Development of a Gaussia luciferase-based human norovirus protease reporter system: Cell type-specific profile of norwalk virus protease precursors and evaluation of inhibitors

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10312-10326

  Qu, Lin ^a   Vongpunsawad, Sompong ^a   Atmar, Robert L ^a   Venkataram Prasad, B V ^a   Estes, Mary K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; ENZYME PRECURSOR; GAUSSIA LUCIFERASE; HYBRID PROTEIN; LUCIFERASE; P41 PROTEIN; PROTEIN PRECURSOR; PROTEINASE INHIBITOR; TOSYLLYSYL CHLOROMETHYL KETONE; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC CHLORIDE; PEPTIDE HYDROLASE; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL SPECIFICITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; ENZYMIC BIOSENSOR; EXPRESSION VECTOR; GENE CONSTRUCT; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; NONHUMAN; NOROGLUC; NOROVIRUS; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN CLEAVAGE; PROTEINASE INHIBITION; RNA REPLICATION; SENSITIVITY AND SPECIFICITY; VIRUS REPLICATION; ANIMAL; COPEPOD; DRUG EFFECTS; ENZYMOLOGY; GASTROENTERITIS; GENETICS; METABOLISM; NORWALK VIRUS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; SPECIES DIFFERENCE; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; COPEPODA; ENZYME PRECURSORS; GASTROENTERITIS; GENES, REPORTER; HUMANS; LUCIFERASES; NORWALK VIRUS; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SPECIES SPECIFICITY; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84906347245     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01111-14     Document Type: Article

References (41)

1. Ramani S, Atmar RL, Estes MK. 2014. Epidemiology of human noroviruses and updates on vaccine development. Curr. Opin. Gastroenterol. 30:25-33. http://dx.doi.org/10.1097/MOG.0000000000000022.
2. Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD. 2013. Norovirus and medically attended gastroenteritis in U.S. children. N. Engl. J. Med. 368:1121-1130. http://dx.doi.org/10.1056/NEJMsa1206589.
3. Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A, Dupont HL, Atmar RL. 2013. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J. Pediatr. Infect. Dis. Soc. 2:57-60. http://dx.doi.org/10.1093/jpids/pis070.
4. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH, Atmar RL, Estes MK. 2007. Norwalk virus RNA is infectious in mammalian cells. J. Virol. 81:12238-12248. http://dx.doi.org/10.1128/JVI.01489-07.
5. Glass PJ, White LJ, Ball JM, Leparc-Goffart I, Hardy ME, Estes MK. 2000. Norwalk virus open reading frame 3 encodes a minor structural protein. J. Virol. 74:6581-6591. http://dx.doi.org/10.1128/JVI.74.14.6581-6591.2000.
6. Jiang X, Wang M, Wang K, Estes MK. 1993. Sequence and genomic organization of Norwalk virus. Virology 195:51-61. http://dx.doi.org/10.1006/viro.1993.1345.
7. Vongpunsawad S, Venkataram Prasad BV, Estes MK. 2013. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J. Virol. 87:4818-4825. http://dx.doi.org/10.1128/JVI.03508-12.
8. Ettayebi K, Hardy ME. 2003. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J. Virol. 77:11790-11797. http://dx.doi.org/10.1128/JVI.77.21.11790-11797.2003.
9. Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. 2010. Inhibition of cellular protein secretion by Norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 5:e13130. http://dx.doi.org/10.1371/journal.pone.0013130.
10. Pfister T, Wimmer E. 2001. Polypeptide p41 of a Norwalk-like virus is a nucleic acid-independent nucleoside triphosphatase. J. Virol. 75:1611-1619. http://dx.doi.org/10.1128/JVI.75.4.1611-1619.2001.
11. Daughenbaugh KF, Fraser CS, Hershey JW, Hardy ME. 2003. The genome-linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J. 22:2852-2859. http://dx.doi.org/10.1093/emboj/cdg251.
12. Liu B, Clarke IN, Lambden PR. 1996. Polyprotein processing in Southampton virus: identification of 3C-like protease cleavage sites by in vitro mutagenesis. J. Virol. 70:2605-2610.
13. Liu BL, Viljoen GJ, Clarke IN, Lambden PR. 1999. Identification of further proteolytic cleavage sites in the Southampton calicivirus polyprotein by expression of the viral protease in E. coli. J. Gen. Virol. 80:291-296.
14. Blakeney SJ, Cahill A, Reilly PA. 2003. Processing of Norwalk virus nonstructural proteins by a 3C-like cysteine proteinase. Virology 308: 216-224. http://dx.doi.org/10.1016/S0042-6822(03)00004-7.
15. Ng KK, Pendas-Franco N, Rojo J, Boga JA, Machin A, Alonso JM, Parra F. 2004. Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J. Biol. Chem. 279:16638-16645. http://dx.doi.org/10.1074/jbc.M400584200.
16. Deng L, Muhaxhiri Z, Estes MK, Palzkill T, Prasad BV, Song Y. 2013. Synthesis, activity and structure-activity relationship of noroviral pro-tease inhibitors. MedChemComm 4(10). http://dx.doi.org/10.1039/C3MD00219E.
17. Rocha-Pereira J, Jochmans D, Debing Y, Verbeken E, Nascimento MS, Neyts J. 2013. The viral polymerase inhibitor 2'-C-methylcytidine inhibits Norwalk virus replication and protects against norovirus-induced diarrhea and mortality in a mouse model. J. Virol. 87:11798-11805. http://dx.doi.org/10.1128/JVI.02064-13.
18. Tarantino D, Pezzullo M, Mastrangelo E, Croci R, Rohayem J, Robel I, Bolognesi M, Milani M. 2013. Naphthalene-sulfonate inhibitors of human norovirus RNA-dependent RNA-polymerase. Antiviral Res. 102:23-28. http://dx.doi.org/10.1016/j.antiviral.2013.11.016.
19. Chang KO, Takahashi D, Prakash O, Kim Y. 2012. Characterization and inhibition of norovirus proteases of genogroups I and II using a fluorescence resonance energy transfer assay. Virology 423:125-133. http://dx.doi.org/10.1016/j.virol.2011.12.002.
20. Kim Y, Lovell S, Tiew KC, Mandadapu SR, Alliston KR, Battaile KP, Groutas WC, Chang KO. 2012. Broad-spectrum antivirals against 3C or 3C-like proteases of picornaviruses, noroviruses, and coronaviruses. J. Virol. 86:11754-11762. http://dx.doi.org/10.1128/JVI.01348-12.
21. Muhaxhiri Z, Deng L, Shanker S, Sankaran B, Estes MK, Palzkill T, Song Y, Prasad BV. 2013. Structural basis of substrate specificity and protease inhibition in Norwalk virus. J. Virol. 87:4281-4292. http://dx.doi.org/10.1128/JVI.02869-12.
22. Prior AM, Kim Y, Weerasekara S, Moroze M, Alliston KR, Uy RA, Groutas WC, Chang KO, Hua DH. 2013. Design, synthesis, and bioevaluation of viral 3C and 3C-like protease inhibitors. Bioorg. Med. Chem. Lett. 23:6317-6320. http://dx.doi.org/10.1016/j.bmcl.2013.09.070.
23. Someya Y, Takeda N, Miyamura T. 2002. Identification of active-site amino acid residues in the Chiba virus 3C-like protease. J. Virol. 76:5949-5958. http://dx.doi.org/10.1128/JVI.76.12.5949-5958.2002.
24. Zeitler CE, Estes MK, Venkataram Prasad BV. 2006. X-ray crystallographic structure of the Norwalk virus protease at 1.5-A resolution. J. Virol. 80:5050-5058. http://dx.doi.org/10.1128/JVI.80.10.5050-5058.2006.
25. Bartok E, Bauernfeind F, Khaminets MG, Jakobs C, Monks B, Fitzgerald KA, Latz E, Hornung V. 2013. iGLuc: a luciferase-based inflammasome and protease activity reporter. Nat. Methods 10:147-154. http://dx.doi.org/10.1038/nmeth.2327.
26. Niers JM, Kerami M, Pike L, Lewandrowski G, Tannous BA. 2011. Multimodal in vivo imaging and blood monitoring of intrinsic and extrinsic apoptosis. Mol. Ther. 19:1090-1096. http://dx.doi.org/10.1038/mt.2011.17.
27. Ketteler R, Sun Z, Kovacs KF, He WW, Seed B. 2008. A pathway sensor for genome-wide screens of intracellular proteolytic cleavage. Genome Biol. 9:R64. http://dx.doi.org/10.1186/gb-2008-9-4-r64.
28. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO. 2005. Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol. Ther. 11:435-443. http://dx.doi.org/10.1016/j.ymthe.2004.10.016.
29. Tannous BA, Teng J. 2011. Secreted blood reporters: insights and applications. Biotechnol. Adv. 29:997-1003. http://dx.doi.org/10.1016/j.biotechadv.2011.08.021.
30. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Ramani S, Hill H, Ferreira J, Graham DY. 2014. Determination of the 50% human infectious dose for Norwalk virus. J. Infect. Dis. 209:1016-1022. http://dx.doi.org/10.1093/infdis/jit620.
31. Asanaka M, Atmar RL, Ruvolo V, Crawford SE, Neill FH, Estes MK. 2005. Replication and packaging of Norwalk virus RNA in cultured mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 102:10327-10332. http://dx.doi.org/10.1073/pnas.0408529102.
32. Cathomen T, Buchholz CJ, Spielhofer P, Cattaneo R. 1995. Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 214:628-632. http://dx.doi.org/10.1006/viro.1995.0075.
33. Ajami NJ, Barry MA, Carrillo B, Muhaxhiri Z, Neill FH, Prasad BV, Opekun AR, Gilger MA, Graham DY, Atmar RL, Estes MK. 2012. Antibody responses to norovirus genogroup GI.1 and GII.4 proteases in volunteers administered Norwalk virus. Clin. Vaccine Immunol. 19: 1980-1983. http://dx.doi.org/10.1128/CVI.00411-12.
34. Jiang X, Wang M, Graham DY, Estes MK. 1992. Expression, selfassembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66:6527-6532.
35. Gilpatrick SG, Schwab KJ, Estes MK, Atmar RL. 2000. Development of an immunomagnetic capture reverse transcription-PCR assay for the detection of Norwalk virus. J. Virol. Methods 90:69-78. http://dx.doi.org/10.1016/S0166-0934(00)00220-2.
36. Belliot G, Sosnovtsev SV, Mitra T, Hammer C, Garfield M, Green KY. 2003. In vitro proteolytic processing of the MD145 norovirus ORF1 nonstructural polyprotein yields stable precursors and products similar to those detected in calicivirus-infected cells. J. Virol. 77:10957-10974. http://dx.doi.org/10.1128/JVI.77.20.10957-10974.2003.
37. Cho MW, Teterina N, Egger D, Bienz K, Ehrenfeld E. 1994. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology 202:129-145. http://dx.doi.org/10.1006/viro.1994.1329.
38. May J, Korba B, Medvedev A, Viswanathan P. 2013. Enzyme kinetics of the human norovirus protease control virus polyprotein processing order. Virology 444:218-224. http://dx.doi.org/10.1016/j.virol.2013.06.013.
39. Chang KO, Sosnovtsev SV, Belliot G, King AD, Green KY. 2006. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353:463-473. http://dx.doi.org/10.1016/j.virol.2006.06.006.
40. Noel JS, Fankhauser RL, Ando T, Monroe SS, Glass RI. 1999. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. J. Infect. Dis. 179:1334-1344. http://dx.doi.org/10.1086/314783.
41. Leshem E, Wikswo M, Barclay L, Brandt E, Storm W, Salehi E, DeSalvo T, Davis T, Saupe A, Dobbins G, Booth HA, Biggs C, Garman K, Woron AM, Parashar UD, Vinje J, Hall AJ. 2013. Effects and clinical significance of GII.4 Sydney norovirus, United States, 2012-2013. Emerg. Infect. Dis. 19:1231-1238. http://dx.doi.org/10.3201/eid1908.130458.