Expression of human decay-accelerating factor on intestinal epithelium of transgenic mice does not facilitate infection by the enteral route

Journal of Virology

Volumn 89, Issue 8, 2015, Pages 4311-4318

  Pan, Jieyan ^a   Zhang, Lili ^a   Odenwald, Matthew A ^b   Shen, Le ^b   Turner, Jerrold R ^b   Bergelson, Jeffrey M ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; DECAY ACCELERATING FACTOR; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; COXSACKIE VIRUS B3; EMBRYO; EPITHELIUM CELL; EX VIVO STUDY; GASTROINTESTINAL TRACT; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INFECTION SENSITIVITY; INNATE IMMUNITY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMALL INTESTINE; TIGHT JUNCTION; TRANSGENIC MOUSE; VIRUS CELL INTERACTION; VIRUS INFECTION; ANIMAL; DISEASE PREDISPOSITION; ELECTRON MICROSCOPY; ENTEROVIRUS B; ENTEROVIRUS INFECTION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

ANIMALIA; COXSACKIEVIRUS; MURINAE; MUS; MUS MUSCULUS;

ANIMALS; ANTIGENS, CD55; DISEASE SUSCEPTIBILITY; DNA PRIMERS; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84925427991     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03468-14     Document Type: Article

References (49)

1. Pallansch M, Roos R. 2007. Enteroviruses: poliovirus, coxsackieviruses, echoviruses, and newer enteroviruses, p 839-894. 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.
2. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323. http://dx.doi.org/10.1126/science.275.5304.1320.
3. Tomko RP, Xu R, Philipson L. 1997. HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci U S A 94:3352-3356. http://dx.doi.org/10.1073/pnas.94.7.3352.
4. Martino TA, Petric M, Weingartl H, Bergelson JM, Opavsky MA, Richardson CD, Modlin JF, Finberg RW, Kain KC, Willis N, Gauntt CJ, Liu PP. 2000. The coxsackie-adenovirus receptor (CAR) is used by reference strains and clinical isolates representing all six serotypes of coxsackievirus group B, and by swine vesicular disease virus. Virology 271:99-108. http://dx.doi.org/10.1006/viro.2000.0324.
5. Cohen CJ, Shieh JT-C, Pickles RJ, Okegawa T, Hsieh J-T, Bergelson JM. 2001. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci U S A 98:15191-15196. http://dx.doi.org/10.1073/pnas.261452898.
6. Bergelson JM, Modlin JF, Wieland-Alter W, Cunningham JA, Crowell RL, Finberg RW. 1997. Clinical coxsackievirus B isolates differ from laboratory strains in their interaction with two cell surface receptors. J Infect Dis 175:697-700. http://dx.doi.org/10.1093/infdis/175.3.697.
7. Bergelson JM, Mohanty JG, Crowell RL, St John NF, Lublin DM, Finberg RW. 1995. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J Virol 69:1903-1906.
8. Shafren DR, Bates RC, Agrez MV, Herd RL, Burns GF, Barry RD. 1995. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 69:3873-3877.
9. Shieh JTC, Bergelson JM. 2002. Interaction with decay-accelerating factor facilitates coxsackievirus B infection of polarized epithelial cells. J Virol 76:9474-9480. http://dx.doi.org/10.1128/JVI.76.18.9474-9480.2002.
10. Coyne CB, Bergelson JM. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124: 119-131. http://dx.doi.org/10.1016/j.cell.2005.10.035.
11. Esfandiarei M, McManus BM. 2008. Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol 3:127-155. http://dx.doi.org/10.1146/annurev.pathmechdis.3.121806.151534.
12. Huber S, Ramsingh AI. 2004. Coxsackievirus-induced pancreatitis. Viral Immunol 17:358-369. http://dx.doi.org/10.1089/vim.2004.17.358.
13. Kallewaard NL, Zhang L, Chen JW, Guttenberg M, Sanchez MD, Bergelson JM. 2009. Tissue-specific deletion of the coxsackievirus and adenovirus receptor protects mice from virus-induced pancreatitis and myocarditis. Cell Host Microbe 6:91-98. http://dx.doi.org/10.1016/j.chom.2009.05.018.
14. Shi Y, Chen C, Lisewski U, Wrackmeyer U, Radke M, Westermann D, Sauter M, Tschope C, Poller W, Klingel K, Gotthardt M. 2009. Cardiac deletion of the coxsackievirus-adenovirus receptor abolishes coxsackievirus B3 infection and prevents myocarditis in vivo. J Am Coll Cardiol 53:1219-1226. http://dx.doi.org/10.1016/j.jacc.2008.10.064.
15. Bopegamage S, Borsanyiova M, Vargova A, Petrovicova A, Benkovicova M, Gomolcak P. 2003. Coxsackievirus infection of mice. I. Viral kinetics and histopathological changes in mice experimentally infected with coxsackieviruses B3 and B4 by oral route. Acta Virol 47:245-251.
16. Bopegamage S, Kovacova J, Vargova A, Motusova J, Petrovicova A, Benkovicova M, Gomolcak P, Bakkers J, van Kuppeveld F, Melchers WJ, Galama JM. 2005. Coxsackie B virus infection of mice: inoculation by the oral route protects the pancreas from damage, but not from infection. J Gen Virol 86:3271-3280. http://dx.doi.org/10.1099/vir.0.81249-0.
17. Loria RM, Shadoff N, Kibrick S, Broitman S. 1976. Maturation of intestinal defenses against peroral infection with group B coxsackievirus in mice. Infect Immun 13:1397-1401.
18. Bergelson JM, Krithivas A, Celi L, Droguett G, Horwitz MS, Wickham T, Crowell RL, Finberg RW. 1998. The murine CAR homologue (mCAR) is a receptor for coxsackie B viruses and adenoviruses. J Virol 72:415-419.
19. Spiller OB, Goodefellow IG, Evans DJ, Almond JW, Morgan BB. 2000. Echoviruses and coxsackie B viruses that use human decay-accelerating factor (DAF) as a receptor do not bind the rodent analogues of DAF. J Infect Dis 181:340-343. http://dx.doi.org/10.1086/315210.
20. Raschperger E, Thyberg J, Pettersson S, Philipson L, Fuxe J, Pettersson RF. 2006. The coxsackie-and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp Cell Res 312:1566-1580. http://dx.doi.org/10.1016/j.yexcr.2006.01.025.
21. Pan J, Narayanan B, Shah S, Yoder JD, Cifuente JO, Hafenstein S, Bergelson JM. 2011. Single amino acid changes in the virus capsid permit coxsackievirus B3 to bind decay-accelerating factor. J Virol 85:7436-7443. http://dx.doi.org/10.1128/JVI.00503-11.
22. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S. 1996. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J Virol 70:7811-7818.
23. Pinto D, Robine S, Jaisser F, El Marjou FE, Louvard D. 1999. Regulatory sequences of the mouse villin gene that efficiently drive transgenic expression in immature and differentiated epithelial cells of small and large intestines. J Biol Chem 274:6476-6482. http://dx.doi.org/10.1074/jbc.274.10.6476.
24. Roundy KM, Spangrude G, Weis JJ, Weis JH. 2005. Partial rescue of B cells in microphthalmic osteopetrotic marrow by loss of response to type I IFNs. Int Immunol 17:1495-1503. http://dx.doi.org/10.1093/intimm/dxh327.
25. Nochi T, Yuki Y, Matsumura A, Mejima M, Terahara K, Kim DY, Fukuyama S, Iwatsuki-Horimoto K, Kawaoka Y, Kohda T, Kozaki S, Igarashi O, Kiyono H. 2007. A novel M cell-specific carbohydratetargeted mucosal vaccine effectively induces antigen-specific immune responses. J Exp Med 204:2789-2796. http://dx.doi.org/10.1084/jem.20070607.
26. Sato T, Clevers H. 2013. Primary mouse small intestinal epithelial cell cultures. Methods Mol Biol 945:319-328. http://dx.doi.org/10.1007/978-1-62703-125-7_19.
27. Miyoshi H, Stappenbeck TS. 2013. In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat Protoc 8:2471-2482. http://dx.doi.org/10.1038/nprot.2013.153.
28. Cohen CJ, Xiang ZQ, Gao G-P, Ertl HCJ, Wilson JM, Bergelson JM. 2002. Chimpanzee adenovirus CV-68 adapted as a gene delivery vector interacts with the coxsackievirus and adenovirus receptor (CAR). J Gen Virol 83:151-155.
29. Kraehenbuhl J-P, Neutra MR. 2000. Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16:301-332. http://dx.doi.org/10.1146/annurev.cellbio.16.1.301.
30. Wolf JL, Rubin DH, Finberg R, Kauffman RS, Sharpe AH, Trier JS, Fields BN. 1981. IntestinalMcells: a pathway for entry of reovirus into the host. Science 212:471-472. http://dx.doi.org/10.1126/science.6259737.
31. Sicinski P, Rowinski J, Warchol JB, Jarzabek Z, Gut W, Szczygiel B, Bielecki K, Koch G. 1990. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56-58.
32. Takahashi Y, Misumi S, Muneoka A, Masuyama M, Tokado H, Fukuzaki K, Takamune N, Shoji S. 2008. Nonhuman primate intestinal villous M-like cells: an effective poliovirus entry site. Biochem Biophys Res Commun 368:501-507. http://dx.doi.org/10.1016/j.bbrc.2008.01.120.
33. Fotopoulos G, Harari A, Michetti P, Trono D, Pantaleo G, Kraehenbuhl J-P. 2002. Transepithelial transport of HIV-1 by M cells is receptormediated. Proc Natl Acad Sci U S A 99:9410-9414. http://dx.doi.org/10.1073/pnas.142586899.
34. Ouzilou L, Caliot E, Pelletier I, Prévost M-C, Pringault E, Colbere-Garapin F. 2002. Poliovirus transcytosis through M-like cells. J Gen Virol 83:2177-2182.
35. Reagan KJ, Goldberg B, Crowell RL. 1984. Altered receptor specificity of coxsackie B3 after growth in rhabdomyosarcoma cells. J Virol 49:635-640.
36. Coyne CB, Shen L, Turner JR, Bergelson JM. 2007. Coxsackievirus entry from epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2:181-192. http://dx.doi.org/10.1016/j.chom.2007.07.003.
37. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262-265. http://dx.doi.org/10.1038/nature07935.
38. Moon C, VanDussen KL, Miyoshi H, Stappenbeck TS. 2014. Development of a primary mouse intestinal epithelial cell monolayer culture system to evaluate factors that modulate IgA transcytosis. Mucosal Immunol 7:818-828. http://dx.doi.org/10.1038/mi.2013.98.
39. Aust G, Kerner C, Gonsior S, Sittig D, Schneider H, Buske P, Scholz M, Dietrich N, Oldenburg S, Karpus ON, Galle J, Amasheh S, Hamann J. 2013. Mice overexpressing CD97 in intestinal epithelial cells provide a unique model for mammalian postnatal intestinal cylindrical growth. Mol Biol Cell 24:2256-2268. http://dx.doi.org/10.1091/mbc.E13-04-0175.
40. Ohka S, Igarashi H, Nagata N, Sakai M, Koike S, Nochi T, Kiyono H, Nomoto A. 2007. Establishment of a poliovirus oral infection system in human poliovirus receptor-expressing transgenic mice that are deficient in alpha/beta interferon receptor. J Virol 81:7902-7912. http://dx.doi.org/10.1128/JVI.02675-06.
41. Zhang S, Racaniello VR. 1997. Expression of the poliovirus receptor in intestinal epithelial cells is not sufficient to permit poliovirus replication in the mouse gut. J Virol 71:4915-4920.
42. Fujita M, Kinoshita T. 2012. GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim Biophys Acta 1821:1050-1058. http://dx.doi.org/10.1016/j.bbalip.2012.01.004.
43. Kamitani T, Chang HM, Rollins C, Waneck GL, Yeh ET. 1993. Correction of the class H defect in glycosylphosphatidylinositol anchor biosynthesis in Ltk- cells by a human cDNA clone. J Biol Chem 268:20733-20736.
44. Racaniello VR. 2006. One hundred years of poliovirus pathogenesis. Virology 344:9-16. http://dx.doi.org/10.1016/j.virol.2005.09.015.
45. Sabin AB. 1956. Pathogenesis of poliomyelitis: reappraisal in the light of new data. Science 123:1151-1157. http://dx.doi.org/10.1126/science.123.3209.1151.
46. Bodian D. 1955. Emerging concept of poliomyelitis infection. Science 122:105-108. http://dx.doi.org/10.1126/science.122.3159.105.
47. Iwasaki A, Welker R, Mueller S, Linehan M, Nomoto A, Wimmer E. 2002. Immunofluorescence analysis of poliovirus receptor expression in Peyer's patches of humans, primates and CD155 transgenic mice: implications for poliovirus infection. J Infect Dis 186:585-592. http://dx.doi.org/10.1086/342682.
48. Kuss SK, Etheredge CA, Pfeiffer JK. 2008. Multiple host barriers restrict poliovirus trafficking in mice. PLoS Pathog 4:e1000082. http://dx.doi.org/10.1371/journal.ppat.1000082.
49. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, Dermody TS, Pfeiffer JK. 2011. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334:249-252. http://dx.doi.org/10.1126/science.1211057.