Tumour heterogeneity poses a significant challenge to cancer biomarker research

British Journal of Cancer

Volumn 117, Issue 3, 2017, Pages 367-375

  Cyll, Karolina ^a,b   Ersvær, Elin ^a,b   Vlatkovic, Ljiljana ^a   Pradhan, Manohar ^a,b   Kildal, Wanja ^a,b   Avranden Kjær, Marte ^a,b   Kleppe, Andreas ^a,b   Hveem, Tarjei S ^a,b   Carlsen, Birgitte ^c   Gill, Silje ^c   Löffeler, Sven ^c   Haug, Erik Skaaheim ^c   Wæhre, Håkon ^a,b   Sooriakumaran, Prasanna ^d   Danielsen, Håvard E ^a,b,d  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c VESTFOLD HOSPITAL TRUST   (Norway)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; DNA; PTEN PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER RESEARCH; CANCER SURGERY; COHORT ANALYSIS; CONTROLLED STUDY; FOLLOW UP; GENETIC HETEROGENEITY; GLEASON SCORE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; NEEDLE BIOPSY; PLOIDY; PRIORITY JOURNAL; PROSTATE; PROSTATE BIOPSY; PROSTATE CANCER; PROSTATECTOMY; SURGICAL MARGIN; TUMOR VOLUME; CANCER GRADING; CHEMISTRY; GENETICS; MIDDLE AGED; PATHOLOGY; PROSTATE TUMOR; THERAPY; TUMOR BURDEN; TUMOR RECURRENCE; WATCHFUL WAITING;

AGED; BIOMARKERS, TUMOR; BIOPSY, NEEDLE; DNA, NEOPLASM; GENETIC HETEROGENEITY; HUMANS; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM RECURRENCE, LOCAL; PLOIDIES; PROSTATE; PROSTATECTOMY; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; TUMOR BURDEN; WATCHFUL WAITING;

EID: 85029280290     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2017.171     Document Type: Article

References (38)

1. Aihara M, Wheeler TM, Ohori M, Scardino PT (1994) Heterogeneity of prostate cancer in radical prostatectomy specimens. Urology 43(1): 60-66.
2. Andor N, Graham TA, Jansen M, Xia LC, Aktipis CA, Petritsch C, Ji HP, Maley CC (2015) Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nat Med 22(1): 105-113.
3. Andreoiu M, Cheng L (2010) Multifocal prostate cancer: Biologic, prognostic, and therapeutic implications. Hum Pathol 41(6): 781-793.
4. Arora R, Koch MO, Eble JN, Ulbright TM, Li L, Cheng L (2004) Heterogeneity of Gleason grade in multifocal adenocarcinoma of the prostate. Cancer 100(11): 2362-2366.
5. Attard G, Parker C, Eeles RA, Schröder F, Tomlins SA, Tannock I, Drake CG, De Bono JS (2016) Prostate cancer. Lancet 387(10013): 70-82.
6. Boutros PC, Fraser M, Harding NJ, de Borja R, Trudel D, Lalonde E, Meng A, Hennings-Yeomans PH, McPherson A, Sabelnykova VY, Zia A, Fox NS, Livingstone J, Shiah Y-J, Wang J, Beck TA, Have CL, Chong T, Sam M, Johns J, Timms L, Buchner N, Wong A, Watson JD, Simmons TT, P'ng C, Zafarana G, Nguyen F, Luo X, Chu KC, Prokopec SD, Sykes J, Dal Pra A, Berlin A, Brown A, Chan-Seng-Yue MA, Yousif F, Denroche RE, Chong LC, Chen GM, Jung E, Fung C, Starmans MHW, Chen H, Govind SK, Hawley J, D'Costa A, Pintilie M, Waggott D, Hach F, Lambin P, Muthuswamy LB, Cooper C, Eeles R, Neal D, Tetu B, Sahinalp C, Stein LD, Fleshner N, Shah SP, Collins CC, Hudson TJ, McPherson JD, van der Kwast T, Bristow RG (2015) Spatial genomic heterogeneity within localized, multifocal prostate cancer. Nat Genet 47(7): 736-745.
7. Burrell RA, McGranahan N, Bartek J, Swanton C (2013) The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501(7467): 338-345.
8. Böcking A, Tils M, Schramm M, Dietz J, Biesterfeld S (2014) DNA-cytometric grading of prostate cancer systematic review with descriptive data analysis. Pathol Discov 2(1): 7.
9. Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O, Bray F (2012) International variation in prostate cancer incidence and mortality rates. Eur Urol 61(6): 1079-1092.
10. Cooper CS, Eeles R, Wedge DC, Van Loo P, Gundem G, Alexandrov LB, Kremeyer B, Butler A, Lynch AG, Camacho N, Massie CE, Kay J, Luxton HJ, Edwards S, Kote-Jarai Z, Dennis N, Merson S, Leongamornlert D, Zamora J, Corbishley C, Thomas S, Nik-Zainal S, O'Meara S, Matthews L, Clark J, Hurst R, Mithen R, Bristow RG, Boutros PC, Fraser M, Cooke S, Raine K, Jones D, Menzies A, Stebbings L, Hinton J, Teague J, McLaren S, Mudie L, Hardy C, Anderson E, Joseph O, Goody V, Robinson B, Maddison M, Gamble S, Greenman C, Berney D, Hazell S, Livni N, Fisher C, Ogden C, Kumar P, Thompson A, Woodhouse C, Nicol D, Mayer E, Dudderidge T, Shah NC, Gnanapragasam V, Voet T, Campbell P, Futreal A, Easton D, Warren AY, Foster CS, Stratton MR, Whitaker HC, McDermott U, Brewer DS, Neal DE (2015) Analysis of the genetic phylogeny of multifocal prostate cancer identifies multiple independent clonal expansions in neoplastic and morphologically normal prostate tissue. Nat Genet 47(4): 367-372.
11. Cooperberg MR, Davicioni E, Crisan A, Jenkins RB, Ghadessi M, Karnes RJ (2015) Combined value of validated clinical and genomic risk stratification tools for predicting prostate cancer mortality in a high-risk prostatectomy cohort. Eur Urol 67(2): 326-333.
12. Cuzick J, Yang ZH, Fisher G, Tikishvili E, Stone S, Lanchbury JS, Camacho N, Merson S, Brewer D, Cooper CS, Clark J, Berney DM, Møller H, Scardino P, Sangale Z (2013) Prognostic value of PTEN loss in men with conservatively managed localised prostate cancer. Br J Cancer 108(12): 2582-2589.
13. Cyll K, Callaghan P, Kildal W, Danielsen HE (2015) Preparing for image based DNA ploidy (2015). [Online Video]. Available at https://www.youtube.com/watchv=-24EkrYAwOc.
14. Danielsen HE, Pradhan M, Novelli M (2016) Revisiting tumour aneuploidy-the place of ploidy assessment in the molecular era. Nat Rev Clin Oncol 13: 291-314.
15. Deitch AD, Miller GJ, deVere WR (1993) Significance of abnormal diploid DNA histograms in localized prostate cancer and adjacent benign prostatic tissue. Cancer 72(5): 1692-1700.
16. Epstein JI (2010) An update of the gleason grading system. J Urol 183(2): 433-440.
17. Epstein JI, Egevad L, Amin MB, Delahunt B, Srigley JR, Humphrey PA. Grading Committee (2016) The 2014 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma Definition of Grading Patterns and Proposal for a New Grading System. Am J Surg Pathol 40(2): 244-252.
18. Ferraldeschi R, Nava Rodrigues D, Riisnaes R, Miranda S, Figueiredo I, Rescigno P, Ravi P, Pezaro C, Omlin A, Lorente D, Zafeiriou Z, Mateo J, Altavilla A, Sideris S, Bianchini D, Grist E, Thway K, Perez Lopez R, Tunariu N, Parker C, Dearnaley D, Reid A, Attard G, De Bono J (2015) PTEN protein loss and clinical outcome from castration-resistant prostate cancer treated with abiraterone acetate. Eur Urol 67(4): 795-802.
19. Fraser M, Berlin A, Bristow RG, van der Kwast T (2014) Genomic, pathological, and clinical heterogeneity as drivers of personalized medicine in prostate cancer. Urol Oncol 33(2): 85-94.
20. Freedland SJ, Choeurng V, Howard L, De Hoedt A, du Plessis M, Yousefi K, Lam LL, Buerki C, Ra S, Robbins B, Trabulsi EJ, Shah NL, Abdollah F, Feng FY, Davicioni E, Dicker AP, Karnes RJ, Den RB (2016) Utilization of a genomic classifier for prediction of metastasis following salvage radiation therapy after radical prostatectomy. Eur Urol 70: 588-596.
21. Freedland SJ, Gerber L, Reid J, Welbourn W, Tikishvili E, Park J, Younus A, Gutin A, Sangale Z, Lanchbury JS, Salama JK, Stone S (2013) Prognostic utility of cell cycle progression score in men with prostate cancer after primary external beam radiation therapy. Int J Radiat Oncol Biol Phys 86(5): 848-853.
22. Gerlinger M, Catto JW, Orntoft TF, Real FX, Zwarthoff EC, Swanton C (2015) Intratumour heterogeneity in urologic cancers: From molecular evidence to clinical implications. Eur Urol 67(4): 729-737.
23. Haffner M, Mosbruger T (2013) Tracking the clonal origin of lethal prostate cancer. J Clin Invest 123(11): 4918-4922.
24. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5): 646-674.
25. Karavitakis M, Ahmed HU, Abel PD, Hazell S, Winkler MH (2011) Tumor focality in prostate cancer: Implications for focal therapy. Nat Rev Clin Oncol 8(1): 48-55.
26. Keyes M, Macaulay C, Hayes M, Korbelik J, Morris WJ, Palcic B (2013) DNA ploidy measured on archived pretreatment biopsy material may correlate with prostate-specific antigen recurrence after prostate brachytherapy. Int J Radiat Oncol Biol Phys 86(5): 829-834.
27. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, Meyerson M, Gabriel SB, Lander ES, Getz G (2014) Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505(7484): 495-501.
28. López-Garcá C, Sansregret L, Domingo E, McGranahan N, Hobor S, Birkbak NJ, Horswell S, Grönroos E, Favero F, Rowan AJ, Matthews N, Begum S, Phillimore B, Burrell R, Oukrif D, Spencer-Dene B, Kovac M, Stamp G, Stewart A, Danielsen H, Novelli M, Tomlinson I, Swanton C (2017) BCL9L dysfunction impairs caspase-2 expression permitting aneuploidy tolerance in colorectal cancer. Cancer Cell 31(1): 79-93.
29. McGranahan N, Burrell RA, Endesfelder D, Novelli MR, Swanton C (2012) Cancer chromosomal instability: Therapeutic and diagnostic challenges. EMBO Rep 13(6): 528-538.
30. O'Malley FP, Grignon DJ, Keeney M, Kerkvliet N, McLean C (1993) DNA Heterogeneity in prostatic adenocarcinoma. A DNA flow cytometric mapping study with whole organ sections of prostate. Cancer 71(9): 2797-2802.
31. Perera M, Lawrentschuk N, Bolton D, Clouston D (2014) Comparison of contemporary methods for estimating prostate tumour volume in pathological specimens. BJU Int 113(Suppl 2): 29-34.
32. Punt CJA, Buyse M, Köhne CH, Hohenberger P, Labianca R, Schmoll HJ, Påhlman L, Sobrero A, Douillard JY (2007) Endpoints in adjuvant treatment trials: A systematic review of the literature in colon cancer and proposed definitions for future trials. J Natl Cancer Inst 99(13): 998-1003.
33. Sengupta S, Cheville JC, Lohse CM, Zincke H, Myers RP, Riehle DL, Pankratz VS, Blute ML, Sebo TJ (2006) Conventional assessment of needle biopsy specimens is more useful than digital image analysis of proliferation and DNA ploidy in prediction of positive surgical margins at radical prostatectomy. Urology 68(1): 94-98.
34. Stark JR, Perner S, Stampfer MJ, Sinnott JA, Finn S, Eisenstein AS, Ma J, Fiorentino M, Kurth T, Loda M, Giovannucci EL, Rubin MA, Mucci LA (2009) Gleason score and lethal prostate cancer: Does 3\+44\+3 J Clin Oncol 27(21): 3459-3464.
35. Talantov D, Jatkoe TA, Böhm M, Zhang Y, Ferguson AM, Stricker PD, Kattan MW, Sutherland RL, Kench JG, Wang Y, Henshall SM (2010) Gene based prediction of clinically localized prostate cancer progression after radical prostatectomy. J Urol 184(4): 1521-1528.
36. Wang N, Wilkin C (2000) Evaluation of tumor heterogeneity of prostate carcinoma by flow-A nd image DNA cytometry and histopathological grading. Anal Cell Pathol 20(1): 49-62.
37. Wei L, Wang J, Lampert E, Schlanger S, DePriest AD, Hu Q, Gomez EC, Murakam M, Glenn ST, Conroy J, Morrison C, Azabdaftari G, Mohler JL, Liu S, Heemers HV (2017) Intratumoral and intertumoral genomic heterogeneity of multifocal localized prostate cancer impacts molecular classifications and genomic prognosticators. Eur Urol 71(2): 183-192.
38. Yin Y, Shen WH (2008) PTEN: A new guardian of the genome. Oncogene 27(41): 5443-5453.