The folate receptor as a rational therapeutic target for personalized cancer treatment

Drug Resistance Updates

Volumn 17, Issue 4-6, 2014, Pages 89-95

  Assaraf, Yehuda G ^a   Leamon, Christopher P ^b   Reddy, Joseph A ^b  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b Endocyte Inc   (United States)

Author keywords

Cancer; Endocytosis; Folate; Folate receptor; Personalized medicine; Small molecule drug conjugates; Targeted therapeutics

Indexed keywords

FOLATE TRANSPORTER; FOLIC ACID; FOLIC ACID ANTAGONIST;

ANIMAL; HUMAN; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PERSONALIZED MEDICINE; PROCEDURES;

ANIMALS; FOLIC ACID; FOLIC ACID ANTAGONISTS; FOLIC ACID TRANSPORTERS; HUMANS; INDIVIDUALIZED MEDICINE; MOLECULAR TARGETED THERAPY; NEOPLASMS;

EID: 84914125162     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2014.10.002     Document Type: Review

References (68)

1. D.K. Armstrong, A.J. White, S.C. Weil, M. Phillips, and R.L. Coleman Farletuzumab (a monoclonal antibody against folate receptor alpha) in relapsed platinum-sensitive ovarian cancer Gynecol. Oncol. 129 2013 452 458
2. A. Awada, and P.G. Aftimos Targeted therapies of solid cancers: new options, new challenges Curr. Opin. Oncol. 25 2013 296 304
3. S. Banerjee, and S.B. Kaye New strategies in the treatment of ovarian cancer: current clinical perspectives and future potential Clin. Cancer Res. 19 2013 961 968
4. K.H. Baumann, U. Wagner, and A. du Bois The changing landscape of therapeutic strategies for recurrent ovarian cancer Future Oncol. 8 2012 1135 1147
5. R.E. Bremer, T.S. Scoggin, E.B. Somers, D.J. O'Shannessy, and D.E. Tacha Interobserver agreement and assay reproducibility of folate receptor alpha expression in lung adenocarcinoma: a prognostic marker and potential therapeutic target Arch. Pathol. Lab. Med. 137 2013 1747 1752
6. R. Bueno, K. Appasani, H. Mercer, S. Lester, and D. Sugarbaker The alpha folate receptor is highly activated in malignant pleural mesothelioma J. Thorac. Cardiovasc. Surg. 121 2001 225 233
7. R.A. Burrell, N. McGranahan, J. Bartek, and C. Swanton The causes and consequences of genetic heterogeneity in cancer evolution Nature 501 2013 338 345
8. Y.L. Chen, M.C. Chang, C.Y. Huang, Y.C. Chiang, H.W. Lin, C.A. Chen, C.Y. Hsieh, and W.F. Cheng Serous ovarian carcinoma patients with high alpha-folate receptor had reducing survival and cytotoxic chemo-response Mol. Oncol. 6 2012 360 369
9. D.C. Christoph, B.R. Asuncion, B. Hassan, C. Tran, J.D. Maltzman, D.J. O'Shannessy, M.W. Wynes, T.C. Gauler, J. Wohlschlaeger, M. Hoiczyk, M. Schuler, W.E. Eberhardt, and F.R. Hirsch Significance of folate receptor alpha and thymidylate synthase protein expression in patients with non-small-cell lung cancer treated with pemetrexed J. Thorac. Oncol. 8 2013 19 30
10. L.M. Crane, H.J. Arts, M. van Oosten, P.S. Low, A.G. van der Zee, G.M. van Dam, and J. Bart The effect of chemotherapy on expression of folate receptor-alpha in ovarian cancer Cell Oncol. 35 2012 9 18
11. S. Della-Longa, and A. Arcovito Structural and functional insights on folate receptor alpha (FRalpha) by homology modeling, ligand docking and molecular dynamics J. Mol. Graph. Model. 44 2013 197 207
12. E. Despierre, S. Lambrechts, K. Leunen, P. Berteloot, P. Neven, F. Amant, D.J. O'Shannessy, E.B. Somers, and I. Vergote Folate receptor alpha (FRA) expression remains unchanged in epithelial ovarian and endometrial cancer after chemotherapy Gynecol. Oncol. 130 2013 192 199
13. F. Dosio, P. Milla, and L. Cattel EC-145, a folate-targeted Vinca alkaloid conjugate for the potential treatment of folate receptor-expressing cancers Curr. Opin. Investig. Drugs 11 2010 1424 1433
14. J.A. Drebin, V.C. Link, R.A. Weinberg, and M.I. Greene Inhibition of tumor growth by a monoclonal antibody reactive with an oncogene-encoded tumor antigen Proc. Natl. Acad. Sci. U. S. A. 83 1986 9129 9133
15. M.J. Edelman, W.A. Harb, S.E. Pal, R.V. Boccia, M.J. Kraut, P. Bonomi, B.A. Conley, J.S. Rogers, R.A. Messmann, and E.B. Garon Multicenter trial of EC145 in advanced, folate-receptor positive adenocarcinoma of the lung J. Thorac. Oncol. 7 2012 1618 1621
16. M.J. Edelman, P. Bonomi, W. Harb, S. Pal, R. Boccia, M. Kraut, J. Rogers, D. Morgenstern, B. Conley, and E. Garon Co-development of a folate receptor targeted drug conjugate (EC145) and a folate receptor targeted imaging agent (EC20) in the treatment of advanced adenocarcinoma NSCLC J. Thorac. Oncol. 7 6 (Suppl. 1) 2012 S63
17. H. Elnakat, and M. Ratnam Role of folate receptor genes in reproduction and related cancers Front. Biosci. 11 2006 506 519
18. R.E. Fisher, B.A. Siegel, S.L. Edell, N.M. Oyesiku, D.E. Morgenstern, R.A. Messmann, and R.J. Amato Exploratory study of 99mTc-EC20 imaging for identifying patients with folate receptor-positive solid tumors J. Nucl. Med. 49 2008 899 906
19. W.A. Franklin, M. Waintrub, D. Edwards, K. Christensen, P. Prendegrast, J. Woods, P.A. Bunn, and J.F. Kolhouse New anti-lung-cancer antibody cluster 12 reacts with human folate receptors present on adenocarcinoma Int. J. Cancer 57 Suppl. 8 1994 89 95
20. P. Garin-Chesa, I. Campbell, P.E. Saigo, J.L. Lewis Jr., L.J. Old, and W.J. Rettig Trophoblast and ovarian cancer antigen LK26. Sensitivity and specificity in immunopathology and molecular identification as a folate-binding protein Am. J. Pathol. 142 1993 557 567
21. M. Gerlinger, S. Horswell, J. Larkin, A.J. Rowan, M.P. Salm, I. Varela, R. Fisher, N. McGranahan, N. Matthews, C.R. Santos, P. Martinez, B. Phillimore, S. Begum, A. Rabinowitz, B. Spencer-Dene, S. Gulati, P.A. Bates, G. Stamp, L. Pickering, M. Gore, D.L. Nicol, S. Hazell, P.A. Futreal, A. Stewart, and C. Swanton Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing Nat. Genet. 46 2014 225 233
22. N. Gonen, and Y.G. Assaraf Antifolates in cancer therapy: structure, activity and mechanisms of drug resistance Drug Resist. Updat. 15 2012 183 210
23. D. Gonzalez de Castro, P.A. Clarke, B. Al-Lazikani, and P. Workman Personalized cancer medicine: molecular diagnostics, predictive biomarkers, and drug resistance Clin. Pharmacol. Ther. 93 2013 252 259
24. L.C. Hartmann, G.L. Keeney, W.L. Lingle, T.J. Christianson, B. Varghese, D. Hillman, A.L. Oberg, and P.S. Low Folate receptor overexpression is associated with poor outcome in breast cancer Int. J. Cancer 121 2007 938 942
25. I. Ifergan, and Y.G. Assaraf Molecular mechanisms of adaptation to folate deficiency Vitam. Horm. 79 2008 99 143
26. N.A. Jager, N. Teteloshvili, C.J. Zeebregts, J. Westra, and M. Bijl Macrophage folate receptor-beta (FR-beta) expression in auto-immune inflammatory rheumatic diseases: a forthcoming marker for cardiovascular risk? Autoimmun. Rev. 11 2012 621 626
27. B. Jonsson, and J. Bergh Hurdles in anticancer drug development from a regulatory perspective Nat. Rev. Clin. Oncol. 9 2012 236 243
28. K.R. Kalli, A.L. Oberg, G.L. Keeney, T.J. Christianson, P.S. Low, K.L. Knutson, and L.C. Hartmann Folate receptor alpha as a tumor target in epithelial ovarian cancer Gynecol. Oncol. 108 2008 619 626
29. C. Kurkjian, P. LoRusso, K.K. Sankhala, M.J. Birrer, M. Kirby, S. Ladd, S. Hawes, K.L. Running, J.J. O'Leary, and K.N. Moore A phase I, first-in-human study to evaluate the safety, pharmacokinetics (PK), and pharmacodynamics (PD) of IMGN853 in patients (Pts) with epithelial ovarian cancer (EOC) and other FOLR1-positive solid tumors J. Clin. Oncol. 31 15 Suppl. 2013 2573
30. J.A. Konner, K.M. Bell-McGuinn, P. Sabbatini, M.L. Hensley, W.P. Tew, N. Pandit-Taskar, E.N. Vander, M.D. Phillips, C. Schweizer, S.C. Weil, S.M. Larson, and L.J. Old Farletuzumab, a humanized monoclonal antibody against folate receptor alpha, in epithelial ovarian cancer: a phase I study Clin. Cancer Res. 16 2010 5288 5295
31. I. Lasry, B. Berman, R. Straussberg, Y. Sofer, H. Bessler, M. Sharkia, F. Glaser, G. Jansen, S. Drori, and Y.G. Assaraf A novel loss-of-function mutation in the proton-coupled folate transporter from a patient with hereditary folate malabsorption reveals that Arg 113 is crucial for function Blood 112 2008 2055 2061
32. C.P. Leamon, M.A. Parker, I.R. Vlahov, L.C. Xu, J.A. Reddy, M. Vetzel, and N. Douglas Synthesis and biological evaluation of EC20: a new folate-derived (99m)Tc-based radiopharmaceutical Bioconjug. Chem. 13 2002 1200 1210
33. C.P. Leamon, J.A. Reddy, A. Bloomfield, R. Dorton, M. Nelson, P.J. Klein, I.R. Vlahov, and M. Vetzel Predicting response to EC145 therapy using the folate receptor-specific radiodiagnostic imaging agent, 99mTc-EC20 Cancer Res. 72 8 (Suppl. 1) 2012 3622
34. P.Y. Li, V.S. Del, R. Fonti, M.V. Carriero, M.I. Potena, G. Botti, S. Miotti, S. Lastoria, S. Menard, M.I. Colnaghi, and M. Salvatore Local concentration of folate binding protein GP38 in sections of human ovarian carcinoma by in vitro quantitative autoradiography J. Nucl. Med. 37 1996 665 672
35. Y.D. Livney, and Y.G. Assaraf Rationally designed nanovehicles to overcome cancer chemoresistance Adv. Drug Deliv. Rev. 65 2013 1716 1730
36. L.H. Matherly, M.R. Wilson, and Z. Hou The major facilitative folate transporters solute carrier 19A1 and solute carrier 46A1: biology and role in antifolate chemotherapy of cancer Drug Metab. Dispos. 42 2014 632 649
37. J. Mendelsohn Personalizing oncology: perspectives and prospects J. Clin. Oncol. 31 2013 1904 1911
38. R. Morris, R.N. Joyrich, R.W. Naumann, N.P. Shah, A.H. Mauer, H.W. Strauss, J.M. Uszler, J.T. Symanowski, P.R. Ellis, and W.A. Harb Phase II study of treatment of advanced ovarian cancer with folate-receptor-targeted therapeutic (vintafolide) and companion SPECT-based imaging agent (99mTc-etarfolatide) Ann. Oncol. 25 2014 852 858
39. C. Muller Folate based radiopharmaceuticals for imaging and therapy of cancer and inflammation Curr. Pharm. Des. 18 2012 1058 1083
40. R.W. Naumann, R.L. Coleman, R.A. Burger, E.A. Sausville, E. Kutarska, S.A. Ghamande, N.Y. Gabrail, S.E. DePasquale, E. Nowara, L. Gilbert, R.H. Gersh, M.G. Teneriello, W.A. Harb, P.A. Konstantinopoulos, R.T. Penson, J.T. Symanowski, C.D. Lovejoy, C.P. Leamon, D.E. Morgenstern, and R.A. Messmann PRECEDENT: a randomized phase II trial comparing vintafolide (EC145) and pegylated liposomal doxorubicin (PLD) in combination versus PLD alone in patients with platinum-resistant ovarian cancer J. Clin. Oncol. 31 2013 4400 4406
41. M.I. Nunez, C. Behrens, D.M. Woods, H. Lin, M. Suraokar, H. Kadara, W. Hofstetter, N. Kalhor, J.J. Lee, W. Franklin, D.J. Stewart, and I.I. Wistuba High expression of folate receptor alpha in lung cancer correlates with adenocarcinoma histology and EGFR [corrected] mutation J. Thorac. Oncol. 7 2012 833 840
42. D.J. O'Shannessy, E.B. Somers, E. Albone, X. Cheng, Y.C. Park, B.E. Tomkowicz, Y. Hamuro, T.O. Kohl, T.M. Forsyth, R. Smale, Y.S. Fu, and N.C. Nicolaides Characterization of the human folate receptor alpha via novel antibody-based probes Oncotarget 2 2011 1227 1243
43. D.J. O'Shannessy, E.B. Somers, L.M. Palmer, R.P. Thiel, P. Oberoi, R. Heath, and L. Marcucci Serum folate receptor alpha, mesothelin and megakaryocyte potentiating factor in ovarian cancer: association to disease stage and grade and comparison to CA125 and HE4 J. Ovarian Res. 6 2013 29
44. O. Ab, L.M. Bartle, L. Rui, J. Coccia, H.A. Johnson, K.R. Whiteman, B. Kellogg, L. Clancy, X. Sun, and V.S. Goldmacher IMGN853, an anti-folate receptor I antibody-maytansinoid conjugate for targeted cancer therapy Cancer Res. 71 8 (Suppl. 1) 2011 4576
45. N. Parker, M.J. Turk, E. Westrick, J.D. Lewis, P.S. Low, and C.P. Leamon Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay Anal. Biochem. 338 2005 284 293
46. P. Pribble, and M.J. Edelman EC145: a novel targeted agent for adenocarcinoma of the lung Expert Opin. Investig. Drugs 21 2012 755 761
47. A. Qiu, M. Jansen, A. Sakaris, S.H. Min, S. Chattopadhyay, E. Tsai, C. Sandoval, R. Zhao, M.H. Akabas, and I.D. Goldman Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption Cell 127 2006 917 928
48. J.A. Reddy, R. Dorton, E. Westrick, A. Dawson, T. Smith, L.C. Xu, M. Vetzel, P. Kleindl, I.R. Vlahov, and C.P. Leamon Preclinical evaluation of EC145, a folate-vinca alkaloid conjugate Cancer Res. 67 2007 4434 4442
49. J.A. Reddy, L.C. Xu, N. Parker, M. Vetzel, and C.P. Leamon Preclinical evaluation of (99m)Tc-EC20 for imaging folate receptor-positive tumors J. Nucl. Med. 45 2004 857 866
50. J.F. Ross, P.K. Chaudhuri, and M. Ratnam Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines. Physiologic and clinical implications Cancer 73 1994 2432 2443
51. M.D. Salazar, and M. Ratnam The folate receptor: what does it promise in tissue-targeted therapeutics? Cancer Metastasis Rev. 26 2007 141 152
52. E.I. Sega, and P.S. Low Tumor detection using folate receptor-targeted imaging agents Cancer Metastasis Rev. 27 2008 655 664
53. J. Shia, D.S. Klimstra, J.R. Nitzkorski, P.S. Low, M. Gonen, R. Landmann, M.R. Weiser, W.A. Franklin, F.G. Prendergast, L. Murphy, L.H. Tang, L. Temple, J.G. Guillem, W.D. Wong, and P.B. Paty Immunohistochemical expression of folate receptor alpha in colorectal carcinoma: patterns and biological significance Hum. Pathol. 39 2008 498 505
54. D. Sia, C. Alsinet, P. Newell, and A. Villanueva VEGF signaling in cancer treatment Curr. Pharm. Des. 20 2013 2834 2842
55. M.K. Siu, D.S. Kong, H.Y. Chan, E.S. Wong, P.P. Ip, L. Jiang, H.Y. Ngan, X.F. Le, and A.N. Cheung Paradoxical impact of two folate receptors, FRalpha and RFC, in ovarian cancer: effect on cell proliferation, invasion and clinical outcome PLOS ONE 7 2012 e47201
56. R. Straussman, T. Morikawa, K. Shee, M. Barzily-Rokni, Z.R. Qian, J. Du, A. Davis, M.M. Mongare, J. Gould, D.T. Frederick, Z.A. Cooper, P.B. Chapman, D.B. Solit, A. Ribas, R.S. Lo, K.T. Flaherty, S. Ogino, J.A. Wargo, and T.R. Golub Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion Nature 487 2012 500 504
57. L. Teng, J. Xie, L. Teng, and R.J. Lee Clinical translation of folate receptor-targeted therapeutics Expert Opin. Drug Deliv. 9 2012 901 908
58. A. Thomas, J. Maltzman, and R. Hassan Farletuzumab in lung cancer Lung Cancer 80 2013 15 18
59. G. Toffoli, C. Cernigoi, A. Russo, A. Gallo, M. Bagnoli, and M. Boiocchi Overexpression of folate binding protein in ovarian cancers Int. J. Cancer 74 1997 193 198
60. G. Toffoli, A. Russo, A. Gallo, C. Cernigoi, S. Miotti, R. Sorio, S. Tumolo, and M. Boiocchi Expression of folate binding protein as a prognostic factor for response to platinum-containing chemotherapy and survival in human ovarian cancer Int. J. Cancer 79 1998 121 126
61. M. Vanneman, and G. Dranoff Combining immunotherapy and targeted therapies in cancer treatment Nat. Rev. Cancer 12 2012 237 251
62. R. Veggian, S. Fasolato, S. Menard, D. Minucci, P. Pizzetti, M. Regazzoni, E. Tagliabue, and M.I. Colnaghi Immunohistochemical reactivity of a monoclonal antibody prepared against human ovarian carcinoma on normal and pathological female genital tissues Tumori 75 1989 510 513
63. C.L. Walters, R.C. Arend, D.K. Armstrong, R.W. Naumann, and R.D. Alvarez Folate and folate receptor alpha antagonists mechanism of action in ovarian cancer Gynecol. Oncol. 131 2013 493 498
64. S.D. Weitman, R.H. Lark, L.R. Coney, D.W. Fort, V. Frasca, V.R. Zurawski Jr., and B.A. Kamen Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues Cancer Res. 52 1992 3396 3401
65. A.S. Wibowo, M. Singh, K.M. Reeder, J.J. Carter, A.R. Kovach, W. Meng, M. Ratnam, F. Zhang, and C.E. Dann 3rd Structures of human folate receptors reveal biological trafficking states and diversity in folate and antifolate recognition Proc. Natl. Acad. Sci. U. S. A. 110 2013 15180 15188
66. A.C. Wolff, M.E. Hammond, J.N. Schwartz, K.L. Hagerty, D.C. Allred, R.J. Cote, M. Dowsett, P.L. Fitzgibbons, W.M. Hanna, A. Langer, L.M. McShane, S. Paik, M.D. Pegram, E.A. Perez, M.F. Press, A. Rhodes, C. Sturgeon, S.E. Taube, R. Tubbs, G.H. Vance, M. van de Vijver, T.M. Wheeler, and D.F. Hayes American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer Arch. Pathol. Lab. Med. 131 2007 18 43
67. R. Zhao, and I.D. Goldman The proton-coupled folate transporter: physiological and pharmacological roles Curr. Opin. Pharmacol. 13 2013 875 880
68. R. Zhao, S.H. Min, A. Qiu, A. Sakaris, G.L. Goldberg, C. Sandoval, J.J. Malatack, D.S. Rosenblatt, and I.D. Goldman The spectrum of mutations in the PCFT gene, coding for an intestinal folate transporter, that are the basis for hereditary folate malabsorption Blood 110 2007 1147 1152