Murine norovirus transcytosis across an in vitro polarized murine intestinal epithelial monolayer is mediated by M-like cells

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12685-12693

  Gonzalez Hernandez, Mariam B ^a   Liu, Thomas ^a   Blanco, Luz P ^a,b   Auble, Heather ^a   Payne, Hilary C ^a   Wobus, Christiane E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A RECEPTOR; IMMUNOGLOBULIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL DISRUPTION; CONTROLLED STUDY; DENDRITIC CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; MACROPHAGE; MICROFOLD CELL; MONOLAYER CULTURE; MOUSE; MYELOMA CELL; NONHUMAN; NOROVIRUS; POLARIZATION; PRIORITY JOURNAL; TIGHT JUNCTION; TRANSCYTOSIS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ANIMALS; CALICIVIRIDAE INFECTIONS; CELL LINE; CELL POLARITY; EPITHELIAL CELLS; HUMANS; INTESTINES; MICE; NOROVIRUS; TRANSCYTOSIS; VIRUS INTERNALIZATION;

EID: 84887137803     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02378-13     Document Type: Article

References (56)

1. Hansman GS, Jiang XJ, Green KY (ed). 2010. Caliciviruses:molecular and cellular virology, 1st ed, vol 1. Caister Academic Press, Norfolk, United Kingdom.
2. Green KY. 2007. Caliciviridae, p 949-980. In Knipe DM Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
3. Widdowson MA, Monroe SS, Glass RI. 2005. Are noroviruses emerging? Emerg. Infect. Dis. 11:735-737.
4. Blanton LH, Adams SM, Beard RS, Wei G, Bulens SN, Widdowson MA, Glass RI, Monroe SS. 2006. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. J. Infect. Dis. 193:413-421.
5. Koopmans M, Vinje J, Duizer E, de Wit M, van Duijnhoven Y. 2001. Molecular epidemiology of human enteric caliciviruses in The Netherlands. Novartis Found. Symp. 238:197-214.
6. Noda M, Fukuda S, Nishio O. 2008. Statistical analysis of attack rate in norovirus foodborne outbreaks. Int. J. Food Microbiol. 122:216-220.
7. Bernard H, Hohne M, Niendorf S, Altmann D, Stark K. 21 March 2013. Epidemiology of norovirus gastroenteritis in Germany 2001-2009:eight seasons of routine surveillance. Epidemiol. Infect. doi:10.1017/S0950268813000435.
8. Matthews JE, Dickey BW, Miller RD, Felzer JR, Dawson BP, Lee AS, Rocks JJ, Kiel J, Montes JS, Moe CL, Eisenberg JN, Leon JS. 2012. The epidemiology of published norovirus outbreaks:a review of risk factors associated with attack rate and genogroup. Epidemiol. Infect. 140:1161-1172.
9. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
10. Hall AJ, Curns AT, McDonald LC, Parashar UD, Lopman BA. 2012. The roles of Clostridium difficile and norovirus among gastroenteritisassociated deaths in the United States, 1999-2007. Clin. Infect. Dis. 55:216-223.
11. Herbst-Kralovetz MM, Radtke AL, Lay MK, Hjelm BE, Bolick AN, Sarker SS, Atmar RL, Kingsley DH, Arntzen CJ, Estes MK, Nickerson CA. 2013. Lack of norovirus replication and histo-blood group antigen expression in 3-dimensional intestinal epithelial cells. Emerg. Infect. Dis. 19:431-438.
12. Duizer E, Schwab KJ, Neill FH, Atmar RL, Koopmans MP, Estes MK. 2004. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85:79-87.
13. Taube S, Kolawole AO, Hoehne M, Wilkinson JE, Hanley SA, Perry JW, Thackray LB, Akkina R, Wobus CE. 2013. A mouse model for human norovirus. mBio 4(4):e00450-13. doi:10.1128/mBio.00450-13.
14. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW, IV. 2003. STAT1-dependent innate immunity to a Norwalk-like virus. Science 299:1575-1578.
15. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW. 2004. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2:e432. doi:10.1371/journal.pbio.0020432.
16. Wobus CE, Thackray LB, Virgin HW, IV. 2006. Murine norovirus:a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104-5112.
17. Thackray LB, Wobus CE, Chachu KA, Liu B, Alegre ER, Henderson KS, Kelley ST, Virgin HW, IV. 2007. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J. Virol. 81:10460-10473.
18. Smith DB, McFadden N, Blundell RJ, Meredith A, Simmonds P. 2012. Diversity of murine norovirus in wild-rodent populations:speciesspecific associations suggest an ancient divergence. J. Gen. Virol. 93:259-266.
19. Muller B, Klemm U, Mas Marques A, Schreier E. 2007. Genetic diversity and recombination of murine noroviruses in immunocompromised mice. Arch. Virol. 152:1709-1719.
20. Nice TJ, Strong DW, McCune BT, Pohl CS, Virgin HW. 2013. A single-amino-acid change in murine norovirus NS1/2 is sufficient for colonic tropism and persistence. J. Virol. 87:327-334.
21. Taube S, Perry JW, Yetming K, Patel SP, Auble H, Shu L, Nawar HF, Lee CH, Connell TD, Shayman JA, Wobus CE. 2009. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J. Virol. 83:4092-4101.
22. Taube S, Perry JW, McGreevy E, Yetming K, Perkins C, Henderson K, Wobus CE. 2012. Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. J. Virol. 86:5584-5593.
23. Perry JW, Taube S, Wobus CE. 2009. Murine norovirus-1 entry into permissive macrophages and dendritic cells is pH-independent. Virus Res. 143:125-129.
24. Perry JW, Wobus CE. 2010. Endocytosis of murine norovirus 1 into murine macrophages is dependent on dynamin II and cholesterol. J. Virol. 84:6163-6176.
25. Gerondopoulos A, Jackson T, Monaghan P, Doyle N, Roberts LO. 2010. Murine norovirus-1 cell entry is mediated through a non-clathrin, noncaveolae, dynamin and cholesterol dependent pathway. J. Gen. Virol. 91:1428-1438.
26. Kraehenbuhl JP, Neutra MR. 2000. EpithelialMcells:differentiation and function. Annu. Rev. Cell Dev. Biol. 16:301-332.
27. Neutra MR, Mantis NJ, Frey A, Giannasca PJ. 1999. The composition and function of M cell apical membranes:implications for microbial pathogenesis. Semin. Immunol. 11:171-181.
28. Corr SC, Gahan CC, Hill C. 2008. M-cells:origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol. Med. Microbiol. 52:2-12.
29. Bens M, Bogdanova A, Cluzeaud F, Miquerol L, Kerneis S, Kraehenbuhl JP, Kahn A, Pringault E, Vandewalle A. 1996. Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am. J. Physiol. 270:C1666-C1674.
30. El Bahi S, Caliot E, Bens M, Bogdanova A, Kerneis S, Kahn A, Vandewalle A, Pringault E. 2002. Lymphoepithelial interactions trigger specific regulation of gene expression in the M cell-containing follicle-associated epithelium of Peyer's patches. J. Immunol. 168:3713-3720.
31. Kerneis S, Caliot E, Stubbe H, Bogdanova A, Kraehenbuhl J, Pringault E. 2000. Molecular studies of the intestinal mucosal barrier physiopathology using cocultures of epithelial and immune cells:a technical update. Microbes Infect. 2:1119-1124.
32. Blanco LP, DiRita VJ. 2006. Bacterial-associated cholera toxin and GM1 binding are required for transcytosis of classical biotype Vibrio cholerae through an in vitro M cell model system. Cell. Microbiol. 8:982-998.
33. Blanco LP, Dirita VJ. 2006. Antibodies enhance interaction of Vibrio cholerae with intestinal M-like cells. Infect. Immun. 74:6957-6964.
34. Ouzilou L, Caliot E, Pelletier I, Prevost MC, Pringault E, Colbere-Garapin F. 2002. Poliovirus transcytosis through M-like cells. J. Gen. Virol. 83:2177-2182.
35. Fotopoulos G, Harari A, Michetti P, Trono D, Pantaleo G, Kraehenbuhl JP. 2002. Transepithelial transport of HIV-1 by M cells is receptormediated. Proc. Natl. Acad. Sci. U.S.A. 99:9410-9414.
36. Martin-Latil S, Gnadig NF, Mallet A, Desdouits M, Guivel-Benhassine F, Jeannin P, Prevost MC, Schwartz O, Gessain A, Ozden S, Ceccaldi PE. 2012. Transcytosis of HTLV-1 across a tight human epithelial barrier and infection of subepithelial dendritic cells. Blood 120:572-580.
37. Kearney JF, Radbruch A, Liesegang B, Rajewsky K. 1979. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J. Immunol. 123: 1548-1550.
38. Gonzalez-Hernandez MB, Bragazzi Cunha J, Wobus CE. 2012. Plaque assay for murine norovirus. J. Vis. Exp. 66:e4297. doi:10.3791/4297.
39. Man AL, Lodi F, Bertelli E, Regoli M, Pin C, Mulholland F, Satoskar AR, Taussig MJ, Nicoletti C. 2008. Macrophage migration inhibitory factor plays a role in the regulation of microfold (M) cell-mediated transport in the gut. J. Immunol. 181:5673-5680.
40. Lambert D, O'Neill CA, Padfield PJ. 2007. Methyl-beta-cyclodextrin increases permeability of Caco-2 cell monolayers by displacing specific claudins from cholesterol rich domains associated with tight junctions. Cell Physiol. Biochem. 20:495-506.
41. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, Hogle JM. 2007. Imaging poliovirus entry in live cells. PLoS Biol. 5:e183. doi:10.1371/journal.pbio.0050183.
42. Hocini H, Becquart P, Bouhlal H, Chomont N, Ancuta P, Kazatchkine MD, Belec L. 2001. Active and selective transcytosis of cell-free human immunodeficiency virus through a tight polarized monolayer of human endometrial cells. J. Virol. 75:5370-5374.
43. Masuda K, Kajikawa A, Igimi S. 2011. Establishment and evaluation of an in vitro M cell model using B2BBe1 cells and Raji cells. Biosci. Microflora 30:37-44.
44. Mantis NJ, Cheung MC, Chintalacharuvu KR, Rey J, Corthesy B, Neutra MR. 2002. Selective adherence of IgA to murine Peyer's patch M cells:evidence for a novel IgA receptor. J. Immunol. 169:1844-1851.
45. Jepson MA, Simmons NL, Savidge TC, James PS, Hirst BH. 1993. Selective binding and transcytosis of latex microspheres by rabbit intestinal M cells. Cell Tissue Res. 271:399-405.
46. Troeger H, Loddenkemper C, Schneider T, Schreier E, Epple HJ, Zeitz M, Fromm M, Schulzke JD. 2009. Structural and functional changes of the duodenum in human norovirus infection. Gut 58:1070-1077.
47. Kerneis S, Bogdanova A, Kraehenbuhl JP, Pringault E. 1997. Conversion by Peyer's patch lymphocytes of human enterocytes intoMcells that transport bacteria. Science 277:949-952.
48. Tahoun A, Mahajan S, Paxton E, Malterer G, Donaldson DS, Wang D, Tan A, Gillespie TL, O'Shea M, Roe AJ, Shaw DJ, Gally DL, Lengeling A, Mabbott NA, Haas J, Mahajan A. 2012. Salmonella transforms follicle-associated epithelial cells into m cells to promote intestinal invasion. Cell Host Microbe 12:645-656.
49. Ohno H, Kanaya T, Williams IR. 2012. M cell differentiation:distinct lineage or phenotypic transition? Salmonella provides answers. Cell Host Microbe 12:607-609.
50. Wang J, Gusti V, Saraswati A, Lo DD. 2011. Convergent and divergent development amongMcell lineages in mouse mucosal epithelium. J. Immunol. 187:5277-5285.
51. Kanaya T, Hase K, Takahashi D, Fukuda S, Hoshino K, Sasaki I, Hemmi H, Knoop KA, Kumar N, Sato M, Katsuno T, Yokosuka O, Toyooka K, Nakai K, Sakamoto A, Kitahara Y, Jinnohara T, McSorley SJ, Kaisho T, Williams IR, Ohno H. 2012. The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat. Immunol. 13:729-736.
52. Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A. 2013. Microfold (M) cells:important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 6:666-677.
53. Hsieh EH, Fernandez X, Wang J, Hamer M, Calvillo S, Croft M, Kwon BS, Lo DD. 2010. CD137 is required forMcell functional maturation but not lineage commitment. Am. J. Pathol. 177:666-676.
54. de Lau W, Kujala P, Schneeberger K, Middendorp S, Li VS, Barker N, Martens A, Hofhuis F, DeKoter RP, Peters PJ, Nieuwenhuis E, Clevers H. 2012. Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured "miniguts." Mol. Cell. Biol. 32:3639-3647.
55. Asai T, Morrison SL. 2013. The SRC family tyrosine kinase HCK and the ETS family transcription factors SPIB and EHF regulate transcytosis across a human follicle-associated epithelium model. J. Biol. Chem. 288: 10395-10405.
56. Jepson MA, Clark MA, Hirst BH. 2004. M cell targeting by lectins:a strategy for mucosal vaccination and drug delivery. Adv. Drug Deliv. Rev. 56:511-525.