Scholar
  25. 25.
    Papouli E, Chen S, Davies AA et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol Cell 2005; 19:123–33.PubMedCrossRefGoogle Scholar
  26. 26.
    Girdwood D, Bumpass D, Vaughan OA et al. P300 transcriptional repression is mediated by SUMO modification. Mol Cell 2003; 11:1043–54.PubMedCrossRefGoogle Scholar
  27. 27.
    Baba D, Maita N, Jee JG et al. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 2005; 435:979–82.PubMedCrossRefGoogle Scholar
  28. 28.
    Johnson ES, Schwienhorst I, Dohmen RJ et al. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J 1997; 16:5509–19.PubMedCrossRefGoogle Scholar
  29. 29.
    Desterro JM, Rodriguez MS, Kemp GD et al. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J Biol Chem 1999; 274:10618–24.PubMedCrossRefGoogle Scholar
  30. 30.
    Johnson ES, Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J Biol Chem 1997; 272:26799–802.PubMedCrossRefGoogle Scholar
  31. 31.
    Okuma T, Honda R, Ichikawa G et al. In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem Biophys Res Commun 1999; 254:693–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Johnson ES, Gupta AA. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 2001; 106:735–44.PubMedCrossRefGoogle Scholar
  33. 33.
    Reverter D, Lima CD. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 2005; 435:687–92.PubMedCrossRefGoogle Scholar
  34. 34.
    Kim JH, Baek SH. Emerging roles of desumoylating enzymes. Biochim Biophys Acta 2009; 1792:155–62.PubMedGoogle Scholar
  35. 35.
    Yeh ET. SUMOylation and De-SUMOylation: wrestling with life’s processes. J Biol Chem 2009; 284:8223–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Hay RT. SUMO-specific proteases: a twist in the tail. Trends Cell Biol 2007; 17:370–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Mukhopadhyay D, Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem Sci 2007; 32:286–95.PubMedCrossRefGoogle Scholar
  38. 38.
    Hietakangas V, Ahlskog JK, Jakobsson AM et al. Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol Cell Biol 2003; 23:2953–68.PubMedCrossRefGoogle Scholar
  39. 39.
    Kang J, Gocke CB, Yu H. Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity. BMC Biochem 2006; 7:5.PubMedCrossRefGoogle Scholar
  40. 40.
    Mohideen F, Capili AD, Bilimoria PM et al. A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat Struct Mol Biol 2009; 16: 945–52.PubMedCrossRefGoogle Scholar
  41. 41.
    Lin JY, Ohshima T, Shimotohno K. Association of Ubc9, an E2 ligase for SUMO conjugation, with p53 is regulated by phosphorylation of p53. FEBS Lett 2004; 573:15–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Desterro JM, Rodriguez MS, Hay RT. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 1998; 2:233–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Muller S, Berger M, Lehembre Fet al c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 2000; 275:13321–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Bossis G, Malnou CE, Farras R et al. Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol Cell Biol 2005; 25:6964–79.PubMedCrossRefGoogle Scholar
  45. 45.
    Yang SH, Jaffray E, Hay RT et al. Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity. Mol Cell 2003; 12:63–74.PubMedCrossRefGoogle Scholar
  46. 46.
    Hoege C, Pfander B, Moldovan GL et al. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002; 419:135–41.PubMedCrossRefGoogle Scholar
  47. 47.
    Sapetschnig A, Rischitor G, Braun H et al. Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J 2002; 21:5206–15.PubMedCrossRefGoogle Scholar
  48. 48.
    Nathan D, Ingvarsdottir K, Sterner DE et al. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev 2006; 20:966–76.PubMedCrossRefGoogle Scholar
  49. 49.
    Sternsdorf T, Jensen K, Reich B et al. The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization and modification by small ubiquitin-like modifiers. J Biol Chem 1999; 274:12555–66.PubMedCrossRefGoogle Scholar
  50. 50.
    Saitoh H, Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 2000; 275:6252–8.PubMedCrossRefGoogle Scholar
  51. 51.
    Xu Z, Au SW. Mapping residues of SUMO precursors essential in differential maturation by SUMO-specific protease, SENP1. Biochem J 2005; 386:325–30.PubMedCrossRefGoogle Scholar
  52. 52.
    Comerford KM, Leonard MO, Karhausen J et al. Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc Natl Acad Sci USA 2003; 100:986–91.PubMedCrossRefGoogle Scholar
  53. 53.
    Shao R, Zhang FP, Tian F et al. Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF-1alpha in adult mouse brain and heart in vivo. FEBS Lett 2004; 569:293–300.PubMedCrossRefGoogle Scholar
  54. 54.
    Lallemand-Breitenbach V, Jeanne M, Benhenda S et al. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 2008; 10:547–55.PubMedCrossRefGoogle Scholar
  55. 55.
    Matic I, Macek B, Hilger M et al. Phosphorylation of SUMO-1 occurs in vivo and is conserved through evolution. J Proteome Res 2008; 7:4050–7.PubMedCrossRefGoogle Scholar
  56. 56.
    Wei W, Yang P, Pang J et al. A stress-dependent SUMO4 sumoylation of its substrate proteins. Biochem Biophys Res Commun 2008; 375:454–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Boggio R, Colombo R, Hay RT et al. A mechanism for inhibiting the SUMO pathway. Mol Cell 2004; 16:549–61.PubMedCrossRefGoogle Scholar
  58. 58.
    Bossis G, Melchior F. Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol Cell 2006; 21:349–57.PubMedCrossRefGoogle Scholar
  59. 59.
    Qu J, Liu GH, Wu K et al. Nitric oxide destabilizes Pias3 and regulates sumoylation. PLoS One 2007; 2: e1085.PubMedCrossRefGoogle Scholar
  60. 60.
    Kovalenko OV, Plug AW, Haaf T et al. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 1996; 93:2958–63.PubMedCrossRefGoogle Scholar
  61. 61.
    Mo YY, Moschos SJ. Targeting Ubc9 for cancer therapy. Expert Opin Ther Targets 2005; 9:1203–16.PubMedCrossRefGoogle Scholar
  62. 62.
    McDoniels-Silvers AL, Nimri CF, Stoner GD et al. Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clin Cancer Res 2002; 8:1127–38.PubMedGoogle Scholar
  63. 63.
    Wu F, Zhu S, Ding Y et al. MicroRNA-mediated regulation of Ubc9 expression in cancer cells. Clin Cancer Res 2009; 15:1550–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Ihara M, Stein P, Schultz RM. UBE2I (UBC9), a SUMO-conjugating enzyme, localizes to nuclear speckles and stimulates transcription in mouse oocytes. Biol Reprod 2008; 79:906–13.PubMedCrossRefGoogle Scholar
  65. 65.
    Sachdev S, Bruhn L, Sieber H et al. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 2001; 15:3088–103.PubMedCrossRefGoogle Scholar
  66. 66.
    Reindle A, Belichenko I, Bylebyl GR et al. Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J Cell Sci 2006; 119:4749–57.PubMedCrossRefGoogle Scholar
  67. 67.
    Duval D, Duval G, Kedinger C et al. The ‘PINIT’ motif, of a newly identified conserved domain of the PIAS protein family, is essential for nuclear retention of PIAS3L. FEBS Lett 2003; 554:111–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Cheng CH, Lo YH, Liang SS et al. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 2006; 20:2067–81.PubMedCrossRefGoogle Scholar
  69. 69.
    Mabb AM, Wuerzberger-Davis SM, Miyamoto S. PIASy mediates NEMO sumoylation and NF-kappaB activation in response to genotoxic stress. Nat Cell Biol 2006; 8:986–93.PubMedCrossRefGoogle Scholar
  70. 70.
    Yang SH, Sharrocks AD. PIASxalpha differentially regulates the amplitudes of transcriptional responses following activation of the ERK and p38 MAPK pathways. Mol Cell 2006; 22:477–87.PubMedCrossRefGoogle Scholar
  71. 71.
    Li X, Lee YK, Jeng JC et al. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 2007; 282:36177–89.PubMedCrossRefGoogle Scholar
  72. 72.
    Yang X, Li H, Zhou Z et al. Plk1-mediated phosphorylation of Topors regulates p53 stability. J Biol Chem 2009; 284:18588–92.PubMedCrossRefGoogle Scholar
  73. 73.
    Roscic A, Moller A, Calzado MA et al. Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol Cell 2006; 24:77–89.PubMedCrossRefGoogle Scholar
  74. 74.
    Ihara M, Yamamoto H, Kikuchi A. SUMO-1 modification of PIASy, an E3 ligase, is necessary for PIASy-dependent activation of Tcf-4. Mol Cell Biol 2005; 25:3506–18.PubMedCrossRefGoogle Scholar
  75. 75.
    Wu J, Matunis MJ, Kraemer D et al. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain and a leucine-rich region. J Biol Chem 1995; 270:14209–13.PubMedCrossRefGoogle Scholar
  76. 76.
    Yokoyama N, Hayashi N, Seki T et al. A giant nucleopore protein that binds Ran/TC4. Nature 1995; 376:184–8.PubMedCrossRefGoogle Scholar
  77. 77.
    Joseph J, Tan SH, Karpova TS et al. SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 2002; 156:595–602.PubMedCrossRefGoogle Scholar
  78. 78.
    Swaminathan S, Kiendl F, Korner R et al. RanGAP1*SUMO1 is phosphorylated at the onset of mitosis and remains associated with RanBP2 upon NPC disassembly. J Cell Biol 2004; 164:965–71.PubMedCrossRefGoogle Scholar
  79. 79.
    Pichler A, Melchior F. Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 2002; 3:381–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Li SJ, Hochstrasser M. A new protease required for cell-cycle progression in yeast. Nature 1999; 398:246–51.PubMedCrossRefGoogle Scholar
  81. 81.
    Gong L, Millas S, Maul GG et al. Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J Biol Chem 2000; 275:3355–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Hang J, Dasso M. Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem 2002; 277:19961–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Zhang H, Saitoh H, Matunis MJ. Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol Cell Biol 2002; 22:6498–508.PubMedCrossRefGoogle Scholar
  84. 84.
    Mukhopadhyay D, Ayaydin F, Kolli N et al. SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J Cell Biol 2006; 174:939–49.PubMedCrossRefGoogle Scholar
  85. 85.
    Li SJ, Hochstrasser M. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol Cell Biol 2000; 20:2367–77.PubMedCrossRefGoogle Scholar
  86. 86.
    Reverter D, Lima CD. A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex. Structure 2004; 12:1519–31.PubMedCrossRefGoogle Scholar
  87. 87.
    Shen L, Tatham MH, Dong C et al. SUMO protease SENP1 induces isomerization of the scissile peptide bond. Nat Struct Mol Biol 2006; 13:1069–77.PubMedCrossRefGoogle Scholar
  88. 88.
    Cheng J, Bawa T, Lee P et al. Role of desumoylation in the development of prostate cancer. Neoplasia 2006; 8:667–76.PubMedCrossRefGoogle Scholar
  89. 89.
    Nishida T, Tanaka H, Yasuda H. A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur J Biochem 2000; 267:6423–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Gong L, Yeh ET. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J Biol Chem 2006; 281:15869–77.PubMedCrossRefGoogle Scholar
  91. 91.
    Di Bacco A, Ouyang J, Lee HY et al. The SUMO-specific protease SENP5 is required for cell division. Mol Cell Biol. 2006; 26:4489–98.PubMedCrossRefGoogle Scholar
  92. 92.
    Li SJ, Hochstrasser M. The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization and substrate specificity. J Cell Biol 2003; 160:1069–81.PubMedCrossRefGoogle Scholar
  93. 93.
    Zunino R, Braschi E, Xu L et al. Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem 2009; 284:17783–95.PubMedCrossRefGoogle Scholar
  94. 94.
    Zhu S, Goeres J, Sixt KM et al. Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1. Mol Cell 2009; 33:570–80.PubMedCrossRefGoogle Scholar
  95. 95.
    Lee MH, Lee SW, Lee EJ et al. SUMO-specific protease SUSP4 positively regulates p53 by promoting Mdm2 self-ubiquitination. Nat Cell Biol 2006; 8:1424–31.PubMedCrossRefGoogle Scholar
  96. 96.
    Kuo ML, den Besten W, Thomas MC et al. Arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease Senp3. Cell Cycle 2008; 7:3378–87.PubMedCrossRefGoogle Scholar
  97. 97.
    Xu Z, Lam LS, Lam LH et al. Molecular basis of the redox regulation of SUMO proteases: a protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation. FASEB J 2008; 22:127–37.PubMedCrossRefGoogle Scholar
  98. 98.
    Huang RY, Kowalski D, Minderman H et al. Small ubiquitin-related modifier pathway is a major determinant of doxorubicin cytotoxicity in Saccharomyces cerevisiae. Cancer Res 2007; 67:765–72.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.Max-Planck-Institute of ImmunobiologyFreiburgGermany
  2. 2.Max F. Perutz LaboratoriesMedical University ViennaWienAustria

Personalised recommendations