Anti-norovirus therapeutics: a patent review (2010-2015)

References

• Pringle K, Lopman BA, Vega E, et al. Noroviruses: epidemiology, immunity and prospects for prevention. Future Microbiol. 2015;10:53–67.
   PubMed Web of Science ®Google Scholar
• Belliott G, Lopman BA, Ambert-Balay K, et al. The burden of norovirus gastroenteritis: an important foodborne and healthcare-related infection. Clin Microbiol Infect. 2014;20:724–730.
   PubMed Web of Science ®Google Scholar
• Koo HL, Ajami N, Atmar RL, et al. Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med. 2010;10:61–70.
   PubMedGoogle Scholar
• Green KY The Noroviruses in Green’s Virology: Caliciviridae. Knipe DM, Howley PM, eds. Vol. 1, Philadelphia: Lippincott Williams & Wilkins; 2007. p. 949–979.
   Google Scholar
• www.cdc.gov/norovirus [cited 2015 Dec 10].
   Google Scholar
• Hall AJ, Lopman BA, Payne DC, et al. Norovirus disease in the United States. Emerg Infect Dis. 2013;19:1198–1205.
   PubMed Web of Science ®Google Scholar
• Bok K, Green KY. Norovirus gastroenteritis in immunocompromised patients. N Engl J Med. 2012;367:2126–2132.
   PubMed Web of Science ®Google Scholar
• Patel MM, Widdowson MA, Glass RI, et al. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Inf Dis. 2008;14:1224–1231.
   PubMed Web of Science ®Google Scholar
• Robilotti E, Derensiski S, Pinsky BA. Norovirus. Clin Microbiol Rev. 2015;28:134–164.
   PubMed Web of Science ®Google Scholar
• Hall AJ. Noroviruses: the perfect human pathogen? J Infect Dis. 2015;28:134–164.
   Google Scholar
• Verhoef L, Hewitt J, Barclay L, et al Norovirus genotype profiles associated with foodborne transmission, 1999-2012. Emerg Inf Dis. 2015;21:592–599.
   PubMed Web of Science ®Google Scholar
• Kaufman SS, Green KY, Korba BE. Treatment of norovirus infections: moving antivirals from the bench to the bedside. Antiviral Res. 2014;105:80–91.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Neyts J, Jochmans D. Norovirus: targets and tools in antiviral drug discovery. Biochem Pharmacol. 2014;91:1–11.
   PubMed Web of Science ®Google Scholar
• Karst SM, Zhu S, Goodfellow IG. The molecular pathology of noroviruses. J Pathol. 2015;235:206–216.
   PubMed Web of Science ®Google Scholar
• Karst SM, Wobus CE, Goodfellow IG, et al. Advances in norovirus biology. Cell Host Microbe. 2014;15:668–680.
   PubMed Web of Science ®Google Scholar
• Taube S, Kolawole AO, Hohne M, et al. A mouse model for human norovirus. MBio. 2013;4:e00450–13.
   Web of Science ®Google Scholar
• Wobus CE, Thackray LB, Virgin HW. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol. 2006;78:5104–5112.
   Web of Science ®Google Scholar
• Chang K-O, Sosnovtsev SV, Belliot G, et al. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology. 2006;353:463–473.
   PubMed Web of Science ®Google Scholar
• Cheetham S, Souza M, Meulia T, et al. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol. 2006;80:10372–10381.
   PubMed Web of Science ®Google Scholar
• Souza M, Azevedo MS, Jung K, et al. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol. 2008;82:1777–1786.
   PubMed Web of Science ®Google Scholar
• Bok K, Parra GI, Mitra T, et al. Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci USA. 2011;108:325–330.
   PubMed Web of Science ®Google Scholar
• Rockx BH, Bogers WM, Heeney JL, et al. Experimental norovirus infections in non-human primates. J Med Virol. 2005;75:313–320.
   PubMed Web of Science ®Google Scholar
• Lee BE, Pang X-L. New strains of norovirus and the mystery of viral gastroenteritis epidemics. Can Med Assoc J. 2013;185:1381–1382.
   PubMed Web of Science ®Google Scholar
• White PA. Evolution of norovirus. Clin Microbiol Infect. 2014;20:741–745.
   PubMed Web of Science ®Google Scholar
• Xi JN, Graham DY, Wang KN, et al. Norwalk virus genome cloning and characterization. Science. 1990;250:1580–1583.
   PubMed Web of Science ®Google Scholar
• Clarke IN, Lambden PR. Organization and expression of calicivirus genes. J Infect Dis. 2000;181(Suppl 2):S309–S316.
   PubMed Web of Science ®Google Scholar
• Thorne LG, Goodfellow IG. Norovirus gene expression and replication. J Gen Virol. 2014;95:278–291.
   PubMed Web of Science ®Google Scholar
• Hardy ME. Norovirus protein structure and function. Microbiol Lett. 2005;253:1–8.
   PubMed Web of Science ®Google Scholar
• Kato K, Ishiwa A. The role of carbohydrates in infection strategies of enteric pathogens. Trop Med Health. 2015;43:41–52.
   PubMedGoogle Scholar
• Tan M, Jiang X. Norovirus-host interaction: implications for disease control and prevention. Expert Rev Mol Med. 2007;9:1–21.
   PubMedGoogle Scholar
• Ming T, Jiang X. Norovirus gastroenteritis, carbohydrate receptors and animal models. PLoS Pathogens. 2010;6(8):e1000983.
   PubMedGoogle Scholar
• Wobus CE, Karst SM, Thackray LB, et al. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biology. 2004;2:e432.
   PubMed Web of Science ®Google Scholar
• Jones MK, Watanabe M, Zhu S, et al. Enteric bacteria promote human and murine norovirus infection in B cells. Science. 2014;346:755–759.
   PubMed Web of Science ®Google Scholar
• Karst SM, Wobus CE. A working model of how noroviruses infect the intestine. PLoS Pathogens. 2015;11(2):e1004626.
   PubMedGoogle Scholar
• Prasad BV, Hardy ME, Dokland T, et al. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286:287–290.
   PubMed Web of Science ®Google Scholar
• Parra GI, Abente EJ, Sandoval-Jaime C, et al. Multiple antigenic sites are involved in blocking the interaction of GII.4 norovirus capsid with ABH histo-blood group antigens. J Virol. 2012;86:7414–7426.
   PubMed Web of Science ®Google Scholar
• Tan M, Xia M, Chen Y, et al. Conservation of carbohydrate binding interfaces – evidence of human HBGA selection in norovirus evolution. PLoS One. 2009;4:e5058.
   PubMed Web of Science ®Google Scholar
• Han L, Kitova EN, Tan M, et al. Affinities of human histo-blood group antigens for norovirus capsid protein complexes. Glycobiology. 2015;25:170–180.
   PubMed Web of Science ®Google Scholar
• Tan M, Jiang X. The P domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol. 2005;79:14017–14030.
   PubMed Web of Science ®Google Scholar
• Hansman GS, Biertumpfel C, Goergiev I, et al. Crystal structures of GII.10 and GII.12 norovirus protruding domains in complex with histo-blood group antigens reveal details for a potential site of vulnerability. J Virol. 2011;85:6687–6701.
   PubMed Web of Science ®Google Scholar
• Choi M, Hutson AM, Estes MK, et al. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Nat Acad Sci USA. 2008;105:9175–9180.
   PubMed Web of Science ®Google Scholar
• Chen Y, Tan M, Xia M, et al. Crystallography of a Lewis-binding norovirus, elucidation of strain-specificity to the polymorphic human histo-blood group antigens. PLoS Pathogens. 2011;7:e1002152.
   PubMedGoogle Scholar
• Bu W, Mamedova A, Tan M, et al. Structural basis for the receptor binding specificity of Norwalk virus. J Virol. 2008;82:5340–5347.
   PubMed Web of Science ®Google Scholar
• Shanker S, Czako R, Sankaran B, et al. Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses. J Virol. 2014;88:6168–6180.
   PubMed Web of Science ®Google Scholar
• El-Hawiet A, Shoemaker GK, Daneshfar R, et al. Applications of a catch and release electrospray ionization mass spectrometry assay for carbohydrate library screening. Anal Chem. 2012;84:50–58.
   PubMed Web of Science ®Google Scholar
• Han L, Tran M, Kitova EN, et al. Gangliosides are ligands for human noroviruses. J Am Chem Soc. 2014;136:12631–12637.
   PubMed Web of Science ®Google Scholar
• Han L, Kitova EN, Tan M, et al. Identifying carbohydrate ligands of a norovirus P particle using a catch and release electrospray ionization mass spectrometry assay. J Am Soc Mass Spectrom. 2014;25:111–119.
   PubMed Web of Science ®Google Scholar
• Feng X, Jiang X. Library screen for inhibitors targeting norovirus binding to histo-blood group antigen receptors. Antimicrob Agents Chemother. 2007;51:324–331.
   PubMed Web of Science ®Google Scholar
• Zhang X, Tan M, Chhabra M, et al. Inhibition of histo-blood group antigen binding as a novel strategy to block norovirus infections. PLoS One. 2013;8:e69379.
   PubMed Web of Science ®Google Scholar
• Blakeney SJ, Cahill A, Reilly PA. Processing of Norwalk virus nonstructural proteins by a 3C-like cysteine proteinase. Virology. 2003;308:216–224.
   PubMed Web of Science ®Google Scholar
• Hussey RJ, Coates L, Gill RS, et al. A structural study of norovirus 3C protease specificity: binding of a designed active site-directed enzyme inhibitor. Biochemistry. 2011;50:240–249.
   PubMed Web of Science ®Google Scholar
• Hardy ME, Crone TJ, Brower JE, et al. Substrate specificity of the Norwalk virus 3C-like proteinase. Virus Res. 2002;89:29–39.
   PubMed Web of Science ®Google Scholar
• Chang K-O, Takahashi D, Prakash O, et al. Characterization and inhibition of norovirus proteases of genogroups I and II using a fluorescence resonance energy transfer assay. Virology. 2012;423:125–133.
   PubMed Web of Science ®Google Scholar
• Tiew K-C, He G, Aravapalli S, et al. Design, synthesis, and evaluation of inhibitors of Norwalk virus 3C protease. Bioorg Med Chem Lett. 2011;21:5315–5319.
   PubMed Web of Science ®Google Scholar
• Galasiti Kankanamalage AC, Kim Y, Weerawarna PM, et al. Structure-guided design and optimization of dipeptidyl inhibitors of norovirus 3CL protease. Structure-activity relationships, biochemical, X-ray crystallographic, cell-based and in vivo studies. J Med Chem. 2015;58:3144–3155.
   PubMed Web of Science ®Google Scholar
• Mandadapu SR, Weerawarna PM, Gunnam MR, et al. Potent inhibition of norovirus 3CL protease by peptidyl α-ketoamides and α-ketoheterocycles. Bioorg Med Chem Lett. 2012;22:4820–4826.
   PubMed Web of Science ®Google Scholar
• Kim Y, Lovell S, Tiew K-C, et al. Broad-spectrum antivirals against 3C or 3C-like proteases of picornaviruses, noroviruses, and coronaviruses. J Virol. 2012;86:11754–11762.
   PubMed Web of Science ®Google Scholar
• Prior AM, Kim Y, Weerasekara S, et al. Design, synthesis and bioevaluation of of viral 3C and 3C-like protease inhibitors. Bioorg Med Chem Lett. 2013;23:6317–6320.
   PubMed Web of Science ®Google Scholar
• Mandadapu SR, Gunnam MR, Tiew K-C, et al. Inhibition of norovirus 3CL protease by bisulfite adducts of transition state inhibitors. Bioorg Med Chem Lett. 2013;23:62–65.
   PubMed Web of Science ®Google Scholar
• Mandadapu SR, Gunnam MR, Galasiti Kankanamalage AC, et al. Potent inhibition of norovirus by dipeptidyl α-hydroxyphosphonate transition state mimics. Bioorg Med Chem Lett. 2013;23:5941–5944.
   PubMed Web of Science ®Google Scholar
• Muhazhiri Z, Deng L, Shanker S, et al. Structural basis of substrate specificity and protease inhibition in Norwalk virus. J Virol. 2013;87:4281–4292.
   PubMed Web of Science ®Google Scholar
• Deng L, Muhazhiri Z, Estes MK, et al. Synthesis, activity, and structure-activity relationship of noroviral protease inhibitors. Med Chem Comm. 2013;4:1354–1359.
   Web of Science ®Google Scholar
• Zeitler CE, Estes MK, Venkataram Prasad BV. X-ray crystallographic structure of the Norwalk virus protease at 1.5 A resolution. J Virol. 2006;80:5050–5058.
   PubMed Web of Science ®Google Scholar
• Nakamura K, Someya Y, Kumasaka T, et al. Norovirus protease structure provides insights into active and substrate binding site integrity. J Virol. 2005;79:13685–13693.
   PubMed Web of Science ®Google Scholar
• Takahashi D, Hiromasa Y, Kim Y, et al. Structural and dynamics characterization of norovirus protease. Protein Sci. 2013;22:347–357.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Nascimento MSJ, Ma Q, et al. The enterovirus protease inhibitor rupintrivir exerts cross-genotypic anti-norovirus activity and clears cells from the norovirus replicon. Antimicrob Agents Chemother. 2014;58:4675–4681.
   PubMed Web of Science ®Google Scholar
• Mandadapu SR, Weerawarna PM, Prior AM, et al. Macrocyclic inhibitors of 3C and 3C-like proteases of picornavirus, norovirus, and coronavirus. Bioorg Med Chem Lett. 2013;23:3709–3712.
   PubMed Web of Science ®Google Scholar
• Eltahla AA, Luciani F, White PA, et al. Inhibitors of the hepatitis C virus polymerase; mode of action and resistance. Viruses. 2015;7:5206–5224.
   PubMed Web of Science ®Google Scholar
• Sofia MJ. Nucleotide prodrugs for the treatment of HCV infection. Adv Pharmacol. 2013;67:39–73.
   PubMedGoogle Scholar
• Sofia MJ, Chang W, Furman PA, et al. Nucleoside, nucleotide, and non-nucleoside inhibitors of hepatitis C virus NS5B RNA-dependent RNA-polymerase. J Med Chem. 2012;55:2481–2531.
   PubMed Web of Science ®Google Scholar
• Pradere U, Garnier-Ambland EC, Coats SJ, et al. Synthesis of nucleoside phosphate and phosphonate prodrugs. Chem Rev. 2014;114:9154–9218.
   PubMed Web of Science ®Google Scholar
• Alam I, Lee JH, Cho KJ, et al. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase in complex with 2-thiouridine or ribavirin. Virology. 2012;426:143–151.
   PubMed Web of Science ®Google Scholar
• Mastrangelo E, Pezzullo M, Tarantino D, et al. Structure-based inhibition of norovirus RNA-dependent RNA polymerase. J Mol Biol. 2012;419:198–210.
   PubMed Web of Science ®Google Scholar
• Croci R, Pezzulo M, Tarantino D, et al. Structural bases of norovirus RNA dependent RNA polymerase inhibition by novel suramin-related compounds. PLoS One. 2014;9(3):e91765.
   PubMed Web of Science ®Google Scholar
• Lee JH, Alam I, Han KR, et al. Crystal structures of murine norovirus-1- RNA dependent RNA polymerase. J Gen Virol. 2011;92:1607–1616.
   PubMed Web of Science ®Google Scholar
• Alios BioPharma, Inc. compositions and methods for the treatment of norovirus infection. WO 0,096,78A2. 2013 Jan 17.
   Google Scholar
• Alios BioPharma, Inc. substituted nucleosides, nucleotides and analogs thereof. United State patent US 0,011,497A1. 2015 Jan 8.
   Google Scholar
• Ashburn TT, Thor KB. Drug repositioning: identifying and developing new uses for existing drugs. Nat Rev Drug Discov. 2004;3:673–683.
   PubMed Web of Science ®Google Scholar
• Costantini VP, Whitaker T, Barclay L, et al. Antiviral activity of nucleoside analogues against norovirus. Antivir Ther. 2012;17:981–991.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Jochmans D, Debing Y, et al. The viral polymerase inhibitor 2ʹ-C-methylcytidine inhibits Norwalk virus replication and protects against norovirus-induced diarrhea and mortality in a mouse model. J Virol. 2013;87:11798–11805.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Jochmans D, Neyts J. Prophylactic treatment with the nucleoside analogue 2ʹ-C-methylcytidine completely prevents transmission of norovirus. J Antimicrob Chemother. 2015;70:190–197.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Jochmans D, Dallmeir K, et al. Favipiravir (T-705) inhibits in vitro norovirus replication. Biochem Biophys Res Comm. 2012;424:777–780.
   PubMed Web of Science ®Google Scholar
• Jin Z, Tucker K, Lin X, et al. Biochemical evaluation of the inhibition properties of favipiravir and 2ʹ-C-methyl-cytidine triphosphate against human and mouse norovirus RNA polymerases. Antimicrob Chemother. 2015;59:7504–7516.
   PubMed Web of Science ®Google Scholar
• Eltahla AA, Lim KL, Eden JS, et al. Nonnucleoside inhibitors of norovirus RNA polymerase: scaffolds for rational drug design. Antimicrob Agents Chemother. 2014;58:3115–3123.
   PubMed Web of Science ®Google Scholar
• Envirgen Inc. Inhibition of calicivirus (norovirus). WO 0,196,98A2. 2010 Feb 18.
   Google Scholar
• Vashist S, Urena L, Gonzalez-Hernandez MB, et al. The molecular chaperone Hsp90 is a therapeutic target for noroviruses. J Virol. 2015;89:6352–6363.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Hernandez MB, Pal A, Gyan KE, et al. Chemical derivatives of a small molecule deubiquitinase inhibitor have antiviral activity against several RNA viruses. PLoS One. 2014;9(4):e94491.
   PubMed Web of Science ®Google Scholar
• Chaudhry Y, Nayak A, Bordeleau M-E, et al. Caliciviruses differ in their functional requirements for elF4F components. J Biol Chem. 2006;281:25315–25325.
   PubMed Web of Science ®Google Scholar
• Chang K-O. Role of cholesterol pathways in norovirus replication. J Virol. 2009;83:8587–8595.
   PubMed Web of Science ®Google Scholar
• Dou D, Tiew K-C, He G, et al. Potent inhibition of Norwalk virus by cyclic sulfamide derivatives. Bioorg Med Chem. 2011;19:5975–5983.
   PubMed Web of Science ®Google Scholar
• Dou D, Mandadapu SR, Alliston KR, et al. Cyclosulfamide-based derivatives as inhibitors of noroviruses. Eur J Med Chem. 2012;47:59–64.
   PubMed Web of Science ®Google Scholar
• Dou D, Tiew K-C, Mandadapu SR, et al. Potent norovirus inhibitors based on the acyclic sulfamide scaffold. Bioorg Med Chem. 2012;20:2111–2118.
   PubMed Web of Science ®Google Scholar
• Dou D, He G, Mandadapu SR, et al. Inhibition of noroviruses by piperazine derivatives. Bioorg Med Chem Lett. 2012;22:377–379.
   PubMed Web of Science ®Google Scholar
• Dou D, Mandadapu SR, Alliston KR, et al. Design and synthesis of potent inhibitors of noroviruses by scaffold hopping. Bioorg Med Chem. 2011;19:5782–5787.
   PubMedGoogle Scholar
• Pokhreil L, Kim Y, Nguyen TD, et al. Synthesis and anti-norovirus activity of pyranobenzopyrone compounds. Bioorg Med Chem Lett. 2012;22:3480–3484.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira J, Cunha R, Pinto DC, et al. (E)-2-Styrylchromones as potential anti-norovirus agents. Bioorg Med Chem. 2010;18:4195–4201.
   PubMed Web of Science ®Google Scholar
• Rossignol JF, El-Gohary Y. Nitazoxanide in treatment of viral gastroenteritis: a randomized double-blind, placebo-controlled clinical trial. Aliment Pharmacol Ther. 2006;24:1423–1430.
   PubMed Web of Science ®Google Scholar
• Siddiq DM, Koo HL, Adachi JA, et al Norovirus gastroenteritis successfully treated with nitazoxanide. J Infect. 2011;63:394–397.
   PubMed Web of Science ®Google Scholar
• Rossignol JF. Nitazoxanide: a first-in-class broad-spectrum antiviral agent. Antiviral Res. 2014;110:94–103.
   PubMed Web of Science ®Google Scholar
• Armando A, Emmott E, Vashist S, et al. Progress towards the prevention and treatment of norovirus infections. Future Microbiol. 2013;8:1475–1487.
   PubMed Web of Science ®Google Scholar
• Ecolab USA. Antiviral compositions and methods for inactivating non-enveloped viruses using alkyl 2-hydroxycarboxylic acids. WO 1,640,21A1. 2014 Oct 9.
   Google Scholar
• Hiroshima University, Japan. Anti-norovirus agent and composition containing the same. United State patent US 0,240,600A1. 2010 Sep 23.
   Google Scholar
• Altan Co. Method of disinfection or infection control against norovirus. Unites State patent US 0,023,582A1. 2013 Jan 24.
   Google Scholar
• Chang KO, George DW. Interferons and ribavirin effectively inhibit Norwalk virus replication in the replicon-bearing cells. J Virol. 2007;82:9306–9317.
   Google Scholar