Significance of folate receptor alpha and thymidylate synthase protein expression in patients with non-small-cell lung cancer treated with pemetrexed

Journal of Thoracic Oncology

Volumn 8, Issue 1, 2013, Pages 19-30

  Christoph, Daniel C ^a,c   Asuncion, Bernadette Reyna ^a   Hassan, Biftu ^a   Tran, Cindy ^a   Maltzman, Julia D ^b   O'Shannessy, Daniel J ^b   Wynes, Murry W ^a   Gauler, Thomas C ^c   Wohlschlaeger, Jeremias ^d   Hoiczyk, Mathias ^c   Schuler, Martin ^c   Eberhardt, Wilfried E ^c   Hirsch, Fred R ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Morphotek Inc   (United States)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d RUHRLANDKLINIK   (Germany)

Author keywords

Biomarker; Folate receptor alpha; Non small cell lung cancer; Pemetrexed; Thymidylate synthase

Indexed keywords

FOLATE RECEPTOR 1; PEMETREXED; THYMIDYLATE SYNTHASE;

ADULT; AGED; ARTICLE; CANCER CHEMOTHERAPY; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; RADIOGRAPHY; SCORING SYSTEM; TREATMENT OUTCOME; TREATMENT RESPONSE;

EID: 84871950953     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1097/JTO.0b013e31827628ff     Document Type: Article

References (49)

1. Jemal A, Thun MJ, Ries LA, et al. Annual report to the nation on the status of cancer, 1975-2005, featuring trends in lung cancer, tobacco use, and tobacco control. J Natl Cancer Inst 2008;100:1672-1694.
2. Chang MH, Ahn JS, Lee J, et al. The effcacy of pemetrexed as a third-or fourth-line therapy and the signifcance of thymidylate synthase expression in patients with advanced non-small cell lung cancer. Lung Cancer 2010;69:323-329.
3. Scagliotti G V, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008;26:3543-3551.
4. Grønberg BH, Bremnes RM, Fløtten O, et al. Phase III study by the Norwegian lung cancer study group: pemetrexed plus carboplatin compared with gemcitabine plus carboplatin as frst-line chemotherapy in advanced non-small-cell lung cancer. J Clin Oncol 2009;27:3217-3224.
5. Ciuleanu T, Brodowicz T, Zielinski C, et al. Maintenance pemetrexed plus best supportive care versus placebo plus best supportive care for non-small-cell lung cancer: a randomised, double-blind, phase 3 study. Lancet 2009;374:1432-1440.
6. Belani C P, Wu YL, Chen YM, et al. Effcacy and safety of pemetrexed maintenance therapy versus best supportive care in patients from East Asia with advanced, nonsquamous non-small cell lung cancer: an exploratory subgroup analysis of a global, randomized, phase 3 clinical trial. J Thorac Oncol 2012;7:567-573.
7. Bearz A, Garassino I, Cavina R, et al. Pemetrexed single agent in previously treated non-small cell lung cancer: a multi-institutional observational study. Lung Cancer 2008;60:240-245.
8. Adjei AA. Pharmacology and mechanism of action of pemetrexed. Clin Lung Cancer 2004;5 Suppl 2:S51-S55.
9. Chen C Y, Chang YL, Shih J Y, et al. Thymidylate synthase and dihydrofo-late reductase expression in non-small cell lung carcinoma: the association with treatment effcacy of pemetrexed. Lung Cancer 2011;74:132-138.
10. Sun JM, Han J, Ahn JS, Park K, Ahn MJ. Signifcance of thymidylate synthase and thyroid transcription factor 1 expression in patients with nonsquamous non-small cell lung cancer treated with pemetrexed-based chemotherapy. J Thorac Oncol 2011;6:1392-1399.
11. Assaraf YG. Molecular basis of antifolate resistance. Cancer Metastasis Rev 2007;26:153-181.
12. Zhao, R and Goldman, ID. Resistance to antifolates. Oncogene 2003; 22:7431-7457.
13. Chattopadhyay S, Moran RG, Goldman ID. Pemetrexed: biochemical and cellular pharmacology, mechanisms, and clinical applications. Mol Cancer Ther 2007;6:404-417.
14. O'Shannessy DJ, Somers EB, Albone E, et al. Characterization of the human folate receptor alpha via novel antibody-based probes. Oncotarget 2011;2:1227-1243.
15. Leamon C P, Low PS. Folate-mediated targeting: from diagnostics to drug and gene delivery. Drug Discov Today 2001;6:44-51.
16. Antony AC. Folate receptors. Annu Rev Nutr 1996;16:501-521.
17. Elnakat H, Ratnam M. Distribution, functionality and gene regulation of folate receptor isoforms: implications in targeted therapy. Adv Drug Deliv Rev 2004;56:1067-1084.
18. Franklin WA, Waintrub M, Edwards D, et al. New anti-lung-cancer antibody cluster 12 reacts with human folate receptors present on adenocar-cinoma. Int J Cancer Suppl 1994;8:89-95.
19. Parker N, Turk MJ, Westrick E, Lewis JD, Low PS, Leamon C P. Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Anal Biochem 2005;338:284-293.
20. Weitman, SD, Weinberg, AG, Coney, LR et al. Cellular localization of the folate receptor: potential role in drug toxicity and folate homeostasis. Cancer Res 1992:6708-6711. 52, 23.
21. Gruner BA, Weitman SD. The folate receptor as a potential therapeutic anticancer target. Invest New Drugs 1998;16:205-219.
22. Smith AE, Pinkney M, Piggott NH, Calvert H, Milton ID, Lunec J. A novel monoclonal antibody for detection of folate receptor alpha in paraffn-embedded tissues. Hybridoma (Larchmt) 2007;26:281-288.
23. Nunez MI, Behrens C, Woods DM, et al. High expression of folate receptor alpha in lung cancer correlates with adenocarcinoma histology and EGFR [corrected] mutation. J Thorac Oncol 2012;7:833-840.
24. Pribble P, Edelman MJ. EC145: a novel targeted agent for adenocarci-noma of the lung. Expert Opin Investig Drugs 2012;21:755-761.
25. Ebel W, Routhier EL, Foley B, et al. Preclinical evaluation of MORAb-003, a humanized monoclonal antibody antagonizing folate receptor-alpha. Cancer Immun 2007;7:6.
26. Chattopadhyay S, Wang Y, Zhao R, Goldman ID. Lack of impact of the loss of constitutive folate receptor alpha expression, achieved by RNA Interference, on the activity of the new generation antifolate pemetrexed in HeLa cells. Clin Cancer Res 2004;10:7986-7993.
27. Kamen BA, Smith AK. Farletuzumab, an anti-folate receptor α antibody, does not block binding of folate or anti-folates to receptor nor does it alter the potency of anti-folates in vitro. Cancer Chemother Pharmacol 2012;70:113-120.
28. O'Shannessy DJ, Yu G, Smale R, et al. Folate receptor alpha expression in lung cancer: diagnostic and prognostic signifcance. Oncotarget 2012;3:414-425.
29. Iwakiri S, Sonobe M, Nagai S, Hirata T, Wada H, Miyahara R. Expression status of folate receptor alpha is signifcantly correlated with prognosis in non-small-cell lung cancers. Ann Surg Oncol 2008;15:889-899.
30. Detterbeck FC, Boffa DJ, Tanoue LT. The new lung cancer staging system. Chest 2009;136:260-271.
31. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009;45:228-247.
32. Wynes M W, Konopa K, Singh S, et al. Thymidylate synthase protein expression by IHC and gene copy number by SISH correlate and show great variability in non-small cell lung cancer. J Thorac Oncol 2012;7:982-992.
33. Christoph DC, Asuncion BR, Mascaux C, et al. Folylpoly-glutamate syn-thetase expression is associated with tumor response and outcome from pemetrexed-based chemotherapy in malignant pleural mesothelioma. J Thorac Oncol 2012;7:1440-1448.
34. Monica V, Scagliotti G V, Ceppi P, et al. Differential thymidylate synthase expression in different variants of large-cell carcinoma of the lung. Clin Cancer Res 2009;15:7547-7552.
35. Spearman C. The proof and measurement of association between two things. Int J Epidemiol 2010;39:1137-1150.
36. Kruskal, WH and Wallis, WA. Use of ranks in one-criterion variance analysis. Am Stat 1952; 47:583-621.
37. Fawcett, T. ROC graphs: notes and practical considerations for researchers. ReCALL 2004; 31:1-38.
38. Ruopp MD, Perkins NJ, Whitcomb B W, Schisterman EF. Youden Index and optimal cut-point estimated from observations affected by a lower limit of detection. Biom J 2008;50:419-430.
39. Halpern, J. Maximally selected chi square statistics for small samples. Biometrics 1982; 38:1017-1023.
40. Miller, R and Siegmund, D. Maximally selected chi square statistics. Biometrics 1982; 38:1011-1016.
41. Ceppi P, Volante M, Saviozzi S, et al. Squamous cell carcinoma of the lung compared with other histotypes shows higher messenger RNA and protein levels for thymidylate synthase. Cancer 2006;107:1589-1596.
42. Gandara, DR, Mack, PC, Omori, A et al. Thymidylate synthase (TS) RNA expression in non-small cell lung cancer (NSCLC): implications for personalizing pemetrexed therapy. J Thorac Oncol 2009; 4 (Suppl 1):D7.1.
43. Zheng Z, Li X, Schell MJ, et al. Thymidylate synthase in situ protein expression and survival in stage I nonsmall-cell lung cancer. Cancer 2008;112:2765-2773.
44. Nutt JE, Razak AR, O'Toole K, et al. The role of folate receptor alpha (FRalpha) in the response of malignant pleural mesothelioma to peme-trexed-containing chemotherapy. Br J Cancer 2010;102:553-560.
45. Dosio F, Milla P, Cattel L. EC-145, a folate-targeted Vinca alkaloid conjugate for the potential treatment of folate receptor-expressing cancers. Curr Opin Investig Drugs 2010;11:1424-1433.
46. Ghamande, S, Gilbert, L, Penson, R et al. The co-development of a folate receptor molecular diagnostic imaging agent (99mTc-EC20) and folate receptor targeted drug conjugate (EC145) in the treatment of ovarian cancer patients. Eur J Cancer 2011; 47:OP93.
47. Bonnon C, Wendeler M W, Paccaud J P, Hauri H P. Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J Cell Sci 2010;123(Pt 10):1705-1715.
48. Rijnboutt S, Jansen G, Posthuma G, Hynes JB, Schornagel JH, Strous GJ. Endocytosis of GPI-linked membrane folate receptor-alpha. J Cell Biol 1996;132:35-47.
49. Shia J, Klimstra DS, Nitzkorski JR, et al. Immunohistochemical expression of folate receptor alpha in colorectal carcinoma: patterns and biological signifcance. Hum Pathol 2008;39:498-505.