The tight junction protein JAM-A functions as coreceptor for rotavirus entry into MA104 cells

Virology

Volumn 475, Issue , 2015, Pages 172-178

  Torres Flores, Jesús M ^a   Silva Ayala, Daniela ^a   Espinoza, Marco A ^a   López, Susana ^a   Arias, Carlos F ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

JAM A; Occludin; Rotavirus; Tight junction proteins; Virus entry; ZO 1

Indexed keywords

GLYCAN; HEAT SHOCK COGNATE PROTEIN 70; INTEGRIN; JUNCTIONAL ADHESION MOLECULE A; OCCLUDIN; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; VIRUS SPIKE PROTEIN; CELL SURFACE RECEPTOR; SMALL INTERFERING RNA;

ARTICLE; BINDING ASSAY; CONTROLLED STUDY; IMMUNOFLUORESCENCE; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; ROTAVIRUS; ROTAVIRUS INFECTION; UNITED KINGDOM; VIRUS ENTRY; VIRUS STRAIN; ANIMAL; CELL LINE; GENETICS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; RHESUS MONKEY; RNA INTERFERENCE;

ROTAVIRUS;

ANIMALS; CELL LINE; HUMANS; MACACA MULATTA; MICE; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; RNA, SMALL INTERFERING; ROTAVIRUS; TIGHT JUNCTION PROTEINS; VIRUS INTERNALIZATION;

EID: 84913553760     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.11.016     Document Type: Article

References (39)

1. Barton E.S., Forrest J.C., Connolly J.L., Chappell J.D., Liu Y., Schnell F.J., Nusrat A., Parkos C.A., Dermody T.S. Junction adhesion molecule is a receptor for reovirus. Cell 2001, 104:441-451.
2. Bass D.M., Baylor M.R., Chen C., Mackow E.M., Bremont M., Greenberg H.B. Liposome-mediated transfection of intact viral particles reveals that plasma membrane penetration determines permissivity of tissue culture cells to rotavirus. J. Clin. Investig. 1992, 90:2313-2320.
3. Beau I., Cotte-Laffitte J., Amsellem R., Servin A.L. A protein kinase A-dependent mechanism by which rotavirus affects the distribution and mRNA level of the functional tight junction-associated protein, occludin, in human differentiated intestinal Caco-2 cells. J. Virol. 2007, 81:8579-8586.
4. Benedicto I., Molina-Jimenez F., Garcia-Buey L., Gondar V., Lopez-Cabrera M., Moreno-Otero R., Majano P.L. Role of tight junctions in hepatitis C virus infection. Rev. Esp. Enferm. Dig. 2012, 104:255-263.
5. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., Finberg R.W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275:1320-1323.
6. Blutt S.E., Conner M.E. Rotavirus: to the gut and beyond!. Curr. Opin. Gastroenterol. 2007, 23:39-43.
7. Boehme K.W., Lai C.M., Dermody T.S. Mechanisms of reovirus bloodstream dissemination. Adv. Virus Res. 2013, 87:1-35.
8. Chi C.N., Bach A., Stromgaard K., Gianni S., Jemth P. Ligand binding by PDZ domains. Biofactors 2012, 38:338-348.
9. Coyne C.B., Shen L., Turner J.R., Bergelson J.M. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2007, 2:181-192.
10. Cuadras M.A., Arias C.F., Lopez S. Rotaviruses induce an early membrane permeabilization of MA104 cells and do not require a low intracellular Ca2+ concentration to initiate their replication cycle. J. Virol. 1997, 71:9065-9074.
11. Cummins P.M. Occludin: one protein, many forms. Mol. Cell Biol. 2012, 32:242-250.
12. Diaz-Salinas M.A., Romero P., Espinosa R., Hoshino Y., Lopez S., Arias C.F. The spike protein VP4 defines the endocytic pathway used by rotavirus to enter MA104 cells. J. Virol. 2013, 87:1658-1663.
13. Diaz-Salinas M.A., Silva-Ayala D., Lopez S., Arias C.F. Rotaviruses reach late endosomes and require the cation-dependent mannose-6-phosphate receptor and the activity of cathepsin proteases to enter the cell. J. Virol. 2014, 88:4389-4402.
14. Fanning A.S., Jameson B.J., Jesaitis L.A., Anderson J.M. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 1998, 273:29745-29753.
15. Feng N., Sen A., Nguyen H., Vo P., Hoshino Y., Deal E.M., Greenberg H.B. Variation in antagonism of the interferon response to rotavirus NSP1 results in differential infectivity in mouse embryonic fibroblasts. J. Virol. 2009, 83:6987-6994.
16. Gonzalez-Mariscal L., Garay E., Lechuga S. Virus interaction with the apical junctional complex. Front. Biosci. (Landmark Ed.) 2009, 14:731-768.
17. Guerrero C.A., Zarate S., Corkidi G., Lopez S., Arias C.F. Biochemical characterization of rotavirus receptors in MA104 cells. J. Virol. 2000, 74:9362-9371.
18. Gutierrez M., Isa P., Sanchez-San Martin C., Perez-Vargas J., Espinosa R., Arias C.F., Lopez S. Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis. J. Virol. 2010, 84:9161-9169.
19. Hu L., Crawford S.E., Czako R., Cortes-Penfield N.W., Smith D.F., Le Pendu J., Estes M.K., Prasad B.V. Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 2012, 485:256-259.
20. Huang P., Xia M., Tan M., Zhong W., Wei C., Wang L., Morrow A., Jiang X. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 2012, 86:4833-4843.
21. Iden S., Misselwitz S., Peddibhotla S.S., Tuncay H., Rehder D., Gerke V., Robenek H., Suzuki A., Ebnet K. aPKC phosphorylates JAM-A at Ser285 to promote cell contact maturation and tight junction formation. J. Cell Biol. 2012, 196:623-639.
22. Ikenouchi J., Umeda K., Tsukita S., Furuse M. Requirement of ZO-1 for the formation of belt-like adherens junctions during epithelial cell polarization. J. Cell Biol. 2007, 176:779-786.
23. Isa P., Arias C.F., Lopez S. Role of sialic acids in rotavirus infection. Glycoconj. J. 2006, 23:27-37.
24. Kirchner E., Guglielmi K.M., Strauss H.M., Dermody T.S., Stehle T. Structure of reovirus sigma1 in complex with its receptor junctional adhesion molecule-A. PLoS Pathog. 2008, 4:e1000235.
25. Lopez S., Arias C.F. Early steps in rotavirus cell entry. Curr. Top. Microbiol. Immunol. 2006, 309:39-66.
26. Lopez T., Silva-Ayala D., Lopez S., Arias C.F. Methods suitable for high-throughput screening of siRNAs and other chemical compounds with the potential to inhibit rotavirus replication. J. Virol. Methods 2012, 179:242-249.
27. Luissint A.C., Nusrat A., Parkos C.A. JAM-related proteins in mucosal homeostasis and inflammation. Semin. Immunopathol. 2014, 36:211-226.
28. Makino A., Shimojima M., Miyazawa T., Kato K., Tohya Y., Akashi H. Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J. Virol. 2006, 80:4482-4490.
29. Martinez M.A., Lopez S., Arias C.F., Isa P. Gangliosides have a functional role during rotavirus cell entry. J. Virol. 2013, 87:1115-1122.
30. Pando V., Isa P., Arias C.F., Lopez S. Influence of calcium on the early steps of rotavirus infection. Virology 2002, 295:190-200.
31. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., Rice C.M. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009, 457:882-886.
32. Rodgers L.S., Beam M.T., Anderson J.M., Fanning A.S. Epithelial barrier assembly requires coordinated activity of multiple domains of the tight junction protein ZO-1. J. Cell Sci. 2013, 126:1565-1575.
33. Ruiz A.M., Lopez I.V., Lopez S., Espejo R.T., Arias C.F. Molecular and antigenic characterization of porcine rotavirus YM, a possible new rotavirus serotype. J. Virol. 1988, 62:4331-4336.
34. Silva-Ayala D., Lopez T., Gutierrez M., Perrimon N., Lopez S., Arias C.F. Genome-wide RNAi screen reveals a role for the ESCRT complex in rotavirus cell entry. Proc. Natl. Acad. Sci. USA 2013, 110:10270-10275.
35. Stang E., Kartenbeck J., Parton R.G. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 1997, 8:47-57.
36. Tate J.E., Burton A.H., Boschi-Pinto C., Steele A.D., Duque J., Parashar U.D. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12:136-141.
37. Umeda K., Ikenouchi J., Katahira-Tayama S., Furuse K., Sasaki H., Nakayama M., Matsui T., Tsukita S., Furuse M. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 2006, 126:741-754.
38. Zárate S., Espinosa R., Romero P., Méndez E., Arias C.F., López S. The VP5 domain of VP4 can mediate attachment of rotaviruses to cells. J. Virol. 2000, 74:593-599.
39. Zhang B., Lim T.S., Vedula S.R., Li A., Lim C.T., Tan V.B. Investigation of the binding preference of reovirus sigma1 for junctional adhesion molecule A by classical and steered molecular dynamics. Biochemistry 2010, 49:1776-1786.