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Ribofuranosylselenazole-4-Carboxamide, a New Antiviral Agentt JORMA J

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Ribofuranosylselenazole-4-Carboxamide, a New Antiviral Agentt JORMA J ANTiMICROBIAL AGENTS AND CHEMOTHERAPY, Sept. 1983, P. 353-361 Vol. 24, No. 3 0066-4804/83/090353-09$02.00/0 Copyright 0 1983, American Society for Microbiology Broad-Spectrum Antiviral Activity of 2-p-D- Ribofuranosylselenazole-4-Carboxamide, a New Antiviral Agentt JORMA J. KIRSI,'* JAMES A. NORTH,1 PATRICIA A. McKERNAN,1 BYRON K. MURRAY,2 PETER G. CANONICO,3 JOHN W. HUGGINS,3 PREM C. SRIVASTAVA,4 AND ROLAND K. ROBINS5 Department ofMicrobiology1 and Cancer Research Center, Department of Chemistry,5 Brigham Young University, Provo, Utah 84602; Department ofMicrobiology and Immunology, Virginia Commonwealth University, Richmond, Virginia 232982; Department ofAntiviral Studies, U.S. Army Medical Research Institute ofInfectious Diseases, Fort Detrick, Frederick, Maryland 217103; and Health and Safety Research Division (Nuclear Medicine Technology Group), Oak Ridge National Laboratory, Oak Ridge, Tennessee 378304 Received 7 February 1983/Accepted 13 June 1983 The relative in vitro antiviral activities of three related nucleoside carboxam- ides, ribavirin (1-3-D-ribofuranosyl-1,2,4-triazole-3-carboxamide), tiazofurin (2- 3-D-ribofuranosylthiazole-4-carboxamide), and selenazole (2-p-D-ribofuranosyl- selenazole-4-carboxamide), were studied against selected DNA and RNA viruses. Although the activity of selenazole against different viruses varied, it was significantly more potent than ribavirin and tiazofurin against all tested represen- tatives of the families Paramyxoviridae (parainfluenza virus type 3, mumps virus, measles virus), Reoviridae (reovirus type 3), Poxviridae (vaccinia virus), Herpes- viridae (herpes simplex virus types 1 and 2), Togaviridae (Venezuelan equine encephalomyelitis virus, yellow fever virus, Japanese encephalitis virus), Bunya- viridae (Rift Valley fever virus, sandfly fever virus [strain Sicilian], Korean hemorrhagic fever virus), Arenaviridae (Pichinde virus), Picornaviridae (coxsack- ieviruses B1 and B4, echovirus type 6, encephalomyocarditis virus), Adenoviri- dae (adenovirus type 2), and Rhabdoviridae (vesicular stomatitis virus). The antiviral activity of selenazole was also cell line dependent, being greatest in HeLa, Vero-76, and Vero E6 cells. Selenazole was relatively nontoxic for Vero, Vero-76, Vero E6, and HeLa cells at concentrations of up to 1,000 ,g/ml. The relative plating efficiency at that concentration was over 90%. The effects of selenazole on viral replication were greatest when this agent was present at the time of viral infection. The removal of selenazole from the medium of infected cells did not reverse the antiviral effect against vaccinia virus, but there was a gradual resumption of viral replication in cells infected with parainfluenza type 3 or herpes simplex virus type 1 (strain KOS). However, the antiviral activity of ribavirin against the same viruses was reversible when the drig was removed. A novel selenazole carboxamide nucleoside, 3 osyl-1,2,4-triazole-3-carboxamide) and that it (2-a-D-ribofuranosylselenazole-4-carboxamide) has a significant activity against several experi- (Fig. 1), has recently been synthesized in our mental neoplasms, including those of the lung laboratory (34). Its antiviral activity has not (15, 18, 26). been previously evaluated, although our prelimi- Ribavirin, a related ribofuranosylcarboxam- nary studies indicated that selenazole 3 pos- ide, has a broad spectrum of antiviral activity sesses significant antitumor effects (34). Selena- (32), both in vitro (2, 14, 20, 24) and in vivo (13, zole was designed as an analog oftiazofurin 2 (2- 16, 19, 31, 37), and is currently under clinical P-D-ribofuranosylthiazole-4-carboxamide). evaluation for safety and efficacy in humans. Preliminary studies of tiazofurin 2 (33) indicated Recent studies have shown that ribavirin is that it possesses a spectrum of antiviral activity remarkably effective clinically against influenza in cell culture similar to, but somewhat less A and B (17, 21), hepatitis (23), and respiratory potent than, that of ribavirin I (1-P-D-ribofuran- syncytial virus infection (11). These recent stud- ies in humans have renewed considerable inter- t Contribution no. 1669, Army Research Program on Anti- est in the potential therapeutic utility of ribavirin parasitic Drugs. (7). 353 354 KIRSI ET AL. ANTIMICROB. AGENTS CHEMOTHER. MATERIUS AND METHODS Cels. Five types of continuous cell lines were used in this study: three strains of Afric#n green monkey kidney ceils (Vero, ATCC CCL 1;'Vero #6, ATCC CRL 15S6; Vero-76, ATCC CRL 1387) and one strain of rhesus monkey kidney cells (LLC-MK2, ATCC CCL 7; American Type Culture Collection Cell Repos- itory, Rockville, Md. and human epithelioid cervical carcinoma cells (HeLa; Flow Laboratories, Ingel- wood, Calif.). Cells were grown- in antibiotic-free Eage sninimum essential medium (EMEM) with Earle salts supplemented with 10%6 newborn bovine serum (GIBCO Loratories, Grand Island, N.Y.), except for Vero-76 cells which were grown in EMEM with Earie salts and 1 x nonessential amino acids supple- A mented with 10%16 fetal bovine serum (FBS; KC Biolo- gicals Inc., Lenexa, Kans). LLC-MK2 cells were grown in medium 199 with Earle salts supplemented with 10% FBS. All cells were passaged in 75-cm3 plastic flasks (Corning Glass Works, Corning, N.Y.) at 37°C under humidified 5% COA9% air. All of the expermnts reported in this paper were conducted with cells which had been ipesago between 5 and 30 times in our laboratory. All cell culturs were periodi- cally tested and found to be free of bacterial and mycoplasmal contminaon. Vses. Twenty viruses, rQpresenting the major families of DNA and RNA viruses pathogenic for humans, were used in these experiments. Herpes simplex virus type 1 (HSV-1) strain KOS was supplied by Byron K. Murray, Virginia Commwnwealth Uni- versity, Richmond, Va. Herpes simplex virus type 2 (HSV-2) strain MS, vaccinia virus (VV) strain Elstree, adenovirus type Z (Ad2) strain Adenoid 6, coxsackie- virus Bi strain Ha 201468, coxackievirus B4 strain J.V.B. (Benschoten), echovirus type 6 strain Damori, mumps virus strain Enders, measles virus strain Ed- monston, reovirus type 3 strain Abney, and encepha- lomyocarditis viwus strain EMC were obtained from the American Type Culture Collection. Vesicular sto- matitis virus (VSV) strain Indiana was acquired from Ron W. Leavitt, Brigham Young University, Provo, Utah. Parainluenza vims type 3 (Para-3) strain C243 wps donated by R. W. Sidwell, Utah State University, Virus pools were preparedby infecting confluent monolayers of HeLa or Vero cells. Infected monolay- ers were incubated for 2 to 6 days at 37°C in 5% CO2 and then harvested when cultures exhibited 90% cyto- pathic effect (CPE). Viruses were passaged least twice in each cell line before the virus pool was used. The cell line used in any given antiviral experiment cO OH was infected with vus produced only in that same cell FIG. 1. Chemical structures of selenazole 3 (A), line. Infected cells and fluids were frozen at -7(C. tiazofurin 2 (B), and ribavirin I (C), the three related Intracellular virus was released by disrupting infected nucleoside carboxamides used in this study. cells by freeze-thawing and vigorous trituration ast the flask wall. Viral stock cultures were divid- In.view of the close struct ual relationship of ed into 0.5-ml samples, frozen, and stored PA -70C nucleosides 2 and 3 to ribavirin 1, we compared until used. Samples of eacb virus were assayed for infectious virus by a plaque formation assay (PFU per the -in vitro antiviral activities of these nucleo- milliliter) and by determination of the 50% tissue sides against a number of DNA and RNA virus- culture infective dose by the method of Reed and es. In the prsent in vitro study, we report that Muench (25). selenazole 3 appears to have superior in vitro Rift Valley fever virus, g 501 strain (8), was antiviral activity as compared with those of passaged once in Vero-76 cells. Venezuelan equine ribavirin and tiazofurin. encephalomyelitis virus (VEE), Trinidad donkey VOL. 24, 1983 ANTIVIRAL ACTIVITY OF SELENAZOLE 355 strain (12), was passaged once in Peking duck primary (0.1 ml per well), and the cells were overlaid with 1% cells. Pichinde virus, CoAn 3739, ATCC VR-708, was methylcellulose in EMEM with 2% newborn calf se- passaged once in Vero-76 cells. Yellow fever virus rum (1.0 ml per well). The plates were incubated for 2 (YF), Asibi strain, was obtained as plasma from a to 3 days to allow for plaque formation. Cells were single infected rhesus monkey (Macaca mulatta) and then fixed with 10%o Formalin and stained with 1% plaqued on LLC-MK2 cells without adaptation in crystal violet in water. Plaques were counted, and the tissue culture (35). Japanese encephalitis virus (JE), ED,0 was extrapolated graphically from the plotted strain Nakayama, was obtained at suckling mouse values. The concentration of compound that resulted passage 54 from Robert Shope, Yale Arbovirus Re- in a 50% reduction of plaque formation, as compared search Unit, New Haven, Conn., and passaged one with nondrug controls, was designated the ED50. additional time in Vero-76 cells. Sandfly fever virus YF was assayed as described by Canonico et al. (3); (Sicilian), Brownell strain, was from a human isolate Rift Valley fever virus, sandfly fever virus (Sicilian), (1). Hantaan virus, the etiological agent of Korean VEE, JE, and Pichinde virus were assayed in triplicate hemorrhagic fever, strain HBL7990, was isolated by in Linbro six-well plates (9.6 cm2 per well; Flow Ho Wang Lee, Institute for Viral Diseases, Korea Laboratories) in confluent monolayers of Vero-76 University, Seoul, from human material and passaged cells. The compounds were tested using a threefold 1 time in Apodemus agarius corae and 16 times in dilution series of the drug prepared in diluent medium Vero E6 cells. All studies involving Rift Valley fever consisting of EMEM-nonessential amino acids, 10 mM virus, sandfly fever virus (Sicilian), YF, JE, VEE, HEPES (N-2-hydroxyethylpiperazine-N'-2-ethanesul- Pichinde virus, and Korean hemorrhagic fever virus fonic acid), 10 ,ug of gentamicin per ml, and 5% were performed in compliance with guidelines (4, 36) (vol/vol) heat-inactivated FBS.
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