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

Open Access 01-12-2010 | Research article

Up-regulation of cell cycle arrest protein BTG2 correlates with increased overall survival in breast cancer, as detected by immunohistochemistry using tissue microarray

Authors: Elin Möllerström, Anikó Kovács, Kristina Lövgren, Szilard Nemes, Ulla Delle, Anna Danielsson, Toshima Parris, Donal J Brennan, Karin Jirström, Per Karlsson, Khalil Helou

Published in: BMC Cancer | Issue 1/2010

Login to get access

Abstract

Background

Previous studies have shown that the ADIPOR1, ADORA1, BTG2 and CD46 genes differ significantly between long-term survivors of breast cancer and deceased patients, both in levels of gene expression and DNA copy numbers. The aim of this study was to characterize the expression of the corresponding proteins in breast carcinoma and to determine their correlation with clinical outcome.

Methods

Protein expression was evaluated using immunohistochemistry in an independent breast cancer cohort of 144 samples represented on tissue microarrays. Fisher's exact test was used to analyze the differences in protein expression between dead and alive patients. We used Cox-regression multivariate analysis to assess whether the new markers predict the survival status of the patients better than the currently used markers.

Results

BTG2 expression was demonstrated in a significantly lower proportion of samples from dead patients compared to alive patients, both in overall expression (P = 0.026) and cell membrane specific expression (P = 0.013), whereas neither ADIPOR1, ADORA1 nor CD46 showed differential expression in the two survival groups. Furthermore, a multivariate analysis showed that a model containing BTG2 expression in combination with HER2 and Ki67 expression along with patient age performed better than a model containing the currently used prognostic markers (tumour size, nodal status, HER2 expression, hormone receptor status, histological grade, and patient age). Interestingly, BTG2 has previously been described as a tumour suppressor gene involved in cell cycle arrest and p53 signalling.

Conclusions

We conclude that high-level BTG2 protein expression correlates with prolonged survival in patients with breast carcinoma.
Appendix
Available only for authorised users
Literature
1.
go back to reference Parkin DM, Bray F, Ferlay J, Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 2005, 55: 74-108. 10.3322/canjclin.55.2.74.CrossRefPubMed Parkin DM, Bray F, Ferlay J, Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 2005, 55: 74-108. 10.3322/canjclin.55.2.74.CrossRefPubMed
2.
go back to reference Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, Mandelblatt JS, Yakovlev AY, Habbema JD, Feuer EJ: Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005, 353: 1784-1792. 10.1056/NEJMoa050518.CrossRefPubMed Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, Mandelblatt JS, Yakovlev AY, Habbema JD, Feuer EJ: Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005, 353: 1784-1792. 10.1056/NEJMoa050518.CrossRefPubMed
3.
go back to reference Goldhirsch A, Wood WC, Gelber RD, Coates AS, Thurlimann B, Senn HJ: Progress and promise: highlights of the international expert consensus on the primary therapy of early breast cancer 2007. Ann Oncol. 2007, 18: 1133-1144. 10.1093/annonc/mdm271.CrossRefPubMed Goldhirsch A, Wood WC, Gelber RD, Coates AS, Thurlimann B, Senn HJ: Progress and promise: highlights of the international expert consensus on the primary therapy of early breast cancer 2007. Ann Oncol. 2007, 18: 1133-1144. 10.1093/annonc/mdm271.CrossRefPubMed
4.
go back to reference Coleman MP, Quaresma M, Berrino F, Lutz JM, De Angelis R, Capocaccia R, Baili P, Rachet B, Gatta G, Hakulinen T, et al: Cancer survival in five continents: a worldwide population-based study (CONCORD). Lancet Oncol. 2008, 9: 730-756. 10.1016/S1470-2045(08)70179-7.CrossRefPubMed Coleman MP, Quaresma M, Berrino F, Lutz JM, De Angelis R, Capocaccia R, Baili P, Rachet B, Gatta G, Hakulinen T, et al: Cancer survival in five continents: a worldwide population-based study (CONCORD). Lancet Oncol. 2008, 9: 730-756. 10.1016/S1470-2045(08)70179-7.CrossRefPubMed
5.
go back to reference van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, et al: Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002, 415: 530-536. 10.1038/415530a.CrossRef van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, et al: Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002, 415: 530-536. 10.1038/415530a.CrossRef
6.
go back to reference Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, et al: Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet. 2005, 365: 671-679.CrossRefPubMed Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, et al: Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet. 2005, 365: 671-679.CrossRefPubMed
7.
go back to reference Karlsson E, Delle U, Danielsson A, Olsson B, Abel F, Karlsson P, Helou K: Gene expression variation to predict 10-year survival in lymph-node-negative breast cancer. BMC Cancer. 2008, 8: 254-10.1186/1471-2407-8-254.CrossRefPubMedPubMedCentral Karlsson E, Delle U, Danielsson A, Olsson B, Abel F, Karlsson P, Helou K: Gene expression variation to predict 10-year survival in lymph-node-negative breast cancer. BMC Cancer. 2008, 8: 254-10.1186/1471-2407-8-254.CrossRefPubMedPubMedCentral
8.
go back to reference Naderi A, Teschendorff AE, Barbosa-Morais NL, Pinder SE, Green AR, Powe DG, Robertson JF, Aparicio S, Ellis IO, Brenton JD, Caldas C: A gene-expression signature to predict survival in breast cancer across independent data sets. Oncogene. 2006 Naderi A, Teschendorff AE, Barbosa-Morais NL, Pinder SE, Green AR, Powe DG, Robertson JF, Aparicio S, Ellis IO, Brenton JD, Caldas C: A gene-expression signature to predict survival in breast cancer across independent data sets. Oncogene. 2006
9.
go back to reference Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, et al: A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med. 2004, 351: 2817-2826. 10.1056/NEJMoa041588.CrossRefPubMed Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, et al: A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med. 2004, 351: 2817-2826. 10.1056/NEJMoa041588.CrossRefPubMed
10.
go back to reference Mollerstrom E, Delle U, Danielsson A, Parris T, Olsson B, Karlsson P, Helou K: High-resolution genomic profiling to predict 10-year overall survival in node-negative breast cancer. Cancer Genet Cytogenet. 2010, 198: 79-89. 10.1016/j.cancergencyto.2009.12.012.CrossRefPubMed Mollerstrom E, Delle U, Danielsson A, Parris T, Olsson B, Karlsson P, Helou K: High-resolution genomic profiling to predict 10-year overall survival in node-negative breast cancer. Cancer Genet Cytogenet. 2010, 198: 79-89. 10.1016/j.cancergencyto.2009.12.012.CrossRefPubMed
11.
go back to reference Ryden L, Landberg G, Stal O, Nordenskjold B, Ferno M, Bendahl PO: HER2 status in hormone receptor positive premenopausal primary breast cancer adds prognostic, but not tamoxifen treatment predictive, information. Breast Cancer Res Treat. 2008, 109: 351-357. 10.1007/s10549-007-9660-2.CrossRefPubMed Ryden L, Landberg G, Stal O, Nordenskjold B, Ferno M, Bendahl PO: HER2 status in hormone receptor positive premenopausal primary breast cancer adds prognostic, but not tamoxifen treatment predictive, information. Breast Cancer Res Treat. 2008, 109: 351-357. 10.1007/s10549-007-9660-2.CrossRefPubMed
12.
go back to reference Gehan EA: A Generalized Wilcoxon Test for Comparing Arbitrarily Singly-Censored Samples. Biometrika. 1965, 52: 203-223.CrossRefPubMed Gehan EA: A Generalized Wilcoxon Test for Comparing Arbitrarily Singly-Censored Samples. Biometrika. 1965, 52: 203-223.CrossRefPubMed
13.
go back to reference Heymans MW, van Buuren S, Knol DL, van Mechelen W, de Vet HC: Variable selection under multiple imputation using the bootstrap in a prognostic study. BMC Med Res Methodol. 2007, 7: 33-10.1186/1471-2288-7-33.CrossRefPubMedPubMedCentral Heymans MW, van Buuren S, Knol DL, van Mechelen W, de Vet HC: Variable selection under multiple imputation using the bootstrap in a prognostic study. BMC Med Res Methodol. 2007, 7: 33-10.1186/1471-2288-7-33.CrossRefPubMedPubMedCentral
14.
go back to reference Heagerty PJ, Zheng Y: Survival model predictive accuracy and ROC curves. Biometrics. 2005, 61: 92-105. 10.1111/j.0006-341X.2005.030814.x.CrossRefPubMed Heagerty PJ, Zheng Y: Survival model predictive accuracy and ROC curves. Biometrics. 2005, 61: 92-105. 10.1111/j.0006-341X.2005.030814.x.CrossRefPubMed
15.
go back to reference Montagnoli A, Guardavaccaro D, Starace G, Tirone F: Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ. 1996, 7: 1327-1336.PubMed Montagnoli A, Guardavaccaro D, Starace G, Tirone F: Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ. 1996, 7: 1327-1336.PubMed
16.
go back to reference Varnum BC, Reddy ST, Koski RA, Herschman HR: Synthesis, degradation, and subcellular localization of proteins encoded by the primary response genes TIS7/PC4 and TIS21/PC3. J Cell Physiol. 1994, 158: 205-213. 10.1002/jcp.1041580125.CrossRefPubMed Varnum BC, Reddy ST, Koski RA, Herschman HR: Synthesis, degradation, and subcellular localization of proteins encoded by the primary response genes TIS7/PC4 and TIS21/PC3. J Cell Physiol. 1994, 158: 205-213. 10.1002/jcp.1041580125.CrossRefPubMed
17.
go back to reference Ficazzola MA, Fraiman M, Gitlin J, Woo K, Melamed J, Rubin MA, Walden PD: Antiproliferative B cell translocation gene 2 protein is down-regulated post-transcriptionally as an early event in prostate carcinogenesis. Carcinogenesis. 2001, 22: 1271-1279. 10.1093/carcin/22.8.1271.CrossRefPubMed Ficazzola MA, Fraiman M, Gitlin J, Woo K, Melamed J, Rubin MA, Walden PD: Antiproliferative B cell translocation gene 2 protein is down-regulated post-transcriptionally as an early event in prostate carcinogenesis. Carcinogenesis. 2001, 22: 1271-1279. 10.1093/carcin/22.8.1271.CrossRefPubMed
18.
go back to reference Kawakubo H, Carey JL, Brachtel E, Gupta V, Green JE, Walden PD, Maheswaran S: Expression of the NF-kappaB-responsive gene BTG2 is aberrantly regulated in breast cancer. Oncogene. 2004, 23: 8310-8319. 10.1038/sj.onc.1208008.CrossRefPubMed Kawakubo H, Carey JL, Brachtel E, Gupta V, Green JE, Walden PD, Maheswaran S: Expression of the NF-kappaB-responsive gene BTG2 is aberrantly regulated in breast cancer. Oncogene. 2004, 23: 8310-8319. 10.1038/sj.onc.1208008.CrossRefPubMed
19.
go back to reference Melamed J, Kernizan S, Walden PD: Expression of B-cell translocation gene 2 protein in normal human tissues. Tissue Cell. 2002, 34: 28-32. 10.1054/tice.2001.0220.CrossRefPubMed Melamed J, Kernizan S, Walden PD: Expression of B-cell translocation gene 2 protein in normal human tissues. Tissue Cell. 2002, 34: 28-32. 10.1054/tice.2001.0220.CrossRefPubMed
20.
go back to reference Duriez C, Moyret-Lalle C, Falette N, El-Ghissassi F, Puisieux A: BTG2, its family and its tutor. Bull Cancer. 2004, 91: E242-253.PubMed Duriez C, Moyret-Lalle C, Falette N, El-Ghissassi F, Puisieux A: BTG2, its family and its tutor. Bull Cancer. 2004, 91: E242-253.PubMed
21.
go back to reference Boiko AD, Porteous S, Razorenova OV, Krivokrysenko VI, Williams BR, Gudkov AV: A systematic search for downstream mediators of tumor suppressor function of p53 reveals a major role of BTG2 in suppression of Ras-induced transformation. Genes Dev. 2006, 20: 236-252. 10.1101/gad.1372606.CrossRefPubMedPubMedCentral Boiko AD, Porteous S, Razorenova OV, Krivokrysenko VI, Williams BR, Gudkov AV: A systematic search for downstream mediators of tumor suppressor function of p53 reveals a major role of BTG2 in suppression of Ras-induced transformation. Genes Dev. 2006, 20: 236-252. 10.1101/gad.1372606.CrossRefPubMedPubMedCentral
22.
go back to reference Lim IK, Lee MS, Lee SH, Kim NK, Jou I, Seo JS, Park SC: Differential expression of TIS21 and TIS1 genes in the various organs of Balb/c mice, thymic carcinoma tissues and human cancer cell lines. J Cancer Res Clin Oncol. 1995, 121: 279-284. 10.1007/BF01209594.CrossRefPubMed Lim IK, Lee MS, Lee SH, Kim NK, Jou I, Seo JS, Park SC: Differential expression of TIS21 and TIS1 genes in the various organs of Balb/c mice, thymic carcinoma tissues and human cancer cell lines. J Cancer Res Clin Oncol. 1995, 121: 279-284. 10.1007/BF01209594.CrossRefPubMed
23.
go back to reference Elmore LW, Di X, Dumur C, Holt SE, Gewirtz DA: Evasion of a single-step, chemotherapy-induced senescence in breast cancer cells: implications for treatment response. Clin Cancer Res. 2005, 11: 2637-2643. 10.1158/1078-0432.CCR-04-1462.CrossRefPubMed Elmore LW, Di X, Dumur C, Holt SE, Gewirtz DA: Evasion of a single-step, chemotherapy-induced senescence in breast cancer cells: implications for treatment response. Clin Cancer Res. 2005, 11: 2637-2643. 10.1158/1078-0432.CCR-04-1462.CrossRefPubMed
24.
go back to reference Cortes U, Moyret-Lalle C, Falette N, Duriez C, Ghissassi FE, Barnas C, Morel AP, Hainaut P, Magaud JP, Puisieux A: BTG gene expression in the p53-dependent and -independent cellular response to DNA damage. Mol Carcinog. 2000, 27: 57-64. 10.1002/(SICI)1098-2744(200002)27:2<57::AID-MC1>3.0.CO;2-I.CrossRefPubMed Cortes U, Moyret-Lalle C, Falette N, Duriez C, Ghissassi FE, Barnas C, Morel AP, Hainaut P, Magaud JP, Puisieux A: BTG gene expression in the p53-dependent and -independent cellular response to DNA damage. Mol Carcinog. 2000, 27: 57-64. 10.1002/(SICI)1098-2744(200002)27:2<57::AID-MC1>3.0.CO;2-I.CrossRefPubMed
25.
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
26.
go back to reference Lim IK, Lee MS, Ryu MS, Park TJ, Fujiki H, Eguchi H, Paik WK: Induction of growth inhibition of 293 cells by downregulation of the cyclin E and cyclin-dependent kinase 4 proteins due to overexpression of TIS21. Mol Carcinog. 1998, 23: 25-35. 10.1002/(SICI)1098-2744(199809)23:1<25::AID-MC4>3.0.CO;2-G.CrossRefPubMed Lim IK, Lee MS, Ryu MS, Park TJ, Fujiki H, Eguchi H, Paik WK: Induction of growth inhibition of 293 cells by downregulation of the cyclin E and cyclin-dependent kinase 4 proteins due to overexpression of TIS21. Mol Carcinog. 1998, 23: 25-35. 10.1002/(SICI)1098-2744(199809)23:1<25::AID-MC4>3.0.CO;2-G.CrossRefPubMed
27.
go back to reference Ryu MS, Lee MS, Hong JW, Hahn TR, Moon E, Lim IK: TIS21/BTG2/PC3 is expressed through PKC-delta pathway and inhibits binding of cyclin B1-Cdc2 and its activity, independent of p53 expression. Exp Cell Res. 2004, 299: 159-170. 10.1016/j.yexcr.2004.05.014.CrossRefPubMed Ryu MS, Lee MS, Hong JW, Hahn TR, Moon E, Lim IK: TIS21/BTG2/PC3 is expressed through PKC-delta pathway and inhibits binding of cyclin B1-Cdc2 and its activity, independent of p53 expression. Exp Cell Res. 2004, 299: 159-170. 10.1016/j.yexcr.2004.05.014.CrossRefPubMed
28.
go back to reference Hong JW, Ryu MS, Lim IK: Phosphorylation of serine 147 of tis21/BTG2/pc3 by p-Erk1/2 induces Pin-1 binding in cytoplasm and cell death. J Biol Chem. 2005, 280: 21256-21263. 10.1074/jbc.M500318200.CrossRefPubMed Hong JW, Ryu MS, Lim IK: Phosphorylation of serine 147 of tis21/BTG2/pc3 by p-Erk1/2 induces Pin-1 binding in cytoplasm and cell death. J Biol Chem. 2005, 280: 21256-21263. 10.1074/jbc.M500318200.CrossRefPubMed
29.
go back to reference Tirone F: The gene PC3(TIS21/BTG2), prototype member of the PC3/BTG/TOB family: regulator in control of cell growth, differentiation, and DNA repair?. J Cell Physiol. 2001, 187: 155-165. 10.1002/jcp.1062.CrossRefPubMed Tirone F: The gene PC3(TIS21/BTG2), prototype member of the PC3/BTG/TOB family: regulator in control of cell growth, differentiation, and DNA repair?. J Cell Physiol. 2001, 187: 155-165. 10.1002/jcp.1062.CrossRefPubMed
30.
go back to reference Chen JG, Yang CP, Cammer M, Horwitz SB: Gene expression and mitotic exit induced by microtubule-stabilizing drugs. Cancer Res. 2003, 63: 7891-7899.PubMed Chen JG, Yang CP, Cammer M, Horwitz SB: Gene expression and mitotic exit induced by microtubule-stabilizing drugs. Cancer Res. 2003, 63: 7891-7899.PubMed
31.
go back to reference Islaih M, Halstead BW, Kadura IA, Li B, Reid-Hubbard JL, Flick L, Altizer JL, Thom Deahl J, Monteith DK, Newton RK, Watson DE: Relationships between genomic, cell cycle, and mutagenic responses of TK6 cells exposed to DNA damaging chemicals. Mutat Res. 2005, 578: 100-116.CrossRefPubMed Islaih M, Halstead BW, Kadura IA, Li B, Reid-Hubbard JL, Flick L, Altizer JL, Thom Deahl J, Monteith DK, Newton RK, Watson DE: Relationships between genomic, cell cycle, and mutagenic responses of TK6 cells exposed to DNA damaging chemicals. Mutat Res. 2005, 578: 100-116.CrossRefPubMed
32.
go back to reference Lim YB, Park TJ, Lim IK: B cell translocation gene 2 enhances susceptibility of HeLa cells to doxorubicin-induced oxidative damage. J Biol Chem. 2008, 283: 33110-33118. 10.1074/jbc.M804255200.CrossRefPubMedPubMedCentral Lim YB, Park TJ, Lim IK: B cell translocation gene 2 enhances susceptibility of HeLa cells to doxorubicin-induced oxidative damage. J Biol Chem. 2008, 283: 33110-33118. 10.1074/jbc.M804255200.CrossRefPubMedPubMedCentral
33.
go back to reference Calzolari F, Appolloni I, Tutucci E, Caviglia S, Terrile M, Corte G, Malatesta P: Tumor progression and oncogene addiction in a PDGF-B-induced model of gliomagenesis. Neoplasia. 2008, 10: 1373-1382. following 1382CrossRefPubMedPubMedCentral Calzolari F, Appolloni I, Tutucci E, Caviglia S, Terrile M, Corte G, Malatesta P: Tumor progression and oncogene addiction in a PDGF-B-induced model of gliomagenesis. Neoplasia. 2008, 10: 1373-1382. following 1382CrossRefPubMedPubMedCentral
34.
go back to reference Kawakubo H, Brachtel E, Hayashida T, Yeo G, Kish J, Muzikansky A, Walden PD, Maheswaran S: Loss of B-cell translocation gene-2 in estrogen receptor-positive breast carcinoma is associated with tumor grade and overexpression of cyclin d1 protein. Cancer Res. 2006, 66: 7075-7082. 10.1158/0008-5472.CAN-06-0379.CrossRefPubMed Kawakubo H, Brachtel E, Hayashida T, Yeo G, Kish J, Muzikansky A, Walden PD, Maheswaran S: Loss of B-cell translocation gene-2 in estrogen receptor-positive breast carcinoma is associated with tumor grade and overexpression of cyclin d1 protein. Cancer Res. 2006, 66: 7075-7082. 10.1158/0008-5472.CAN-06-0379.CrossRefPubMed
35.
go back to reference Kaklamani VG, Sadim M, Hsi A, Offit K, Oddoux C, Ostrer H, Ahsan H, Pasche B, Mantzoros C: Variants of the adiponectin and adiponectin receptor 1 genes and breast cancer risk. Cancer Res. 2008, 68: 3178-3184. 10.1158/0008-5472.CAN-08-0533.CrossRefPubMedPubMedCentral Kaklamani VG, Sadim M, Hsi A, Offit K, Oddoux C, Ostrer H, Ahsan H, Pasche B, Mantzoros C: Variants of the adiponectin and adiponectin receptor 1 genes and breast cancer risk. Cancer Res. 2008, 68: 3178-3184. 10.1158/0008-5472.CAN-08-0533.CrossRefPubMedPubMedCentral
36.
go back to reference Mirza A, Basso A, Black S, Malkowski M, Kwee L, Pachter JA, Lachowicz JE, Wang Y, Liu S: RNA interference targeting of A1 receptor-overexpressing breast carcinoma cells leads to diminished rates of cell proliferation and induction of apoptosis. Cancer Biol Ther. 2005, 4: 1355-1360.CrossRefPubMed Mirza A, Basso A, Black S, Malkowski M, Kwee L, Pachter JA, Lachowicz JE, Wang Y, Liu S: RNA interference targeting of A1 receptor-overexpressing breast carcinoma cells leads to diminished rates of cell proliferation and induction of apoptosis. Cancer Biol Ther. 2005, 4: 1355-1360.CrossRefPubMed
37.
go back to reference Madjd Z, Durrant LG, Pinder SE, Ellis IO, Ronan J, Lewis S, Rushmere NK, Spendlove I: Do poor-prognosis breast tumours express membrane cofactor proteins (CD46)?. Cancer Immunol Immunother. 2005, 54: 149-156. 10.1007/s00262-004-0590-0.CrossRefPubMed Madjd Z, Durrant LG, Pinder SE, Ellis IO, Ronan J, Lewis S, Rushmere NK, Spendlove I: Do poor-prognosis breast tumours express membrane cofactor proteins (CD46)?. Cancer Immunol Immunother. 2005, 54: 149-156. 10.1007/s00262-004-0590-0.CrossRefPubMed
Metadata
Title
Up-regulation of cell cycle arrest protein BTG2 correlates with increased overall survival in breast cancer, as detected by immunohistochemistry using tissue microarray
Authors
Elin Möllerström
Anikó Kovács
Kristina Lövgren
Szilard Nemes
Ulla Delle
Anna Danielsson
Toshima Parris
Donal J Brennan
Karin Jirström
Per Karlsson
Khalil Helou
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2010
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-10-296

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