Norovirus narita 104 virus-like particles expressed in nicotiana benthamiana induce serum and mucosal immune responses

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Mathew, Lolita George ^a,b   Herbst Kralovetz, Melissa M ^a,c   Mason, Hugh S ^a,b  

^a Arizona State University   (United States)

^b Arizona State University Main Campus   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; NARITA 104 VIRUS CAPSID PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; FEMALE; GENOTYPE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MOUSE; MUCOSAL IMMUNITY; NARITA 104 VIRUS; NICOTIANA BENTHAMIANA; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PROTEIN PURIFICATION; VIRUS LIKE AGENT; VIRUS PURIFICATION; ANIMAL; BIOSYNTHESIS; CELLULAR IMMUNITY; GASTROENTERITIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PATHOLOGY; TOBACCO; VIROLOGY;

ANIMALS; CAPSID PROTEINS; GASTROENTERITIS; GENE EXPRESSION REGULATION, PLANT; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMUNITY, CELLULAR; MICE; NOROVIRUS; TOBACCO;

EID: 84901759333     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/807539     Document Type: Article

References (51)

1. Glass R. I., Parashar U. D., Estes M. K., Norovirus gastroenteritis. New England Journal of Medicine 2009 361 18 1726 1785 2-s2.0-70350553836 10.1056/NEJMra0804575
2. Clarke I. N., Lambden P. R., The molecular biology of human caliciviruses. Novartis Foundation Symposium 2001 238 180 196 2-s2.0-0035237764 (Pubitemid 33603770)
3. Glass P. J., White L. J., Ball J. M., Leparc-Goffart I., Hardy M. E., Estes M. K., Norwalk virus open reading frame 3 encodes a minor structural protein. Journal of Virology 2000 74 14 6581 6591 2-s2.0-0033935684 10.1128/JVI.74.14.6581-6591.2000 (Pubitemid 30429827)
4. Jiang X., Wang M., Wang K., Estes M. K., Sequence and genomic organization of Norwalk virus. Virology 1993 195 1 51 61 2-s2.0-0027295302 10.1006/viro.1993.1345
5. Katayama K., Shirato-Horikoshi H., Kojima S., Kageyama T., Oka T., Hoshino F. B., Fukushi S., Shinohara M., Uchida K., Suzuki Y., Gojobori T., Takeda N., Phylogenetic analysis of the complete genome of 18 norwalk-like viruses. Virology 2002 299 2 225 239 2-s2.0-18744369021 10.1006/viro.2002.1568 (Pubitemid 35356599)
6. Noel J. S., Fankhauser R. L., Ando T., Monroe S. S., Glass R. I., Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. Journal of Infectious Diseases 1999 179 6 1334 1344 2-s2.0-0033029555 10.1086/314783 (Pubitemid 29246580)
7. Bull R. A., Tu E. T. V., McIver C. J., Rawlinson W. D., White P. A., Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. Journal of Clinical Microbiology 2006 44 2 327 333 2-s2.0-32344446102 10.1128/JCM.44.2.327-333.2006 (Pubitemid 43222218)
8. Fankhauser R. L., Monroe S. S., Noel J. S., Humphrey C. D., Bresee J. S., Parashar U. D., Ando T., Glass R. I., Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. Journal of Infectious Diseases 2002 186 1 1 7 2-s2.0-0036642439 10.1086/341085 (Pubitemid 34666907)
9. Kroneman A., Vennema H., Harris J., Reuter G., von Bonsdorff C. H., Hedlund K. O., Vainio K., Jackson V., Pothier P., Koch J., Schreier E., Böttiger B. E., Koopmans M., Increase in norovirus activity reported in Europe. Euro Surveillance 2006 11 12, article E061214.1 2-s2.0-33847055822
10. Lopman B., Vennema H., Kohli E., Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. The Lancet 2004 363 9410 682 688 2-s2.0-4344630154 10.1016/S0140-6736(04)16892-X (Pubitemid 39140621)
11. Medici M. C., Martinelli M., Abelli L. A., Ruggeri F. M., Di Bartolo I., Arcangeletti M. C., Pinardi F., De Conto F., Izzi G., Bernasconi S., Chezzi C., Dettori G., Molecular epidemiology of norovirus infections in sporadic cases of viral gastroenteritis among children in Northern Italy. Journal of Medical Virology 2006 78 11 1486 1492 2-s2.0-33749559015 10.1002/jmv.20723 (Pubitemid 44533880)
12. Phan T. G., Kuroiwa T., Kaneshi K., Ueda Y., Nakaya S., Nishimura S., Yamamoto A., Sugita K., Nishimura T., Yagyu F., Okitsu S., Müller W. E. G., Maneekarn N., Ushijima H., Changing distribution of norovirus genotypes and genetic analysis of recombinant GIIb among infants and children with diarrhea in Japan. Journal of Medical Virology 2006 78 7 971 978 2-s2.0-33744964905 10.1002/jmv.20649 (Pubitemid 43856707)
13. Vinjé J., Altena S. A., Koopmans M. P. G., The incidence and genetic variability of small round-structured viruses in outbreaks of gastroenteritis in The Netherlands. Journal of Infectious Diseases 1997 176 5 1374 1378 2-s2.0-0030785492 (Pubitemid 27461007)
14. Vipond I. B., Caul E. O., Hirst D., Carmen B., Curry A., Lopman B. A., Pead P., Pickett M. A., Lambden P. R., Clarke I. N., National epidemic of Lordsdale Norovirus in the UK. Journal of Clinical Virology 2004 30 3 243 247 2-s2.0-2442570836 10.1016/j.jcv.2003.11.011 (Pubitemid 38622007)
15. Widdowson M. A., Cramer E. H., Hadley L., Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus-United States, 2002. Journal of Infectious Diseases 2004 190 1 27 36 2-s2.0-10444228247 (Pubitemid 38858401)
16. Zheng D. P., Ando T., Fankhauser R. L., Beard R. S., Glass R. I., Monroe S. S., Norovirus classification and proposed strain nomenclature. Virology 2006 346 2 312 323 2-s2.0-33644817227 10.1016/j.virol.2005.11.015 (Pubitemid 43357875)
17. Jiang X., Wang M., Graham D. Y., Estes M. K., Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. Journal of Virology 1992 66 11 6527 6532 2-s2.0-0026649563
18. Mason H. S., Ball J. M., Shi J. J., Jiang X., Estes M. K., Arntzen C. J., Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proceedings of the National Academy of Sciences of the United States of America 1996 93 11 5335 5340 2-s2.0-0029891823 10.1073/pnas.93.11.5335 (Pubitemid 26159450)
19. White L. J., Hardy M. E., Estes M. K., Biochemical characterization of a smaller form of recombinant Norwalk virus capsids assembled in insect cells. Journal of Virology 1997 71 10 8066 8072 2-s2.0-0030823649 (Pubitemid 27391767)
20. Ball J. M., Hardy M. E., Atmar R. L., Conner M. E., Estes M. K., Oral immunization with recombinant Norwalk virus-like particles induces a systemic and mucosal immune response in mice. Journal of Virology 1998 72 2 1345 1353 2-s2.0-0031906229 (Pubitemid 28116920)
21. Santi L., Batchelor L., Huang Z., Hjelm B., Kilbourne J., Arntzen C. J., Chen Q., Mason H. S., An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 2008 26 15 1846 1854 2-s2.0-40849140609 10.1016/j.vaccine.2008.01.053
22. Mathew L. G., Maloney B., Takeda N., Mason H. S., Spurious polyadenylation of Norovirus Narita 104 capsid protein mRNA in transgenic plants. Plant Molecular Biology 2011 75 3 263 275 2-s2.0-79151478470 10.1007/s11103-010-9725-1
23. Gleba Y., Klimyuk V., Marillonnet S., Magnifection-a new platform for expressing recombinant vaccines in plants. Vaccine 2005 23 17-18 2042 2048 2-s2.0-14844293838 10.1016/j.vaccine.2005.01.006 (Pubitemid 40341424)
24. Marillonnet S., Giritch A., Gils M., Kandzia R., Klimyuk V., Gleba Y., In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium. Proceedings of the National Academy of Sciences of the United States of America 2004 101 18 6852 6857 2-s2.0-2342525801 10.1073/pnas.0400149101 (Pubitemid 38596407)
25. Marillonnet S., Thoeringer C., Kandzia R., Klimyuk V., Gleba Y., Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nature Biotechnology 2005 23 6 718 723 2-s2.0-24944498904 10.1038/nbt1094 (Pubitemid 41716362)
26. Green J., Vinje J., Gallimore C. I., Koopmans M., Hale A., Brown D. W. G., Capsid protein diversity among norwalk-like viruses. Virus Genes 2000 20 3 227 236 2-s2.0-17944377945 10.1023/A:1017468929961 (Pubitemid 30479541)
27. Hardy M. E., Tanaka T. N., Kitamoto N., White L. J., Ball J. M., Jang X., Estes M. K., Antigenic mapping of the recombinant Norwalk virus capsid protein using monoclonal antibodies. Virology 1996 217 1 252 261 2-s2.0-0029977575 10.1006/viro.1996.0112 (Pubitemid 26103614)
28. Kitamoto N., Tanaka T., Natori K., Takeda N., Nakata S., Jiang X., Estes M. K., Cross-reactivity among several recombinant calicivirus virus-like particles (VLPs) with monoclonal antibodies obtained from mice immunized orally with one type of VLP. Journal of Clinical Microbiology 2002 40 7 2459 2465 2-s2.0-0036305288 10.1128/JCM.40.7.2459-2465.2002 (Pubitemid 34747347)
29. Faye L., Gomord V., Success stories in molecular farming-a brief overview. Plant Biotechnology Journal 2010 8 5 525 528 2-s2.0-77954018329 10.1111/j.1467-7652.2010.00521.x
30. Mason H. S., Warzecha H., Mor T., Arntzen C. J., Edible plant vaccines: applications for prophylactic and therapeutic molecular medicine. Trends in Molecular Medicine 2002 8 7 324 329 2-s2.0-0036305744 10.1016/S1471-4914(02) 02360-2 (Pubitemid 34733385)
31. Gils M., Kandzia R., Marillonnet S., Klimyuk V., Gleba Y., High-yield production of authentic human growth hormone using a plant virus-based expression system. Plant Biotechnology Journal 2005 3 6 613 620 2-s2.0-33744933668 10.1111/j.1467-7652.2005.00154.x (Pubitemid 44944500)
32. Golovkin M., Spitsin S., Andrianov V., Smirnov Y., Xiao Y., Pogrebnyak N., Markley K., Brodzik R., Gleba Y., Isaacs S. N., Koprowski H., Smallpox subunit vaccine produced in planta confers protection in mice. Proceedings of the National Academy of Sciences of the United States of America 2007 104 16 6864 6869 2-s2.0-34249860300 10.1073/pnas.0701451104 (Pubitemid 47175592)
33. Huang Z., Santi L., LePore K., Kilbourne J., Arntzen C. J., Mason H. S., Rapid, high-level production of hepatitis B core antigen in plant leaf and its immunogenicity in mice. Vaccine 2006 24 14 2506 2513 2-s2.0-33344479476 10.1016/j.vaccine.2005.12.024 (Pubitemid 43290380)
34. Santi L., Huang Z., Mason H., Virus-like particles production in green plants. Methods 2006 40 1 66 76 2-s2.0-33748780696 10.1016/j.ymeth.2006.05.020 (Pubitemid 44415500)
35. Mason H. S., Lam D. M. K., Arntzen C. J., Expression of hepatitis B surface antigen in transgenic plants. Proceedings of the National Academy of Sciences of the United States of America 1992 89 24 11745 11749 2-s2.0-0027048769 10.1073/pnas.89.24.11745 (Pubitemid 23004720)
36. Zor T., Selinger Z., Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Analytical Biochemistry 1996 236 2 302 308 2-s2.0-0029917011 10.1006/abio.1996.0171 (Pubitemid 26136110)
37. Lai H., Chen Q., Bioprocessing of plant-derived virus-like particles of Norwalk virus capsid protein under current Good Manufacture Practice regulations. Plant Cell Reports 2012 31 3 573 584 2-s2.0-84856962688 10.1007/s00299-011-1196-6
38. Velasquez L. S., Hjelm B. E., Arntzen C. J., Herbst-Kralovetz M. M., An intranasally delivered toll-like receptor 7 agonist elicits robust systemic and mucosal responses to Norwalk virus-like particles. Clinical and Vaccine Immunology 2010 17 12 1850 1858 2-s2.0-78649863790 10.1128/CVI.00230-10
39. Huang Z., Chen Q., Hjelm B., Arntzen C., Mason H., A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnology and Bioengineering 2009 103 4 706 714 2-s2.0-67650156117 10.1002/bit.22299
40. Zhang X., Buehner N. A., Hutson A. M., Estes M. K., Mason H. S., Tomato is a highly effective vehicle for expression and oral immunization with Norwalk virus capsid protein. Plant Biotechnology Journal 2006 4 4 419 432 2-s2.0-33745085830 10.1111/j.1467-7652.2006.00191.x (Pubitemid 43886814)
41. Jackson E. M., Herbst-Kralovetz M. M., Intranasal vaccination with murabutide enhances humoral and mucosal immune responses to a virus-like particle vaccine. PLoS ONE 2012 7 7 e41529 10.1371/journal.pone.0041529
42. Schiller J. T., Castellsague X., Garland S. M., A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 2012 30 supplement 5 F123 F138 10.1016/j.vaccine.2012.04.108
43. Ball J. M., Estes M. K., Hardy M. E., Conner M. E., Opekun A. R., Graham D. Y., Recombinant Norwalk virus-like particles as an oral vaccine. Archives of Virology, Supplement 1996 1996 12 243 249 2-s2.0-0030346069 (Pubitemid 126446232)
44. Hardy M. E., White L. J., Ball J. M., Estes M. K., Specific proteolytic cleavage of recombinant Norwalk virus capsid protein. Journal of Virology 1995 69 3 1693 1698 2-s2.0-0028861304
45. Green K. Y., Lew J. F., Jiang X., Kapikian A. Z., Estes M. K., Comparison of the reactivities of baculovirus-expressed recombinant Norwalk virus capsid antigen with those of the native Norwalk virus antigen in serologic assays and some epidemiologic observations. Journal of Clinical Microbiology 1993 31 8 2185 2191 2-s2.0-0027240069 (Pubitemid 23210516)
46. Velasquez L. S., Shira S., Berta A. N., Kilbourne J., Medi B. M., Tizard I., Ni Y., Arntzen C. J., Herbst-Kralovetz M. M., Intranasal delivery of Norwalk virus-like particles formulated in an in situ gelling, dry powder vaccine. Vaccine 2011 29 32 5221 5231 2-s2.0-79960323464 10.1016/j.vaccine.2011.05.027
47. Huang Z., Elkin G., Maloney B. J., Beuhner N., Arntzen C. J., Thanavala Y., Mason H. S., Virus-like particle expression and assembly in plants: hepatitis B and Norwalk viruses. Vaccine 2005 23 15 1851 1858 2-s2.0-14744283794 10.1016/j.vaccine.2004.11.017 (Pubitemid 40331858)
48. Vega E., Barclay L., Gregoricus N., Shirley S. H., Lee D., Vinje J., Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. Journal of Clinical Microbiology 2014 52 1 147 155 10.1128/JCM.02680-13
49. Gleba Y., Klimyuk V., Marillonnet S., Viral vectors for the expression of proteins in plants. Current Opinion in Biotechnology 2007 18 2 134 141 2-s2.0-34147095513 10.1016/j.copbio.2007.03.002 (Pubitemid 46575232)
50. Prasad B. V. V., Hardy M. E., Dokland T., Bella J., Rossmann M. G., Estes M. K., X-ray crystallographic structure of the Norwalk virus capsid. Science 1999 286 5438 287 290 2-s2.0-0033536662 10.1126/science.286.5438.287 (Pubitemid 29484691)
51. Ellis R. J., The most abundant protein in the world. Trends in Biochemical Sciences 1979 4 11 241 244 2-s2.0-49249144575