The nitric oxide prodrug JS-K and its structural analogues as cancer therapeutic agents

Anti-Cancer Agents in Medicinal Chemistry

Volumn 9, Issue 7, 2009, Pages 798-803

  Maciag, Anna E ^a   Saavedra, Joseph E ^a   Chakrapani, Harinath ^b  

^a SAIC FREDERICK INC   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; GLUTATHIONE TRANSFERASE; NITRIC OXIDE; O (2,4 DINITROPHENYL) 1 [(4 ETHOXYCARBONYL)PIPERAZIN 1 YL]DIAZEN 1 IUM 1,2 DIOLATE; O (2,4 DINITROPHENYL) 1 [(4 ETHOXYCARBONYL)PIPERAZIN 1 YL]DIAZEN 1 IUM 1,2 DIOLATE DERIVATIVE; O [2,4 DINITRO 5 [4 (N METHYLAMINO)BENZOYLOXY]PHENYL] 1 (N,N DIMETHYLAMINO)DIAZEN 1 IUM 1,2 DIOLATE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER INHIBITION; CANCER THERAPY; CELL MEMBRANE PERMEABILITY; CHEMICAL MODIFICATION; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG RESEARCH; DRUG SCREENING; DRUG STRUCTURE; HUMAN; LEUKEMIA; NONHUMAN; OVARY CANCER; PROSTATE CARCINOMA; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTINEOPLASTIC AGENTS; AZO COMPOUNDS; CELL PROLIFERATION; HUMANS; MOLECULAR CONFORMATION; NEOPLASMS; NITRIC OXIDE DONORS; PIPERAZINES; PRODRUGS;

EID: 73449128278     PISSN: 18715206     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152009789056949     Document Type: Review

References (35)

1. Shami, P. J.; Saavedra, J. E.; Wang, L. Y.; Bonifant, C. L.; Diwan, B. A.; Singh, S. V.; Gu, Y. J.; Fox, S. D.; Buzard, G. S.; Citro, M. L.; Waterhouse, D. J.; Davies, K. M.; Ji, X.; Keefer, L. K. JS-K, a glutathione/glutathione S-transferase-activated nitric oxide donor of the diazeniumdiolate class with potent antineoplastic activity. Mol. Cancer Ther., 2003, 2(4), 409-417.
2. Ren, Z. G.; Kar, S.; Wang, Z. Q.; Wang, M. F.; Saavedra, J. E.; Carr, B. I. JS-K, a novel non-ionic diazeniumdiolate derivative, inhibits Hep 3B hepatoma cell growth and induces c-Jun phosphorylation via multiple MAP kinase pathways. J. Cell. Physiol., 2003, 197(3), 426-434.
3. Liu, J.; Li, C. X.; Qu, W.; Leslie, E.; Bonifant, C. L.; Buzard, G. S.; Saavedra, J. E.; Keefer, L. K.; Waalkes, M. P. Nitric oxide prodrugs and metallochemotherapeutics: JS-K and CB-3-100 enhance arsenic and cisplatin cytolethality by increasing cellular accumulation. Mol. Cancer Ther., 2004, 3(6), 709-714.
4. Shami, P. J.; Saavedra, J. E.; Bonifant, C. L.; Chu, J. X.; Udupi, V.; Malaviya, S.; Carr, B. I.; Kar, S.; Wang, M. F.; Jia, L.; Ji, X. H.; Keefer, L. K. Antitumor activity of JS-K [O2-(2,4-dinitrophenyl) 1-[(4-ethoxycarbonyl) piperazin-1-yl]diazen-1-ium-1,2-diolate] and related O2-aryl diazeniumdiolates in vitro and in vivo. J. Med. Chem., 2006, 49(14), 4356-4366.
5. Udupi, V.; Yu, M.; Malaviya, S.; Saavedra, J. E.; Shami, P. J. JSK, a nitric oxide prodrug, induces cytochrome c release and caspase activation in HL-60 myeloid leukemia cells. Leuk. Res., 2006, 30(10), 1279-1283.
6. Kiziltepe, T.; Hideshima, T.; Ishitsuka, K.; Ocio, E. M.; Raje, N.; Catley, L.; Li, C. Q.; Trudel, L. J.; Yasui, H.; Vallet, S.; Kutok, J. L.; Chauhan, D.; Mitsiades, C. S.; Saavedra, J. E.; Wogan, G. N.; Keefers, L. K.; Shami, P. J.; Anderson, K. C. JS-K, a GSTactivated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood, 2007, 110(13), 709-718.
7. Chakrapani, H.; Goodblatt, M. M.; Udupi, V.; Malaviya, S.; Shami, P. J.; Keefer, L. K.; Saavedra, J. E. Synthesis and in vitro antileukemic activity of structural analogues of JS-K, an anti-cancer lead compound. Bioorg. Med. Chem. Lett., 2008, 18(3), 950-953.
8. Chakrapani, H.; Kalathur, R. C.; Maciag, A. E.; Citro, M. L.; Ji, X. H.; Keefer, L. K.; Saavedra, J. E. Synthesis, mechanistic studies, and anti-proliferative activity of glutathione/glutathione Stransferase-activated nitric oxide prodrugs. Bioorg. Med. Chem., 2008, 16(22), 9764-9771.
9. Kitagaki, J.; Yang, Y.; Saavedra, J. E.; Colburn, N. H.; Keefer, L. K.; Perantoni, A. O. Nitric oxide prodrug JS-K inhibits ubiquitin E1 and kills tumor cells retaining wild-type p53. Oncogene, 2009, 28(4), 619-624.
10. Simeone, A. M.; McMurtry, V.; Nieves-Alicea, R.; Saavedra, J. E.; Keefer, L. K.; Johnson, M. M.; Tari, A. M. TIMP-2 mediates the anti-invasive effects of the nitric oxide-releasing prodrug JS-K in breast cancer cells. Breast Cancer Res., 2008, 10, R44.
11. Shami, P. J.; Maciag, A. E.; Eddington, J. K.; Udupi, V.; Kosak, K. M.; Saavedra, J. E.; Keefer, L. K. JS-K, an arylating nitric oxide (NO) donor, has synergistic anti-leukemic activity with cytarabine (ARA-C). Leukemia Res., 2009, [Epub ahead of print]
12. Nandurdikar, R. S.; Maciag, A. E.; Citro, M. L.; Shami, P. J.; Keefer, L. K.; Saavedra, J. E.; Chakrapani, H. Synthesis and evaluation of piperazine and homopiperazine analogues of JS-K, an anti-cancer lead compound. Bioorg. Med. Chem. Lett., 2009, 19(10), 2760-2762.
13. Keefer, L. K. Nitric oxide (NO)- and nitroxyl (HNO)-generating diazeniumdiolates (NONOates): emerging commercial opportunities. Curr. Med. Chem., 2005, 5(7), 625-636.
14. Keefer, L. K. Progress toward clinical application of the nitric oxide-releasing diazeniumdiolates. Ann. Rev. Pharmacol. Toxicol., 2003, 43, 585-607.
15. Hrabie, J. A.; Keefer, L. K. Chemistry of the nitric oxide-releasing diazeniumdiolate ("nitrosohydroxylamine") functional group and its oxygen-substituted derivatives. Chem. Rev., 2002, 102(4), 1135-1154.
16. Armstrong, R. N. Glutathione S-transferases: reaction mechanism, structure, and function. Chem. Res. Toxicol., 1991, 4(2), 131-140.
17. Armstrong, R. N. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol., 1997, 10(1), 2-18.
18. Drago, R. S.; Karstetter, B. R. The reaction of nitrogen(II) oxide with various primary and secondary amines J. Am. Chem. Soc., 1961, 83(8), 1819-1822.
19. Drago, R. S.; Paulik, F. E. The reaction of nitrogen(II) oxide with diethylamine J. Am. Chem. Soc., 1960, 82(1), 96-98.
20. Saavedra, J. E.; Dunams, T. M.; Flippen-Anderson, J. L.; Keefer, L.K. Secondary amine nitric-oxide complex-ions, R2N[N(O) NO] - O-functionalization chemistry J. Org. Chem., 1992, 57(23), 6134-6138.
21. Ridnour, L. A.; Thomas, D. D.; Donzelli, S.; Espey, M. G.; Roberts, D. D.; Wink, D. A.; Isenberg, J. S. The biphasic nature of nitric oxide responses in tumor biology. Antioxidants Redox Signal., 2006, 8(7), 1329-1337.
22. Thomas, D. D.; Ridnour, L. A.; Isenberg, J. S.; Flores-Santana, W.; Switzer, C. H.; Donzelli, S.; Hussain, P.; Vecoli, C.; Paolocci, N.; Ambs, S.; Colton, C. A.; Harris, C. C.; Roberts, D. D.; Wink, D. A. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic. Biol. Med., 2008, 45(1), 18-31.
23. Ridnour, L. A.; Thomas, D. D.; Switzer, C.; Flores-Santana, W.; Isenberg, J. S.; Ambs, S.; Roberts, D. D.; Wink, D. A. Molecular mechanisms for discrete nitric oxide levels in cancer. Nitric Oxide Biol. Chem., 2008, 19(2), 73-76.
24. Wolf, D.; Rotter, V. Major deletions in the gene encoding the p53 tumor antigen cause lack of p53 expression in HL-60 cells. Proc. Natl. Acad. Sci. USA, 1985, 82(3), 790-794.
25. Waxman, S.; Anderson, K. C. History of the development of arsenic derivatives in cancer therapy. Oncologist, 2001, 6(Suppl 2), 3-10.
26. Chakrapani, H.; Maciag, A. E.; Citro, M. L.; Keefer, L. K.; Saavedra, J. E. Cell-permeable esters of diazeniumdiolate-based nitric oxide prodrugs. Org. Lett., 2008, 10(22), 5155-5158.
27. Wardman, P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic. Biol. Med., 2007, 43(7), 995-1022.
28. Findlay, V. J.; Townsend, D. M.; Saavedra, J. E.; Buzard, G. S.; Citro, M. L.; Keefer, L. K.; Ji, X.; Tew, K. D. Tumor cell responses to a novel glutathione S-transferase-activated nitric oxide-releasing prodrug. Mol. Pharmacol., 2004, 65(5), 1070-1079.
29. Townsend D. M.; Findlay, V. L.; Tew, K. D. Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods Enzymol., 2005, 401, 287-307.
30. Saavedra, J. E.; Srinivasan, A.; Buzard, G. S.; Davies, K. M.; Waterhouse, D. J.; Inami, K.; Wilde, T. C.; Citro, M. L.; Cuellar, M.; Deschamps, J. R.; Parrish, D.; Shami, P. J.; Findlay, V. J.; Townsend, D. M.; Tew, K. D.; Singh, S.; Jia, L.; Ji, X.; Keefer, L. K. PABA/NO as an anticancer lead: analogue synthesis, structure revision, solution chemistry, reactivity toward glutathione, and in vitro activity. J. Med. Chem., 2006, 49(3), 1157-1164.
31. Townsend, D. M.; Findlay, V. J.; Fazilev, F.; Ogle, M.; Fraser, J. P.; Saavedra, J. E.; Ji, X.; Keefer, L. K.; Tew, K. D. A glutathione S-transferase pi-activated prodrug causes kinase activation concurrent with S-glutathionylation of proteins. Mol. Pharmacol., 2006, 69(2), 501-508.
32. Findlay, V. J.; Townsend, D. M.; Morris, T. E.; Fraser, J. P.; He, L.; Tew, K. D. A novel role for human sulfiredoxin in the reversal of glutathionylation. Cancer Res., 2006, 66(13), 6800-6806.
33. Townsend, D. M.; Manevich, Y.; He, L.; Hutchens, S.; Pazoles, C. J.; Tew, K. D. Novel role for glutathione S-transferase pi. Regulator of protein S-Glutathionylation following oxidative and nitrosative stress. J. Biol. Chem., 2009, 284(1), 436-445.
34. Chakrapani, H.; Wilde, T. C.; Citro, M. L.; Goodblatt, M. G.; Keefer, L. K.; Saavedra, J. E. Synthesis, nitric oxide release, and anti-leukemic activity of glutathione-activated nitric oxide prodrugs: Structural analogues of PABA/NO, an anti-cancer lead compound. Bioorg. Med. Chem., 2008, 16(5), 2657-2664.
35. Andrei, D. A.; Maciag, A. E.; Chakrapani, H.; Citro, M. L.; Keefer, L. K.; Saavedra, J. E. Aryl bis(diazeniumdiolates): potent inducers of S-glutathionylation of cellular proteins and their in vitro antiproliferative activities. J. Med. Chem., 2008, 51(24), 7944-7952.