Decreased expression of ABAT and STC2 hallmarks ER-positive inflammatory breast cancer and endocrine therapy resistance in advanced disease

Molecular Oncology

Volumn 9, Issue 6, 2015, Pages 1218-1233

  Jansen, Maurice P H M ^a   Sas, Leen ^b,c   Sieuwerts, Anieta M ^a   Van Cauwenberghe, Caroline ^d,e   Ramirez Ardila, Diana ^a   Look, Maxime ^a   Ruigrok Ritstier, Kirsten ^a   Finetti, Pascal ^f   Bertucci, François ^f   Timmermans, Mieke M ^a   van Deurzen, Carolien H M ^a   Martens, John W M ^a   Simon, Iris ^g   Roepman, Paul ^g   Linn, Sabine C ^h   van Dam, Peter ^b   Kok, Marleen ^h   Lardon, Filip ^c   Vermeulen, Peter B ^b   Foekens, John A ^a   Dirix, Luc ^b   Berns, Els M J J ^a   Van Laere, Steven ^b,i   more..

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b Translational Cancer Research Unit   (Belgium)

^c ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f INSTITUT PAOLI CALMETTES   (France)

^g Agendia NV   (Netherlands)

^h NETHERLANDS CANCER INSTITUTE   (Netherlands)

ⁱ UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Endocrine therapy resistance; Inflammatory breast cancer; Metastatic disease

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; BIOLOGICAL MARKER; ESTROGEN RECEPTOR; HYPOCALCIN; STANNIOCALCIN 2; TAMOXIFEN; UNCLASSIFIED DRUG; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; GLYCOPROTEIN; SIGNAL PEPTIDE; STC2 PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN;

ABAT GENE; ADVANCED CANCER; ARTICLE; CANCER ADJUVANT THERAPY; CANCER HORMONE THERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RESISTANCE; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOLOGY; INFLAMMATORY BREAST CANCER; MAJOR CLINICAL STUDY; METAGENOME; METASTASIS FREE SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STC2 GENE; TISSUE MICROARRAY; TREATMENT OUTCOME; BIOSYNTHESIS; COMPARATIVE STUDY; DISEASE FREE SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; METABOLISM; MORTALITY; PATHOLOGY; SURVIVAL RATE;

4-AMINOBUTYRATE TRANSAMINASE; ANTINEOPLASTIC AGENTS, HORMONAL; BIOMARKERS, TUMOR; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; INFLAMMATORY BREAST NEOPLASMS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM PROTEINS; SURVIVAL RATE; TAMOXIFEN;

EID: 84929516763     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2015.02.006     Document Type: Article

References (45)

1. Bekhouche I., Finetti P., Adelaide J., Ferrari A., Tarpin C., Charafe-Jauffret E., Charpin C., Houvenaeghel G., Jacquemier J., Bidaut G., Birnbaum D., Viens P., Chaffanet M., Bertucci F. High-resolution comparative genomic hybridization of inflammatory breast cancer and identification of candidate genes. PLoS One 2011, 6:e16950.
2. Bertucci F., Finetti P., Rougemont J., Charafe-Jauffret E., Nasser V., Loriod B., Camerlo J., Tagett R., Tarpin C., Houvenaeghel G., Nguyen C., Maraninchi D., Jacquemier J., Houlgatte R., Birnbaum D., Viens P. Gene expression profiling for molecular characterization of inflammatory breast cancer and prediction of response to chemotherapy. Cancer Res. 2004, 64:8558-8565.
3. Bouras T., Southey M.C., Chang A.C., Reddel R.R., Willhite D., Glynne R., Henderson M.A., Armes J.E., Venter D.J. Stanniocalcin 2 is an estrogen-responsive gene coexpressed with the estrogen receptor in human breast cancer. Cancer Res. 2002, 62:1289-1295.
4. Budczies J., Brockmoller S.F., Muller B.M., Barupal D.K., Richter-Ehrenstein C., Kleine-Tebbe A., Griffin J.L., Oresic M., Dietel M., Denkert C., Fiehn O. Comparative metabolomics of estrogen receptor positive and estrogen receptor negative breast cancer: alterations in glutamine and beta-alanine metabolism. J. Proteomics 2013, 94:279-288.
5. Dawood S., Merajver S.D., Viens P., Vermeulen P.B., Swain S.M., Buchholz T.A., Dirix L.Y., Levine P.H., Lucci A., Krishnamurthy S., Robertson F.M., Woodward W.A., Yang W.T., Ueno N.T., Cristofanilli M. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann. Oncol. 2011, 22:515-523.
6. Dawood S., Ueno N.T., Valero V., Andreopoulou E., Hsu L., Lara J., Woodward W., Buchholz T.A., Hortobagyi G.N., Cristofanilli M. Incidence of and survival following brain metastases among women with inflammatory breast cancer. Ann. Oncol. 2010, 21:2348-2355.
7. Desmedt C., Piette F., Loi S., Wang Y., Lallemand F., Haibe-Kains B., Viale G., Delorenzi M., Zhang Y., d'Assignies M.S., Bergh J., Lidereau R., Ellis P., Harris A.L., Klijn J.G., Foekens J.A., Cardoso F., Piccart M.J., Buyse M., Sotiriou C., Consortium T. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res. 2007, 13:3207-3214.
8. Dirix L.Y., Van Dam P., Prove A., Vermeulen P.B. Inflammatory breast cancer: current understanding. Curr. Opin. Oncol. 2006, 18:563-571.
9. Dowsett M., Cuzick J., Wale C., Forbes J., Mallon E.A., Salter J., Quinn E., Dunbier A., Baum M., Buzdar A., Howell A., Bugarini R., Baehner F.L., Shak S. Prediction of risk of distant recurrence using the 21-gene recurrence score in node-negative and node-positive postmenopausal patients with breast cancer treated with anastrozole or tamoxifen: a TransATAC study. J. Clin. Oncol. 2010, 28:1829-1834.
10. 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, G.
11. Ellis M.J., Suman V.J., Hoog J., Lin L., Snider J., Prat A., Parker J.S., Luo J., DeSchryver K., Allred D.C., Esserman L.J., Unzeitig G.W., Margenthaler J., Babiera G.V., Marcom P.K., Guenther J.M., Watson M.A., Leitch M., Hunt K., Olson J.A. Randomized phase II neoadjuvant comparison between letrozole, anastrozole, and exemestane for postmenopausal women with estrogen receptor-rich stage 2 to 3 breast cancer: clinical and biomarker outcomes and predictive value of the baseline PAM50-based intrinsic subtype-ACOSOG Z1031. J. Clin. Oncol. 2011, 29:2342-2349.
12. Fan C., Oh D.S., Wessels L., Weigelt B., Nuyten D.S., Nobel A.B., van't Veer L.J., Perou C.M. Concordance among gene-expression-based predictors for breast cancer. N. Engl. J. Med. 2006, 355:560-569.
13. Goeman J.J., van de Geer S.A., de Kort F., van Houwelingen H.C. A global test for groups of genes: testing association with a clinical outcome. Bioinformatics 2004, 20:93-99.
14. Hance K.W., Anderson W.F., Devesa S.S., Young H.A., Levine P.H. Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute. J. Natl. Cancer Inst. 2005, 97:966-975.
15. Hayward J.L., Rubens R.D., Carbone P.P., Heuson J.C., Kumaoka S., Segaloff A. Assessment of response to therapy in advanced Breast-Cancer. Br. J. Cancer 1978, 38:201.
16. Jansen M.P., Foekens J.A., van Staveren I.L., Dirkzwager-Kiel M.M., Ritstier K., Look M.P., Meijer-van Gelder M.E., Sieuwerts A.M., Portengen H., Dorssers L.C., Klijn J.G., Berns E.M. Molecular classification of tamoxifen-resistant breast carcinomas by gene expression profiling. J. Clin. Oncol. 2005, 23:732-740.
17. Jansen M.P., Knijnenburg T., Reijm E.A., Simon I., Kerkhoven R., Droog M., Velds A., van Laere S., Dirix L., Alexi X., Foekens J.A., Wessels L., Linn S.C., Berns E.M., Zwart W. Hallmarks of aromatase inhibitor drug resistance revealed by epigenetic profiling in breast cancer. Cancer Res. 2013, 73:6632-6641.
18. Jansen M.P., Sieuwerts A.M., Look M.P., Ritstier K., Meijer-van Gelder M.E., van Staveren I.L., Klijn J.G., Foekens J.A., Berns E.M. HOXB13-to-IL17BR expression ratio is related with tumor aggressiveness and response to tamoxifen of recurrent breast cancer: a retrospective study. J. Clin. Oncol. 2007, 25:662-668.
19. Kok M., Linn S.C., Van Laar R.K., Jansen M.P., van den Berg T.M., Delahaye L.J., Glas A.M., Peterse J.L., Hauptmann M., Foekens J.A., Klijn J.G., Wessels L.F., Van't Veer L.J., Berns E.M. Comparison of gene expression profiles predicting progression in breast cancer patients treated with tamoxifen. Breast Cancer Res. Treat. 2009, 113:275-283.
20. Krijgsman O., Roepman P., Zwart W., Carroll J.S., Tian S., de Snoo F.A., Bender R.A., Bernards R., Glas A.M. A diagnostic gene profile for molecular subtyping of breast cancer associated with treatment response. Breast Cancer Res. Treat. 2012, 133:37-47.
21. Leary A.F., Drury S., Detre S., Pancholi S., Lykkesfeldt A.E., Martin L.A., Dowsett M., Johnston S.R. Lapatinib restores hormone sensitivity with differential effects on estrogen receptor signaling in cell models of human epidermal growth factor receptor 2-negative breast cancer with acquired endocrine resistance. Clin. Cancer Res. 2010, 16:1486-1497.
22. Lerebours F., Vacher S., Andrieu C., Espie M., Marty M., Lidereau R., Bieche I. NF-kappa B genes have a major role in inflammatory breast cancer. BMC Cancer 2008, 8:41.
23. Loi S., Haibe-Kains B., Desmedt C., Wirapati P., Lallemand F., Tutt A.M., Gillet C., Ellis P., Ryder K., Reid J.F., Daidone M.G., Pierotti M.A., Berns E.M., Jansen M.P., Foekens J.A., Delorenzi M., Bontempi G., Piccart M.J., Sotiriou C. Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen. BMC Genomics 2008, 9:239.
24. Ma X.J., Hilsenbeck S.G., Wang W., Ding L., Sgroi D.C., Bender R.A., Osborne C.K., Allred D.C., Erlander M.G. The HOXB13:IL17BR expression index is a prognostic factor in early-stage breast cancer. J. Clin. Oncol. 2006, 24:4611-4619.
25. Ma X.J., Wang Z., Ryan P.D., Isakoff S.J., Barmettler A., Fuller A., Muir B., Mohapatra G., Salunga R., Tuggle J.T., Tran Y., Tran D., Tassin A., Amon P., Wang W., Enright E., Stecker K., Estepa-Sabal E., Smith B., Younger J., Balis U., Michaelson J., Bhan A., Habin K., Baer T.M., Brugge J., Haber D.A., Erlander M.G., Sgroi D.C. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004, 5:607-616.
26. McShane L.M., Altman D.G., Sauerbrei W., Taube S.E., Gion M., Clark G.M. REporting recommendations for tumor MARKer prognostic studies (REMARK). Breast Cancer Res. Treat. 2006, 100:229-235. Statistics Subcommittee of, N.C.I.E.W.G.o.C.D.
27. Opolski A., Mazurkiewicz M., Wietrzyk J., Kleinrok Z., Radzikowski C. The role of GABA-ergic system in human mammary gland pathology and in growth of transplantable murine mammary cancer. J. Exp. Clin. Cancer Res. 2000, 19:383-390.
28. Paik S., Shak S., Tang G., Kim C., Baker J., Cronin M., Baehner F.L., Walker M.G., Watson D., Park T., Hiller W., Fisher E.R., Wickerham D.L., Bryant J., Wolmark N. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 2004, 351:2817-2826.
29. Paquet E.R., Hallett M.T. Absolute assignment of breast cancer intrinsic molecular subtype. J. Natl. Cancer Inst. 2015, 107:357.
30. Raulic S., Ramos-Valdes Y., DiMattia G.E. Stanniocalcin 2 expression is regulated by hormone signalling and negatively affects breast cancer cell viability in vitro. J. Endocrinol. 2008, 197:517-529.
31. Reijm E.A., Timmermans A.M., Look M.P., Meijer-van Gelder M.E., Stobbe C.K., van Deurzen C.H., Martens J.W., Sleijfer S., Foekens J.A., Berns P.M., Jansen M.P. High protein expression of EZH2 is related to unfavorable outcome to tamoxifen in metastatic breast cancer. Ann. Oncol. 2014, 25:2185-2190.
32. Schmidt M., Bohm D., von Torne C., Steiner E., Puhl A., Pilch H., Lehr H.A., Hengstler J.G., Kolbl H., Gehrmann M. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 2008, 68:5405-5413.
33. Sieuwerts A.M., Meijer-van Gelder M.E., Timmermans M., Trapman A.M., Garcia R.R., Arnold M., Goedheer A.J., Portengen H., Klijn J.G., Foekens J.A. How ADAM-9 and ADAM-11 differentially from estrogen receptor predict response to tamoxifen treatment in patients with recurrent breast cancer: a retrospective study. Clin. Cancer Res. 2005, 11:7311-7321.
34. Tibshirani R., Hastie T., Narasimhan B., Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6567-6572.
35. Torres-Arzayus M.I., Zhao J., Bronson R., Brown M. Estrogen-dependent and estrogen-independent mechanisms contribute to AIB1-mediated tumor formation. Cancer Res. 2010, 70:4102-4111.
36. Urruticoechea A., Aguilar H., Sole X., Capella G., Martin L.A., Dowsett M., Germa-Lluch J.R. Pre-clinical validation of early molecular markers of sensitivity to aromatase inhibitors in a mouse model of post-menopausal hormone-sensitive breast cancer. Breast Cancer Res. Treat. 2008, 109:463-470.
37. van Agthoven T., Sieuwerts A.M., Meijer-van Gelder M.E., Look M.P., Smid M., Veldscholte J., Sleijfer S., Foekens J.A., Dorssers L.C. Relevance of breast cancer antiestrogen resistance genes in human breast cancer progression and tamoxifen resistance. J. Clin. Oncol. 2009, 27:542-549.
38. Van der Auwera I., Yu W., Suo L., Van Neste L., van Dam P., Van Marck E.A., Pauwels P., Vermeulen P.B., Dirix L.Y., Van Laere S.J. Array-based DNA methylation profiling for breast cancer subtype discrimination. PLoS One 2010, 5:e12616.
39. Van Laere S., Beissbarth T., Van der Auwera I., Van den Eynden G., Trinh X.B., Elst H., Van Hummelen P., van Dam P., Van Marck E., Vermeulen P., Dirix L. Relapse-free survival in breast cancer patients is associated with a gene expression signature characteristic for inflammatory breast cancer. Clin. Cancer Res. 2008, 14:7452-7460.
40. Van Laere S., Limame R., Van Marck E.A., Vermeulen P.B., Dirix L.Y. Is there a role for mammary stem cells in inflammatory breast carcinoma?: a review of evidence from cell line, animal model, and human tissue sample experiments. Cancer 2010, 116:2794-2805.
41. Van Laere S., Van der Auwera I., Van den Eynden G., Van Hummelen P., van Dam P., Van Marck E., Vermeulen P.B., Dirix L. Distinct molecular phenotype of inflammatory breast cancer compared to non-inflammatory breast cancer using Affymetrix-based genome-wide gene-expression analysis. Br. J. Cancer 2007, 97:1165-1174.
42. Van Laere S., Van der Auwera I., Van den Eynden G.G., Fox S.B., Bianchi F., Harris A.L., van Dam P., Van Marck E.A., Vermeulen P.B., Dirix L.Y. Distinct molecular signature of inflammatory breast cancer by cDNA microarray analysis. Breast Cancer Res. Treat. 2005, 93:237-246.
43. Van Laere S.J., Van der Auwera I., Van den Eynden G.G., Elst H.J., Weyler J., Harris A.L., van Dam P., Van Marck E.A., Vermeulen P.B., Dirix L.Y. Nuclear factor-kappaB signature of inflammatory breast cancer by cDNA microarray validated by quantitative real-time reverse transcription-PCR, immunohistochemistry, and nuclear factor-kappaB DNA-binding. Clin. Cancer Res. 2006, 12:3249-3256.
44. Van Laere S.J., Van der Auwera I., Van den Eynden G.G., van Dam P., Van Marck E.A., Vermeulen P.B., Dirix L.Y. NF-kappaB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br. J. Cancer 2007, 97:659-669.
45. Wang Y., Klijn J.G., Zhang Y., Sieuwerts A.M., Look M.P., Yang F., Talantov D., Timmermans M., Meijer-van Gelder M.E., Yu J., Jatkoe T., Berns E.M., Atkins D., Foekens J.A. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005, 365:671-679.