Thiazolides, a new class of antiviral agents effective against rotavirus infection, target viral morphogenesis, inhibiting viroplasm formation

Journal of Virology

Volumn 87, Issue 20, 2013, Pages 11096-11106

  La Frazia, Simone ^a   Ciucci, Alessandra ^a   Arnoldi, Francesca ^b   Coira, Maurizio ^a   Gianferretti, Patrizia ^a   Angelini, Mara ^a   Belardo, Giuseppe ^a   Burrone, Oscar R ^c   Rossignol, Jean Francois ^d   Santoro, M Gabriella ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^d Romark Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; NITAZOXANIDE; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 5;

ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG TARGETING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ROTAVIRUS; ROTAVIRUS INFECTION; VIROPLASM; VIRUS ENTRY; VIRUS MORPHOGENESIS; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; HAPLORHINI; HUMANS; INCLUSION BODIES, VIRAL; MICROBIAL SENSITIVITY TESTS; PROTEIN BINDING; ROTAVIRUS; THIAZOLES; VIRAL NONSTRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 84886911101     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01213-13     Document Type: Article

References (37)

1. Trask SD, McDonald SM, Patton JT. 2012. Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 10:165-177.
2. Estes MK, Kapikian ZA. 2007. Rotaviruses, p 1917-1974. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
3. Cuadras MA, Greenberg HB. 2003. Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo. Virology 313:308-321.
4. Widdowson MA, Bresee JS, Gentsch JR, Glass RI. 2005. Rotavirus disease and its prevention. Curr. Opin. Gastroenterol. 21:26-31.
5. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, WHO-Coordinated Global Rotavirus Surveillance Network. 2012. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 12:136-141.
6. Rossignol JF, Abu-Zekry M, Hussein A, Santoro MG. 2006. Effect of nitazoxanide for treatment of severe rotavirus gastroenteritis diarrhoea: randomised double-blind placebo-controlled trial. Lancet 368:124-129.
7. Rossignol JF, El-Gohary YM. 2006. Nitazoxanide in the treatment of viral gastroenteritis: a randomized double-blind placebo controlled clinical trial. Aliment. Pharmacol. Ther. 24:1423-1430.
8. Eichwald C, Rodriguez JF, Burrone OR. 2004. Characterization of rotavirus NSP2/NSP5 interactions and the dynamics of viroplasm formation. J. Gen. Virol. 85:625-634.
9. Rossi A, Ciafrè S, Balsamo M, Pierimarchi P, Santoro MG. 2006. Targeting the heat shock factor 1 by RNA interference: a potent tool to enhance hyperthermochemotherapy efficacy in cervical cancer. Cancer Res. 66:7678-7685.
10. Afrikanova I, Fabbretti E, Miozzo MC, Burrone OR. 1998. Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. J. Gen. Virol. 79:2679-2686.
11. Fabbretti E, Afrikanova I, Vascotto F, Burrone OR. 1999. Two nonstructural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80:333-339.
12. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning, a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
13. Superti F, Amici C, Tinari A, Donelli G, Santoro MG. 1998. Inhibition of rotavirus replication by prostaglandin A: evidence for a block of virus maturation. J. Infect. Dis. 178:564-568.
14. Rossignol JF, La Frazia S, Chiappa L, Ciucci A, Santoro MG. 2009. Thiazolides, a new class of anti-influenza molecules targeting viral hemagglutinin at the post-translational level. J. Biol. Chem. 284: 29798-29808.
15. Brunelli C, Amici C, Angelini M, Fracassi C, Belardo G, Santoro MG. 2012. The non-steroidal anti-inflammatory drug indomethacin activates the eIF2 kinase PKR, causing a translational block in human colorectal cancer cells. Biochem. J. 443:379-386.
16. Arnoldi F, Campagna M, Eichwald C, Desselberger U, Burrone OR. 2007. Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. J. Virol. 81:2128-2137.
17. Patton J, Chizhikov V, Taraporewala Z, Chen DY. 2000. Virus replication, p 33-36In Gray J, Desselberger U (ed), Rotaviruses: methods and protocols. Humana Press, Totowa, NJ.
18. Afrikanova I, Miozzo MC, Giambiagi S, Burrone OR. 1996. Phosphorylation generates different forms of rotavirus NSP5. J. Gen. Virol. 77: 2059-2065.
19. Rossi A, Trotta E, Brandi R, Arisi I, Coccia M, Santoro MG. 2010. AIRAP, a new human heat shock gene regulated by heat shock factor 1. J. Biol. Chem. 285:13607-13615.
20. DeWitte-Orr SJ, Mehta DR, Collins SE, Suthar MS, Gale M, Jr, Mossman KL. 2009. Long double-stranded RNA induces an antiviral response independent of IFN regulatory factor 3, IFN-beta promoter stimulator 1, and IFN. J. Immunol. 183:6545-6553.
21. Jao CY, Salic A. 2008. Exploring RNA transcription and turnover in vivo by using click chemistry. Proc. Natl. Acad. Sci. U. S. A. 105:15779-15784.
22. Offit PA, Clark HF, Ward RL. 2003. Current state of development of human rotavirus vaccines, p 345-356. In Desselberger U, Gray J (ed), Viral gastroenteritis. Elsevier Science BV, Amsterdam, Netherlands.
23. Petrie BL, Greenberg HB, Graham DY, Estes MK. 1984. Ultrastructural localization of rotavirus antigens using colloidal gold. Virus Res. 1:133-152.
24. Campagna M, Eichwald C, Vascotto F, Burrone OR. 2005. RNA interference of rotavirus segment 11mRNAreveals the essential role of NSP5 in the virus replicative cycle. J. Gen. Virol. 86:1481-1487.
25. Silvestri LS, Taraporewala ZF, Patton JT. 2004. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78:7763-7774.
26. McDonald SM, Patton JT. 2011. Assortment and packaging of the segmented rotavirus genome. Trends Microbiol. 19:136-144.
27. Ayala-Breton C, Arias M, Espinosa R, Romero P, Arias CF, Lopez S. 2009. Analysis of the kinetics of transcription and replication of the rotavirus genome by RNA interference. J. Virol. 83:8819-8831.
28. White CA, Jr. 2004. Nitazoxanide: a new broad spectrum antiparasitic agent. Expert Rev. Anti Infect. Ther. 2:43-49.
29. De Carvalho LP, Lin G, Jiang X, Nathan C. 2009. Nitazoxanide kills replicating and non-replicating Mycobacterium tuberculosis and evades resistance. J. Med. Chem. 52:5789-5792.
30. Rossignol JF, Elfert A, El-Gohary Y, Keeffe EB. 2009. Improved virologic response in chronic hepatitis C genotype 4 treated with nitazoxanide, peginterferon, and ribavirin. Gastroenterology 136:856-862.
31. Rossignol JF, Samudrala S, Hoppers M, Haffizulla J, Resnick H, Hartman A, Comhaire S, Carrion M, Bardin M. 2011. A randomized doubleblind, placebo (PCB) controlled study of nitazoxanide (NTZ) in adults and adolescents with acute uncomplicated influenza, abstr LB-35, p 46. Abstr. 49th Annu. Meet. Infect. Dis. Soc. Am., Boston, MA.
32. Hoffman PS, Sisson G, Croxen MA, Welch K, Harman WD, Cremades N, Morash MG. 2007. Antiparasitic drug nitazoxanide inhibits the pyruvate oxidoreductases of Helicobacter pylori, selected anaerobic bacteria and parasites, and Campylobacter jejuni. Antimicrob. Agents Chemother. 51:868-876.
33. Lam KK, Zheng X, Forestieri R, Balgi AD, Nodwell M, Vollett S, Anderson HJ, Andersen RJ, Av-Gay Y, Roberge M. 2012. Nitazoxanide stimulates autophagy and inhibits mTORC1 signaling and intracellular proliferation of Mycobacterium tuberculosis. PLoS Pathog. 8:e1002691. doi:10.1371/journal.ppat.1002691.
34. Korba BE, Montero AB, Farrar K, Gaye K, Mukerjee S, Ayers MS, Rossignol JF. 2008. Nitazoxanide, tizoxanide and other thiazolides arepotent inhibitors of hepatitis B virus and hepatitis C virus replication. Antiviral Res. 77:56-63.
35. Elazar M, Liu M, McKenna SA, Liu P, Gehrig EA, Puglisi JD, Rossignol JF, Glenn JS. 2009. The anti-hepatitis C agent nitazoxanide induces phosphorylation of eukaryotic initiation factor 2alpha via protein kinase activated by double-stranded RNA activation. Gastroenterology 137:1827-1835.
36. Teran CG, Teran-Escalera CN, Villarroel P. 2009. Nitazoxanide vs. probiotics for the treatment of acute rotavirus diarrhea in children: a randomized, single-blind, controlled trial in Bolivian children. Int. J. Infect. Dis. 13:518-523.
37. Broekhuysen J, Stockis A, Lins RL, De Graeve J, Rossignol JF. 2000. Nitazoxanide: pharmacokinetics and metabolism in man. Int. J. Clin. Pharmacol. Ther. 38:387-394.