Endometrial Carcinoma Recurrence Score (ECARS) validates to identify aggressive disease and associates with markers of epithelial–mesenchymal transition and PI3K alterations

Gynecologic Oncology

Volumn 134, Issue 3, 2014, Pages 599-606

  Wik, E ^a,b   Trovik, J ^a,c   Kusonmano, K ^a,c   Birkeland, E ^a,b   Raeder, M B ^a,c   Pashtan, I ^d   Hoivik, E A ^a,c   Krakstad, C ^a,c   Werner, H M J ^a,c   Holst, F ^a,c   Mjos S ^a,c   Halle, M K ^a,c   Mannelqvist, M ^a,b   Mauland, K K ^a,c   Oyan, A M ^c   Stefansson, I M ^a,b   Petersen, K ^a   Simon, R ^e   Cherniack, A D ^f   Meyerson, M ^d,f,g   Kalland, K H ^a,c   Akslen, L A ^a,b   Salvesen, H B ^a,c   more..

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

ECARS; Endometrial Carcinoma Recurrence Score; Epithelial mesenchymal transition; PI3K; Prognosis

Indexed keywords

ALPHA CATENIN; CATENIN; ESTROGEN RECEPTOR ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P120; UVOMORULIN; TUMOR MARKER;

ARTICLE; ASSESSMENT OF HUMANS; CANCER GRADING; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; DNA SEQUENCE; ENDOMETRIAL CARCINOMA RECURRENCE SCORE; ENDOMETRIUM CARCINOMA; EPITHELIAL MESENCHYMAL TRANSITION; EXON; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FOLLOW UP; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LOW RISK PATIENT; MAJOR CLINICAL STUDY; PHENOTYPE; PRIORITY JOURNAL; PROSPECTIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; RECURRENCE FREE SURVIVAL; SANGER SEQUENCING; UPREGULATION; ECARS; ENDOMETRIUM TUMOR; GENETICS; PATHOLOGY; PI3K; PROGNOSIS; TUMOR RECURRENCE;

ECARS; ENDOMETRIAL CARCINOMA RECURRENCE SCORE; EPITHELIAL-MESENCHYMAL TRANSITION; PI3K; PROGNOSIS;

ENDOMETRIAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; NEOPLASM RECURRENCE, LOCAL; PHOSPHATIDYLINOSITOL 3-KINASES; TUMOR MARKERS, BIOLOGICAL;

EID: 84908330736     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2014.06.026     Document Type: Article

References (40)

1. Salvesen, H.B., Haldorsen, I.S., Trovik, J., Markers for individualised therapy in endometrial carcinoma. Lancet Oncol 13:8 (Aug 2012), e353–e361.
2. Salvesen, H.B., Carter, S.L., Mannelqvist, M., Dutt, A., Getz, G., Stefansson, I.M., et al. Integrated genomic profiling of endometrial carcinoma associates aggressive tumors with indicators of PI3 kinase activation. Proc Natl Acad Sci U S A 106:12 (Mar 24 2009), 4834–4839.
3. Perou, C.M., Sorlie, T., Eisen, M.B., van de Rijn, M., Jeffrey, S.S., Rees, C.A., et al. Molecular portraits of human breast tumours. Nature 406:6797 (Aug 17 2000), 747–752.
4. Sotiriou, C., Neo, S.Y., McShane, L.M., Korn, E.L., Long, P.M., Jazaeri, A., et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A 100:18 (Sep 2 2003), 10393–10398.
5. Li, W., Wang, R., Yan, Z., Bai, L., Sun, Z., High accordance in prognosis prediction of colorectal cancer across independent datasets by multi-gene module expression profiles. PLoS One, 7(3), 2012, e33653.
6. van ‘t Veer, L.J., Dai, H., van de Vijver, M.J., He, Y.D., Hart, A.A., Mao, M., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:6871 (Jan 31 2002), 530–536.
7. Minn, A.J., Gupta, G.P., Padua, D., Bos, P., Nguyen, D.X., Nuyten, D., et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci U S A 104:16 (Apr 17 2007), 6740–6745.
8. Minn, A.J., Kang, Y., Serganova, I., Gupta, G.P., Giri, D.D., Doubrovin, M., et al. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest 115:1 (Jan 2005), 44–55.
9. Chang, J.C., Wooten, E.C., Tsimelzon, A., Hilsenbeck, S.G., Gutierrez, M.C., Elledge, R., et al. Gene expression profiling for the prediction of therapeutic response to docetaxel in patients with breast cancer. Lancet 362:9381 (Aug 2 2003), 362–369.
10. Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351:27 (Dec 30 2004), 2817–2826.
11. Majewski, I.J., Bernards, R., Taming the dragon: genomic biomarkers to individualize the treatment of cancer. Nat Med 17:3 (Mar 2011), 304–312.
12. Cancer Genome Atlas Research N, Kandoth, C., Schultz, N., Cherniack, A.D., Akbani, R., Liu, Y., et al. Integrated genomic characterization of endometrial carcinoma. Nature 497:7447 (May 2 2013), 67–73.
13. Halle, M.K., Werner, H.M., Krakstad, C., Birkeland, E., Wik, E., Trovik, J., et al. Stratification based on high tumour cell content in fresh frozen tissue promotes selection of aggressive endometrial carcinomas. Histopathology 60:3 (Feb 2011), 516–519.
14. Engelsen, I.B., Mannelqvist, M., Stefansson, I.M., Carter, S.L., Beroukhim, R., Oyan, A.M., et al. Low BMI-1 expression is associated with an activated BMI-1-driven signature, vascular invasion, and hormone receptor loss in endometrial carcinoma. Br J Cancer 98:10 (May 20 2008), 1662–1669.
15. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(− Delta Delta C(T)) Method. Methods 25:4 (Dec 2001), 402–408.
16. Wik, E., Raeder, M.B., Krakstad, C., Trovik, J., Birkeland, E., Hoivik, E.A., et al. Lack of estrogen receptor-alpha is associated with epithelial–mesenchymal transition and PI3K alterations in endometrial carcinoma. Clin Cancer Res 19:5 (Mar 1 2013), 1094–1105.
17. Gustafson, A.M., Soldi, R., Anderlind, C., Scholand, M.B., Qian, J., Zhang, X., et al. Airway PI3K pathway activation is an early and reversible event in lung cancer development. Sci Transl Med, 2(26), Apr 7 2010 (26ra5).
18. Mannelqvist, M., Stefansson, I.M., Bredholt, G., Hellem Bo, T., Oyan, A.M., Jonassen, I., et al. Gene expression patterns related to vascular invasion and aggressive features in endometrial cancer. Am J Pathol 178:2 (2011 Feb), 861–871.
19. Jechlinger, M., Grunert, S., Tamir, I.H., Janda, E., Ludemann, S., Waerner, T., et al. Expression profiling of epithelial plasticity in tumor progression. Oncogene 22:46 (2003 Oct 16), 7155–7169.
20. Huang, E., Ishida, S., Pittman, J., Dressman, H., Bild, A., Kloos, M., et al. Gene expression phenotypic models that predict the activity of oncogenic pathways. Nat Genet 34:2 (2003 Jun), 226–230.
21. Wik, E., Ræder, M.B., Krakstad, C., Trovik, J., Birkeland, E., Hoivik, E.A., et al. Lack of estrogen receptor-α is associated with epithelial-mesenchymal transition and PI3K alterations in endometrial carcinoma. Clin Cancer Res 19:5 (2013 Mar 1), 1094–1105.
22. Krakstad, C., Trovik, J., Wik, E., Engelsen, I.B., Werner, H.M., Birkeland, E., et al. Loss of GPER identifies new targets for therapy among a subgroup of ERalpha-positive endometrial cancer patients with poor outcome. Br J Cancer 106:10 (2012 May 8), 1682–1688.
23. Trovik, J., Wik, E., Stefansson, I.M., Marcickiewicz, J., Tingulstad, S., Staff, A.C., et al. Stathmin overexpression identifies high-risk patients and lymph node metastasis in endometrial cancer. Clin Cancer Res 17:10 (2011 May 15), 3368–3377.
24. Stefansson, I.M., Salvesen, H.B., Immervoll, H., Akslen, L.A., Prognostic impact of histological grade and vascular invasion compared with tumour cell proliferation in endometrial carcinoma of endometrioid type. Histopathology 44:5 (May 2004), 472–479.
25. Birkeland, E., Wik, E., Mjos, S., Hoivik, E.A., Trovik, J., Werner, H.M., et al. KRAS gene amplification and overexpression but not mutation associates with aggressive and metastatic endometrial cancer. Br J Cancer 107:12 (Dec 4 2012), 1997–2004.
26. Wik, E., Birkeland, E., Trovik, J., Werner, H.M., Hoivik, E.A., Mjos, S., et al. High Phospho-Stathmin(Serine38) expression identifies aggressive endometrial cancer and suggests an association with PI3Kinase inhibition. Clin Cancer Res 19:9 (2013 May 1), 2331–2341.
27. (TCGA) TCGA, Integrated genomic characterization of endometrial carcinoma. Nature 497:7447 (2013 May 2), 67–73.
28. Saal, L.H., Johansson, P., Holm, K., Gruvberger-Saal, S.K., She, Q.B., Maurer, M., et al. Poor prognosis in carcinoma is associated with a gene expression signature of aberrant PTEN tumor suppressor pathway activity. Proc Natl Acad Sci U S A 104:18 (May 1 2007), 7564–7569.
29. Network, C.G.A., Comprehensive molecular portraits of human breast tumours. Nature 490:7418 (Oct 4 2012), 61–70.
30. Dedes, K.J., Wetterskog, D., Ashworth, A., Kaye, S.B., Reis-Filho, J.S., Emerging therapeutic targets in endometrial cancer. Nat Rev Clin Oncol 8:5 (2011 May), 261–271.
31. McShane, L.M., Altman, D.G., Sauerbrei, W., Taube, S.E., Gion, M., Clark, G.M., Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 97:16 (Aug 17 2005), 1180–1184.
32. Taube, S.E., Clark, G.M., Dancey, J.E., McShane, L.M., Sigman, C.C., Gutman, S.I., A perspective on challenges and issues in biomarker development and drug and biomarker codevelopment. J Natl Cancer Inst 101:21 (2009 Nov 4), 1453–1463.
33. Noel, A., Gutierrez-Fernandez, A., Sounni, N.E., Behrendt, N., Maquoi, E., Lund, I.K., et al. New and paradoxical roles of matrix metalloproteinases in the tumor microenvironment. Front Pharmacol, 3, 2012, 140.
34. Brooks, S.P., Coccia, M., Tang, H.R., Kanuga, N., Machesky, L.M., Bailly, M., et al. The Nance-Horan syndrome protein encodes a functional WAVE homology domain (WHD) and is important for co-ordinating actin remodelling and maintaining cell morphology. Hum Mol Genet 19:12 (2010 Jun 15), 2421–2432.
35. Ciro, M., Prosperini, E., Quarto, M., Grazini, U., Walfridsson, J., McBlane, F., et al. ATAD2 is a novel cofactor for MYC, overexpressed and amplified in aggressive tumors. Cancer Res 69:21 (2009 Nov 1), 8491–8498.
36. Fouret, R., Laffaire, J., Hofman, P., Beau-Faller, M., Mazieres, J., Validire, P., et al. A comparative and integrative approach identifies ATPase family, AAA domain containing 2 as a likely driver of cell proliferation in lung adenocarcinoma. Clin Cancer Res 18:20 (2012 Oct 15), 5606–5616.
37. Kalashnikova, E.V., Revenko, A.S., Gemo, A.T., Andrews, N.P., Tepper, C.G., Zou, J.X., et al. ANCCA/ATAD2 overexpression identifies breast cancer patients with poor prognosis, acting to drive proliferation and survival of triple-negative cells through control of B-Myb and EZH2. Cancer Res 70:22 (2010 Nov 15), 9402–9412.
38. Courtney, K.D., Corcoran, R.B., Engelman, J.A., The PI3K pathway as drug target in human cancer. J Clin Oncol 28:6 (2010 Feb 20), 1075–1083.
39. Iwatsuki, M., Mimori, K., Yokobori, T., Ishi, H., Beppu, T., Nakamori, S., et al. Epithelial–mesenchymal transition in cancer development and its clinical significance. Cancer Sci 101:2 (2010 Feb), 293–299.
40. Krasnapolski, M.A., Todaro, L.B., de Kier Joffe, E.B., Is the epithelial-to-mesenchymal transition clinically relevant for the cancer patient?. Curr Pharm Biotechnol 12:11 (2011 Nov), 1891–1899.