Downregulation of BRCA1-BRCA2-containing complex subunit 3 sensitizes glioma cells to temozolomide

Oncotarget

Volumn 5, Issue 21, 2014, Pages 10901-10915

  Chai, Kit Man ^a   Wang, Chih Yen ^a   Liaw, Hung Jiun ^a   Fang, Kuan Min ^a   Yang, Chung Shi ^b   Tzeng, Shun Fen ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

BRCC3; BRCC36; DNA repair; Glioblastoma; H2AX

Indexed keywords

BRCA1 BRCA2 CONTAINING COMPLEX SUBUNIT 3 PROTEIN; CELL DNA; CELL PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; HISTONE H2AX; RAD51 PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG; ALKYLATING AGENT; BRCC3 PROTEIN, HUMAN; DACARBAZINE; MEMBRANE PROTEIN; MESSENGER RNA; SMALL INTERFERING RNA;

A172 CELL LINE; ARTICLE; BRCC3 GENE; CELL MIGRATION; CHEMOSENSITIZATION; CLONOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; DRUG TARGETING; FANCD2 GENE; GENE SILENCING; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; GLIOMA CELL; HISTONE PHOSPHORYLATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAD51 GENE; TUMOR SUPPRESSOR GENE; U251 CELL LINE; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BRAIN NEOPLASMS; CANCER GRADING; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; METABOLISM; PATHOLOGY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; DACARBAZINE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; MEMBRANE PROTEINS; NEOPLASM GRADING; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84916912447     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2543     Document Type: Article

References (53)

1. Robins HI, Peterson CG, Mehta MP. Combined modality treatment for central nervous system malignancies. Semin Oncol. 2003; 30:11-22.
2. Watters JJ, Schartner JM, Badie B. Microglia function in brain tumors. J Neurosci Res. 2005; 81:447-455.
3. Lam-Himlin D, Espey MG, Perry G, Smith MA, Castellani RJ. Malignant glioma progression and nitric oxide. Neurochem Int. 2006; 49:764-768.
4. Stiles CD, Rowitch DH. Glioma stem cells: a midterm exam. Neuron. 2008; 58:832-846.
5. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. The New England journal of medicine. 2005; 352:987-996.
6. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. The lancet oncology. 2009; 10:459-466.
7. Kast RE, Boockvar JA, Bruning A, Cappello F, Chang WW, Cvek B, Dou QP, Duenas-Gonzalez A, Efferth T, Focosi D, Ghaffari SH, Karpel-Massler G, Ketola K, KhoshnevisanA, Keizman D, Magne N, et al. A conceptuallynewtreatmentapproachfor relapsed glioblastoma:coordinated underminingof survival paths with nine repurposed drugs(CUSP9) by the International Initiative for AcceleratedImprovement of Glioblastoma Care. Oncotarget. 2013;4:502-530.
8. Hau P, Koch D, Hundsberger T, Marg E, Bauer B, Rudolph R, Rauch M, Brenner A, Rieckmann P, Schuth J, Jauch T, Koch H, Bogdahn U. Safety and feasibility oflong-term temozolomide treatment in patients with highgradeglioma. Neurology. 2007; 68:688-690.
9. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastomacancer stemcells-muchmore complex than expected. Molecular cancer. 2011; 10:128.
10. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, MirimanoffRO, Cairncross JG, Janzer RC, Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. The New England ournal of medicine. 2005; 352:997-1003.
11. Shinsato Y, Furukawa T, Yunoue S, Yonezawa H, Minami K, Nishizawa Y, Ikeda R, Kawahara K, Yamamoto M, Hirano H, Tokimura H, Arita K. Reduction of MLH1 and PMS2 confers temozolomide resistance and is associated with recurrence of glioblastoma. Oncotarget. 2013; 4:2261-2270.
12. Short SC, Giampieri S, Worku M, Alcaide-German M, Sioftanos G, Bourne S, Lio KI, Shaked-Rabi M, Martindale C. Rad51 inhibition is an effective means of targeting DNA repair in glioma models and CD133+ tumorderived cells. Neuro Oncol. 2011; 13:487-499.
13. Quiros S, Roos WP, Kaina B. Rad51 and BRCA2-New molecular targets for sensitizing glioma cells to alkylating anticancer drugs. PLoS One. 2011; 6:e27183.
14. Zhang N, Wu X, Yang L, Xiao F, Zhang H, Zhou A, Huang Z, Huang S. FoxM1 inhibition sensitizes resistant glioblastoma cells to temozolomide by downregulating the expression of DNA-repair gene Rad51. Clin Cancer Res. 2012; 18:5961-5971.
15. Kondo N, Takahashi A, Ono K, Ohnishi T. DNA damage induced by alkylating agents and repair pathways. J Nucleic Acids. 2010; 2010:543531.
16. Feng L, Wang J, Chen J. The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J Biol Chem. 2010; 285:30982-30988.
17. Ambroggio XI, Rees DC, Deshaies RJ. JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol. 2004; 2:E2.
18. Verma R, Aravind L, Oania R, McDonald WH, Yates JR, 3rd, Koonin EV, Deshaies RJ. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science. 2002; 298:611-615.
19. Dong Y, Hakimi MA, Chen X, Kumaraswamy E, Cooch NS, Godwin AK, Shiekhattar R. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol Cell. 2003; 12:1087-1099.
20. Okamoto K, Bartocci C, Ouzounov I, Diedrich JK, Yates JR, 3rd, Denchi EL. A two-step mechanism for TRF2-mediated chromosome-end protection. Nature. 2013; 494:502-505.
21. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell. 2007; 28:739-745.
22. Hu X, Kim JA, Castillo A, Huang M, Liu J, Wang B. NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J Biol Chem. 2011; 286: 11734-11745.
23. Sims JJ, Cohen RE. Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol Cell. 2009; 33:775-783.
24. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, Livingston DM, Greenberg RA. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science. 2007; 316:1198-1202.
25. Wang B, Matsuoka S, Ballif BA, Zhang D, Smogorzewska A, Gygi SP, Elledge SJ. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science. 2007; 316:1194-1198.
26. Kennedy RD, Quinn JE, Mullan PB, Johnston PG, Harkin DP. The role of BRCA1 in the cellular response to chemotherapy. J Natl Cancer Inst. 2004; 96:1659-1668.
27. Chen X, Arciero CA, Wang C, Broccoli D, Godwin AK. BRCC36 is essential for ionizing radiation-induced BRCA1 phosphorylation and nuclear foci formation. Cancer Res. 2006; 66:5039-5046.
28. Fang KM, Yang CS, Lin TC, Chan TC, Tzeng SF. Induced interleukin-33 expression enhances the tumorigenic activity of rat glioma cells. Neuro Oncol. 2014; 16:552-566.
29. Shao G, Lilli DR, Patterson-Fortin J, Coleman KA, Morrissey DE, Greenberg RA. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc 13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci U S A. 2009; 106:3166-3171.
30. Davies AA, Masson JY, McIlwraith MJ, Stasiak AZ, Stasiak A, Venkitaraman AR, West SC. Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol Cell. 2001; 7:273-282.
31. Yamamoto K, Ishiai M, Matsushita N, Arakawa H, Lamerdin JE, Buerstedde JM, Tanimoto M, Harada M, Thompson LH, Takata M. Fanconi anemia FANCG protein in mitigating radiation- and enzyme-induced DNA doublestrand breaks by homologous recombination in vertebrate cells. Mol Cell Biol. 2003; 23:5421-5430.
32. Roos WP, Nikolova T, Quiros S, Naumann SC, Kiedron O, Zdzienicka MZ, Kaina B. Brca2/Xrcc2 dependent HR, but not NHEJ, is required for protection against O(6)-methylguanine triggered apoptosis, DSBs and chromosomal aberrations by a process leading to SCEs. DNA Repair (Amst). 2009; 8:72-86.
33. Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW. The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res. 2005; 65:6394-6400.
34. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004; 11:448-457.
35. Hermisson M, Klumpp A, Wick W, Wischhusen J, Nagel G, Roos W, Kaina B, Weller M. O6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem. 2006; 96:766-776.
36. Gratas C, Sery Q, Rabe M, Oliver L, Vallette FM. Bak and Mcl-1 are essential for Temozolomide induced cell death in human glioma. Oncotarget. 2014; 5:2428-2435.
37. Hiddingh L, Tannous BA, Teng J, Tops B, Jeuken J, Hulleman E, Boots-Sprenger SH, Vandertop WP, Noske DP, Kaspers GJ, Wesseling P, Wurdinger T. EFEMP1 induces gamma-secretase/Notch-mediated temozolomide resistance in glioblastoma. Oncotarget. 2014; 5:363-374.
38. Rebbeck TR, Mitra N, Domchek SM, Wan F, Friebel TM, Tran TV, Singer CF, Tea MK, Blum JL, Tung N, Olopade OI, Weitzel JN, Lynch HT, Snyder CL, Garber JE, Antoniou AC, et al. Modification of BRCA1-Associated Breast and Ovarian Cancer Risk by BRCA1-Interacting Genes. Cancer Res. 2011; 71:5792-5805.
39. Kennedy RD, D'Andrea AD. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 2005; 19:2925-2940.
40. Taniguchi T, D'Andrea AD. Molecular pathogenesis of Fanconi anemia: recent progress. Blood. 2006; 107: 4223-4233.
41. Joenje H, Patel KJ. The emerging genetic and molecular basis of Fanconi anaemia. Nat Rev Genet. 2001; 2:446-457.
42. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, D'Andrea AD. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell. 2001; 7:249-262.
43. Chen CC, Taniguchi T, D'Andrea A. The Fanconi anemia (FA) pathway confers glioma resistance to DNA alkylating agents. J Mol Med (Berl). 2007; 85:497-509.
44. Wang B, Elledge SJ. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci U S A. 2007; 104:20759-20763.
45. Feng L, Huang J, Chen J. MERIT40 facilitates BRCA1 localization and DNA damage repair. Genes Dev. 2009; 23:719-728.
46. Tan DS, Rothermundt C, Thomas K, Bancroft E, Eeles R, Shanley S, Ardern-Jones A, Norman A, Kaye SB, Gore ME. "BRCAness" syndrome in ovarian cancer: a casecontrol study describing the clinical features and outcome of patients with epithelial ovarian cancer associated with BRCA1 and BRCA2 mutations. J Clin Oncol. 2008; 26: 5530-5536.
47. Chen X, Arciero CA, Godwin AK. BRCA1-associated complexes: new targets to overcome breast cancer radiation resistance. Expert Rev Anticancer Ther. 2006; 6: 187-196.
48. Pospelova TV, Demidenko ZN, Bukreeva EI, Pospelov VA, Gudkov AV, Blagosklonny MV. Pseudo-DNA damage response in senescent cells. Cell cycle. 2009; 8: 4112-4118.
49. Cooper EM, Cutcliffe C, Kristiansen TZ, Pandey A, Pickart CM, Cohen RE. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J. 2009; 28:621-631.
50. Cooper EM, Boeke JD, Cohen RE. Specificity of the BRISC deubiquitinating enzyme is not due to selective binding to Lys63-linked polyubiquitin. J Biol Chem. 2010; 285:10344-10352.
51. Py BF, Kim MS, Vakifahmetoglu-Norberg H, Yuan J. Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol Cell. 2013; 49:331-338.
52. Fang KM, Lin TC, Chan TC, Ma SZ, Tzou BC, Chang WR, Liu JJ, Chiou SH, Yang CS, Tzeng SF. Enhanced cell growth and tumorigenicity of rat glioma cells by stable expression of human CD133 through multiple molecular actions. Glia. 2013; 61:1402-1417.
53. Liu YP, Yang CS, Tzeng SF. Inhibitory regulation of glutamate aspartate transporter (GLAST) expression in astrocytes by cadmium-induced calcium influx. Journal of neurochemistry. 2008; 105:137-150.