Evidence for a time-dependent association between FOLR1 expression and survival from ovarian carcinoma: implications for clinical testing. An Ovarian Tumour Tissue Analysis consortium study
FULL PAPER
British Journal of Cancer (2014) 111, 2297–2307 | doi: 10.1038/bjc.2014.567
Keywords: ovarian cancer; folate receptor alpha; FRA; immunohistochemistry; prognosis; TCGA
Evidence for a time-dependent association
between FOLR1 expression and survival from
ovarian carcinoma: implications for clinical
testing. An Ovarian Tumour Tissue Analysis
consortium study
M Köbel1, J Madore2,3, S J Ramus4, B A Clarke5, P D P Pharoah6,7, S Deen8, D D Bowtell9,10,11, K Odunsi12,
U Menon13, C Morrison14, S Lele12,15, W Bshara14, L Sucheston15, M W Beckmann16, A Hein16, F C Thiel16,
A Hartmann17, D L Wachter17, M S Anglesio2, E Høgdall18,19, A Jensen18, C Høgdall20, K R Kalli21, B L Fridley22,
G L Keeney23, Z C Fogarty24, R A Vierkant24, S Liu25, S Cho1, G Nelson26, P Ghatage26, A Gentry-Maharaj13,
S A Gayther4, E Benjamin27, M Widschwendter28, M P Intermaggio4, B Rosen29, M Q Bernardini29, H Mackay30,
A Oza29, P Shaw29, M Jimenez-Linan31,32, K E Driver7, J Alsop7, M Mack7, J M Koziak33, H Steed34,
C Ewanowich35, A DeFazio36, G Chenevix-Trench37, S Fereday9, B Gao36, S E Johnatty37, J George9,
L Galletta9, AOCS Study Group9, E L Goode38, S K Kjær18,20, D G Huntsman2,39, P A Fasching16,40,
K B Moysich15, J D Brenton32,41,42,43 and L E Kelemen*,44
1
Department of Pathology and Laboratory Medicine, University of Calgary, Foothills Medical Center, 1403 29 ST NW,
Calgary, AB T2N 2T9, Canada; 2Department of Pathology and Laboratory Medicine, University of British Columbia,
BC Cancer Agency, 600 West 10th Avenue, Vancouver, BC V5E 4E6, Canada; 3Melanoma Institute Australia, University of
Sydney, Royal Prince Alfred Hospital, Gloucester House–level 3, Missenden Road, Camperdown, NSW 2050, Australia;
4
Department of Preventive Medicine, Keck School of Medicine, USC/Norris Comprehensive Cancer Center, University of Southern
California, Harlyne Norris Research Tower, 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA; 5Department of
Laboratory Medicine and Pathobiology, Princess Margaret Cancer Centre, University of Toronto, 610 Univeristy Avenue,
M-700, Toronto, ON M5T 2M9, Canada; 6Department of Public Health and Primary Care, University of Cambridge, Strangeways
Research Laboratory, Worts Causeway, Cambridge CB1 8RN, UK; 7Department of Oncology, University of Cambridge,
Strangeways Research Laboratory, Worts Causeway, Cambridge CB1 8RN, UK; 8Department of Histopathology, Queen’s Medical
Centre, Nottingham University Hospitals NHS Trust, Nottingham NG7 2UH, UK; 9Department of Cancer Genomics and
Genetics, Peter MacCallum Cancer Centre, Locked Bag I, A’Beckett Street, East Melbourne, VIC 8006, Australia; 10Department
of Biochemistry and Molecular Biology, University of Melbourne, 30 Flemington Road, Melbourne, VIC 3010, Australia;
11
Sir Peter MacCallum Department of Oncology, University of Melbourne, 30 Flemington Road, Melbourne, VIC 3010, Australia;
12
Department of Gynecological Oncology, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USA;
13
Gynaecological Cancer Research Centre, Department of Women’s Cancer, Institute for Women’s Health, University College
London, Maple House 1st Floor, 149 Tottenham Court Road, London W1T 7DN, UK; 14Department of Pathology and Laboratory
Medicine, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USA; 15Department of Cancer Prevention and
Control, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USA; 16Department of Gynecology and
*Correspondence: Dr LE Kelemen; E-mail:
Revised 3 September 2014; accepted 2 October 2014; published online 30 October 2014
& 2014 Cancer Research UK. All rights reserved 0007 – 0920/14
www.bjcancer.com | DOI:10.1038/bjc.2014.567
2297
BRITISH JOURNAL OF CANCER
FOLR1 in ovarian cancer
Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center
Erlangen-EMN, Universitaetsstrasse 21-23, 91054 Erlangen, Germany; 17Institute of Pathology, University Hospital Erlangen,
Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Krankenhausstrasse 8-10,
91054 Erlangen, Germany; 18Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Ø, Denmark; 19Department of Pathology, Herlev Hospital, University of Copenhagen, Herlev
Ringvej 75, DK-2370 Herlev, Denmark; 20The Juliane Marie Center, Department of Obstetrics and Gynecology, Rigshospitalet,
University of Copenhagen, Blegdamsvej 9, DK-2100 Copenhagen, Ø, Denmark; 21Department of Medical Oncology, Mayo Clinic,
200 First Street SW, Charlton 6, Rochester, MN 55905, USA; 22Department of Biostatistics, University of Kansas Medical Center,
3901 Rainbow Boulevard, Kansas City, KS 66160, USA; 23Department of Laboratory Medicine and Pathology, Division of Anatomic
Pathology, Mayo Clinic, 200 First Street SW, Stabile 13, Rochester, MN 55905, USA; 24Department of Health Sciences Research,
Division of Biomedical Statistics and Informatics, Mayo Clinic, 200 First Street SW, Charlton 6, Rochester, MN 55905, USA;
25
Anatomic Pathology Research Laboratory, Calgary Laboratory Services, Foothills Medical Center, 1403 29 ST NW, Calgary, AB
T2N 2T9, Canada; 26Department of Obstetrics and Gynecology, Division of Oncology, Tom Baker Cancer Centre, University of
Calgary, Foothills Medical Center, 1403 29 ST NW, Calgary, AB T2N 2T9, Canada; 27Department of Pathology, Cancer Institute,
University College London, Maple House, 149 Tottenham Court Road, London WC1E 6JJ, UK; 28Department of Women’s Cancer,
UCL EGA Institute for Womeńs Health, University College London, 74 Huntley Street, London WC1E 6AU, UK; 29Department of
Obstetrics and Gynecology, University of Toronto, Princess Margaret Cancer Centre, 610 University Avenue, M-700, Toronto, ON
M5T 2M9, Canada; 30Department of Medicine, Division of Medical Oncology, University of Toronto, Princess Margaret Hospital,
610 University Avenue, Toronto, ON M5G 2M9, Canada; 31Department of Pathology, Addenbrooke’s Hospital, Cambridge
University Hospital NHS Foundation Trust, Hills Road, Cambridge CB2 0QQ, UK; 32National Institute for Health Research
Cambridge Biomedical Research Centre, Cambridge CB2 2QQ, UK; 33Department of Population Health Research, Alberta Health
Services-Cancer Care, 2210 2nd Street SW, Calgary, AB, T2S 3C3, Canada; 34Department of Obstetrics and Gynecology, Division
of Gynecologic Oncology, Royal Alexandra Hospital, 10240 Kingsway Ave, Edmonton, AB T5H 3V9, Canada; 35Department of
Laboratory Medicine and Pathology, Royal Alexandra Hospital, 10240 Kingsway Ave, Edmonton, AB T5H 3V9, Canada;
36
Department of Gynaecological Oncology and Westmead Institute for Cancer Research, University of Sydney at Westmead
Millennium Institute, Westmead Hospital, Westmead, NSW 2145, Australia; 37Genetics and Computational Biology Department,
QIMR Berghofer Medical Research Institute, 300 Herston Ro (...truncated)