The SARS coronavirus E protein interacts with PALS1 and alters tight junction formation and epithelial morphogenesis

Molecular Biology of the Cell

Volumn 21, Issue 22, 2010, Pages 3838-3852

  Teoh, Kim Tat ^a,b   Siu, Yu Lam ^a   Chan, Wing Lim ^a,b   Schlüter, Marc A ^c   Liu, Chia Jen ^d   Peiris, J S Malik ^a,b   Bruzzone, Roberto ^a   Margolis, Benjamin ^d   Nal, Béatrice ^a,b  

^a HKU PASTEUR RESEARCH CENTRE   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENDOPLASMIC RETICULUM GOLGI INTERMEDIATE COMPARTMENT PROTEIN 53; GLYCOPROTEIN E; PROTEIN; PROTEIN ASSOCIATED WITH LIN SEVEN 1; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYST; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LUNG ALVEOLUS EPITHELIUM; MAMMAL CELL; NONHUMAN; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SARS CORONAVIRUS; TIGHT JUNCTION; VIRUS MORPHOGENESIS;

ANIMALS; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; EPITHELIAL CELLS; EPITHELIUM; GLUTATHIONE TRANSFERASE; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOBLOTTING; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MORPHOGENESIS; NUCLEOSIDE-PHOSPHATE KINASE; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SARS VIRUS; TIGHT JUNCTIONS; TWO-HYBRID SYSTEM TECHNIQUES; VERO CELLS; VIRAL ENVELOPE PROTEINS;

MAMMALIA; SARS CORONAVIRUS;

EID: 78649684164     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0338     Document Type: Article

References (60)

1. Beuming, T., Skrabanek, L., Niv, M. Y., Mukherjee, P., and Weinstein, H. (2005). PDZBase: a protein-protein interaction database for PDZ-domains. Bioinformatics 21, 827-828. (Pubitemid 40439423)
2. Chan, R.W.Y., Yuen, K. M., Yu, W.C.L., Ho, C.C.C., Nicholls, J. M., Peiris, J.S.M., and Chan, M.C.W. (2010). Influenza H5N1 and H1N1 virus replication and innate immune responses in bronchial epithelial cells are influenced by the state of differentiation. PLoS ONE. 5, e8713
3. Chen, J., and Subbarao, K. (2007). The Immunobiology of SARS*. Annu. Rev. Immunol. 25, 443-472.
4. DeDiego, M. L., Alvarez, E., Almazan, F., Rejas, M. T., Lamirande, E., Roberts, A., Shieh, W.-J., Zaki, S. R., Subbarao, K., and Enjuanes, L. (2007). A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 81, 1701-1713. (Pubitemid 46214445)
5. DeDiego, M. L., Pewe, L., Alvarez, E., Rejas, M. T., Perlman, S., and Enjuanes, L. (2008). Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376, 379-389.
6. Farcas, G. A., Poutanen, S. M., Mazzulli, T., Willey, B. M., Butany, J., Asa, S. L., Faure, P., Akhavan, P., Low, D. E., and Kain, K. C. (2005). Fatal severe acute respiratory syndrome is associated with multiorgan involvement by coronavirus. J. Infect. Dis. 191, 193-197.
7. Formstecher, E., et al. (2005). Protein interaction mapping: a Drosophila case study. Genome Res. 15, 376-384.
8. Fouchier, R. A., Meyer, B. E., Simon, J. H., Fischer, U., and Malim, M. H. (1997). HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16, 4531-4539.
9. Fromont-Racine, M., Rain, J. C., and Legrain, P. (1997). Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16, 277-282.
10. Gaush, C. R., Hard, W. L., and Smith, T. F. (1966). Characterization of an established line of canine kidney cells (MDCK). Proc. Soc. Exp. Biol. Med. 122, 931-935.
11. Gu, J., et al. (2005). Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 202, 415-424.
12. Horikoshi, Y., Suzuki, A., Yamanaka, T., Sasaki, K., Mizuno, K., Sawada, H., Yonemura, S., and Ohno, S. (2009). Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J. Cell. Sci. 122, 1595-1606.
13. Hurd, T. W., Gao, L., Roh, M. H., Macara, I. G., and Margolis, B. (2003). Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell. Biol. 5, 137-142.
14. Jackson, D., Hossain, M. J., Hickman, D., Perez, D. R., and Lamb, R. A. (2008). A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc. Natl. Acad. Sci. USA. 105, 4381-4386.
15. Jaffe, A. B., Kaji, N., Durgan, J., and Hall, A. (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell. Biol. 183, 625-633.
16. Javier, R. T. (2008). Cell polarity proteins: common targets for tumorigenic human viruses. Oncogene 27, 7031-7046.
17. Kam, Y. W., et al. (2007). Antibodies against trimeric S glycoprotein protect hamsters against SARS-CoV challenge despite their capacity to mediate FcγRII-dependent entry into B cells in vitro. Vaccine 25, 729-740.
18. Kamberov, E., Makarova, O., Roh, M., Liu, A., Karnak, D., Straight, S., and Margolis, B. (2000). Molecular cloning and characterization of Pals, proteins associated with mLin-7. J. Biol. Chem. 275, 11425-11431.
19. Kuiken, T., et al. (2003). Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362, 263-270.
20. Latorre, I. J., Roh, M. H., Frese, K. K., Weiss, R. S., Margolis, B., and Javier, R. T. (2005). Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell. Sci. 118, 4283-4293.
21. Lau, Y. L., and Peiris, J. S. (2005). Pathogenesis of severe acute respiratory syndrome. Curr. Opin. Immunol. 17, 404-410.
22. Li, B.-j., et al. (2005). Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Nat. Med. 11, 944-951.
23. Liu, D. X., Yuan, Q., and Liao, Y. (2007). Coronavirus envelope protein: a small membrane protein with multiple functions. Cell. Mol. Life Sci. 64, 2043-2048.
24. Liu, Y., and Baleja, J. D. (2008). Structure and function of the papillomavirus E6 protein and its interacting proteins. Front Biosci. 13, 121-134.
25. Makarova, O., Roh, M. H., Liu, C. J., Laurinec, S., and Margolis, B. (2003). Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302, 21-29. (Pubitemid 36078394)
26. Miyoshi, J., and Takai, Y. (2005). Molecular perspective on tight-junction assembly and epithelial polarity. Adv. Drug Deliv Rev. 57, 815-855.
27. Nal, B., et al. (2005). Differential maturation and subcellular localization of severe acute respiratory syndrome coronavirus surface proteins S, M and E. J. Gen. Virol. 86, 1423-1434.
28. Nicholls, J. M., Butany, J., Poon, L. L., Chan, K. H., Beh, S. L., Poutanen, S., Peiris, J. S., and Wong, M. (2006). Time course and cellular localization of SARS-CoV nucleoprotein and RNA in lungs from fatal cases of SARS. PLoS Med. 3, e27
29. Nicholls, J. M., et al. (2003). Lung pathology of fatal severe acute respiratory syndrome. Lancet 361, 1773-1778.
30. O'Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P., and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell. Biol. 3, 831-838.
31. Obenauer, J. C., et al. (2006). Large-scale sequence analysis of avian influenza isolates. Science 311, 1576-1580.
32. Peiris, J. S., Guan, Y., and Yuen, K. Y. (2004). Severe acute respiratory syndrome. Nat. Med. 10, S88-97.
33. Peiris, J.S.M., et al. (2003). Coronavirus as a possible cause of severe acute respiratory syndrome. The Lancet 361, 1319-1325. (Pubitemid 36514862)
34. Perlman, S., and Netland, J. (2009). Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7, 439-450.
35. Qin, Y., Meisen, W. H., Hao, Y., and Macara, I. G. (2010). Tuba, a Cdc42 GEF, is required for polarized spindle orientation during epithelial cyst formation. J. Cell. Biol. 189, 661-669.
36. Rain, J. C., et al. (2001). The protein-protein interaction map of Helicobacter pylori. Nature 409, 211-215.
37. Roh, M. H., Fan, S., Liu, C. J., and Margolis, B. (2003). The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J. Cell. Sci. 116, 2895-2906.
38. Roh, M. H., Makarova, O., Liu, C. J., Shin, K., Lee, S., Laurinec, S., Goyal, M., Wiggins, R., and Margolis, B. (2002). The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell. Biol. 157, 161-172.
39. Schlüter, M. A., and Margolis, B. (2009). Apical lumen formation in renal epithelia. J. Am. Soc. Nephrol. 20, 1444-1452.
40. Schlüter, M. A., Pfarr, C. S., Pieczynski, J., Whiteman, E. L., Hurd, T. W., Fan, S., Liu, C.-J., and Margolis, B. (2009). Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol. Biol. Cell. 20, 4652-4663.
41. Schneeberger, E. E., and Lynch, R. D. (2004). The tight junction: a multifunctional complex. Am. J. Physiol Cell. Physiol. 286, C1213-C1228.
42. Schweizer, A., Fransen, J. A., Bachi, T., Ginsel, L., and Hauri, H. P. (1988). Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J. Cell. Biol. 107, 1643-1653.
43. Shin, K., Fogg, V. C., and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
44. Shin, K., Straight, S., and Margolis, B. (2005). PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J. Cell. Biol. 168, 705-711.
45. Sims, A. C., Baric, R. S., Yount, B., Burkett, S. E., Collins, P. L., and Pickles, R. J. (2005). Severe acute respiratory syndrome coronavirus infection of human ciliated airway epithelia: role of ciliated cells in viral spread in the conducting airways of the lungs. J Virol. 79, 15511-15524.
46. Siu, Y. L., et al. (2008). The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles. J. Virol. 82, 11318-11330.
47. Soneoka, Y., Cannon, P. M., Ramsdale, E. E., Griffiths, J. C., Romano, G., Kingsman, S. M., and Kingsman, A. J. (1995). A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucl. Acids Res. 23, 628-633.
48. Straight, S. W., Shin, K., Fogg, V. C., Fan, S., Liu, C. J., Roh, M., and Margolis, B. (2004). Loss of PALS1 expression leads to tight junction and polarity defects. Mol. Biol. Cell. 15, 1981-1990.
49. Suzuki, A., and Ohno, S. (2006). The PAR-aPKC system: lessons in polarity. J. Cell. Sci. 119, 979-987.
50. Tepass, U. (1996). Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev Biol. 177, 217-225.
51. Thiel, V., and Weber, F. (2008). Interferon and cytokine responses to SARS-coronavirus infection. Cytokine Growth Factor Rev. 19, 121-132.
52. Thomas, M., Narayan, N., Pim, D., Tomaic, V., Massimi, P., Nagasaka, K., Kranjec, C., Gammoh, N., and Banks, L. (2008). Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27, 7018-7030.
53. Tomaic, V., Gardiol, D., Massimi, P., Ozbun, M., Myers, M., and Banks, L. (2009). Human and primate tumour viruses use PDZ binding as an evolutionarily conserved mechanism of targeting cell polarity regulators. Oncogene 28, 1-8.
54. Tonikian, R., et al. (2008). A specificity map for the PDZ domain family. PLoS Biol. 6, e239
55. Tungteakkhun, S. S., Filippova, M., Neidigh, J. W., Fodor, N., and Duerksen-Hughes, P. J. (2008). The interaction between human papillomavirus type 16 and FADD is mediated by a novel E6 binding domain. J. Virol. 82, 9600-9614.
56. Wang, Q., Chen, X.-W., and Margolis, B. (2007). PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol. Biol. Cell. 18, 874-885.
57. Wang, Q., and Margolis, B. (2007). Apical junctional complexes and cell polarity. Kidney Int. 72, 1448-1458.
58. Wise-Draper, T. M., and Wells, S. I. (2008). Papillomavirus E6 and E7 proteins and their cellular targets. Front Biosci. 13, 1003-1017.
59. Yamanaka, T., and Ohno, S. (2008). Role of Lgl/Dlg/Scribble in the regulation of epithelial junction, polarity and growth. Front Biosci. 13, 6693-6707.
60. Yoshikawa, T., Hill, T., Li, K., Peters, C. J., and Tseng, C. T. (2009). Severe acute respiratory syndrome (SARS) coronavirus-induced lung epithelial cytokines exacerbate SARS pathogenesis by modulating intrinsic functions of monocyte-derived macrophages and dendritic cells. J Virol 83, 3039-3048.