Targeted inhibition of prostate cancer metastases with an RNA aptamer to prostate-specific membrane antigen

Molecular Therapy

Volumn 22, Issue 11, 2014, Pages 1910-1922

  Dassie, Justin P ^a   Hernandez, Luiza I ^a   Thomas, Gregory S ^a   Long, Matthew E ^b   Rockey, William M ^a   Howell, Craig A ^a   Chen, Yani ^a   Hernandez, Frank J ^a   Liu, Xiu Ying ^a   Wilson, Mary E ^a,b   Allen, Lee Ann ^a,b   Vaena, Daniel A ^a   Meyerholz, David K ^a   Giangrande, Paloma H ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; PROSTATE SPECIFIC MEMBRANE ANTIGEN; RNA; A9G RNA APTAMER; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMATE CARBOXYPEPTIDASE II, HUMAN; MEMBRANE ANTIGEN;

ADVANCED CANCER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER STAGING; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG SAFETY; DRUG SPECIFICITY; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VIVO STUDY; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL; RNA ANALYSIS; RNA TRANSLATION; ANIMAL; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; METABOLISM; METASTASIS; MOLECULARLY TARGETED THERAPY; PROCEDURES; PROSTATIC NEOPLASMS; TUMOR CELL LINE;

ANIMALS; ANTIGENS, SURFACE; APTAMERS, NUCLEOTIDE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GLUTAMATE CARBOXYPEPTIDASE II; HUMANS; MALE; MICE; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84964313160     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.117     Document Type: Article

References (50)

1. Cereda, V, Formica, V, Massimiani, G, Tosetto, L and Roselli, M (2014). Targeting metastatic castration-resistant prostate cancer: Mechanisms of progression and novel early therapeutic approaches. Expert Opin Investig Drugs 23: 469-487.
2. Pal, SK, Twardowski, P and Sartor, O (2010). Critical appraisal of cabazitaxel in the management of advanced prostate cancer. Clin Interv Aging 5: 395-402.
3. Shah, N and Dizon, DS (2009). New-generation platinum agents for solid tumors. Future Oncol 5: 33-42.
4. Ghosh, A and Heston, WD (2004). Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J Cell Biochem 91: 528-539.
5. Israeli, RS, Powell, CT, Corr, JG, Fair, WR and Heston, WD (1994). Expression of the prostate-specific membrane antigen. Cancer Res 54: 1807-1811.
6. Sweat, SD, Pacelli, A, Murphy, GP and Bostwick, DG (1998). Prostate-specific membrane antigen expression is greatest in prostate adenocarcinoma and lymph node metastases. Urology 52: 637-640.
7. Mlcochová, P, Barinka, C, Tykvart, J, Sácha, P and Konvalinka, J (2009). Prostatespecific membrane antigen and its truncated form PSM'. Prostate 69: 471-479.
8. Schmittgen, TD, Teske, S, Vessella, RL, True, LD and Zakrajsek, BA (2003). Expression of prostate specific membrane antigen and three alternatively spliced variants of PSMA in prostate cancer patients. Int J Cancer 107: 323-329.
9. Silver, DA, Pellicer, I, Fair, WR, Heston, WD and Cordon-Cardo, C (1997). Prostatespecific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 3: 81-85.
10. Wright, GL Jr, Grob, BM, Haley, C, Grossman, K, Newhall, K, Petrylak, D et al. (1996). Upregulation of prostate-specific membrane antigen after androgen-deprivation therapy. Urology 48: 326-334.
11. Yates, DR, Rouprêt, M, Drouin, SJ, Comperat, E, Ricci, S, Lacave, R et al. (2012). Quantitative RT-PCR analysis of PSA and prostate-specific membrane antigen mRNA to detect circulating tumor cells improves recurrence-free survival nomogram prediction after radical prostatectomy. Prostate 72: 1382-1388.
12. Chang, SS, O'Keefe, DS, Bacich, DJ, Reuter, VE, Heston, WD and Gaudin, PB (1999). Prostate-specific membrane antigen is produced in tumor-associated neovasculature. Clin Cancer Res 5: 2674-2681.
13. Chang, SS, Reuter, VE, Heston, WD, Bander, NH, Grauer, LS and Gaudin, PB (1999). Five different anti-prostate-specific membrane antigen (PSMA) antibodies confirm PSMA expression in tumor-associated neovasculature. Cancer Res 59: 3192-3198.
14. Elsässer-Beile, U, Bühler, P and Wolf, P (2009). Targeted therapies for prostate cancer against the prostate specific membrane antigen. Curr Drug Targets 10: 118-125.
15. Olson, WC and Israel, RJ (2014). Antibody-drug conjugates targeting prostate-specific membrane antigen. Front Biosci (Landmark Ed) 19: 12-33.
16. McNamara JO, 2nd, Andrechek ER, Wang Y, Viles KD, Rempel RE, Gilboa E et al. (2006). Cell type-specific delivery of sirnas with aptamer-sirna chimeras. Nat Biotechnol 24: 1005-1015.
17. Pastor, F, Kolonias, D, Giangrande, PH and Gilboa, E (2010). Induction of tumour immunity by targeted inhibition of nonsense-mediated mRNA decay. Nature 465: 227-230.
18. Dassie, JP, Liu, XY, Thomas, GS, Whitaker, RM, Thiel, KW, Stockdale, KR et al. (2009). Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat Biotechnol 27: 839-849.
19. Ni, X, Zhang, Y, Ribas, J, Chowdhury, WH, Castanares, M, Zhang, Z et al. (2011). Prostate-targeted radiosensitization via aptamer-shRNA chimeras in human tumor xenografts. J Clin Invest 121: 2383-2390.
20. Pinto, JT, Suffoletto, BP, Berzin, TM, Qiao, CH, Lin, S, Tong, WP et al. (1996). Prostatespecific membrane antigen: A novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res 2: 1445-1451.
21. Carter, RE, Feldman, AR and Coyle, JT (1996). Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci USA 93: 749-753.
22. Lapidus, RG, Tiffany, CW, Isaacs, JT and Slusher, BS (2000). Prostate-specific membrane antigen (PSMA) enzyme activity is elevated in prostate cancer cells. Prostate 45: 350-354.
23. Yao, V, Berkman, CE, Choi, JK, O'Keefe, DS and Bacich, DJ (2010). Expression of prostate-specific membrane antigen (PSMA), increases cell folate uptake and proliferation and suggests a novel role for PSMA in the uptake of the nonpolyglutamated folate, folic acid. Prostate 70: 305-316.
24. Conway, RE, Petrovic, N, Li, Z, Heston, W, Wu, D and Shapiro, LH (2006). Prostatespecific membrane antigen regulates angiogenesis by modulating integrin signal transduction. Mol Cell Biol 26: 5310-5324.
25. Rockey, WM, Hernandez, FJ, Huang, SY, Cao, S, Howell, CA, Thomas, GS et al. (2011). Rational truncation of an RNA aptamer to prostate-specific membrane antigen using computational structural modeling. Nucleic Acid Ther 21: 299-314.
26. Lupold, SE, Hicke, BJ, Lin, Y and Coffey, DS (2002). Identification and characterization of nuclease-stabilized RNA molecules that bind human prostate cancer cells via the prostate-specific membrane antigen. Cancer Res 62: 4029-4033.
27. Keefe, AD, Pai, S and Ellington, A (2010). Aptamers as therapeutics. Nat Rev Drug Discov 9: 537-550.
28. Yao, V, Parwani, A, Maier, C, Heston, WD and Bacich, DJ (2008). Moderate expression of prostate-specific membrane antigen, a tissue differentiation antigen and folate hydrolase, facilitates prostate carcinogenesis. Cancer Res 68: 9070-9077.
29. Herlich, JA, Taggart, P, Proctor, J, Stahle, P, Colis, R, Hall, L et al. (2009). The non-GLP toleration/dose range finding study: Design and methodology used in an early toxicology screening program. Proc West Pharmacol Soc 52: 94-98.
30. Robbins, M, Judge, A and MacLachlan, I (2009). siRNA and innate immunity. Oligonucleotides 19: 89-102.
31. Behlke, MA (2006). Progress towards in vivo use of siRNAs. Mol Ther 13: 644-670.
32. Adams, KE, Ke, S, Kwon, S, Liang, F, Fan, Z, Lu, Y et al. (2007). Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer. J Biomed Opt 12: 024017.
33. Iyer, AK, Khaled, G, Fang, J and Maeda, H (2006). Exploiting the enhanced permeability and retention effect for tumor targeting. Drug Discov Today 11: 812-818.
34. McLean, GW, Carragher, NO, Avizienyte, E, Evans, J, Brunton, VG and Frame, MC (2005). The role of focal-adhesion kinase in cancer -A new therapeutic opportunity. Nat Rev Cancer 5: 505-515.
35. Dienstmann, R, Markman, B and Tabernero, J (2012). Application of monoclonal antibodies as cancer therapy in solid tumors. Curr Clin Pharmacol 7: 137-145.
36. Larsen, PB, Kümler, I and Nielsen, DL (2013). A systematic review of trastuzumab and lapatinib in the treatment of women with brain metastases from HER2-positive breast cancer. Cancer Treat Rev 39: 720-727.
37. Thanopoulou, E and Judson, I (2012). The safety profile of imatinib in CML and GIST: Long-term considerations. Arch Toxicol 86: 1-12.
38. Thiel, KW and Giangrande, PH (2009). Therapeutic applications of DNA and RNA aptamers. Oligonucleotides 19: 209-222.
39. Liu, Y, Kuan, CT, Mi, J, Zhang, X, Clary, BM, Bigner, DD et al. (2009). Aptamers selected against the unglycosylated EGFRvIII ectodomain and delivered intracellularly reduce membrane-bound EGFRvIII and induce apoptosis. Biol Chem 390: 137-144.
40. Sun, W, Du, L and Li, M (2011). Advances and perspectives in cell-specific aptamers. Curr Pharm Des 17: 80-91.
41. Dassie, JP and Giangrande, PH (2013). Current progress on aptamer-targeted oligonucleotide therapeutics. Ther Deliv 4: 1527-1546.
42. Rockey, WM, Huang, L, Kloepping, KC, Baumhover, NJ, Giangrande, PH and Schultz, MK (2011). Synthesis and radiolabeling of chelator-RNA aptamer bioconjugates with copper-64 for targeted molecular imaging. Bioorg Med Chem 19: 4080-4090.
43. Seth, S, Johns, R and Templin, MV (2012). Delivery and biodistribution of siRNA for cancer therapy: Challenges and future prospects. Ther Deliv 3: 245-261.
44. Ifediba, MA and Moore, A (2012). In vivo imaging of the systemic delivery of small interfering RNA. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4: 428-437.
45. Huang, Y, Eckstein, F, Padilla, R and Sousa, R (1997). Mechanism of ribose 2'-group discrimination by an RNA polymerase. Biochemistry 36: 8231-8242.
46. Tiffany, CW and Slusher, BS (2002). Measurement of glutamate carboxypeptidase II (NAALADase) enzyme activity by the hydrolysis of [H]-N-acetylaspartylglutamate (NAAG). Curr Protoc Pharmacol Chapter 3: Unit3.10.
47. Drake, JM, Gabriel, CL and Henry, MD (2005). Assessing tumor growth and distribution in a model of prostate cancer metastasis using bioluminescence imaging. Clin Exp Metastasis 22: 674-684.
48. Freshney RI (1994). Culture of Animal Cells: A Manual of Basic Technique. Wiley-Liss: New York.
49. Franken, NA, Rodermond, HM, Stap, J, Haveman, J and van Bree, C (2006). Clonogenic assay of cells in vitro. Nat Protoc 1: 2315-2319.
50. Freshney, NW, Rawlinson, L, Guesdon, F, Jones, E, Cowley, S, Hsuan, J et al. (1994). Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell 78: 1039-1049.