RUNX family members are covalently modified and regulated by PIAS1-mediated sumoylation

Oncogenesis

Volumn 3, Issue 4, 2014, Pages

  Kim, J H ^a   Jang, J W ^a   Lee, Y S ^a   Lee, J W ^a   Chi, X Z ^a   Li, Y H ^a   Kim, M K ^a   Kim, D M ^a   Choi, B S ^a   Kim, J ^a   Kim, H M ^b   Van Wijnen, A ^c   Park, Ily ^a   Bae, S C ^a  

^a Chungbuk National University   (South Korea)

^b Gachon University   (South Korea)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

AKT1; PIAS1; RUNX3; sumoylation; tumor suppressor

Indexed keywords

LYSINE; PROTEIN PIAS1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR RUNX3; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BREAST CANCER; CANCER INHIBITION; CARCINOGENICITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; DNA MODIFICATION; EYE DEVELOPMENT; GENE INTERACTION; GENE MUTATION; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; MOLECULAR LIBRARY; MOLECULAR MECHANICS; MOUSE; MUTANT DROSOPHILA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SUMOYLATION; TRANSACTIVATION; WILD TYPE;

MAMMALIA; MUS MUSCULUS;

EID: 84920676825     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2014.15     Document Type: Article

References (55)

1. van Wijnen AJ, Stein GS, Gergen JP, Groner Y, Hiebert SW, Ito Y et al. Nomenclature for Runt-related (RUNX) proteins. Oncogene 2004; 23: 4209-4210.
2. Canon J, Banerjee U. Runt and Lozenge function in Drosophila development. Semin Cell Dev Biol 2000; 11: 327-336.
3. Look AT. E2A-HLF chimeric transcription factors in pro-B cell acute lymphoblastic leukemia. Curr Top Microbiol Immunol 1997; 220: 45-53.
4. Speck NA, Gilliland DG. Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer 2002; 2: 502-513.
5. Banerji S, Cibulskis K, Rangel-Escareno C, Brown KK, Carter SL, Frederick AM et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 2012; 486: 405-409.
6. Ellis MJ, Ding L, Shen D, Luo J, Suman VJ, Wallis JW et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 2012; 486: 353-360.
7. Dulak AM, Schumacher SE, van Lieshout J, Imamura Y, Fox C, Shim B et al. Gastrointestinal adenocarcinomas of the esophagus, stomach, and colon exhibit distinct patterns of genome instability and oncogenesis. Cancer Res 2012; 72: 4383-4393.
8. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997; 89: 747-754.
9. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997; 89: 755-764.
10. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997; 89: 765-771.
11. Inoue K, Ozaki S, Shiga T, Ito K, Masuda T, Okado N et al. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat Neurosci 2002; 5: 946-954.
12. Taniuchi I, Osato M, Egawa T, Sunshine MJ, Bae SC, Komori T et al. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 2002; 111: 621-633.
13. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 2002; 109: 113-124.
14. Ito K, Lim AC, Salto-Tellez M, Motoda L, Osato M, Chuang LS et al. RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis. Cancer Cell 2008; 14: 226-237.
15. Kim WJ, Kim EJ, Jeong P, Quan C, Kim J, Li QL et al. RUNX3 inactivation by point mutations and aberrant DNA methylation in bladder tumors. Cancer Res 2005; 65: 9347-9354.
16. Lee KS, Lee YS, Lee JM, Ito K, Cinghu S, Kim JH et al. Runx3 is required for the differentiation of lung epithelial cells and suppression of lung cancer. Oncogene 2010; 29: 3349-3361.
17. Lee YS, Lee JW, Jang JW, Chi XZ, Kim JH, Li YH et al. Runx3 inactivation is a crucial early event in the development of lung adenocarcinoma. Cancer Cell 2013; 24: 603-616.
18. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006; 38: 787-793.
19. Salto-Tellez M, Peh BK, Ito K, Tan SH, Chong PY, Han HC et al. RUNX3 protein is overexpressed in human basal cell carcinomas. Oncogene 2006; 25: 7646-7649.
20. Tsunematsu T, Kudo Y, Iizuka S, Ogawa I, Fujita T, Kurihara H et al. RUNX3 has an oncogenic role in head and neck cancer. PLoS ONE 2009; 4: e5892.
21. Lee CW, Chuang LS, Kimura S, Lai SK, Ong CW, Yan B et al. RUNX3 functions as an oncogene in ovarian cancer. Gynecol Oncol 2011; 122: 410-417.
22. Bae SC, Lee YH. Phosphorylation, acetylation and ubiquitination: the molecular basis of RUNX regulation. Gene 2006; 366: 58-66.
23. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ et al. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 2004; 279: 29409-29417.
24. Kim JH, Choi JK, Cinghu S, Jang JW, Lee YS, Li YH et al. Jab1/CSN5 induces the cytoplasmic localization and degradation of RUNX3. J Cell Biochem 2009; 107: 557-565.
25. Chi XZ, Kim J, Lee YH, Lee JW, Lee KS, Wee H et al. Runt-related transcription factor RUNX3 is a target of MDM2-mediated ubiquitination. Cancer Res 2009; 69: 8111-8119.
26. Hay RT. SUMO: a history of modification. Mol Cell 2005; 18: 1-12.
27. Betz A, Lampen N, Martinek S, Young MW, Darnell Jr. JE. A Drosophila PIAS homologue negatively regulates stat92E. Proc Natl Acad Sci USA 2001; 98: 9563-9568.
28. Shuai K, Liu B. Regulation of gene-Activation pathways by PIAS proteins in the immune system. Nat Rev Immunol 2005; 5: 593-605.
29. Schmidt D, Muller S. PIAS/SUMO: new partners in transcriptional regulation. Cell Mol Life Sci 2003; 60: 2561-2574.
30. Seeler JS, Bischof O, Nacerddine K, Dejean A. SUMO the three Rs and cancer. Curr Top Microbiol Immunol 2007; 313: 49-71.
31. Kim KI, Baek SH. SUMOylation code in cancer development and metastasis. Mol Cell 2006; 22: 247-253.
32. Rodriguez MS, Desterro JM, Lain S, Midgley CA, Lane DP, Hay RT. SUMO-1 modification activates the transcriptional response of p53. EMBO J 1999; 18: 6455-6461.
33. Muller S, Berger M, Lehembre F, Seeler JS, Haupt Y, Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 2000; 275: 13321-13329.
34. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F et al. A module of negative feedback regulators defines growth factor signaling. Nat Genet 2007; 39: 503-512.
35. Crew JR, Batterham P, Pollock JA. Developing compound eye in lozenge mutants of Drosophila: lozenge expression in the R7 equivalence group. Dev Gene Evol 1997; 206: 481-493.
36. Daga A, Karlovich CA, Dumstrei K, Banerjee U. Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev 1996; 10: 1194-1205.
37. Flores GV, Daga A, Kalhor HR, Banerjee U. Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 1998; 125: 3681-3687.
38. St Johnston D. The art and design of genetic screens: Drosophila melanogaster. Nat Rev Genet 2002; 3: 176-188.
39. Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE et al. Energy-dependent regulation of cell structure by AMP-Activated protein kinase. Nature 2007; 447: 1017-1020.
40. Buschmann T, Fuchs SY, Lee CG, Pan ZQ, Ronai Z. SUMO-1 modification of Mdm2 prevents its self-ubiquitination and increases Mdm2 ability to ubiquitinate p53. Cell 2000; 101: 753-762.
41. Kahyo T, Nishida T, Yasuda H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol Cell 2001; 8: 713-718.
42. Johnson ES. Protein modification by SUMO. Annu Rev Biochem 2004; 73: 355-382.
43. Ducy P, Karsenty G. Two distinct osteoblast-specific cis-Acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 1995; 15: 1858-1869.
44. Lin X, Sun B, Liang M, Liang YY, Gast A, Hildebrand J et al. Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol Cell 2003; 11: 1389-1396.
45. Tahirov TH, Inoue-Bungo T, Morii H, Fujikawa A, Sasaki M, Kimura K et al. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. Cell 2001; 104: 755-767.
46. Fujita T, Azuma Y, Fukuyama R, Hattori Y, Yoshida C, Koida M et al. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J Cell Biol 2004; 166: 85-95.
47. Osato M. Point mutations in the RUNX1/AML1 gene: another actor in RUNX leukemia. Oncogene 2004; 23: 4284-4296.
48. Gill G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 2004; 18: 2046-2059.
49. Melchior F. SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol 2000; 16: 591-626.
50. Wheeler JC, Shigesada K, Gergen JP, Ito Y. Mechanisms of transcriptional regulation by Runt domain proteins. Semin Cell Dev Biol 2000; 11: 369-375.
51. Gupta BP, Flores GV, Banerjee U, Rodrigues V. Patterning an epidermal field: Drosophila lozenge, a member of the AML-1/Runt family of transcription factors, specifies olfactory sense organ type in a dose-dependent manner. Dev Biol 1998; 203: 400-411.
52. Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci USA 2006; 103: 45-50.
53. Ito Y. Oncogenic potential of the RUNX gene family: 'overview'. Oncogene 2004; 23: 4198-4208.
54. Chuang LS, Ito Y. RUNX3 is multifunctional in carcinogenesis of multiple solid tumors. Oncogene 2010; 29: 2605-2615.
55. Blyth K, Cameron ER, Neil JC. The RUNX genes: gain or loss of function in cancer. Nat Rev Cancer 2005; 5: 376-387.