PIK3CA mutations, phosphatase and tensin homolog, human epidermal growth factor receptor 2, and insulin-like growth factor 1 receptor and adjuvant tamoxifen resistance in postmenopausal breast cancer patients

Breast Cancer Research

Volumn 16, Issue 1, 2014, Pages

  Beelen, Karin ^a   Opdam, Mark ^a   Severson, Tesa M ^a   Koornstra, Rutger H T ^a   Vincent, Andrew D ^a   Wesseling, Jelle ^a   Muris, Jettie J ^a   Berns, Els M J J ^b   Vermorken, Jan B ^c   van Diest, Paul J ^d   Linn, Sabine C ^a,d  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PIK3CA PROTEIN; PROTEIN; PROTEIN KINASE B; S6 KINASE; SOMATOMEDIN C RECEPTOR; TAMOXIFEN; UNCLASSIFIED DRUG; ERBB2 PROTEIN, HUMAN; ESTROGEN RECEPTOR; MTOR PROTEIN, HUMAN; PIK3CA PROTEIN, HUMAN; PTEN PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TUMOR MARKER;

AGED; ARTICLE; BREAST CANCER; CANCER HORMONE THERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RESISTANCE; CONTROLLED STUDY; DISEASE FREE INTERVAL; EXON; FEMALE; GENE AMPLIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENOTYPE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; MUTATION RATE; POSTMENOPAUSE; PREDICTIVE VALUE; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); SIGNAL TRANSDUCTION; VALIDITY; WILD TYPE; ADJUVANT CHEMOTHERAPY; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BREAST NEOPLASMS; DISEASE FREE SURVIVAL; DNA SEQUENCE; DRUG RESISTANCE; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; RANDOMIZED CONTROLLED TRIAL; RETROSPECTIVE STUDY; TRANSLATIONAL RESEARCH;

AGED; BASE SEQUENCE; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; POSTMENOPAUSE; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTOR, ERBB-2; RECEPTOR, IGF TYPE 1; RECEPTORS, ESTROGEN; RETROSPECTIVE STUDIES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SEQUENCE ANALYSIS, DNA; TAMOXIFEN; TOR SERINE-THREONINE KINASES; TRANSLATIONAL MEDICAL RESEARCH; TUMOR MARKERS, BIOLOGICAL;

EID: 84896820866     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3606     Document Type: Article

References (51)

1. Bachelot T, Bourgier C, Cropet C, Ray-Coquard I, Ferrero JM, Freyer G, Badie-Lacourtoisie S, Eymard JC, Debled M, Spaeth D, Legouffe E, Allouache D, El KC, Pujade-Lauraine E. Randomized phase II trial of everolimus in combination with tamoxifen in patients with hormone receptor-positive, human epidermal growth factor receptor 2-negative metastatic breast cancer with prior exposure to aromatase inhibitors: a GINECO study. J Clin Oncol 2012, 30:2718-2724. 10.1200/JCO.2011.39.0708, 22565002.
2. Baselga J, Campone M, Piccart M, Burris HA, Rugo HS, Sahmoud T, Noguchi S, Gnant M, Pritchard KI, Lebrun F, Beck JT, Ito Y, Yardley D, Deleu I, Perez A, Bachelot T, Vittori L, Xu Z, Mukhopadhyay P, Lebwohl D, Hortobagyi GN. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med 2011, 366:520-529.
3. Isakoff SJ, Engelman JA, Irie HY, Luo J, Brachmann SM, Pearline RV, Cantley LC, Brugge JS. Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res 2005, 65:10992-11000. 10.1158/0008-5472.CAN-05-2612, 16322248.
4. Parsons R, Simpson L. PTEN and cancer. Methods Mol Biol 2003, 222:147-166.
5. Knowlden JM, Hutcheson IR, Barrow D, Gee JM, Nicholson RI. Insulin-like growth factor-I receptor signaling in tamoxifen-resistant breast cancer: a supporting role to the epidermal growth factor receptor. Endocrinology 2005, 146:4609-4618. 10.1210/en.2005-0247, 16037379.
6. Buttitta F, Felicioni L, Barassi F, Martella C, Paolizzi D, Fresu G, Salvatore S, Cuccurullo F, Mezzetti A, Campani D, Marchetti A. PIK3CA mutation and histological type in breast carcinoma: high frequency of mutations in lobular carcinoma. J Pathol 2006, 208:350-355. 10.1002/path.1908, 16353168.
7. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 2001, 276:9817-9824. 10.1074/jbc.M010840200, 11139588.
8. Barbareschi M, Buttitta F, Felicioni L, Cotrupi S, Barassi F, Del Grammastro M, Ferro A, Dalla Palma P, Galligioni E, Marchetti A. Different prognostic roles of mutations in the helical and kinase domains of the PIK3CA gene in breast carcinomas. Clin Cancer Res 2007, 13:6064-6069. 10.1158/1078-0432.CCR-07-0266, 17947469.
9. Li Q, Eklund AC, Juul N, Haibe-Kains B, Workman CT, Richardson AL, Szallasi Z, Swanton C. Minimising immunohistochemical false negative ER classification using a complementary 23 gene expression signature of ER status. PLoS One 2010, 5:e15031. 10.1371/journal.pone.0015031, 2995741, 21152022.
10. Maruyama N, Miyoshi Y, Taguchi T, Tamaki Y, Monden M, Noguchi S. Clinicopathologic analysis of breast cancers with PIK3CA mutations in Japanese women. Clin Cancer Res 2007, 13:408-414. 10.1158/1078-0432.CCR-06-0267, 17202311.
11. Saal LH, Holm K, Maurer M, Memeo L, Su T, Wang X, Yu JS, Malmstrom PO, Mansukhani M, Enoksson J, Hibshoosh H, Borg A, Parsons R. PIK3CA mutations correlate with hormone receptors, node metastasis, and ERBB2, and are mutually exclusive with PTEN loss in human breast carcinoma. Cancer Res 2005, 65:2554-2559. 10.1158/0008-5472-CAN-04-3913, 15805248.
12. Stemke-Hale K, Gonzalez-Angulo AM, Lluch A, Neve RM, Kuo WL, Davies M, Carey M, Hu Z, Guan Y, Sahin A, Symmans WF, Pusztai L, Nolden LK, Horlings H, Berns K, Hung MC, van de Vijver MJ, Valero V, Gray JW, Bernards R, Mills GB, Hennessy BT. An integrative genomic and proteomic analysis of PIK3CA, PTEN, and AKT mutations in breast cancer. Cancer Res 2008, 68:6084-6091. 10.1158/0008-5472.CAN-07-6854, 2680495, 18676830.
13. Beelen K, Zwart W, Linn SC. Can predictive biomarkers in breast cancer guide adjuvant endocrine therapy?. Nat Rev Clin Oncol 2012, 9:529-541. 10.1038/nrclinonc.2012.121, 22825374.
14. Perez-Tenorio G, Alkhori L, Olsson B, Waltersson MA, Nordenskjold B, Rutqvist LE, Skoog L, Stal O. PIK3CA mutations and PTEN loss correlate with similar prognostic factors and are not mutually exclusive in breast cancer. Clin Cancer Res 2007, 13:3577-3584. 10.1158/1078-0432.CCR-06-1609, 17575221.
15. Dowsett M, Smith IE, Ebbs SR, Dixon JM, Skene A, A'Hern R, Salter J, Detre S, Hills M, Walsh G. Prognostic value of Ki67 expression after short-term presurgical endocrine therapy for primary breast cancer. J Natl Cancer Inst 2007, 99:167-170. 10.1093/jnci/djk020, 17228000.
16. Kalinsky K, Jacks LM, Heguy A, Patil S, Drobnjak M, Bhanot UK, Hedvat CV, Traina TA, Solit D, Gerald W, Moynahan ME. PIK3CA mutation associates with improved outcome in breast cancer. Clin Cancer Res 2009, 15:5049-5059. 10.1158/1078-0432.CCR-09-0632, 19671852.
17. Ellis MJ, Lin L, Crowder R, Tao Y, Hoog J, Snider J, Davies S, DeSchryver K, Evans DB, Steinseifer J, Bandaru R, Liu W, Gardner H, Semiglazov V, Watson M, Hunt K, Olson J, Baselga J. Phosphatidyl-inositol-3-kinase alpha catalytic subunit mutation and response to neoadjuvant endocrine therapy for estrogen receptor positive breast cancer. Breast Cancer Res Treat 2010, 119:379-390. 10.1007/s10549-009-0575-y, 2810126, 19844788.
18. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002, 2:489-501. 10.1038/nrc839, 12094235.
19. Dowsett M, Houghton J, Iden C, Salter J, Farndon J, A'Hern R, Sainsbury R, Baum M. Benefit from adjuvant tamoxifen therapy in primary breast cancer patients according to oestrogen receptor, progesterone receptor, EGF receptor and HER2 status. Ann Oncol 2006, 17:818-826. 10.1093/annonc/mdl016, 16497822.
20. Michalides R, van Tinteren H, Balkenende A, Vermorken JB, Benraadt J, Huldij J, van Diest P. Cyclin A is a prognostic indicator in early stage breast cancer with and without tamoxifen treatment. Br J Cancer 2002, 86:402-408. 10.1038/sj.bjc.6600072, 2375223, 11875707.
21. Vermorken JB, Burgers JMV, Taat CW, van de Slee PHT, Hennipman A, Norman JWR, Rozendaal KJ, van Tinteren H, Huldij J, Benraadt J. Adjuvant tamoxifen in breast cancer: interim results of a comprehensive cancer center Amsterdam trial. Breast Cancer Res Treat 1998, 50. abstracts poster session III, p.283 (no. 329).
22. Early Breast Cancer Trialists' Collaborative Group (EBCTCG) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005, 365:1687-1717. Early Breast Cancer Trialists' Collaborative Group (EBCTCG).
23. Iwamoto T, Booser D, Valero V, Murray JL, Koenig K, Esteva FJ, Ueno NT, Zhang J, Shi W, Qi Y, Matsuoka J, Yang EJ, Hortobagyi GN, Hatzis C, Symmans WF, Pusztai L. Estrogen receptor (ER) mRNA and ER-related gene expression in breast cancers that are 1% to 10% ER-positive by immunohistochemistry. J Clin Oncol 2012, 30:729-734. 10.1200/JCO.2011.36.2574, 22291085.
24. CCMO website Central Committee on Research involving Human Subjects (Centrale Commissie Mensgebonden Onderzoek) (text in Dutch) Available: http://www.ccmo.nl/nl/niet-wmo-onderzoek, CCMO website.
25. FMWV website Dutch federation of Biomedical Scientific Societies (Federatie van medisch wetenschappelijke verenigingen) (text in Dutch) Available: http://www.federa.org/code-goed-gebruik-van-lichaamsmateriaal-2011, FMWV website.
26. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991, 19:403-410. 10.1111/j.1365-2559.1991.tb00229.x, 1757079.
27. http://www.nki.nl/divisions/molecular-pathology/linn-s-group/.
28. Kok M, Linn SC, Van Laar RK, Jansen MP, van den Berg TM, Delahaye LJ, Glas AM, Peterse JL, Hauptmann M, Foekens JA, Klijn JG, Wessels LF, Van't Veer LJ, Berns EM. Comparison of gene expression profiles predicting progression in breast cancer patients treated with tamoxifen. Breast Cancer Res Treat 2009, 113:275-283. 10.1007/s10549-008-9939-y, 18311582.
29. Beelen K, Opdam M, Severson T, Koornstra RHT, Vincent AD, Wesseling J, Murris J, Berns EMJJ, Vermorken JB, van Diest PJ, Linn SC. Phosphorylated p-70S6K predicts tamoxifen resistance in postmenopausal breast cancer patients randomized between adjuvant tamoxifen versus no systemic treatment. Breast Cancer Res 2014, 16:R6. 10.1186/bcr3598, 24447434.
30. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 2005, 97:1180-1184. 10.1093/jnci/dji237, 16106022.
31. Cizkova M, Susini A, Vacher S, Cizeron-Clairac G, Andrieu C, Driouch K, Fourme E, Lidereau R, Bieche I. PIK3CA mutation impact on survival in breast cancer patients and in ERalpha, PR and ERBB2-based subgroups. Breast Cancer Res 2012, 14:R28. 10.1186/bcr3113, 3496146, 22330809.
32. Campbell IG, Russell SE, Choong DY, Montgomery KG, Ciavarella ML, Hooi CS, Cristiano BE, Pearson RB, Phillips WA. Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res 2004, 64:7678-7681. 10.1158/0008-5472.CAN-04-2933, 15520168.
33. Sabine VS, Crozier C, Drake C, Piper T, van de Velde CJH, Hasenburg A, Kieback DG, Markopoulos C, Dirix L, Seynaeve C, Rea D, Bartlett JMS. PIK3CA mutations are linked to PgR expression: a Tamoxifen Exemestane Adjuvant Multinational (TEAM) pathology study. Cancer Res 2012, 72:72. S1-5.
34. Loi S, Haibe-Kains B, Majjaj S, Lallemand F, Durbecq V, Larsimont D, Gonzalez-Angulo AM, Pusztai L, Symmans WF, Bardelli A, Ellis P, Tutt AN, Gillett CE, Hennessy BT, Mills GB, Phillips WA, Piccart MJ, Speed TP, McArthur GA, Sotiriou C. PIK3CA mutations associated with gene signature of low mTORC1 signaling and better outcomes in estrogen receptor-positive breast cancer. Proc Natl Acad Sci U S A 2010, 107:10208-10213. 10.1073/pnas.0907011107, 2890442, 20479250.
35. The Cancer Genome Atlas Network Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. 10.1038/nature11412, 3465532, 23000897, The Cancer Genome Atlas Network.
36. Vasudevan KM, Barbie DA, Davies MA, Rabinovsky R, McNear CJ, Kim JJ, Hennessy BT, Tseng H, Pochanard P, Kim SY, Dunn IF, Schinzel AC, Sandy P, Hoersch S, Sheng Q, Gupta PB, Boehm JS, Reiling JH, Silver S, Lu Y, Stemke-Hale K, Dutta B, Joy C, Sahin AA, Gonzalez-Angulo AM, Lluch A, Rameh LE, Jacks T, Root DE, Lander ES, et al. AKT-independent signaling downstream of oncogenic PIK3CA mutations in human cancer. Cancer Cell 2009, 16:21-32. 10.1016/j.ccr.2009.04.012, 2752826, 19573809.
37. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J, Rosen N. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006, 66:1500-1508. 10.1158/0008-5472.CAN-05-2925, 3193604, 16452206.
38. Zhang Y, Moerkens M, Ramaiahgari S, de Bont H, Price L, Meerman J, van de Water B. Elevated insulin-like growth factor 1 receptor signaling induces anti-estrogen resistance through the MAPK/ERK and PI3K/Akt signaling routes. Breast Cancer Res 2011, 13:R52. 10.1186/bcr2883, 3218939, 21595894.
39. Sangale Z, Prass C, Carlson A, Tikishvili E, Degrado J, Lanchbury J, Stone S. A robust immunohistochemical assay for detecting PTEN expression in human tumors. Appl Immunohistochem Mol Morphol 2011, 19:173-183. 10.1097/PAI.0b013e3181f1da13, 20930614.
40. Dekker TJ, Borg ST, Hooijer GK, Meijer SL, Wesseling J, Boers JE, Schuuring E, Bart J, van Gorp J, Mesker WE, Kroep JR, Smit VT, van de Vijver MJ. Determining sensitivity and specificity of HER2 testing in breast cancer using a tissue micro-array approach. Breast Cancer Res 2012, 14:R93. 10.1186/bcr3208, 3446356, 22694844.
41. Gee JM, Robertson JF, Gutteridge E, Ellis IO, Pinder SE, Rubini M, Nicholson RI. Epidermal growth factor receptor/HER2/insulin-like growth factor receptor signalling and oestrogen receptor activity in clinical breast cancer. Endocr Relat Cancer 2005, 12:S99-S111. 10.1677/erc.1.01005, 16113104.
42. Hartog H, Horlings HM, van der Vegt B, Kreike B, Ajouaou A, van de Vijver MJ, Marike Boezen H, de Bock GH, van der Graaf WT, Wesseling J. Divergent effects of insulin-like growth factor-1 receptor expression on prognosis of estrogen receptor positive versus triple negative invasive ductal breast carcinoma. Breast Cancer Res Treat 2010, 129:725-736.
43. Henriksen KL, Rasmussen BB, Lykkesfeldt AE, Moller S, Ejlertsen B, Mouridsen HT. An ER activity profile including ER, PR, Bcl-2 and IGF-IR may have potential as selection criterion for letrozole or tamoxifen treatment of patients with advanced breast cancer. Acta Oncol 2009, 48:522-531. 10.1080/02841860802676383, 19173092.
44. Law JH, Habibi G, Hu K, Masoudi H, Wang MY, Stratford AL, Park E, Gee JM, Finlay P, Jones HE, Nicholson RI, Carboni J, Gottardis M, Pollak M, Dunn SE. Phosphorylated insulin-like growth factor-i/insulin receptor is present in all breast cancer subtypes and is related to poor survival. Cancer Res 2008, 68:10238-10246. 10.1158/0008-5472.CAN-08-2755, 19074892.
45. Peiro G, Benlloch S, Sanchez-Tejada L, Adrover E, Lerma E, Peiro FM, Sanchez-Paya J, Aranda FI. Low activation of Insulin-like Growth Factor 1-Receptor (IGF1R) is associated with local recurrence in early breast carcinoma. Breast Cancer Res Treat 2009, 117:433-441. 10.1007/s10549-008-0139-6, 18683043.
46. Dumont AG, Dumont SN, Trent JC. The favorable impact of PIK3CA mutations on survival: an analysis of 2587 patients with breast cancer. Chin J Cancer 2012, 31:327-334. 10.5732/cjc.012.10032, 3777497, 22640628.
47. Fisher B, Costantino J, Redmond C, Poisson R, Bowman D, Couture J, Dimitrov NV, Wolmark N, Wickerham DL, Fisher ER. A randomized clinical trial evaluating tamoxifen in the treatment of patients with node-negative breast cancer who have estrogen-receptor-positive tumors. N Engl J Med 1989, 320:479-484. 10.1056/NEJM198902233200802, 2644532.
48. CRC Adjuvant Breast Trial Working Party Cyclophosphamide and tamoxifen as adjuvant therapies in the management of breast cancer. Br J Cancer 1988, 57:604-607. 2246453, 2900646, CRC Adjuvant Breast Trial Working Party.
49. " Nolvadex" Adjuvant Trial Organisation: Controlled trial of tamoxifen as a single adjuvant agent in the management of early breast cancer. Br J Cancer 1988, 57:608-611. 2246455, 2900647.
50. Rutqvist LE, Johansson H. Long-term follow-up of the randomized Stockholm trial on adjuvant tamoxifen among postmenopausal patients with early stage breast cancer. Acta Oncol 2007, 46:133-145. 10.1080/02841860601034834, 17453361.
51. Janku F, Wheler JJ, Westin SN, Moulder SL, Naing A, Tsimberidou AM, Fu S, Falchook GS, Hong DS, Garrido-Laguna I, Luthra R, Lee JJ, Lu KH, Kurzrock R. PI3K/AKT/mTOR inhibitors in patients with breast and gynecologic malignancies harboring PIK3CA mutations. J Clin Oncol 2012, 30:777-782. 10.1200/JCO.2011.36.1196, 3295566, 22271473.