Skip to main content
Top
Published in: BMC Cancer 1/2010

Open Access 01-12-2010 | Research article

Microarray analysis of DNA damage repair gene expression profiles in cervical cancer cells radioresistant to 252Cf neutron and X-rays

Authors: Yi Qing, Xue-Qin Yang, Zhao-Yang Zhong, Xin Lei, Jia-Yin Xie, Meng-Xia Li, De-Bing Xiang, Zeng-Peng Li, Zhen-Zhou Yang, Ge Wang, Dong Wang

Published in: BMC Cancer | Issue 1/2010

Login to get access

Abstract

Background

The aim of the study was to obtain stable radioresistant sub-lines from the human cervical cancer cell line HeLa by prolonged exposure to 252Cf neutron and X-rays. Radioresistance mechanisms were investigated in the resulting cells using microarray analysis of DNA damage repair genes.

Methods

HeLa cells were treated with fractionated 252Cf neutron and X-rays, with a cumulative dose of 75 Gy each, over 8 months, yielding the sub-lines HeLaNR and HeLaXR. Radioresistant characteristics were detected by clone formation assay, ultrastructural observations, cell doubling time, cell cycle distribution, and apoptosis assay. Gene expression patterns of the radioresistant sub-lines were studied through microarray analysis and verified by Western blotting and real-time PCR.

Results

The radioresistant sub-lines HeLaNR and HeLaXR were more radioresisitant to 252Cf neutron and X-rays than parental HeLa cells by detecting their radioresistant characteristics, respectively. Compared to HeLa cells, the expression of 24 genes was significantly altered by at least 2-fold in HeLaNR cells. Of these, 19 genes were up-regulated and 5 down-regulated. In HeLaXR cells, 41 genes were significantly altered by at least 2-fold; 38 genes were up-regulated and 3 down-regulated.

Conclusions

Chronic exposure of cells to ionizing radiation induces adaptive responses that enhance tolerance of ionizing radiation and allow investigations of cellular radioresistance mechanisms. The insights gained into the molecular mechanisms activated by these "radioresistance" genes will lead to new therapeutic targets for cervical cancer.
Appendix
Available only for authorised users
Literature
1.
go back to reference Pontén J, Adami HO, Bergström R, Dillner J, Friberg LG, Gustafsson L, Miller AB, Parkin DM, Sparén P, Trichopoulos D: Strategies for global control of cervical cancer. Int J Cancer. 1995, 60: 1-26. 10.1002/ijc.2910600102.CrossRefPubMed Pontén J, Adami HO, Bergström R, Dillner J, Friberg LG, Gustafsson L, Miller AB, Parkin DM, Sparén P, Trichopoulos D: Strategies for global control of cervical cancer. Int J Cancer. 1995, 60: 1-26. 10.1002/ijc.2910600102.CrossRefPubMed
2.
go back to reference Harima Y, Togashi A, Horikoshi K, Imamura M, Sougawa M, Sawada S, Tsunoda T, Nakamura Y, Katagiri T: Prediction of outcome of advanced cervical cancer to thermoradiotherapy according to expression profiles of 35 genes selected by cDNA microarray analysis. Int J Radiat Oncol Biol Phys. 2004, 60: 237-248.CrossRefPubMed Harima Y, Togashi A, Horikoshi K, Imamura M, Sougawa M, Sawada S, Tsunoda T, Nakamura Y, Katagiri T: Prediction of outcome of advanced cervical cancer to thermoradiotherapy according to expression profiles of 35 genes selected by cDNA microarray analysis. Int J Radiat Oncol Biol Phys. 2004, 60: 237-248.CrossRefPubMed
3.
go back to reference Ma BB, Bristow RG, Kim J, Siu LL: Combined-modality treatment of solid tumors using radiotherapy and molecular targeted agents. J Clin Oncol. 2003, 21: 2760-2776. 10.1200/JCO.2003.10.044.CrossRefPubMed Ma BB, Bristow RG, Kim J, Siu LL: Combined-modality treatment of solid tumors using radiotherapy and molecular targeted agents. J Clin Oncol. 2003, 21: 2760-2776. 10.1200/JCO.2003.10.044.CrossRefPubMed
5.
go back to reference Marjina LA, Kiseleva MV, Chekhonadsky VN: Radiation treatment of the cervix uteri cancer with usage of high activity 252Cf sources. Radiother Oncol. 2002, 63 (Suppl): s21- Marjina LA, Kiseleva MV, Chekhonadsky VN: Radiation treatment of the cervix uteri cancer with usage of high activity 252Cf sources. Radiother Oncol. 2002, 63 (Suppl): s21-
6.
go back to reference Tacev T, Ptácková B, Strnad V: Californium-252 (252Cf) versus conventional gamma radiation in the brachytherapy of advanced cervical carcinoma long-term treatment results of a randomized study. Strahlenther Onkol. 2003, 179: 377-384. 10.1007/s00066-003-1006-3.CrossRefPubMed Tacev T, Ptácková B, Strnad V: Californium-252 (252Cf) versus conventional gamma radiation in the brachytherapy of advanced cervical carcinoma long-term treatment results of a randomized study. Strahlenther Onkol. 2003, 179: 377-384. 10.1007/s00066-003-1006-3.CrossRefPubMed
7.
go back to reference Elkind MM: DNA damage and cell killing. Cause and effect?. Cancer. 1985, 56: 2351-2363. 10.1002/1097-0142(19851115)56:10<2351::AID-CNCR2820561002>3.0.CO;2-H.CrossRefPubMed Elkind MM: DNA damage and cell killing. Cause and effect?. Cancer. 1985, 56: 2351-2363. 10.1002/1097-0142(19851115)56:10<2351::AID-CNCR2820561002>3.0.CO;2-H.CrossRefPubMed
8.
go back to reference Thompson LH, Brookman KW, Dillehay LE, Carrano AV, Mazrimas JA, Mooney CL, Minkler JL: A CHO-cell strain having hypersensitivity to mutagens, a defect in DNA strand-break repair, and an extraordinary baseline frequency of sister-chromatid exchange. Mutat Res. 1982, 95: 427-440.CrossRefPubMed Thompson LH, Brookman KW, Dillehay LE, Carrano AV, Mazrimas JA, Mooney CL, Minkler JL: A CHO-cell strain having hypersensitivity to mutagens, a defect in DNA strand-break repair, and an extraordinary baseline frequency of sister-chromatid exchange. Mutat Res. 1982, 95: 427-440.CrossRefPubMed
9.
go back to reference Kelland LR, Edwards SM, Steel GG: Induction and rejoining of DNA double-strand breaks in human cervix carcinoma cell lines of differing radiosensitivity. Radiat Res. 1988, 116: 526-538. 10.2307/3577394.CrossRefPubMed Kelland LR, Edwards SM, Steel GG: Induction and rejoining of DNA double-strand breaks in human cervix carcinoma cell lines of differing radiosensitivity. Radiat Res. 1988, 116: 526-538. 10.2307/3577394.CrossRefPubMed
10.
go back to reference Schwartz JL, Rotmensch J, Giovanazzi S, Cohen MB, Weichselbaum RR: Faster repair of DNA double-strand breaks in radioresistant human tumor cells. Int J Radiat Oncol Biol Phys. 1988, 15: 907-912.CrossRefPubMed Schwartz JL, Rotmensch J, Giovanazzi S, Cohen MB, Weichselbaum RR: Faster repair of DNA double-strand breaks in radioresistant human tumor cells. Int J Radiat Oncol Biol Phys. 1988, 15: 907-912.CrossRefPubMed
11.
go back to reference Russell J, Wheldon TE, Stanton P: A radioresistant variant derived from a human neuroblastoma cell line is less prone to radiation-induced apoptosis. Cancer Res. 1995, 55: 4915-4921.PubMed Russell J, Wheldon TE, Stanton P: A radioresistant variant derived from a human neuroblastoma cell line is less prone to radiation-induced apoptosis. Cancer Res. 1995, 55: 4915-4921.PubMed
12.
go back to reference Dahlberg WK, Azzam EI, Yu Y, Little JB: Response of human tumor cells of varying radiosensitivity and radiocurability to fractionated irradiation. Cancer Res. 1999, 59: 5365-69.PubMed Dahlberg WK, Azzam EI, Yu Y, Little JB: Response of human tumor cells of varying radiosensitivity and radiocurability to fractionated irradiation. Cancer Res. 1999, 59: 5365-69.PubMed
13.
go back to reference Pearce AG, Segura TM, Rintala AC, Rintala-Maki ND, Lee H: The generation and characterization of a radiation-resistant model system to study radioresistance in human breast cancer cells. Radiat Res. 2001, 156: 739-750. 10.1667/0033-7587(2001)156[0739:TGACOA]2.0.CO;2.CrossRefPubMed Pearce AG, Segura TM, Rintala AC, Rintala-Maki ND, Lee H: The generation and characterization of a radiation-resistant model system to study radioresistance in human breast cancer cells. Radiat Res. 2001, 156: 739-750. 10.1667/0033-7587(2001)156[0739:TGACOA]2.0.CO;2.CrossRefPubMed
14.
go back to reference Wei K, Kodym R, Jin C: Radioresistant cell strain of human fibrosarcoma cells obtained after long-term exposure to x-rays. Radiat Environ Biophys. 1998, 37: 133-137. 10.1007/s004110050106.CrossRefPubMed Wei K, Kodym R, Jin C: Radioresistant cell strain of human fibrosarcoma cells obtained after long-term exposure to x-rays. Radiat Environ Biophys. 1998, 37: 133-137. 10.1007/s004110050106.CrossRefPubMed
15.
go back to reference Ewing D: Production of radiation-resistant E. coli strains by daily X-irradiation. Int J Radiat Biol. 1997, 71: 253-258. 10.1080/095530097144120.CrossRefPubMed Ewing D: Production of radiation-resistant E. coli strains by daily X-irradiation. Int J Radiat Biol. 1997, 71: 253-258. 10.1080/095530097144120.CrossRefPubMed
16.
go back to reference Wazer DE, Joyce M, Jung L, Band V: Alterations in growth phenotype and radiosensitivity after fractionated irradiation of breast carcinoma cells from a single patient. Int J Radiat Oncol Biol Phys. 1993, 26: 81-88.CrossRefPubMed Wazer DE, Joyce M, Jung L, Band V: Alterations in growth phenotype and radiosensitivity after fractionated irradiation of breast carcinoma cells from a single patient. Int J Radiat Oncol Biol Phys. 1993, 26: 81-88.CrossRefPubMed
17.
go back to reference Ogawa K, Utsunomiya T, Mimori K, Tanaka F, Haraguchi N, Inoue H, Murayama S, Mori M: Differential gene expression profiles of radioresistant pancreatic cancer cell lines established by fractionated irradiation. Int J Oncol. 2006, 28: 705-713.PubMed Ogawa K, Utsunomiya T, Mimori K, Tanaka F, Haraguchi N, Inoue H, Murayama S, Mori M: Differential gene expression profiles of radioresistant pancreatic cancer cell lines established by fractionated irradiation. Int J Oncol. 2006, 28: 705-713.PubMed
18.
go back to reference Fukuda K, Sakakura C, Miyagawa K, Kuriu Y, Kin S, Nakase Y, Hagiwara A, Mitsufuji S, Okazaki Y, Hayashizaki Y, Yamagishi H: Differential gene expression profiles of radioresistant oesophageal cancer cell lines established by continuous fractionated irradiation. Br J Cancer. 2004, 91: 1543-1550. 10.1038/sj.bjc.6602187.CrossRefPubMedPubMedCentral Fukuda K, Sakakura C, Miyagawa K, Kuriu Y, Kin S, Nakase Y, Hagiwara A, Mitsufuji S, Okazaki Y, Hayashizaki Y, Yamagishi H: Differential gene expression profiles of radioresistant oesophageal cancer cell lines established by continuous fractionated irradiation. Br J Cancer. 2004, 91: 1543-1550. 10.1038/sj.bjc.6602187.CrossRefPubMedPubMedCentral
19.
go back to reference Chang JT, Chan SH, Lin CY, Lin TY, Wang HM, Liao CT, Wang TH, Lee LY, Cheng AJ: Differentially expressed genes in radioresistant nasopharyngeal cancer cells: gp96 and GDF15. Mol Cancer Ther. 2007, 6: 2271-2279. 10.1158/1535-7163.MCT-06-0801.CrossRefPubMed Chang JT, Chan SH, Lin CY, Lin TY, Wang HM, Liao CT, Wang TH, Lee LY, Cheng AJ: Differentially expressed genes in radioresistant nasopharyngeal cancer cells: gp96 and GDF15. Mol Cancer Ther. 2007, 6: 2271-2279. 10.1158/1535-7163.MCT-06-0801.CrossRefPubMed
20.
go back to reference Maity A, Kao GD, Muschel RJ, McKenna WG: Potential molecular targets for manipulating the radiation response. Int J Radiat Oncol Biol Phys. 1997, 37: 639-53.CrossRefPubMed Maity A, Kao GD, Muschel RJ, McKenna WG: Potential molecular targets for manipulating the radiation response. Int J Radiat Oncol Biol Phys. 1997, 37: 639-53.CrossRefPubMed
21.
go back to reference Pawlik TM, Keyomarsi K: Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004, 59: 928-942. 10.1016/j.ijrobp.2004.03.005.CrossRefPubMed Pawlik TM, Keyomarsi K: Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004, 59: 928-942. 10.1016/j.ijrobp.2004.03.005.CrossRefPubMed
22.
go back to reference Iliakis G, Metzger L, Muschel RJ, McKenna WG: Induction and repair of DNA double strand breaks in radiation-resistant cells obtained by transformation of primary rat embryo cells with the oncogenes H-ras and v-myc. Cancer Res. 1990, 50: 6575-6579.PubMed Iliakis G, Metzger L, Muschel RJ, McKenna WG: Induction and repair of DNA double strand breaks in radiation-resistant cells obtained by transformation of primary rat embryo cells with the oncogenes H-ras and v-myc. Cancer Res. 1990, 50: 6575-6579.PubMed
23.
go back to reference Verheij M, Bartelink H: Radiation-induced apoptosis. Cell Tissue Res. 2000, 301: 133-142. 10.1007/s004410000188.CrossRefPubMed Verheij M, Bartelink H: Radiation-induced apoptosis. Cell Tissue Res. 2000, 301: 133-142. 10.1007/s004410000188.CrossRefPubMed
24.
go back to reference Meyn RE, Stephens LC, Milas L: Programmed cell death and radioresistance. Cancer Metastasis Rev. 1996, 15: 119-131. 10.1007/BF00049491.CrossRefPubMed Meyn RE, Stephens LC, Milas L: Programmed cell death and radioresistance. Cancer Metastasis Rev. 1996, 15: 119-131. 10.1007/BF00049491.CrossRefPubMed
25.
go back to reference Bentzen SM: Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer. 2006, 6: 702-713. 10.1038/nrc1950.CrossRefPubMed Bentzen SM: Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer. 2006, 6: 702-713. 10.1038/nrc1950.CrossRefPubMed
26.
go back to reference Kitahara O, Katagiri T, Tsunoda T, Harima Y, Nakamura Y: Classification of sensitivity or resistance of cervical cancers to ionizing radiation according to expression profiles of 62 genes selected by cDNA microarray analysis. Neoplasia. 2002, 4: 295-303. 10.1038/sj.neo.7900251.CrossRefPubMedPubMedCentral Kitahara O, Katagiri T, Tsunoda T, Harima Y, Nakamura Y: Classification of sensitivity or resistance of cervical cancers to ionizing radiation according to expression profiles of 62 genes selected by cDNA microarray analysis. Neoplasia. 2002, 4: 295-303. 10.1038/sj.neo.7900251.CrossRefPubMedPubMedCentral
27.
go back to reference Wong YF, Selvanayagam ZE, Wei N, Porter J, Vittal R, Hu R, Lin Y, Liao J, Shih JW, Cheung TH, Lo KW, Yim SF, Yip SK, Ngong DT, Siu N, Chan LK, Chan CS, Kong T, Kutlina E, McKinnon RD, Denhardt DT, Chin KV, Chung TK: Expression genomics of cervical cancer: molecular classification and prediction of radiotherapy response by DNA microarray. Clin Cancer Res. 2003, 9: 5486-5492.PubMed Wong YF, Selvanayagam ZE, Wei N, Porter J, Vittal R, Hu R, Lin Y, Liao J, Shih JW, Cheung TH, Lo KW, Yim SF, Yip SK, Ngong DT, Siu N, Chan LK, Chan CS, Kong T, Kutlina E, McKinnon RD, Denhardt DT, Chin KV, Chung TK: Expression genomics of cervical cancer: molecular classification and prediction of radiotherapy response by DNA microarray. Clin Cancer Res. 2003, 9: 5486-5492.PubMed
28.
go back to reference Harima Y, Togashi A, Horikoshi K, Imamura M, Sougawa M, Sawada S, Tsunoda T, Nakamura Y, Katagiri T: Prediction of outcome of advanced cervical cancer to thermoradiotherapy according to expression profiles of 35 genes selected by cDNA microarray analysis. Int J Radiat Oncol Biol Phys. 2004, 60: 237-248.CrossRefPubMed Harima Y, Togashi A, Horikoshi K, Imamura M, Sougawa M, Sawada S, Tsunoda T, Nakamura Y, Katagiri T: Prediction of outcome of advanced cervical cancer to thermoradiotherapy according to expression profiles of 35 genes selected by cDNA microarray analysis. Int J Radiat Oncol Biol Phys. 2004, 60: 237-248.CrossRefPubMed
29.
go back to reference Chung YM, Kim BG, Park CS, Huh SJ, Kim J, Park JK, Cho SM, Kim BS, Kim JS, Yoo YD, Bae DS: Increased expression of ICAM-3 is associated with radiation resistance in cervical cancer. Int J Cancer. 2005, 117: 194-201. 10.1002/ijc.21180.CrossRefPubMed Chung YM, Kim BG, Park CS, Huh SJ, Kim J, Park JK, Cho SM, Kim BS, Kim JS, Yoo YD, Bae DS: Increased expression of ICAM-3 is associated with radiation resistance in cervical cancer. Int J Cancer. 2005, 117: 194-201. 10.1002/ijc.21180.CrossRefPubMed
30.
go back to reference Wong YF, Sahota DS, Cheung TH, Lo KW, Yim SF, Chung TK, Chang AM, Smith DI: Gene expression pattern associated with radiotherapy sensitivity in cervical cancer. Cancer J. 2006, 12: 189-193. 10.1097/00130404-200605000-00006.CrossRefPubMed Wong YF, Sahota DS, Cheung TH, Lo KW, Yim SF, Chung TK, Chang AM, Smith DI: Gene expression pattern associated with radiotherapy sensitivity in cervical cancer. Cancer J. 2006, 12: 189-193. 10.1097/00130404-200605000-00006.CrossRefPubMed
31.
go back to reference Harima Y, Sawada S, Miyazaki Y, Kin K, Ishihara H, Imamura M, Sougawa M, Shikata N, Ohnishi T: Expression of Ku80 in cervical cancer correlates with response to radiotherapy and survival. Am J Clin Oncol. 2003, 26: e80-85. 10.1097/00000421-200308000-00028.PubMed Harima Y, Sawada S, Miyazaki Y, Kin K, Ishihara H, Imamura M, Sougawa M, Shikata N, Ohnishi T: Expression of Ku80 in cervical cancer correlates with response to radiotherapy and survival. Am J Clin Oncol. 2003, 26: e80-85. 10.1097/00000421-200308000-00028.PubMed
32.
go back to reference Fornace AJ, Amundson SA, Bittner M, Myers TG, Meltzer P, Weinsten JN, Trent J: The complexity of radiation stress responses: analysis by informatics and functional genomics approaches. Gene Expr. 1999, 7: 387-400.PubMed Fornace AJ, Amundson SA, Bittner M, Myers TG, Meltzer P, Weinsten JN, Trent J: The complexity of radiation stress responses: analysis by informatics and functional genomics approaches. Gene Expr. 1999, 7: 387-400.PubMed
33.
go back to reference Maity A, McKenna WG, Muschel RJ: The molecular basis for cell cycle delays following ionizing radiation: a review. Radiother Oncol. 1994, 31: 1-13. 10.1016/0167-8140(94)90408-1.CrossRefPubMed Maity A, McKenna WG, Muschel RJ: The molecular basis for cell cycle delays following ionizing radiation: a review. Radiother Oncol. 1994, 31: 1-13. 10.1016/0167-8140(94)90408-1.CrossRefPubMed
34.
go back to reference Rouault JP, Falette N, Guéhenneux F, Guillot C, Rimokh R, Wang Q, Berthet C, Moyret-Lalle C, Savatier P, Pain B, Shaw P, Berger R, Samarut J, Magaud JP, Ozturk M, Samarut C, Puisieux A: Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat Genet. 1996, 14: 482-486. 10.1038/ng1296-482.CrossRefPubMed Rouault JP, Falette N, Guéhenneux F, Guillot C, Rimokh R, Wang Q, Berthet C, Moyret-Lalle C, Savatier P, Pain B, Shaw P, Berger R, Samarut J, Magaud JP, Ozturk M, Samarut C, Puisieux A: Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat Genet. 1996, 14: 482-486. 10.1038/ng1296-482.CrossRefPubMed
35.
go back to reference Wang G, Zhang XR, Hu L, Wang J, Leng ER, Fang DC, Yang XM, Zhang Y, He FC: Rapid induction of mRNAs for liver regeneration genes by hepatopoietin and partial hepatectomy. Zhonghua Gan Zang Bing Za Zhi. 2002, 10: 256-259.PubMed Wang G, Zhang XR, Hu L, Wang J, Leng ER, Fang DC, Yang XM, Zhang Y, He FC: Rapid induction of mRNAs for liver regeneration genes by hepatopoietin and partial hepatectomy. Zhonghua Gan Zang Bing Za Zhi. 2002, 10: 256-259.PubMed
36.
go back to reference Guardavaccaro D, Corrente G, Covone F, Micheli L, D'Agnano I, Starace G, Caruso M, Tirone F: Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol Cell Biol. 2000, 20: 1797-1815. 10.1128/MCB.20.5.1797-1815.2000.CrossRefPubMedPubMedCentral Guardavaccaro D, Corrente G, Covone F, Micheli L, D'Agnano I, Starace G, Caruso M, Tirone F: Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol Cell Biol. 2000, 20: 1797-1815. 10.1128/MCB.20.5.1797-1815.2000.CrossRefPubMedPubMedCentral
37.
go back to reference el-Ghissassi F, Valsesia-Wittmann S, Falette N, Duriez C, Walden PD, Puisieux A: BTG2(TIS21/PC3) induces neuronal differentiation and prevents apoptosis of terminally differentiated PC12 cells. Oncogene. 2002, 21: 6772-6778. 10.1038/sj.onc.1205888.CrossRefPubMed el-Ghissassi F, Valsesia-Wittmann S, Falette N, Duriez C, Walden PD, Puisieux A: BTG2(TIS21/PC3) induces neuronal differentiation and prevents apoptosis of terminally differentiated PC12 cells. Oncogene. 2002, 21: 6772-6778. 10.1038/sj.onc.1205888.CrossRefPubMed
38.
go back to reference Klopp AH, Jhingran A, Ramdas L, Story MD, Broadus RR, Lu KH, Eifel PJ, Buchholz TA: Gene expression changes in cervical squamous cell carcinoma after initiation of chemoradiation and correlation with clinical outcome. Int J Radiat Oncol Biol Phys. 2008, 71: 226-236.CrossRefPubMed Klopp AH, Jhingran A, Ramdas L, Story MD, Broadus RR, Lu KH, Eifel PJ, Buchholz TA: Gene expression changes in cervical squamous cell carcinoma after initiation of chemoradiation and correlation with clinical outcome. Int J Radiat Oncol Biol Phys. 2008, 71: 226-236.CrossRefPubMed
39.
go back to reference Jin S, Tong T, Fan W, Fan F, Antinore MJ, Zhu X, Mazzacurati L, Li X, Petrik KL, Rajasekaran B, Wu M, Zhan Q: GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene. 2002, 21: 8696-8704. 10.1038/sj.onc.1206034.CrossRefPubMed Jin S, Tong T, Fan W, Fan F, Antinore MJ, Zhu X, Mazzacurati L, Li X, Petrik KL, Rajasekaran B, Wu M, Zhan Q: GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene. 2002, 21: 8696-8704. 10.1038/sj.onc.1206034.CrossRefPubMed
40.
go back to reference Takekawa M, Saito H: A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell. 1998, 95: 521-530. 10.1016/S0092-8674(00)81619-0.CrossRefPubMed Takekawa M, Saito H: A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell. 1998, 95: 521-530. 10.1016/S0092-8674(00)81619-0.CrossRefPubMed
41.
go back to reference Harkin DP, Bean JM, Miklos D, Song YH, Truong VB, Englert C, Christians FC, Ellisen LW, Maheswaran S, Oliner JD, Haber DA: Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell. 1999, 97: 575-586. 10.1016/S0092-8674(00)80769-2.CrossRefPubMed Harkin DP, Bean JM, Miklos D, Song YH, Truong VB, Englert C, Christians FC, Ellisen LW, Maheswaran S, Oliner JD, Haber DA: Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell. 1999, 97: 575-586. 10.1016/S0092-8674(00)80769-2.CrossRefPubMed
Metadata
Title
Microarray analysis of DNA damage repair gene expression profiles in cervical cancer cells radioresistant to 252Cf neutron and X-rays
Authors
Yi Qing
Xue-Qin Yang
Zhao-Yang Zhong
Xin Lei
Jia-Yin Xie
Meng-Xia Li
De-Bing Xiang
Zeng-Peng Li
Zhen-Zhou Yang
Ge Wang
Dong Wang
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2010
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-10-71

Other articles of this Issue 1/2010

BMC Cancer 1/2010 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine