Overexpression of thymidylate synthase (TYMS) is associated with aggressive tumor features and early PSA recurrence in prostate cancer

Oncotarget

Volumn 6, Issue 10, 2015, Pages 8377-8387

  Burdelski, Christoph ^a   Strauss, Christian ^a   Tsourlakis, Maria Christina ^a   Kluth, Martina ^a   Hube Magg, Claudia ^a   Melling, Nathaniel ^a   Lebok, Patrick ^a   Minner, Sarah ^a   Koop, Christina ^a   Graefen, Markus ^a   Heinzer, Hans ^a   Wittmer, Corinna ^a   Krech, Till ^a   Sauter, Guido ^a   Wilczak, Waldemar ^a   Simon, Ronald ^a   Schlomm, Thorsten ^a   Steurer, Stefan ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Prognosis; Prostate cancer; Tissue microarray; TMPRSS2 ERG fusion; TYMS

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROSTATE SPECIFIC ANTIGEN; THYMIDYLATE SYNTHASE; KALLIKREIN; KALLIKREIN-RELATED PEPTIDASE 3, HUMAN; TYMS PROTEIN, HUMAN;

ADVANCED CANCER; ARTICLE; CANCER GRADING; CANCER RECURRENCE; CANCER STAGING; CANCER SURGERY; CHROMOSOMAL INSTABILITY; CHROMOSOME 3P; CHROMOSOME 5Q; CHROMOSOME 6Q; CHROMOSOME DELETION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; GENETIC LINKAGE; GLEASON SCORE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; PREDICTIVE VALUE; PREOPERATIVE EVALUATION; PROSTATE CANCER; PROSTATE EPITHELIUM; PROSTATECTOMY; PROTEIN EXPRESSION; TISSUE MICROARRAY; BIOSYNTHESIS; ENZYMOLOGY; PATHOLOGY; PROCEDURES; PROGNOSIS; PROSTATIC NEOPLASMS; TUMOR RECURRENCE;

HUMANS; IMMUNOHISTOCHEMISTRY; KALLIKREINS; MALE; NEOPLASM RECURRENCE, LOCAL; PROGNOSIS; PROSTATE-SPECIFIC ANTIGEN; PROSTATECTOMY; PROSTATIC NEOPLASMS; THYMIDYLATE SYNTHASE; TISSUE ARRAY ANALYSIS;

EID: 84928379596     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3107     Document Type: Article

References (59)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA: a cancer journal for clinicians. 2010; 60:277-300.
2. Graefen M, Ahyai S, Heuer R, Salomon G, Schlomm T, Isbarn H, Budaus L, Heinzer H and Huland H. [Active surveillance for prostate cancer]. Urologe A. 2008; 47:261-269.
3. Carreras CW, Santi DV. The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem. 1995; 64:721-762.
4. Rustum YM. Thymidylate synthase: a critical target in cancer therapy? Front Biosci. 2004; 9:2467-2473.
5. Navalgund LG, Rossana C, Muench AJ, Johnson LF. Cell cycle regulation of thymidylate synthetase gene expression in cultured mouse fibroblasts. J Biol Chem. 1980; 255:7386-7390.
6. Rahman L, Voeller D, Rahman M, Lipkowitz S, Allegra C, Barrett JC, Kaye FJ, Zajac-Kaye M. Thymidylate synthase as an oncogene: a novel role for an essential DNA synthesis enzyme. Cancer Cell. 2004; 5:341-351.
7. Kotoula V, Krikelis D, Karavasilis V, Koletsa T, Eleftheraki AG, Televantou D, Christodoulou C, Dimoudis S, Korantzis I, Pectasides D, Syrigos KN, Kosmidis PA, Fountzilas G. Expression of DNA repair and replication genes in non-small cell lung cancer (NSCLC): a role for thymidylate synthetase (TYMS). BMC Cancer. 2012; 12:342.
8. Pestalozzi BC, Peterson HF, Gelber RD, Goldhirsch A, Gusterson BA, Trihia H, Lindtner J, Cortes-Funes H, Simmoncini E, Byrne MJ, Golouh R, Rudenstam CM, Castiglione-Gertsch M, Allegra CJ, Johnston PG. Prognostic importance of thymidylate synthase expression in early breast cancer. J Clin Oncol. 1997; 15:1923-1931.
9. Formentini A, Henne-Bruns D, Kornmann M. Thymidylate synthase expression and prognosis of patients with gastrointestinal cancers receiving adjuvant chemotherapy: a review. Langenbecks Arch Surg. 2004; 389:405-413.
10. Popat S, Matakidou A, Houlston RS. Thymidylate synthase expression and prognosis in colorectal cancer: a systematic review and meta-analysis. J Clin Oncol. 2004; 22:529-536.
11. Mizutani Y, Wada H, Yoshida O, Fukushima M, Nonomura M, Nakao M, Miki T. Significance of thymidylate synthase activity in renal cell carcinoma. Clin Cancer Res. 2003; 9:1453-1460.
12. Li Y, Mizutani Y, Shiraishi T, Okihara K, Ukimura O, Kawauchi A, Nonomura N, Fukushima M, Sakai T, Miki T. Prognostic significance of thymidylate synthase expression in patients with prostate cancer undergoing radical prostatectomy. Urology. 2007; 69:988-995.
13. Miyoshi Y, Uemura H, Ishiguro H, Kitamura H, Nomura N, Danenberg PV, Kubota Y. Expression of thymidylate synthase, dihydropyrimidine dehydrogenase, thymidine phosphorylase, and orotate phosphoribosyl transferase in prostate cancer. Prostate Cancer Prostatic Dis. 2005; 8:260-265.
14. Yano A, Shigematsu Y, Kitano H, Hanayama A, Ozawa A, Tacho T, Fujii M. Possibility of using mRNA expression levels for nucleic acid-metabolizing enzymes within prostate cancer cells as indices for prognostic factors. Oncol Lett. 2010; 1:1049-1053.
15. Inoue T, Segawa T, Shiraishi T, Yamada T, Kinukawa N, Yoshida T, Toda Y, Shimizu Y, Nakamura E, Kinoshita H, Kamoto T, Ogawa O. High-grade and hormone-treated prostate cancer express high levels of thymidylate synthase. BJU Int. 2006; 98:197-200.
16. Schlomm T, Sultmann H, Kollermann J. [Identification and validation of clinically relevant molecular alterations in prostate cancer]. Urologe A. 2008; 47:1193-1198.
17. Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998; 4:844-847.
18. Weischenfeldt J, Simon R, Feuerbach L, Schlangen K, Weichenhan D, Minner S, Wuttig D, Warnatz HJ, Stehr H, Rausch T, Jäger N, Gu L, Bogatyrova O, Stütz A, Claus R, Eils J, et al. Integrative genomic analyses reveal androgendriven somatic alteration landscape in early-onset prostate cancer. Cancer Cell. 2013; 23:159-170.
19. Minner S, Enodien M, Sirma H, Luebke AM, Krohn A, Mayer PS, Simon R, Tennstedt P, Muller J, Scholz L, Brase JC, Liu AY, Schluter H, Pantel K, Schumacher U, Bokemeyer C, et al. ERG Status Is Unrelated to PSA Recurrence in Radically Operated Prostate Cancer in the Absence of Antihormonal Therapy. Clinical cancer research. 2011; 17:5878-5888.
20. Burkhardt L, Fuchs S, Krohn A, Masser S, Mader M, Kluth M, Bachmann F, Huland H, Steuber T, Graefen M, Schlomm T, Minner S, Sauter G, Sirma H, Simon R. CHD1 Is a 5q21 Tumor Suppressor Required for ERG Rearrangement in Prostate Cancer. Cancer research. 2013; 73:2795-2805.
21. Kluth M, Hesse J, Heinl A, Krohn A, Steurer S, Sirma H, Simon R, Mayer PS, Schumacher U, Grupp K, Izbicki JR, Pantel K, Dikomey E, Korbel JO, Plass C, Sauter G, et al. Genomic deletion of MAP3K7 at 6q12-22 is associated with early PSA recurrence in prostate cancer and absence of TMPRSS2:ERG fusions. Modern pathology. 2013; 26:975-983.
22. Krohn A, Diedler T, Burkhardt L, Mayer PS, De Silva C, Meyer-Kornblum M, Kotschau D, Tennstedt P, Huang J, Gerhauser C, Mader M, Kurtz S, Sirma H, Saad F, Steuber T, Graefen M, et al. Genomic deletion of PTEN is associated with tumor progression and early PSA recurrence in ERG fusion-positive and fusion-negative prostate cancer. The American journal of pathology. 2012; 181:401-412.
23. Krohn A, Seidel A, Burkhardt L, Bachmann F, Mader M, Grupp K, Eichenauer T, Becker A, Adam M, Graefen M, Huland H, Kurtz S, Steurer S, Tsourlakis MC, Minner S, Michl U, et al. Recurrent deletion of 3p13 targets multiple tumour suppressor genes and defines a distinct subgroup of aggressive ERG fusion-positive prostate cancers. J Pathol. 2013; 231:130-141.
24. Schlomm T, Iwers L, Kirstein P, Jessen B, Kollermann J, Minner S, Passow-Drolet A, Mirlacher M, Milde-Langosch K, Graefen M, Haese A, Steuber T, Simon R, Huland H, Sauter G, Erbersdobler A. Clinical significance of p53 alterations in surgically treated prostate cancers. Mod Pathol. 2008; 21:1371-1379.
25. El Gammal AT, Bruchmann M, Zustin J, Isbarn H, Hellwinkel OJ, Kollermann J, Sauter G, Simon R, Wilczak W, Schwarz J, Bokemeyer C, Brummendorf TH, Izbicki JR, Yekebas E, Fisch M, Huland H, et al. Chromosome 8p deletions and 8q gains are associated with tumor progression and poor prognosis in prostate cancer. Clin Cancer Res. 2010; 16:56-64.
26. Tennstedt P, Koster P, Bruchmann A, Mirlacher M, Haese A, Steuber T, Sauter G, Huland H, Graefen M, Schlomm T, Minner S, Simon R. The impact of the number of cores on tissue microarray studies investigating prostate cancer biomarkers. International journal of oncology. 2012; 40:261-268.
27. Minner S, Jessen B, Stiedenroth L, Burandt E, Kollermann J, Mirlacher M, Erbersdobler A, Eichelberg C, Fisch M, Brummendorf TH, Bokemeyer C, Simon R, Steuber T, Graefen M, Huland H, Sauter G, et al. Low level HER2 overexpression is associated with rapid tumor cell proliferation and poor prognosis in prostate cancer. Clin Cancer Res. 2010; 16:1553-1560.
28. Muller J, Ehlers A, Burkhardt L, Sirma H, Steuber T, Graefen M, Sauter G, Minner S, Simon R, Schlomm T, Michl U. Loss of p(Ser2448)-mTOR expression is linked to adverse prognosis and tumor progression in ERG-fusionpositive cancers. International journal of cancer. 2012; 132:1333-1340.
29. Minner S, Wittmer C, Graefen M, Salomon G, Steuber T, Haese A, Huland H, Bokemeyer C, Yekebas E, Dierlamm J, Balabanov S, Kilic E, Wilczak W, Simon R, Sauter G, Schlomm T. High level PSMA expression is associated with early PSA recurrence in surgically treated prostate cancer. The Prostate. 2011; 71:281-288.
30. Zhou J, He E, Skog S. The proliferation marker thymidine kinase 1 in clinical use. Molecular and clinical oncology. 2013; 1:18-28.
31. Jakobsen JN, Santoni-Rugiu E, Sorensen JB. Differences in RRM1 protein expression between diagnostic biopsies and resection specimens, and changes during carboplatin and paclitaxel treatment, in non-small-cell lung cancer. Histopathology. 2014; 64:412-420.
32. Palma P, Cano C, Conde-Muino R, Comino A, Bueno P, Ferron JA, Cuadros M. Expression profiling of rectal tumors defines response to neoadjuvant treatment related genes. PloS one. 2014; 9:e112189.
33. Lemee F, Bergoglio V, Fernandez-Vidal A, Machado-Silva A, Pillaire MJ, Bieth A, Gentil C, Baker L, Martin AL, Leduc C, Lam E, Magdeleine E, Filleron T, Oumouhou N, Kaina B, Seki M, et al. DNA polymerase theta up-regulation is associated with poor survival in breast cancer, perturbs DNA replication, and promotes genetic instability. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:13390-13395.
34. Zhou Q, Talvinen K, Sundstrom J, Elzagheid A, Pospiech H, Syvaoja JE, Collan Y. Mutations/polymorphisms in the 55 kDa subunit of DNA polymerase epsilon in human colorectal cancer. Cancer genomics & proteomics. 2009; 6:297-304.
35. Negri FV, Azzoni C, Bottarelli L, Campanini N, Mandolesi A, Wotherspoon A, Cunningham D, Scartozzi M, Cascinu S, Tinelli C, Silini EM, Ardizzoni A. Thymidylate synthase, topoisomerase-1 and microsatellite instability: relationship with outcome in mucinous colorectal cancer treated with fluorouracil. Anticancer research. 2013; 33:4611-4617.
36. Karnes RJ, Cheville JC, Ida CM, Sebo TJ, Nair AA, Tang H, Munz JM, Kosari F, Vasmatzis G. The ability of biomarkers to predict systemic progression in men with high-risk prostate cancer treated surgically is dependent on ERG status. Cancer research. 2010; 70:8994-9002.
37. Oliveira-Costa JP, Zanetti J, Oliveira LR, Soares FA, Ramalho LZ, Silva Ramalho F, Garcia SB, Ribeiro-Silva A. Significance of topoisomerase IIIbeta expression in breast ductal carcinomas: strong associations with diseasespecific survival and metastasis. Human pathology. 2010; 41:1624-1630.
38. Simsek D, Brunet E, Wong SY, Katyal S, Gao Y, McKinnon PJ, Lou J, Zhang L, Li J, Rebar EJ, Gregory PD, Holmes MC, Jasin M. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS genetics. 2011; 7:e1002080.
39. Kuhmann C, Li C, Kloor M, Salou M, Weigel C, Schmidt CR, Ng LW, Tsui WW, Leung SY, Yuen ST, Becker N, Weichenhan D, Plass C, Schmezer P, Chan TL, Popanda O. Altered regulation of DNA ligase IV activity by aberrant promoter DNA methylation and gene amplification in colorectal cancer. Human molecular genetics. 2014; 23:2043-2054.
40. Chen X, Bahrami A, Pappo A, Easton J, Dalton J, Hedlund E, Ellison D, Shurtleff S, Wu G, Wei L, Parker M, Rusch M, Nagahawatte P, Wu J, Mao S, Boggs K, et al. Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell reports. 2014; 7:104-112.
41. Walden H, Deans AJ. The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Annual review of biophysics. 2014; 43:257-278.
42. Sanada S, Futami K, Terada A, Yonemoto K, Ogasawara S, Akiba J, Yasumoto M, Sumi A, Ushijima K, Kamura T, Furuichi Y, Yano H. RECQL1 DNA repair helicase: a potential therapeutic target and a proliferative marker against ovarian cancer. PloS one. 2013; 8:e72820.
43. Daino K, Imaoka T, Morioka T, Tani S, Iizuka D, Nishimura M, Shimada Y. Loss of the BRCA1-interacting helicase BRIP1 results in abnormal mammary acinar morphogenesis. PloS one. 2013; 8:e74013.
44. Adelman CA, Lolo RL, Birkbak NJ, Murina O, Matsuzaki K, Horejsi Z, Parmar K, Borel V, Skehel JM, Stamp G, D'Andrea A, Sartori AA, Swanton C, Boulton SJ. HELQ promotes RAD51 paralogue-dependent repair to avert germ cell loss and tumorigenesis. Nature. 2013; 502:381-384.
45. Kolla V, Zhuang T, Higashi M, Naraparaju K, Brodeur GM. Role of CHD5 in human cancers: 10 years later. Cancer research. 2014; 74:652-658.
46. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005; 310:644-648.
47. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Sivachenko AY, Sboner A, Esgueva R, Pflueger D, Sougnez C, Onofrio R, Carter SL, Park K, Habegger L, Ambrogio L, Fennell T, et al. The genomic complexity of primary human prostate cancer. Nature. 2011; 470:214-220.
48. Lapointe J, Li C, Giacomini CP, Salari K, Huang S, Wang P, Ferrari M, Hernandez-Boussard T, Brooks JD, Pollack JR. Genomic profiling reveals alternative genetic pathways of prostate tumorigenesis. Cancer research. 2007; 67:8504-8510.
49. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell. 2010; 18:11-22.
50. Resnick M, Bercovier H, Mor N, Levy L. Unforeseen death of Mycobacterium lepraemurium in infected susceptible mice. J Infect Dis. 1986; 153:368-370.
51. Kuzel TM, Tallman MS, Shevrin D, Braud E, Kilton L, Johnson P, Kozlowski J, Vogelzang NJ, Blough R, Benson AB. A phase II study of continuous infusion 5-fluorouracil in advanced hormone refractory prostate cancer. An Illinois Cancer Center Study. Cancer. 1993; 72:1965-1968.
52. Birtle AJ, Newby JC, Harland SJ. Epirubicin carboplatin and 5-fluorouracil (ECarboF) chemotherapy in metastatic hormone refractory prostate cancer. Br J Cancer. 2004; 91:1472-1476.
53. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer. 2003; 3:330-338.
54. Malet-Martino M, Martino R. Clinical studies of three oral prodrugs of 5-fluorouracil: a review. Oncologist. 2002; 7:288-323.
55. Shelley M, Harrison C, Coles B, Staffurth J, Wilt TJ, Mason MD. Chemotherapy for hormone-refractory prostate cancer. Cochrane Database Syst Rev. 2006; CD005247.
56. Brody JR, Hucl T, Costantino CL, Eshleman JR, Gallmeier E, Zhu H, van der Heijden MS, Winter JM, Wikiewicz AK, Yeo CJ, Kern SE. Limits to thymidylate synthase and TP53 genes as predictive determinants for fluoropyrimidine sensitivity and further evidence for RNAbased toxicity as a major influence. Cancer research. 2009; 69:984-991.
57. Arienti C, Tesei A, Verdecchia GM, Framarini M, Virzi S, Grassi A, Scarpi E, Turci L, Silvestrini R, Amadori D, Zoli W. Role of conventional chemosensitivity test and tissue biomarker expression in predicting response to treatment of peritoneal carcinomatosis from colon cancer. Clin Colorectal Cancer. 2013; 12:122-127.
58. Cho YB, Chung HJ, Lee WY, Choi SH, Kim HC, Yun SH, Chun HK. Relationship between TYMS and ERCC1 mRNA expression and in vitro chemosensitivity in colorectal cancer. Anticancer research. 2011; 31:3843-3849.
59. Donada M, Bonin S, Barbazza R, Pettirosso D, Stanta G. Management of stage II colon cancer-the use of molecular biomarkers for adjuvant therapy decision. BMC Gastroenterol. 2013; 13:36.