Human norovirus infection of Caco-2 cells grown as a three-dimensional tissue structure

Journal of Water and Health

Volumn 9, Issue 2, 2011, Pages 225-240

  Straub, Timothy M ^a   Bartholomew, Rachel A ^a   Valdez, Catherine O ^a   Valentine, Nancy B ^a   Dohnalkova, Alice ^a   Ozanich, Richard M ^a   Bruckner Lea, Cynthia J ^a   Call, Douglas R ^b  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Cell culture; In vitro organoids; Infectivity; Noroviruses; Quantitative PCR

Indexed keywords

VIRUS ANTIGEN; VIRUS RNA;

BIOREACTOR; EXPERIMENTAL STUDY; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REAL TIME; SAMPLING; THREE-DIMENSIONAL MODELING; VIRUS;

ANTIGEN DETECTION; ARTICLE; BIOREACTOR; CALICIVIRUS INFECTION; CELL GROWTH; CELL LYSATE; CELL STRAIN CACO 2; CELL VACUOLE; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; LARGE INTESTINE; MICROVILLUS; NONHUMAN; NOROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE CULTURE; TISSUE STRUCTURE; VIRUS CAPSID;

CACO-2 CELLS; CALICIVIRIDAE INFECTIONS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CYTOPATHOGENIC EFFECT, VIRAL; DNA, VIRAL; HUMANS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON; MICROSPHERES; NOROVIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MAMMALIA; MIRIDAE; NOROVIRUS;

EID: 79958752788     PISSN: 14778920     EISSN: None     Source Type: Journal    
DOI: 10.2166/wh.2010.106     Document Type: Article

References (36)

1. Asanaka, M., Atmar, R. L., Ruvolo, V., Crawford, S. E., Neill, F. H. & Estes, M. K. 2005 Replication and packaging of norwalk virus RNA in cultured cells. Proc. Natl. Acad. Sci. 102(29), 10327-10332.
2. Atmar, R. L., Opeku, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H. & Graham, D. Y. 2008 Norwalk virus shedding after experimental human infection. Emerg. Infect. Dis. 14(10), 1533-1537.
3. Carterson, A. J., Honer zu Bentrup, K., Ott, C. M., Clarke, M. S., Pierson, D. L., Vanderburg, C. R., Buchanan, K. L., Nickerson, C. A. & Schurr, M. J. 2005 A549 Lung epithelial cells grown as three-dimensional aggregates: Alternative tissue culture model for Psuedomonas aeruginosa. Infect. Immun. 73(2), 1129-1140.
4. Carvalho, H. M., Teel, L. D., Goping, G. & O'Brien, A. D. 2005 A three dimensional tissue culture model for the study of attach and efface lesion formation by enteropathogenic and enterohaemorrhagic Esherichia coli. Cell. Microbiol. 7, 1771-1781.
5. Centers for Disease Control and Prevention (US) 2007 Norovirus activity: United States, 2006-2007. MMWR Morb. Mortal. Wkly. Rep. 56(33), 842-846.
6. Cheetham, S., Souza, M., McGregor, R., Meulia, T., Wang, Q. & Saif, L. J. 2007 Binding patterns of human norovirus-like particles to buccal and intestinal tissue of gnotobiotic pigs in relation to A/H histo-blood group antigen expression. J. Virol. 81, 3535-3544. (Pubitemid 46456662)
7. Cheetham, S., Souza, M.,Meulia, T., Grimes, S., Han,M.-G.&Saif, L. J. 2006 Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J. Virol. 80(21), 10372-10381.
8. Dolin, R., Levy, A. G., Wyatt, R. G., Thornhill, T. S. & Gardner, J. D. 1975 Viral gastroenteritis induced by the Hawaii agent. Jejunal histopathology and serologic response. Am. J. Med. 59, 761-768.
9. Duizer, E., Schwab, K. G., Neill, F. H., Atmar, R. L., Koopmans, M. P. G. & Estes, M. K. 2004 Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85, 79-87.
10. Frankhauser, R. L., Monroe, S. S., Noel, J. S., Humphrey, C. D., Bersee, J. S., Parashar, U. D., Ando, T. & Glass, R. I. 2002 Epidemiologic and molecular trends of 'Norwalk-like viruses' associated with gastroenteritis in the United States. J. Infect. Dis. 186, 1-7.
11. Guix, S., Asanaka, M., Katayama, K., Crawford, S. E., Neill, F. H., Atmar, R. L. & Estes, M. K. 2007 Norwalk virus RNA is infectious in mammalian cells. J. Virol. 81(22), 12238-12248. (Pubitemid 350085839)
12. Harrington, P. R., Lindesmith, L., Yount, B., Moe, C. L. & Baric, R. S. 2002 Binding of norwalk virus-like particles to abh histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 76(23), 12335-12343. (Pubitemid 35304332)
13. Harrington, P. R., Vinje, J., Moe, C. L. & Baric, R. S. 2004 Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J. Virol. 78(6), 3035-3045. (Pubitemid 38314361)
14. Honer zu Bentrup, K., Ramamurthy, R., Ott, M., Emami, K., Nelman-Gonzalez, M., Wilson, J. W., Richter, E. G., Goodwin, T., Pierson, D., Alexander, S., Pellis, N., Buchanan, K.&Nickerson, C. A. 2006 3-D organotypic models of human colonic epithelium to study the early stages of enteric salmonellosis. Microbes Infect. 8(7), 1813-1825.
15. Hutson, A. M., Atmar, R. L., Marcus, D. M. & Estes, M. K. 2003 Norwalk virus-like particle hemagglutination by binding to H histo-blood group antigens. J. Virol. 77(1), 405-415. (Pubitemid 36004980)
16. Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N. & Katayama, K. 2003 Broadly reactive, highly sensitive assay for norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol., 41(4), 1548-1557.
17. Karst, S. M. 2010 Pathogenesis of noroviruses, emerging RNA viruses. Viruses 2 748-781.
18. Lamarca, H. L., Ott, C. M., Honer zu Bentrup, K., Leblanc, C. L., Pierson, D. L., Nelson, A. B., Scandurro, A. B., Whitley, G. S., Nickerson, C. A. & Morris, C. A. 2005 Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta 26(10), 709-720.
19. Lay, M. K., Atmar, R. L., Guix, S., Bharadwaj, U., He, H., Neill, F. H., Sastry, K. J., Yao, Q. & Estes, M. K. 2010 Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology 406(1), 1-11
20. Long, J. P.&Hughes, J. H. 2001 Epstein-Barr virus latently infected cells are selectively deleted in simulated microgravity cultures. In Vitro Cell. Dev. Biol. Anim. 37, 223-230.
21. Long, J. P., Pierson, S. & Hughes, J. H. 1999 Suppression of Epstein-Barr virus reactivation in lymphobalstoid cells cultured in simulated microgravity. In Vitro Cell. Dev. Biol. 35, 49-54. (Pubitemid 29058796)
22. Marionneau, S., Ruvoen, N., Le Moullac-Vaidye, B., Clement, M., Cailleau-Thomas, A., Ruiz-Palacois, G., Huang, P., Jiang, X. & Le Pendu, J. 2002 Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122, 1967-1977. (Pubitemid 34651439)
23. Nickerson, C. A., Goodwin, T. J., Terlonge, J., Ott, C. M., Buchanan, K. L., Uicker, W. C., Emami, K., LeBlanc, C. L., Ramamurthy, R., Clarke, M. S., Vanderburg, C. R., Hammond, T. & Pierson, D. L. 2001 Three dimensional tissue assemblies: Novel models for the study of Salmonella enterica serovar typhimurium pathogenesis. Infect. Immun. 69(11), 7106-7120.
24. Nickerson, C. A. Honer zu Bentrup, K. & Ott, C. M. 2005 Three-dimensional cell culture models for drug discovery and infectious disease. Bioforum Eur. 6, 34-36.
25. Nickerson, C. A. & Ott, C. M. 2004 A new dimension in modeling infectious disease. ASM News 70(4), 169-175. (Pubitemid 41296251)
26. Peterson, M. D. & Mooseker, M. S. 1992 Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J. Cell Sci. 102, 581-600.
27. Reynolds, E. S. 1963 Use of lead citrate as high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17(1), 208-212.
28. Rochelle, P. A., Marshall,M.M., Mead, J. R., Johnson, A.M., Korich, D. G., Rosen, J. S. & DeLeon, R. 2002 Comparison of in vitro cell culture and mouse assay for measuring infectivity of Cryptosporidium parvum. Appl. Environ. Microbiol. 68(8), 3809-3817.
29. Schreiber, D. S., Blacklow, N. R. & Trier, J. S. 1973 The mucosal lesion of the proximal small intestine in acute infectious nonbacterial gastroenteritis. New Engl. J. Med. 288, 1318-1323.
30. Souza, M., Asevedo, M. S. P., Jung, K., Cheetham, S. & Saif, L. J. 2008 Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-hs66 strain of human norovirus. J. Virol. 82(4), 1777-1786. (Pubitemid 351206927)
31. Straub, T. M., Honer zu Bentrup, K., Orosz-Coghlan, P., Dohnalkova, A., Mayer, B.K., Bartholomew, R., Valdez, C.O., Bruckner-Lea, C.J., Gerba, C.P., Abbaszadegan, M. & Nickerson, C.A. 2007 In vitro cell culture assay for human noroviruses. Emerg. Infect. Dis. 13(3), 396-403.
32. Thorven, M., Grahn, A., Hedlund, K.-O., Johansson, H., Wahlfrid, C., Larson, G.&Svensson, L. 2005 A homozygous nonsense mutation (428 G to A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J. Virol. 79(24), 15351-15355.
33. Troeger, H., Loddenkemper, C., Schneider, T., Schreier, E., Eppke, H.-J., Zeitz, M., Fromm, M. & Schulzke, J.-D. 2009 Structural and functional changes of the duodenum in human norovirus infection. Gut 58, 1070-1077.
34. White, L. J., Ball, J. M., Hardy, M. E., Tanaka, T. N., Kitamoto, N. & Estes, M. K. 1996 Attachment and entry of recombinant norwalk virus capsids to cultured human and animal cell lines. J. Virol. 70(10), 6589-6597. (Pubitemid 26307363)
35. Wobus, C. E., Karst, S. E., Thackray, L. B., Chang, K.-O., Sosnovtsev, S. V., Belliot, G., Mackenzie, J. M., Green, K. Y. & Virgin IV, H. W. 2004 Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2(12), 2076-2084.
36. Wobus, C. E., Thackray, L. B. & Virgin IV, H. W. 2006 Murine norovirus: A model system to study norovirus biology and pathogenesis. J. Virol. 80(11), 5104-5112.