Synthesis and anti-BVDV activity of acridones as new potential antiviral agents

Journal of Medicinal Chemistry

Volumn 49, Issue 8, 2006, Pages 2621-2627

  Tabarrini, Oriana ^a   Manfroni, Giuseppe ^a   Fravolini, Arnaldo ^a   Cecchetti, Violetta ^a   Sabatini, Stefano ^a   De Clercq, Erik ^b   Rozenski, Jef ^b   Canard, Bruno ^c   Dutartre, Hélène ^c   Paeshuyse, Jan ^b   Neyts, Johan ^b  

^a UNIVERSITY OF PERUGIA   (Italy)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 AMINO 1,3 DIHYDROXY 10 METHYL 6 [4 (2 PYRIDINYL) 1 PIPERAZINYL] 9(10H) ACRIDINONE; ACRIDONE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BOVINE DIARRHEA VIRUS; CATTLE DISEASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG SYNTHESIS; HEPATITIS C VIRUS; NONHUMAN; PESTIVIRUS; VIRUS INHIBITION; VIRUS REPLICATION;

ACRIDINES; ANIMALS; ANTIVIRAL AGENTS; BINDING SITES; CATTLE; CELL PROLIFERATION; DIARRHEA VIRUSES, BOVINE VIRAL; DRUG DESIGN; KIDNEY; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; STRUCTURE-ACTIVITY RELATIONSHIP; VIRUS REPLICATION;

EID: 33646103675     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm051250z     Document Type: Article

References (57)

1. This work was previously presented in part: Tabarrini, O.; Manfroni, G.; Fravolini, A.; Cecchetti, V.; Sabatini, S.; Paeshuyse, J.; De Clercq, E.; Neyts, J. Selective Anti-BVDV Acridones as New Potential Anti-HCV Agents. Polish-Austrian-German-Hungarian-Italian Joint Meeting on Medicinal Chemistry, Krakow (Poland), October 2003, Abstr. P153.
2. Carman, S.; van Dreumel, T.; Ridpath, J.; Hazlett, M.; Alves, D.; Dubovi, E.; Tremblay, R.; Bolin, S.; Godkin, A.; Anderson, N. Severe Acute Bovine Viral Diarrhea in Ontario, 1993-1995. J. Vet. Diagn. Invest. 1998, 10, 27-35.
3. Ellis, J. A.; West, K. H.; Cortese, V. S.; Myers, S. L.; Carman, S.; Martin, K. M.; Haines, D. M. Lesions and Distribution of Viral Antigen Following an Experimental Infection of Young Seronegative Calves with Virulent Bovine Virus Diarrhea Virus-Type II. Can. J. Vet. Rex. 1998, 62, 161-169.
4. Pellerin, C.; van den Hurk, J.; Lecomte, J.; Tijssen, P. Identification of a new group of bovine viral diarrhea virus stari associate with severe outbreaks and high mortalities. Virology 1994, 203, 260-268.
5. Houe, H. Economic impact of BVDV infection in dairies. Biologicals 2003, 31, 137-143.
6. Bolin, S. R.; Matthews, P. J.; Ridpath, J. F. Methods for detection and frequency of contamination of fetal calf serum with bovine viral diarrhea virus and antibodies against bovine viral diarrhea virus. J. Vet. Diagn. Invest. 1991, 3, 199-203.
7. Harasawa, R.; Sasaki, T. Sequence analysis of the 5′ untranslated region of pestivirus RNA demonstrated in interferons for human use. Biologicals 1995, 23, 263-269.
8. Harasawa, R.; Tomiyama, T. Evidence of pestivirus RNA in human virus vaccines. J. Clin. Microbiol. 1994, 32, 1604-1605.
9. van Oirschot, J. T.; Bruschke, C. J.; van Rijn, P. A. Vaccination of cattle against bovine viral diarrhoea. Vet. Microbiol. 1999, 64, 169-183.
10. Givens, M. D.; Galik, P. K.; Riddell, K. P.; Dykstra, C. C.; Brock, K. V.; Stringfellow, D. A. Effects of Aromatic Cationic Molecules on Bovine Viral diarrhea Virus and Embryonic Development. Theriogenology 2005, 63, 1984-1994.
11. Givens, M. D.; Stringfellow, D. A.; Dykstra, C. C.; Riddell, K. P.; Galik, P. K.; Sullivan, E.; Robl, J.; Kasinathan, P.; Kumar, A.; Boykin, D. W. Prevention and Elimination of Bovine Viral Diarrhea Virus Infections in Fetal Fibroblast Cells. Antiviral Res. 2004, 64, 113-118.
12. Durantel, D.; Carrouée-Durantel, S.; Branza-Nichita, N.; Dwek, R. A.; Zitzmann, N. Effects of Interferon, Ribavirin, and Iminosugar derivatives on cells persistently infected with noncytopathic bovine viral diarrhea virus. Antimicrob. Agents Chemother. 2004, 48, 497-504.
13. Baginski, S. G.; Pevear, D. C.; Seipel, M.; Sun, S. C. C.; Benetatos, C. A.; Chunduru, S. K.; Rice, C. M.; Collett, M. S. Mechanism of action of a pestivirus antiviral compound. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 7981-7986.
14. King, R. W.; Scarnati, H. T.; Priestley, E. S.; De Lucca, I.; Bansal, A.; Williams, J. K. Selection of a thiazole urea-resistant variant of bovine viral diarrhoea virus that maps to the RNA-dependent RNA polymerase. Antiviral Chem. Chemother. 2002, 13, 315-323.
15. Sun, J.-H.; Lemm, J. A.; O'Boyle D. R., II; Racela, J.; Colonno, R.; Gao, M. Specific inhibition of bovine viral diarrhea virus replicase. J. Virol. 2003, 77, 6753-6760.
16. Bukhtiyarova, M.; Rizzo, C. J.; Kettner, C. A.; Korant, B. D.; Scarnati, H. T.; King, R. W. Inhibition of the bovine viral diarrhoea virus NS3 serine protease by a boron-modified peptidyl mimetic of its natural substrate. Antiviral Chem. Chemother. 2002, 12, 367-373.
17. Givens, M. D.; Dykstra, C. C.; Brock, K. V.; Stringfellow, D. A.; Kumar, A.; Stephens, C. E.; Goker, H.; Boykin, D. W. Detection of inhibition of bovine viral diarrhea virus by aromatic cationic molecules. Antimicrob. Agents Chemother. 2003, 47, 2223-2230.
18. Branza-Nichita, N.; Durantel, D.; Carrouée-Durantel, S.; Dwek, R. A.; Zitzmann, N. Antiviral effect of N-butyldeoxynojirimycin against bovine viral diarrhea virus correlates with misfolding of E2 envelope proteins and impairment of Their association into E1-E2 heterodimers. J. Virol. 2001, 75, 3527-3536.
19. Durantel, D.; Branza-Nichita, N.; Carrouée-Durantel, S.; Butters, T. D.; Dwek, R. A.; Zitzmann, N. Study of the mechanism of antiviral action of iminosugar derivatives against bovine viral diarrhea virus. J. Virol. 2001, 75, 8987-8998.
20. Zitzmann, N.; Mehta, A. S.; Carrouée, S.; Butters, T. D.; Platt, F. M.; McCauley, J.; Blumberg, B. S.; Dwek, R. A.; Block, T. M. Imino sugars inhibit the formation and secretion of bovine viral diarrhea virus, a pestivirus model of hepatitis C virus: implications for the development of broad spectrum anti-hepatitis virus agents. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 11878-11882.
21. Markland, W.; McQuaid, T. J.; Jain, J.; Kwong, A. D. Broad-spectrum Antiviral Activity of the IMP Dehydrogenase Inhibitor VX-497: a comparison with ribavirin and Demonstration of Antiviral Additivity with Alpha Interferon. Antimicrob. Agents Chemother. 2000, 44, 859-866.
22. Paeshuyse, J.; Leyssen, P.; Mabery, E.; Boddeker, N.; Vrancken, R.; Froeyen, M.; Ansari, I. H.; Dutartre, H.; Rozenski, J.; Gil, L. H. V. G.; Letellier, C.; Lanford, R.; Canard, B.; Koenen, F.; Kerkhofs, P.; Donis, R. O.; Herdewijn, P.; Watson, J.; De Clercq, E.; Puerstinger, G.; Neyts, J. A novel, highly selective inhibitor of pestivirus replication that targets the viral RNA-dependent RNA Polymerase. J. Virol. 2006, 80, 149-160
23. Blight, K. J.; Grakoui, A.; Hanson, H. L.; Rice, C. M. The molecular biology of hepatitis C virus. In Hepatitis Viruses; Ou, J. H. J., Ed.; Kluwer Academic Publishers: Boston, 2002; pp 81-108.
24. Kim, W. R.; Brown, R. S., Jr.; Terrault, N. A.; El-Serag, H. Burden of liver disease in the United States: summary of a workshop. Hepatology 2002, 36, 227-242.
25. Tan, S.-L.; Pause, A.; Shi, Y.; Sonenberg, N. Hepatitis C Therapeutics: Current Status and Emerging Strategies. Nat. Rev. Drug Discov. 2002, 1, 867-881.
26. Buckwold, V. E.; Beer, B. E.; Donis, R. O. Bovine viral diarrhea virus as a surrogate model of hepatitis C virus for the evaluation of antiviral agents. Antiviral Res. 2003, 60, 1-15.
27. Bartenschlager, R.; Lohmann, V. Novel cell culture systems for the hepatitis C virus. Antiviral Res. 2001, 52, 1-17.
28. Bartenschlager, R. Innovation: Hepatitis C virus Replicons: Potential role for drug Development. Nat. Rev. Drug Discov. 2002, 1, 911-916.
29. Lindenbach, B. D.; Evans, M. J.; Syder, A. J.; Wölk, B.; Tellinghuisen, T. L.; Liu, C. C.; Maruyama, T.; Hynes, R. O.; Burton, D. R.; McKeating, J. A.; Rice, C. M. Complete Replication of Hepatitis C Virus in Cell Culture. Science 2005, 309, 623-626.
30. Wakita, T.; Pietschmann, T.; Kato, T.; Date, T.; Miyamoto, M.; Zhao, Z.; Murthy, K.; Habermann, A.; Kräusslich, H. G.; Mizokami, M.; Bartenschlager, R.; Liang, T. J. Production of Infectious Hepatitis C Virus in Tissue Culture from a Cloned Viral Genome. Nat. Med. 2005, 11, 791-796.
31. Zhong, J.; Gastaminza, P.; Cheng, G.; Kapadia, S.; Kato, T.; Burton, D. R.; Wieland, S. F.; Uprichard, S. L.; Wakita, T.; Chisari, F. V. Robust Hepatitis C Virus Infection in Vitro. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 9294-9299.
32. Fujiwara, M.; Okamoto, M.; Okamoto, M.; Watanabe, M.; Machida, H.; Shigeta, S.; Konno, K.; Yokota, T.; Baba, M. Acridone derivatives are selective inhibitors of HIV-1 replication in chronically infected cells. Antiviral Res. 1999, 43, 179-189.
33. Taraporewala, I. B.; Cessac, J. W.; Chanh, T. C.; Delgado, A. V.; Schinazi, R. F. HIV-1 neutralization and tumor cell proliferation inhibition in vitro by simplified analogues of pyrido[4,3,2-mn]-thyazolo[5,4-b]acridine marine alkaloids. J. Med. Chem. 1992, 35, 2744-2752.
34. Yamamoto, N.; Furukawa, H.; Ito, Y.; Yoshida, S.; Maeno, K.; Nishiyama, Y. Anti-herpesvirus activity of citrusinine-I, a new acridone alkaloid, and related compounds. Antiviral Res. 1989, 12, 21-36.
35. Bastow, K. F.; Itoigawa, M.; Furokawa, H.; Kashiwada, Y.; Bori, I. D.; Ballas, L. M.; Lee, K. H. Antiproliferative actions of 7-substituted 1,3-dihydroxyacridones; possible involvement of DNA topoisomerase II and protein kinase C as biochemical targets. Bioorg. Med. Chem. 1994, 2, 1403-1411.
36. Akanitapichat, P.; Lowden, C. T.; Bastow, K. F. 1,3-dihydroxyacridone derivatives as inhibitors of herpes virus replication. Antiviral Res. 2000, 45, 123-134.
37. Akanitapichat, P.; Bastow, K. F. The antiviral agent 5-chloro-1,3- dihydroxyacridone interferes with assembly and maturation of herpes simplex virus. Antiviral Res. 2002, 55, 113-126.
38. Lowden, C. T.; Bastow, K. F. Cell culture replication of herpes simplex virus and, or human cytomegalovirus is inhibited by 3,7-dialkoxylated, 1-hydroxyacridone derivatives. Antiviral Res. 2003, 59, 143-154.
39. Lowden, C. T.; Bastow, K. F. Anti-Herpes Simplex Virus Activity of Substituted 1-Hydroxyacridones. J. Med. Chem. 2003, 46, 5015-5020.
40. Kramer, M. J.; Cleeland, R.; Grunberg, E. Antiviral activity of 10-carboxymethyl-9-acridanone. Antimicrob. Agents Chemother. 1976, 9, 233-238.
41. Zarubaev, V. V.; Slita, A. V.; Krivitskaya, V. Z.; Sirotkin, A. K.; Kovalenko, A. L.; Chatterjee, N. K. Direct antiviral effect of cycloferon (10-Carboxymethyl-9-acridanone) against adenovirus type 6 in vitro. Antiviral Res. 2003, 58, 131-137.
42. Takemura, Y.; Ju-ichi, M.; Ito, C.; Furukawa, H.; Tokuda, H. Studies on the inhibitory effects of some acridone alkaloids on Epstein-Barr virus activation. Planta Med. 1995, 61, 366-368.
43. Chen, P.; Dhar, T. G. M.; Iwanowicz, E. J.; Watterson, S. H.; Gu, H. H.; Zhao, Y. Heterocyclic acridone inhibitors of IMPDH enzyme. PCT Int. Appl. WO 03/055447, 2003; CAN 139:133475.
44. Iwanowicz, E. J.; Watterson, S. H.; Chen, P.; Dhar, T. G. M.; Gu, H. H.; Zhao, Y. Acridone inhibitors of IMPDH enzyme. PCT Int. Appl. WO 03/059269, 2003, CAN 139:81325.
45. Tabarrini, O.; Cecchetti, V.; Fravolini, A.; Nocentini, G.; Barzi, A.; Sabatini, S.; Miao, H.; Sissi, C. Design and Synthesis of Modified Quinolones as Antitumoral Acridones. J. Med. Chem. 1999, 42, 2136-2144.
46. Cecchetti, V.; Parolin, C.; Moro, S.; Pecere, T.; Filipponi, E.; Calistri, A.; Tabarrini, O.; Gatto, B.; Palumbo, M.; Fravolini, A.; Palù, G. 6-Aminoquinolones as New Potential anti-HIV Agents. J. Med. Chem. 2000, 43, 3799-3802.
47. Tabarrini, O.; Stevens, M.; Cecchetti, V.; Sabatini, S.; Dell'Uomo, M.; Manfroni, G.; Palumbo, M.; Pannecouque, C.; De Clercq, E.; Fravolini, A. Structure Modifications of 6-Aminoquinolones with Potent Anti-HIV Activity. J. Med. Chem. 2004, 47, 5567-5578.
48. Su, T.-L.; Köhler, B.; Chou, T.-C.; Chun, M. W.; Watanabe, K. A. Synthesis of the Acridone Alkaloids Glyfoline and Congeners. Structure-Activity Relationship Studies of Cytotoxic Acridones J. Med. Chem. 1992, 35, 2703-2710.
49. Bastow, K. F. New Acridone Inhibitors of Human Herpes Virus Replication. Curr. Drug Targets-Infect. Disord. 2004, 4, 323-330.
50. Carroll, S. S.; Tomassini, J. E.; Bosserman, M.; Getty, K.; Stahlhut, M. W.; Eldrup, A. B.; Bhat, B.; Hall, D.; Simcoe, A. L.; LaFemina, R.; Rutkowski, C. A.; Wolanski, B.; Yang, Z.; Migliaccio, G.; De Francesco, R.; Kuo, L. C.; MacCoss, M.; Olsen, D. B. Inhibition of Hepatitis C Virus RNA Replication by 2′-Modified Nucleoside Analogs. J. Biol. Chem. 2003, 278, 11979-11984.
51. Eldrup, A. B.; Allerson, C. R.; Bennett, C. F.; Bera, S.; Bhat, B.; Bhat, N.; Bosserman, M. R.; Brooks, J.; Burlein, C.; Carroll, S. S.; Cook, P. D.; Getty, K. L.; MacCoss, M.; McMasters, D. R.; Olsen, D. B.; Prakash, T. P.; Prhavc, M.; Song, Q.; Tomassini, J. E.; Xia, J. Structure-Activity Relationship of Purine Ribonucleosides for Inhibition of Hepatitis C Virus RNA-Dependent RNA Polymerase. J. Med. Chem. 2004, 47, 2283-2295.
52. Letellier, C.; Kerkhofs, P.; Wellemans, G.; Vanopdenbosch, E. Detection and Genotyping of Bovine Diarrhea Virus by Reverse Transcription-Polymerase Chain Amplification of the 5′ Untranslated Region. Vet. Microbiol. 1999, 64, 155-167.
53. Vassilev, V. B.; Collett, M. S.; Donis, R. O. Authentic and Chimeric Full-Length Genomic cDNA Clones of Bovine Viral Diarrhea Virus that Yield Infectious Transcripts. J. Virol. 1997, 71, 471-478.
54. Neyts, J.; Meerbach, A.; McKenna, P.; De Clercq, E. Use of the yellow fever virus vaccine strain 17D for the study of strategies for the treatment of yellow fever virus infections. Antiviral Res. 1996, 30, 125-132.
55. Leyssen, P.; Van Lommel, A.; Drosten, C.; Schmilz, H.; De Clercq, E.; Neyts, J. A novel model for the study of the therapy of flavivirus infections using the Modoc virus. Virology 2001, 279, 27-37.
56. Reed, L. J.; Muench, A. H. A simple method of estimating fifty percent end points. Am. J. Hyg. 1938, 27, 493-497.
57. Zhong, W.; Gutshall, L. L.; Del-Vecchio, A. M. Identification and Characterization of an RNA-dependent RNA Polymerase Activity within the Nonstructural Protein 5B Region of Bovine Viral Diarrhea Virus. J. Virol. 1998, 72, 9365-9369.