Connection between tumor suppressor BRCA1 and PTEN in damaged DNA repair

Frontiers in Oncology

Volumn 4, Issue NOV, 2014, Pages

  Minami, Akari ^a   Nakanishi, Atsuko ^a   Ogura, Yasunori ^a   Kitagishi, Yasuko ^a   Matsuda, Satoru ^a  

^a NARA WOMEN'S UNIVERSITY   (Japan)

Author keywords

BRCA1; carcinogenesis; cell signaling; DNA repair; genome stability; PTEN; reactive oxygen species

Indexed keywords

ALPHA2 INTEGRIN; ALPHA6 INTEGRIN; BETA1 INTEGRIN; BETA4 INTEGRIN; BONE MORPHOGENETIC PROTEIN; CD82 ANTIGEN; DOCETAXEL; ENDOTHELIN 1; FIBROBLAST GROWTH FACTOR; FIBRONECTIN; HEPSIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; KALININ; LAMININ 10; MATRIPTASE; MATRIX METALLOPROTEINASE; PLATELET DERIVED GROWTH FACTOR; PROSTATE SPECIFIC ANTIGEN; PROTEASE NEXIN I; PROTEIN BCL XL; PROTEIN TYROSINE KINASE; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA; UNINDEXED DRUG; UROKINASE; VASCULOTROPIN; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 6; WNT PROTEIN;

ANGIOGENESIS; BONE METASTASIS; CANCER SURVIVAL; CELL ADHESION; CELL DIFFERENTIATION; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; INFLAMMATION; MITOGENESIS; NONHUMAN; OSTEOBLAST; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; PROTEIN EXPRESSION; SHORT SURVEY; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; WOUND HEALING;

EID: 84915759334     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00318     Document Type: Short Survey

References (87)

1. Paul A, Paul S. The breast cancer susceptibility genes (BRCA) in breast and ovarian cancers. Front Biosci (Landmark Ed) (2014) 19:605-18. doi: 10.2741/4230
2. O'Donovan PJ, Livingston DM. BRCA1 and BRCA2: breast/ovarian cancer susceptibility gene products and participants in DNA double-strand break repair. Carcinogenesis (2010) 31:961-7. doi:10.1093/carcin/bgq069
3. Wang L, Di LJ. BRCA1 and estrogen/estrogen receptor in breast cancer: where they interact? Int J Biol Sci (2014) 10:566-75. doi:10.7150/ijbs.8579
4. Bouafia A, Corre S, Gilot D, Mouchet N, Prince S, Galibert MD. p53 requires the stress sensor USF1 to direct appropriate cell fate decision. PLoS Genet (2014) 10:e1004309. doi:10.1371/journal.pgen.1004309
5. Xiang T, Ohashi A, Huang Y, Pandita TK, Ludwig T, Powell SN, et al. Negative regulation of AKT activation by BRCA1. Cancer Res (2008) 68:10040-4. doi:10.1158/0008-5472.CAN-08-3009
6. López-Knowles E, O'Toole SA, McNeil CM, Millar EK, Qiu MR, Crea P, et al. PI3K pathway activation in breast cancer is associated with the basal-like phenotype and cancer-specific mortality. Int J Cancer (2010) 126:1121-31. doi:10.1002/ijc.24831
7. Nelson AC, Lyons TR, Young CD, Hansen KC, Anderson SM, Holt JT. AKT regulates BRCA1 stability in response to hormone signaling. Mol Cell Endocrinol (2010) 319:129-42. doi:10.1016/j.mce.2010.01.019
8. Xiang T, Jia Y, Sherris D, Li S, Wang H, Lu D, et al. Targeting the Akt/mTOR pathway in Brca1-deficient cancers. Oncogene (2011) 30:2443-50. doi:10.1038/onc.2010.603
9. Yi YW, Kang HJ, Kim HJ, Hwang JS, Wang A, Bae I. Inhibition of constitutively activated phosphoinositide 3-kinase/AKT pathway enhances antitumor activity of chemotherapeutic agents in breast cancer susceptibility gene 1-defective breast cancer cells. Mol Carcinog (2013) 52:667-75. doi:10.1002/mc.21905
10. Carnero A, Blanco-Aparicio C, Renner O, Link W, Leal JF. The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr Cancer Drug Targets (2008) 8:187-98. doi:10.2174/156800908784293659
11. Carnero A. The PKB/AKT pathway in cancer. Curr Pharm Des (2010) 16:34-44. doi:10.2174/138161210789941865
12. Gao H, Ouyang X, Banach-Petrosky WA, Shen MM, Abate-Shen C. Emergence of androgen independence at early stages of prostate cancer progression in Nkx3.1; Pten mice. Cancer Res (2006) 66:7929-33. doi:10.1158/0008-5472.CAN-06-1637
13. Skírnisdóttir I, Seidal T. Prognostic impact of concomitant p53 and PTEN on outcome in early stage (FIGO I-II) epithelial ovarian cancer. Int J Gynecol Cancer (2011) 21:1024-31. doi:10.1097/IGC.0b013e31821dc906
14. Pilarski R, Burt R, Kohlman W, Pho L, Shannon KM, Swisher E. Cowden syndrome and the PTEN hamartoma tumor syndrome: systematic review and revised diagnostic criteria. J Natl Cancer Inst (2013) 105:1607-16. doi:10.1093/jnci/djt277
15. Eyfjord JE, Bodvarsdottir SK. Genomic instability and cancer: networks involved in response to DNA damage. Mutat Res (2005) 592:18-28. doi:10.1016/j.mrfmmm.2005.05.010
16. Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res (2010) 108:73-112. doi:10.1016/B978-0-12-380888-2.00003-0
17. Dasika GK, Lin SC, Zhao S, Sung P, Tomkinson A, Lee EY. DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene (1999) 18:7883-99. doi:10.1038/sj.onc.1203283
18. George SH, Shaw P. BRCA and early events in the development of serous ovarian cancer. Front Oncol (2014) 4:5. doi:10.3389/fonc.2014.00005
19. Moorman PG, Havrilesky LJ, Gierisch JM, Coeytaux RR, Lowery WJ, Peragallo Urrutia R, et al. Oral contraceptives and risk of ovarian cancer and breast cancer among high-risk women: a systematic review and meta-analysis. J Clin Oncol (2013) 31:4188-98. doi:10.1200/JCO.2013.48.9021
20. Douglas JA, Levin AM, Zuhlke KA, Ray AM, Johnson GR, Lange EM, et al. Common variation in the BRCA1 gene and prostate cancer risk. Cancer Epidemiol Biomarkers Prev (2007) 16:1510-6. doi:10.1158/1055-9965.EPI-07-0137
21. Gallagher DJ, Gaudet MM, Pal P, KirchhoffT, Balistreri L, Vora K, et al. Germline BRCA mutations denote a clinicopathologic subset of prostate cancer. Clin Cancer Res (2010) 16:2115-21. doi:10.1158/1078-0432.CCR-09-2871
22. De Luca P, Moiola CP, Zalazar F, Gardner K, Vazquez ES, De Siervi A. BRCA1 and p53 regulate critical prostate cancer pathways. Prostate Cancer Prostatic Dis (2013) 16:233-8. doi:10.1038/pcan.2013.12
23. Xia Y, Pao GM, Chen HW, Verma IM, Hunter T. Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J Biol Chem (2003) 278:5255-63. doi:10.1074/jbc. M204591200
24. Laufer M, Nandula SV, Modi AP, Wang S, Jasin M, Murty VV, et al. Structural requirements for the BARD1 tumor suppressor in chromosomal stability and homology-directed DNA repair. J Biol Chem (2007) 282:34325-33. doi:10.1074/jbc. M705198200
25. Thomas JE, Smith M, Tonkinson JL, Rubinfeld B, Polakis P. Induction of phosphorylation on BRCA1 during the cell cycle and after DNA damage. Cell Growth Differ (1997) 8:801-9.
26. Canning MT, Brown DA, Yarosh DB. A bicyclic monoterpene diol and UVB stimulate BRCA1 phosphorylation in human keratinocytes. Photochem Photobiol (2003) 77:46-51. doi:10.1562/0031-8655(2003)0770046ABMDAU2.0.CO2
27. Clark SL, Rodriguez AM, Snyder RR, Hankins GD, Boehning D. Structure-function of the tumor suppressor BRCA1. Comput Struct Biotechnol J (2012) 1:e201204005. doi:10.5936/csbj.201204005
28. Bowen TJ, Yakushiji H, Montagna C, Jain S, Ried T, Wynshaw-Boris A. Atm heterozygosity cooperates with loss of Brca1 to increase the severity of mammary gland cancer and reduce ductal branching. Cancer Res (2005) 65:8736-46. doi:10.1158/0008-5472.CAN-05-1598
29. Khanna KK, Chenevix-Trench G. ATM and genome maintenance: defining its role in breast cancer susceptibility. J Mammary Gland Biol Neoplasia (2004) 9:247-62. doi:10.1023/B:JOMG.0000048772.92326.a1
30. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol (2006) 173:195-206. doi:10.1083/jcb.200510130
31. Stolz A, Ertych N, Kienitz A, Vogel C, Schneider V, Fritz B, et al. The CHK2-BRCA1 tumour suppressor pathway ensures chromosomal stability in human somatic cells. Nat Cell Biol (2010) 12:492-9. doi:10.1038/ncb2051
32. Sirbu BM, Cortez D. DNA damage response: three levels of DNA repair regulation. Cold Spring Harb Perspect Biol (2013) 5:a012724. doi:10.1101/cshperspect.a012724
33. Blazek D, Kohoutek J, Bartholomeeusen K, Johansen E, Hulinkova P, Luo Z, et al. The Cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev (2011) 25:2158-72. doi:10.1101/gad.16962311
34. Jhanwar-Uniyal M. BRCA1 in cancer, cell cycle and genomic stability. Front Biosci (2003) 8:s1107-17. doi:10.2741/1131
35. Okumura N, Yoshida H, Kitagishi Y, Nishimura Y, Iseki S, Matsuda S. Against lung cancer cells: to be, or not to be, that is the problem. Lung Cancer Int (2012) 2012:8. doi:10.1155/2012/659365
36. Petrocelli T, Slingerland JM. PTEN deficiency: a role in mammary carcinogenesis. Breast Cancer Res (2001) 3:356-60. doi:10.1186/bcr322
37. Dong JT. Prevalent mutations in prostate cancer. J Cell Biochem (2006) 97:433-47. doi:10.1002/jcb.20696
38. Li YL, Tian Z, Wu DY, Fu BY, Xin Y. Loss of heterozygosity on 10q23.3 and mutation of tumor suppressor gene PTEN in gastric cancer and precancerous lesions. World J Gastroenterol (2005) 11:285-8. doi:10.3748/wjg.v11.i2.285
39. Wang JY, Huang TJ, Chen FM, Hsieh MC, Lin SR, Hou MF, et al. Mutation analysis of the putative tumor suppressor gene PTEN/MMAC1 in advanced gastric carcinomas. Virchows Arch (2003) 442:437-43.
40. Kim J, Coffey DM, Creighton CJ, Yu Z, Hawkins SM, Matzuk MM. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci U S A (2012) 109:3921-6. doi:10.1073/pnas.1117135109
41. Yoshida H, Okumura N, Kitagishi Y, Nishimura Y, Matsuda S. Ethanol extract of rosemary repressed PTEN expression in K562 culture cells. Int J Appl Biol Pharm Technol (2011) 2:316-22.
42. Zhang P, Chen JH, Guo XL. New insights into PTEN regulation mechanisms and its potential function in targeted therapies. Biomed Pharmacother (2012) 66:485-90. doi:10.1016/j.biopha.2012.04.004
43. Singh G, Chan AM. Post-translational modifications of PTEN and their potential therapeutic implications. Curr Cancer Drug Targets (2011) 11:536-47. doi:10.2174/156800911795655930
44. Dillon LM, Miller TW. Therapeutic targeting of cancers with loss of PTEN function. Curr Drug Targets (2014) 15:65-79. doi:10.2174/1389450114666140106100909
45. Patsoukis N, Li L, Sari D, Petkova V, Boussiotis VA. PD-1 increases PTEN phosphatase activity while decreasing PTEN protein stability by inhibiting casein kinase 2. Mol Cell Biol (2013) 33:3091-8. doi:10.1128/MCB.00319-13
46. Barata JT. The impact of PTEN regulation by CK2 on PI3K-dependent signaling and leukemia cell survival. Adv Enzyme Regul (2011) 51:37-49. doi:10.1016/j.advenzreg.2010.09.012
47. Leslie NR, Downes CP. PTEN: the down side of PI 3-kinase signalling. Cell Signal (2002) 14:285-95. doi:10.1016/S0898-6568(01)00234-0
48. Chu EC, Tarnawski AS. PTEN regulatory functions in tumor suppression and cell biology. Med Sci Monit (2004) 10:RA235-41.
49. Chung JH, Ostrowski MC, Romigh T, Minaguchi T, Waite KA, Eng C. The ERK1/2 pathway modulates nuclear PTEN-mediated cell cycle arrest by cyclin D1 transcriptional regulation. Hum Mol Genet (2006) 15:2553-9. doi:10.1093/hmg/ddl177
50. Chung JH, Eng C. Nuclear-cytoplasmic partitioning of phosphatase and tensin homologue deleted on chromosome 10 (PTEN) differentially regulates the cell cycle and apoptosis. Cancer Res (2005) 65:8096-100. doi:10.1158/0008-5472.CAN-05-1888
51. Qiao L, Paul P, Lee S, Qiao J, Wang Y, Chung DH. Differential regulation of cyclin-dependent kinase inhibitors in neuroblastoma cells. Biochem Biophys Res Commun (2013) 435:295-9. doi:10.1016/j.bbrc.2013.04.023
52. Seminario MC, Precht P, Wersto RP, Gorospe M, Wange RL. PTEN expression in PTEN-null leukaemic T cell lines leads to reduced proliferation via slowed cell cycle progression. Oncogene (2003) 22:8195-204. doi:10.1038/sj.onc.1206872
53. Jacob AI, Romigh T, Waite KA, Eng C. Nuclear PTEN levels and G2 progression in melanoma cells. Melanoma Res (2009) 19:203-10. doi:10.1097/CMR.0b013e32832ccd6e
54. Planchon SM, Waite KA, Eng C. The nuclear affairs of PTEN. J Cell Sci (2008) 121:249-53. doi:10.1242/jcs.022459
55. Xu N, Lao Y, Zhang Y, Gillespie DA. Akt: a double-edged sword in cell proliferation and genome stability. J Oncol (2012) 2012:951724. doi:10.1155/2012/951724
56. Ming M, He YY. PTEN in DNA damage repair. Cancer Lett (2012) 319:125-9. doi:10.1016/j.canlet.2012.01.003
57. Selvendiran K, Tong L, Vishwanath S, Bratasz A, Trigg NJ, Kutala VK, et al. EF24 induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by increasing PTEN expression. J Biol Chem (2007) 282:28609-18. doi:10.1074/jbc. M703796200
58. Zhou Y, Ho WS. Combination of liquiritin, isoliquiritin and isoliquirigenin induce apoptotic cell death through upregulating p53 and p21 in the A549 non-small cell lung cancer cells. Oncol Rep (2014) 31:298-304. doi:10.3892/or.2013.2849
59. Chang CJ, Mulholland DJ, Valamehr B, Mosessian S, Sellers WR, Wu H. PTEN nuclear localization is regulated by oxidative stress and mediates p53-dependent tumor suppression. Mol Cell Biol (2008) 28:3281-9. doi:10.1128/MCB.00310-08
60. Nakanishi A, Wada Y, Kitagishi Y, Matsuda S. Link between PI3K/AKT/PTEN pathway and NOX proteinin diseases. Aging Dis (2014) 5:203-11. doi:10.14336/AD.2014.0500203
61. Li ZY, Yang Y, Ming M, Liu B. Mitochondrial ROS generation for regulation of autophagic pathways in cancer. Biochem Biophys Res Commun (2011) 414:5-8. doi:10.1016/j.bbrc.2011.09.046
62. Leslie NR, Bennett D, Lindsay YE, Stewart H, Gray A, Downes CP. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J (2003) 22:5501-10. doi:10.1093/emboj/cdg513
63. Simone RE, Russo M, Catalano A, Monego G, Froehlich K, Boehm V, et al. Lycopene inhibits NF-kB-mediated IL-8 expression and changes redox and PPAR? signalling in cigarette smoke-stimulated macrophages. PLoS One (2011) 6:e19652. doi:10.1371/journal.pone.0019652
64. Kim JW, Kang KH, Burrola P, Mak TW, Lemke G. Retinal degeneration triggered by inactivation of PTEN in the retinal pigment epithelium. Genes Dev (2008) 22:3147-57. doi:10.1101/gad.1700108
65. Kang KH, Lemke G, Kim JW. The PI3K-PTEN tug-of-war, oxidative stress and retinal degeneration. Trends Mol Med (2009) 15:191-8. doi:10.1016/j.molmed.2009.03.005
66. Mukherjee B, Tomimatsu N, Amancherla K, Camacho CV, Pichamoorthy N, Burma S. The dual PI3K/mTOR inhibitor NVP-BEZ235 is a potent inhibitor of ATM- and DNA-PKCs-mediated DNA damage responses. Neoplasia (2012) 14:34-43.
67. Li JR, Cheng CL, Yang CR, Ou YC, Wu MJ, Ko JL. Dual inhibitor of phosphoinositide 3-kinase/mammalian target of rapamycin NVP-BEZ235 effectively inhibits cisplatin-resistant urothelial cancer cell growth through autophagic flux. Toxicol Lett (2013) 220:267-76. doi:10.1016/j.toxlet.2013.04.021
68. Guo JP, Coppola D, Cheng JQ. IKBKE protein activates Akt independent of phosphatidylinositol 3-kinase/PDK1/mTORC2 and the pleckstrin homology domain to sustain malignant transformation. J Biol Chem (2011) 286:37389-98. doi:10.1074/jbc. M111.287433
69. Chock KL, Allison JM, Shimizu Y, ElShamy WM. BRCA1-IRIS overexpression promotes cisplatin resistance in ovarian cancer cells. Cancer Res (2010) 70:8782-91. doi:10.1158/0008-5472.CAN-10-1352
70. Burstein HJ. Novel agents and future directions for refractory breast cancer. Semin Oncol (2011) 38(Suppl 2):S17-24. doi:10.1053/j.seminoncol.2011.04.002
71. Ma Y, Hu C, Riegel AT, Fan S, Rosen EM. Growth factor signaling pathways modulate BRCA1 repression of estrogen receptor-alpha activity. Mol Endocrinol (2007) 21:1905-23. doi:10.1210/me.2006-0397
72. Hinton CV, Fitzgerald LD, Thompson ME. Phosphatidylinositol 3-kinase/Akt signaling enhances nuclear localization and transcriptional activity of BRCA1. Exp Cell Res (2007) 313:1735-44. doi:10.1016/j.yexcr.2007.03.008
73. Kang HJ, Yi YW, Kim HJ, Hong YB, Seong YS, Bae I. BRCA1 negatively regulates IGF-1 expression through an estrogen-responsive element-like site. Cell Death Dis (2012) 3:e336. doi:10.1038/cddis.2012.78
74. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell (1999) 96:857-68. doi:10.1016/S0092-8674(00)80595-4
75. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr, DiStefano PS, et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science (2002) 296:530-4. doi:10.1126/science.1068712
76. Saal LH, Gruvberger-Saal SK, Persson C, Lövgren K, Jumppanen M, Staaf J, et al. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat Genet (2008) 40:102-7. doi:10.1038/ng.2007.39
77. Foulkes WD. BRCA1-sowing the seeds crooked in the furrow. Nat Genet (2008) 40:8-9. doi:10.1038/ng0108-8
78. Martins FC, De S, Almendro V, Gönen M, Park SY, Blum JL, et al. Evolutionary pathways in BRCA1-associated breast tumors. Cancer Discov (2012) 2:503-11. doi:10.1158/2159-8290.CD-11-0325
79. Shen WH, Balajee AS, Wang J, Wu H, Eng C, PandolfiPP, et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell (2007) 128:157-70. doi:10.1016/j.cell.2006.11.042
80. Shen Z, Huhn S. PTEN sumo-wrestles human RAD52 to mystery land. Cell Cycle (2013) 12:3585. doi:10.4161/cc.26820
81. Jung IL, Kang HJ, Kim KC, Kim IG. PTEN/pAkt/p53 signaling pathway correlates with the radioresponse of non-small cell lung cancer. Int J Mol Med (2010) 25:517-23.
82. Li HF, Kim JS, Waldman T. Radiation-induced Akt activation modulates radioresistance in human glioblastoma cells. Radiat Oncol (2009) 4:43. doi:10.1186/1748-717X-4-43
83. Zhang J, Xiao Y, Guo Y, Breslin P, Zhang S, Wei W, et al. Differential requirements for c-Myc in chronic hematopoietic hyperplasia and acute hematopoietic malignancies in Pten-null mice. Leukemia (2011) 25:1857-68. doi:10.1038/leu.2011.220
84. Guo W, Schubbert S, Chen JY, Valamehr B, Mosessian S, Shi H, et al. Suppression of leukemia development caused by PTEN loss. Proc Natl Acad Sci U S A (2011) 108:1409-14. doi:10.1073/pnas.1006937108
85. Chen J, Zhao KN, Li R, Shao R, Chen C. Activation of PI3K/Akt/mTOR pathway and dual inhibitors of PI3K and mTOR in endometrial cancer. Curr Med Chem (2014) 21:3070-80. doi:10.2174/0929867321666140414095605
86. Kim JY. Control of ovarian primordial follicle activation. Clin Exp Reprod Med (2012) 39:10-4. doi:10.5653/cerm.2012.39.1.10
87. Merritt MA, Cramer DW. Molecular pathogenesis of endometrial and ovarian cancer. Cancer Biomark (2010) 9:287-305. doi:10.3233/CBM-2011-0167