Combination of the PI3K inhibitor ZSTK474 with a PSMA-targeted immunotoxin accelerates apoptosis and regression of prostate cancer

Neoplasia (United States)

Volumn 15, Issue 10, 2013, Pages 1172-1183

  Baiz, Daniele ^a   Hassan, Sazzad ^a   Choi, Young A ^a   Flores, Anabel ^a   Karpova, Yelena ^a   Yancey, Dana ^a   Pullikuth, Ashok ^a   Sui, Guangchao ^a   Sadelain, Michel ^b   Debinski, Waldemar ^a   Kulik, George ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 DIFLUOROMETHYLBENZIMIDAZOL 1 YL) 4, 6 DIMORPHOLINO 1, 3, 5 TRIAZINE; 2 (2 DIFLUOROMETHYLBENZIMIDAZOL 1 YL) 4,6 DIMORPHOLINO 1,3,5 TRIAZINE; CASPASE 3; IMMUNOTOXIN; J591PE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PROSTATE SPECIFIC MEMBRANE ANTIGEN; PROTEIN BAD; PROTEIN KINASE B; PROTEIN MCL 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER REGRESSION; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LABELING INDEX; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; PSEUDOMONAS AERUGINOSA; TIME-LAPSE VIDEO MICROSCOPY; WESTERN BLOTTING;

ADP RIBOSE TRANSFERASES; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, SURFACE; APOPTOSIS; BACTERIAL TOXINS; CELL LINE, TUMOR; EXOTOXINS; GLUTAMATE CARBOXYPEPTIDASE II; HETEROGRAFTS; HUMANS; IMMUNOTOXINS; MALE; MICE, INBRED BALB C; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PHOSPHATIDYLINOSITOL 3-KINASE; PROSTATIC NEOPLASMS; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; TRIAZINES; VIRULENCE FACTORS;

EID: 84887055147     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.13986     Document Type: Article

References (59)

1. Feldman BJ and Feldman D (2001). The development of androgen-independent prostate cancer. Nat Rev Cancer 1, 34-45.
2. Toren PJ and Gleave ME (2013). Evolving landscape and novel treatments in metastatic castrate-resistant prostate cancer. Asian J Androl 15, 342-349.
3. Zhang TY, Agarwal N, Sonpavde G, DiLorenzo G, Bellmunt J, and Vogelzang NJ (2013). Management of castrate resistant prostate cancer-recent advances and optimal sequence of treatments. Curr Urol Rep 14(3), 174-183.
4. Morgan TM, Koreckij TD, and Corey E (2009). Targeted therapy for advanced prostate cancer: inhibition of the PI3K/Akt/mTOR pathway. Curr Cancer Drug Targets 9, 237-249.
5. McMenamin ME, Soung P, Perera S, Kaplan I, Loda M, and Sellers WR (1999). Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res 59, 4291-4296.
6. Lotan TL, Gurel B, Sutcliffe S, Esopi D, Liu W, Xu J, Hicks JL, Park BH, Humphreys E, Partin AW, et al. (2011). PTEN protein loss by immunostaining: analytic validation and prognostic indicator for a high risk surgical cohort of prostate cancer patients. Clin Cancer Res 17, 6563-6573.
7. Bitting RL and Armstrong AJ (2013). Targeting the PI3K/Akt/mTOR pathway in castration-resistant prostate cancer. Endocr Relat Cancer 20(3), R83-R99.
8. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, et al. (2010). Integrative genomic profiling of human prostate cancer. Cancer Cell 18, 11-22.
9. Vivanco I and Sawyers CL (2002). The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2, 489-501.
10. Bouali S, Chrétien AS, Ramacci C, Rouyer M, Becuwe P, and Merlin JL (2009). PTEN expression controls cellular response to cetuximab by mediating PI3K/ AKT and RAS/RAF/MAPK downstream signaling in KRAS wild-type, hormone refractory prostate cancer cells. Oncol Rep 21, 731-735.
11. Sarker D, Reid AH, Yap TA, and de Bono JS (2009). Targeting the PI3K/AKT pathway for the treatment of prostate cancer. Clin Cancer Res 15, 4799-4805.
12. Baiz D, Pinder TA, Hassan S, Karpova Y, Salsbury F, Welker ME, and Kulik G (2012). Synthesis and characterization of a novel prostate cancer-targeted phosphatidylinositol-3-kinase inhibitor prodrug. J Med Chem 55, 8038-8046.
13. Yaguchi S, Fukui Y, Koshimizu I, Yoshimi H, Matsuno T, Gouda H, Hirono S, Yamazaki K, and Yamori T (2006). Antitumor activity of ZSTK474, a new phosphatidylinositol 3-kinase inhibitor. J Natl Cancer Inst 98, 545-556.
14. Mueller A, Bachmann E, Linnig M, Khillimberger K, Schimanski CC, Galle PR, and Moehler M (2012). Selective PI3K inhibition by BKM120 and BEZ235 alone or in combination with chemotherapy in wild-type and mutated human gastrointestinal cancer cell lines. Cancer Chemother Pharmacol 69, 1601-1615.
15. Martelli AM, Chiarini F, Evangelisti C, Cappellini A, Buontempo F, Bressanin D, Fini M, and McCubrey JA (2012). Two hits are better than one: targeting both phosphatidylinositol 3-kinase and mammalian target of rapamycin as a therapeutic strategy for acute leukemia treatment. Oncotarget 3, 371-394.
16. Dubrovska A, Elliott J, Salamone RJ, Kim S, Aimone LJ, Walker JR, Watson J, Sauveur-Michel M, Garcia-Echeverria C, Cho CY, et al. (2010). Combination therapy targeting both tumor-initiating and differentiated cell populations in prostate carcinoma. Clin Cancer Res 16, 5692-5702.
17. Wempe SL, Gamarra-Luques CD, and Telleria CM (2013). Synergistic lethality of mifepristone and LY294002 in ovarian cancer cells. Cancer Growth Metastasis 6, 1-13.
18. Gedaly R, Angulo P, Chen C, Creasy KT, Spear BT, Hundley J, Daily MF, Shah M, and Evers BM (2012). The role of PI3K/mTOR inhibition in combination with sorafenib in hepatocellular carcinoma treatment. Anticancer Res 32, 2531-2536.
19. Posch C, Moslehi H, Feeney L, Green GA, Ebaee A, Feichtenschlager V, Chong K, Peng L, Dimon MT, Phillips T, et al. (2013). Combined targeting of MEK and PI3K/mTOR effector pathways is necessary to effectively inhibit NRAS mutant melanoma in vitro and in vivo. Proc Natl Acad Sci USA 110, 4015-4020.
20. Zhang Y, Guo Z, Du T, Chen J, Wang W, Xu K, Lin T, and Huang H (2013). Prostate specific membrane antigen (PSMA): a novel modulator of p38 for proliferation, migration, and survival in prostate cancer cells. Prostate 73, 835-841.
21. Milowsky MI, Nanus DM, Kostakoglu L, Sheehan CE, Vallabhajosula S, Goldsmith SJ, Ross JS, and Bander NH (2007). Vascular targeted therapy with anti-prostate-specific membrane antigen monoclonal antibody J591 in advanced solid tumors. J Clin Oncol 25, 540-547.
22. 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.
23. Morris MJ, Divgi CR, Pandit-Taskar N, Batraki M, Warren N, Nacca A, SmithJones P, Schwartz L, Kelly WK, Slovin S, et al. (2005). Pilot trial of unlabeled and indium-111-labeled anti-prostate-specific membrane antigen antibody J591 for castrate metastatic prostate cancer. Clin Cancer Res 11, 7454-7461.
24. Kuroda K, Liu H, Kim S, Guo M, Navarro V, and Bander NH (2010). Saporin toxin-conjugated monoclonal antibody targeting prostate-specific membrane antigen has potent anticancer activity. Prostate 70, 1286-1294.
25. Liu T, Nedrow-Byers JR, Hopkins MR, Wu LY, Lee J, Reilly PT, and Berkman CE (2012). Targeting prostate cancer cells with a multivalent PSMA inhibitorguided streptavidin conjugate. Bioorg Med Chem Lett 22, 3931-3934.
26. Osborne JR, Akhtar NH, Vallabhajosula S, Anand A, Deh K, and Tagawa ST (2013). Prostate-specific membrane antigen-based imaging. Urol Oncol 31, 144-154.
27. Tagawa ST, Beltran H, Vallabhajosula S, Goldsmith SJ, Osborne J, Matulich D, Petrillo K, Parmar S, Nanus DM, and Bander NH (2010). Anti-prostatespecific membrane antigen-based radioimmunotherapy for prostate cancer. Cancer 116, 1075-1083.
28. Zhang F, Shan L, Liu Y, Neville D, Woo JH, Chen Y, Korotcov A, Lin S, Huang S, Sridhar R, et al. (2013). An anti-PSMA bivalent immunotoxin exhibits specificity and efficacy for prostate cancer imaging and therapy. Adv Healthc Mater 2, 736-744.
29. Frigerio B, Fracasso G, Luison E, Cingarlini S, Mortarino M, Coliva A, Seregni E, Bombardieri E, Zuccolotto G, Rosato A, et al. (2013). A single-chain fragment against prostate specific membrane antigen as a tool to build theranostic reagents for prostate cancer. Eur J Cancerpii: S0959-8049(13)00087-7. [Epub ahead of print].
30. Debinski W and Pastan I (1994). An immunotoxin with increased activity and homogeneity produced by reducing the number of lysine residues in recombinant Pseudomonas exotoxin. Bioconjug Chem 5, 40-46.
31. Maher J, Brentjens RJ, Gunset G, Rivière I, and Sadelain M (2002). Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCR CD28 receptor. Nat Biotechnol 20, 70-75.
32. Debinski W and Pastan I (1992). Monovalent immunotoxin containing truncated form of Pseudomonas exotoxin as potent antitumor agent. Cancer Res 52, 5379-5385.
33. Debinski W, Karlsson B, Lindholm L, Siegall CB, Willingham MC, FitzGerald D, and Pastan I (1992). Monoclonal antibody C242-Pseudomonas exotoxin A. A specific and potent immunotoxin with antitumor activity on a human colon cancer xenograft in nude mice. J Clin Invest 90, 405-411.
34. Madhankumar AB, Mintz A, and Debinski W (2002). Alanine-scanning mutagenesis of α-helix D segment of interleukin-13 reveals new functionally important residues of the cytokine. J Biol Chem 277, 43194-43205.
35. Smith AJ, Karpova Y, D'Agostino R Jr, Willingham M, and Kulik G (2009). Expression of the Bcl-2 protein BAD promotes prostate cancer growth. PLoS One 4, e6224.
36. Sastry KS, Karpova Y, Prokopovich S, Smith AJ, Essau B, Gersappe A, Carson JP, Weber MJ, Register TC, Chen YQ, et al. (2007). Epinephrine protects cancer cells from apoptosis via activation of cAMP-dependent protein kinase and BAD phosphorylation. J Biol Chem 282, 14094-14100.
37. Sui G and Shi Y (2005). Gene silencing by a DNA vector-based RNAi technology. Methods Mol Biol 309, 205-218.
38. Ross JS, Gray KE, Webb IJ, Gray GS, Rolfe M, Schenkein DP, Nanus DM, Millowsky MI, and Bander NH (2005). Antibody-based therapeutics: focus on prostate cancer. Cancer Metastasis Rev 24, 521-537.
39. Gong MC, Chang SS, Sadelain M, Bander NH, and Heston WD (1999). Prostatespecific membrane antigen (PSMA)-specific monoclonal antibodies in the treatment of prostate and other cancers. Cancer Metastasis Rev 18, 483-490.
40. Akhtar NH, Pail O, Saran A, Tyrell L, and Tagawa ST (2012). Prostate-specific membrane antigen-based therapeutics. Adv Urol 2012, 973820.
41. Liu H, Rajasekaran AK, Moy P, Xia Y, Kim S, Navarro V, Rahmati R, and Bander NH (1998). Constitutive and antibody-induced internalization of prostate-specific membrane antigen. Cancer Res 58, 4055-4060.
42. Hwang J, Fitzgerald DJ, Adhya S, and Pastan I (1987). Functional domains of Pseudomonas exotoxin identified by deletion analysis of the gene expressed in E. coli. Cell 48, 129-136.
43. Sastry KS, Smith AJ, Karpova Y, Datta SR, and Kulik G (2006). Diverse antiapoptotic signaling pathways activated by vasoactive intestinal polypeptide, epidermal growth factor, and phosphatidylinositol 3-kinase in prostate cancer cells converge on BAD. J Biol Chem 281, 20891-20901.
44. Yan J, Xiang J, Lin Y, Ma J, Zhang J, Zhang H, Sun J, Danial NN, Liu J, and Lin A (2013). Inactivation of BAD by IKK inhibits TNFα-induced apoptosis independently of NF-κB activation. Cell 152, 304-315.
45. Lindqvist LM, Vikström I, Chambers JM, McArthur K, Ann AM, Henley KJ, Happo L, Cluse L, Johnstone RW, Roberts AW, et al. (2012). Translation inhibitors induce cell death by multiple mechanisms and Mcl-1 reduction is only a minor contributor. Cell Death Dis 3, e409.
46. Zang C, Eucker J, Liu H, Müller A, Possinger K, and Scholz CW (2012). Concurrent inhibition of PI3-kinase and mTOR induces cell death in diffuse large B cell lymphomas, a mechanism involving down regulation of Mcl-1. Cancer Lett, pii: S0304-3835(12)00660-X. E-pub ahead of print.
47. Mattoo AR and Fitzgerald DJ (2013). Combination treatments with ABT-263 and an immunotoxin produce synergistic killing of ABT-263-resistant small cell lung cancer cell lines. Int J Cancer 132, 978-987.
48. Hassan S, Karpova Y, Baiz D, Yancey D, Pullikuth A, Flores A, Register T, Cline JM, D'Agostino R Jr, Danial N, et al. (2013). Behavioral stress accelerates prostate cancer development in mice. J Clin Invest 123, 874-886.
49. Loriot Y, Massard C, and Fizazi K (2012). Recent developments in treatments targeting castration-resistant prostate cancer bone metastases. Ann Oncol 23(5), 1085-1094.
50. Fizazi KS, Higano CS, Nelson JB, Gleave M, Miller K, Morris T, Nathan FE, McIntosh S, Pemberton K, and Moul JW (2013). Phase III, randomized, placebocontrolled study of docetaxel in combination with zibotentan in patients with metastatic castration-resistant prostate cancer. J Clin Oncol 31(14), 1740-1747.
51. Cohen MB and Rokhlin OW (2009). Mechanisms of prostate cancer cell survival after inhibition of AR expression. J Cell Biochem 106, 363-371.
52. Shuttleworth SJ, Silva FA, Cecil AR, Tomassi CD, Hill TJ, Raynaud FI, Clarke PA, and Workman P (2011). Progress in the preclinical discovery and clinical development of class I and dual class I/IV phosphoinositide 3-kinase (PI3K) inhibitors. Curr Med Chem 18, 2686-2714.
53. Holmes D (2011). Pathway inhibitors approach junction. Nat Rev Drug Discov 10, 563-564.
54. Robert F, Carrier M, Rawe S, Chen S, Lowe S, and Pelletier J (2009). Altering chemosensitivity by modulating translation elongation. PLoS One 4, e5428.
55. Wetzler M and Segal D (2011). Omacetaxine as an anticancer therapeutic: what is old is new again. Curr Pharm Des 17, 59-64.
56. Sastry KS, Karpova Y, and Kulik G (2006). Epidermal growth factor protects prostate cancer cells from apoptosis by inducing BAD phosphorylation via redundant signaling pathways. J Biol Chem 281, 27367-27377.
57. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, and Huang DC (2005). Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17, 393-403.
58. Jackson RS, Placzek W, Fernandez A, Ziaee S, Chu CY, Wei J, Stebbins J, Kitada S, Fritz G, Reed JC, et al. (2012). Sabutoclax, a Mcl-1 antagonist, inhibits tumorigenesis in transgenic mouse and human xenograft models of prostate cancer. Neoplasia 14, 656-665.
59. Rockey WM, Hernandez FJ, Huang SY, Cao S, Howell CA, Thomas GS, Liu XY, Lapteva N, Spencer DM, McNamara JO, et al. (2011). Rational truncation of an RNA aptamer to prostate-specific membrane antigen using computational structural modeling. Nucleic Acid Ther 21, 299-314.