Ubiquitination and degradation of ribonucleotide reductase M1 by the polycomb group proteins RNF2 and Bmi1 and cellular response to gemcitabine

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Zhang, Yingtao ^a   Li, Xin ^a   Chen, Zhengming ^a   Bepler, Gerold ^a  

^a KARMANOS CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; GEMCITABINE; RIBONUCLEOTIDE REDUCTASE; RIBONUCLEOTIDE REDUCTASE M1; RING FINGER PROTEIN; RING FINGER PROTEIN 2; UNCLASSIFIED DRUG; BMI1 PROTEIN, HUMAN; DEOXYCYTIDINE; POLYUBIQUITIN; PROTEASOME; PROTEIN BINDING; RNF2 PROTEIN, HUMAN; RRM1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CANCER STAGING; CONTROLLED STUDY; DRUG EFFICACY; DRUG RESISTANCE; DRUG RESPONSE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME DEGRADATION; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; FEMALE; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IMMUNOHISTOCHEMISTRY; LIMIT OF QUANTITATION; LUNG CANCER; MAJOR CLINICAL STUDY; MALE; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ANALOGS AND DERIVATIVES; DRUG EFFECTS; LUNG TUMOR; METABOLISM; PROTEIN DEGRADATION; TUMOR CELL LINE;

CELL LINE, TUMOR; DEOXYCYTIDINE; HUMANS; LUNG NEOPLASMS; POLYCOMB REPRESSIVE COMPLEX 1; POLYUBIQUITIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84897492457     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091186     Document Type: Article

References (32)

1. Mao SS, Holler TP, Yu GX, Bollinger JM, Booker S, et al. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing. Biochemistry 31: 7933-7943.
2. Perez MA, Cerqueira NM, Fernandes PA, Ramos MJ (2010) Ribonucleotide reductase: a mechanistic portrait of substrate analogues inhibitors. Curr Med Chem 17: 2854-2872.
3. Chen Z, Zhou J, Zhang Y, Bepler G (2011) Modulation of the ribonucleotide reductase M1 - gemcitabine interaction in vivo by N-ethylmaleimide. Biochem Biophys Res Commun 413: 383-388.
4. Fan H, Huang A, Villegas C, Wright JA (1997) The R1 component of mammalian ribonucleotide reductase has malignancy-suppressing activity as demonstrated by gene transfer experiments. Proc Natl Acad Sci USA 94: 13181-13186.
5. Gautam A, Li ZR, Bepler G (2003) RRM1-induced metastasis suppression through PTEN-regulated pathways. Oncogene 22: 2135-2142. (Pubitemid 36539563)
6. Davidson JD, Ma L, Flagella M, Geeganage S, Gelbert LM, et al. (2004) An increase in the expression of ribonucleotide reductase large subunit 1 is associated with gemcitabine resistance in non-small cell lung cancer cell lines. Cancer Res 64: 3761-3766. (Pubitemid 38697284)
7. Bergman A, Eijk P, van Haperen V, Smid K, Veerman G, et al. (2005) In vivo induction of resistance to gemcitabine results in increased expression of ribonucleotide reductase subunit M1 as a major determinant. Cancer Res 65: 9510-9516. (Pubitemid 41508021)
8. Bepler G, Kusmartseva I, Sharma S, Gautam A, Cantor A, et al. (2006) RRM1 modulated in vitro and in vivo efficacy of gemcitabine and platinum in non-small-cell lung cancer. J Clin Oncol 24: 4731-4737. (Pubitemid 46646245)
9. Nakahira S, Nakamori S, Tsujie M, Takahashi Y, Okami J, et al. (2007) Involvement of ribonucleotide reductase M1 subunit overexpression in gemcitabine resistance of human pancreatic cancer. Int J Cancer 120: 1355-1363.
10. Reynolds C, Obasaju C, Schell MJ, Li X, Zheng Z, et al. (2009) Randomized phase III trial of gemcitabine-based chemotherapy with in situ RRM1 and ERCC1 protein levels for response prediction in non-small-cell lung cancer. J Clin Oncol 27: 5808-5815.
11. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, et al. (2004) Role of histone H2A ubiquitination in polycomb silencing. Nature 431: 873-878. (Pubitemid 39434086)
12. Bentley ML, Corn JE, Dong KC, Phung Q, Cheung TK, et al. (2011) Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex. Embo J 30: 3285-3297.
13. Hoeller D, Hecker CM, Dikic I (2006) Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat Rev Cancer 6: 776-788. (Pubitemid 44450466)
14. Ardley HC, Robinson PA (2005) E3 ubiquitin ligases. Essays Biochem 41: 15-30. (Pubitemid 41500968)
15. Frezza M, Schmitt S, Dou QP (2011) Targeting the ubiquitin-proteasome pathway: an emerging concept in cancer therapy. Curr Top Med Chem 11: 2888-2905.
16. Joazeiro CA, Weissman AM (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102: 549-552.
17. Ben-Saadon R, Zaaroor D, Ziv T, Ciechanover A (2006) The polycomb protein Ring1B generates self atypical mixed ubiquitin chains required for its in vitro histone H2A ligase activity. Mol Cell 24: 701-711. (Pubitemid 44839211)
18. Cao R, Tsukada Y, Zhang Y (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20: 845-854. (Pubitemid 41814874)
19. Zheng Z, Chen T, Li X, Haura E, Sharma A, et al. (2007) The DNA synthesis and repair genes RRM1 and ERCC1 in lung cancer. N Engl J Med 356: 800-808. (Pubitemid 46294612)
20. Hernández-Muñoz I, Lund AH, van der Stoop P, Boutsma E, Muijrers I, et al. (2005) Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci 102: 7635-7640. (Pubitemid 40741023)
21. Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM (1991) Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E mu-myc transgenic mice. Cell 65: 753-763. (Pubitemid 121001307)
22. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, et al. (1991) Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65: 737-752. (Pubitemid 121001306)
23. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168. (Pubitemid 29050921)
24. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260. (Pubitemid 40852690)
25. Bruggeman SW, Hulsman D, Tanger E, Buckle T, Blom M, et al. (2007) Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 12: 328-341. (Pubitemid 47539307)
26. Dovey JS, Zacharek SJ, Kim CF, Lees JA (2008) Bmi1 is critical for lung tumorigenesis and bronchioalveolar stem cell expansion. Proc Natl Acad Sci 105: 11857-11862.
27. Wang E, Bhattacharyya S, Szabolcs A, Rodriguez-Aguayo C, Jennings NB, et al. (2011) Enhancing chemotherapy response with Bmi-1 silencing in ovarian cancer. PLoS One 6: e17918.
28. Yin T, Wei H, Leng Z, Yang Z, Gou S, et al. (2011) Bmi-1 promotes the chemoresistance, invasion and tumorigenesis of pancreatic cancer cells. Chemotherapy 57: 488-496.
29. Bhattacharyya J, Mihara K, Ohtsubo M, Yasunaga S, Takei Y, et al. (2012) Overexpression of BMI-1 correlates with drug resistance in B-cell lymphoma cells through the stabilization of survivin expression. Cancer Sci 103: 34-41.
30. Ryan DP, Appleman LJ, Lynch T, Supko JG, Fidias P, et al. (2006) Phase I clinical trial of bortezomib in patients with advanced solid tumors. Cancer 107: 2482-2489. (Pubitemid 44748533)
31. Davies AM, Chansky K, Lara PN, Gumerlock PH, Crowley J, et al. (2009) Bortezomib plus gemcitabine/carboplatin as first-line treatment of advanced non-small cell lung cancer: a phase II Southwest Oncology Group Study (S0339). J Thorac Oncol 4: 87-92.
32. Camp RL, Chung GG, Rimm DL (2002) Automated subcellular localization and quantification of protein expression in tissue microarrays. Nat Med 8: 1323-1327. (Pubitemid 35373567)