Computational identification of interplay between phosphorylation and O-β-glycosylation of human occludin as potential mechanism to impair hepatitis C virus entry

Infection, Genetics and Evolution

Volumn 12, Issue 6, 2012, Pages 1235-1245

  Butt, Azeem Mehmood ^a,b   Feng, Dandan ^a   Nasrullah, Izza ^c   Tahir, Shifa ^c   Idrees, Muhammad ^b   Tong, Yigang ^d   Lu, Jun ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF THE PUNJAB   (Pakistan)

^c QUAID I AZAM UNIVERSITY   (Pakistan)

^d BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

Hepatitis C; O glycosylation; Occludin; Phosphorylation; Posttranslational modifications

Indexed keywords

CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE; OCCLUDIN; PHOSPHOTRANSFERASE; PROTEIN TYROSINE KINASE; SERINE; TYROSINE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HEPATITIS C VIRUS; HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; VIRUS ENTRY;

AMINO ACID SEQUENCE; AMINO ACIDS; COMPUTER SIMULATION; GLYCOSYLATION; HEPACIVIRUS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OCCLUDIN; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ALIGNMENT; VIRUS INTERNALIZATION;

HEPATITIS C VIRUS;

EID: 84861950211     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.04.001     Document Type: Article

References (68)

1. Agnello V., Abel G., Elfahal M., Knight G.B., Zhang Q.X. Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Natl. Acad. Sci. USA 1999, 96:12766-12771.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Barth H., Robinet E., Liang T.J., Baumert T.F. Mouse models for the study of HCV infection and virus-host interactions. J. Hepatol. 2008, 49:134-142.
4. Barth H., Schafer C., Adah M.I., Zhang F., Linhardt R.J., Toyoda H., Kinoshita-Toyoda A., Toida T., Van Kuppevelt T.H., Depla E., Von Weizsacker F., Blum H.E., Baumert T.F. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 2003, 278:41003-41012.
5. Basuroy S., Seth A., Elias B., Naren A.P., Rao R. MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem. J. 2006, 393:69-77.
6. Bernsel A., Viklund H., Hennerdal A., Elofsson A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 2009, 37:W465-W468.
7. Blanchard E., Belouzard S., Goueslain L., Wakita T., Dubuisson J., Wychowski C., Rouille Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 2006, 80:6964-6972.
8. Blom N., Gammeltoft S., Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 1999, 294:1351-1362.
9. Boeckmann B., Bairoch A., Apweiler R., Blatter M.C., Estreicher A., Gasteiger E., Martin M.J., Michoud K., O'Donovan C., Phan I., Pilbout S., Schneider M. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003, 31:365-370.
10. Butt A.M., Feng D., Idrees M., Tong Y., Lu J. Computational Identification and Modeling of Crosstalk between Phosphorylation, O-β-glycosylation and Methylation of FoxO3 and Implications for Cancer Therapeutics. Int. J. Mol. Sci. 2012, 13:2918-2938.
11. Butt A.M., Khan I.B., Hussain M., Idress M., Lu J., Tong Y. Role of post translational modifications and novel crosstalk between phosphorylation and O-beta-GlcNAc modifications in human claudin-1, -3 and -4. Mol. Biol. Rep. 2012, 39:1359-1369.
12. Chiba H., Osanai M., Murata M., Kojima T., Sawada N. Transmembrane proteins of tight junctions. Biochim. Biophys. Acta 2008, 1778:588-600.
13. Clarke H., Soler A.P., Mullin J.M. Protein kinase C activation leads to dephosphorylation of occludin and tight junction permeability increase in LLC-PK1 epithelial cell sheets. J. Cell Sci. 2000, 113(Pt 18):3187-3196.
14. Cordenonsi M., Turco F., D'Atri F., Hammar E., Martinucci G., Meggio F., Citi S. Xenopus laevis occludin. Identification of in vitro phosphorylation sites by protein kinase CK2 and association with cingulin. Eur. J. Biochem. 1999, 264:374-384.
15. Cukierman L., Meertens L., Bertaux C., Kajumo F., Dragic T. Residues in a highly conserved claudin-1 motif are required for hepatitis C virus entry and mediate the formation of cell-cell contacts. J. Virol. 2009, 83:5477-5484.
16. Cummins P.M. Occludin: one protein, many forms. Mol. Cell. Biol. 2012, 32:242-250.
17. Din N., Ahmad I., Ul Haq I., Elahi S., Hoessli D.C., Shakoori A.R. The function of GluR1 and GluR2 in cerebellar and hippocampal LTP and LTD is regulated by interplay of phosphorylation and O-GlcNAc modification. J. Cell Biochem. 2010, 109:585-597.
18. Dinkel H., Chica C., Via A., Gould C.M., Jensen L.J., Gibson T.J., Diella F. Nucleic Acids Res. 2010.
19. Dorfel M.J., Huber O. Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J. Biomed. Biotechnol. 2012, 2012:807356.
20. Dorfel M.J., Westphal J.K., Huber O. Differential phosphorylation of occludin and tricellulin by CK2 and CK1. Ann. NY Acad. Sci. 2009, 1165:69-73.
21. Elias B.C., Suzuki T., Seth A., Giorgianni F., Kale G., Shen L., Turner J.R., Naren A., Desiderio D.M., Rao R. Phosphorylation of Tyr-398 and Tyr-402 in occludin prevents its interaction with ZO-1 and destabilizes its assembly at the tight junctions. J. Biol. Chem. 2009, 284:1559-1569.
22. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wolk B., Hatziioannou T., McKeating J.A., Bieniasz P.D., Rice C.M. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
23. Feldman G.J., Mullin J.M., Ryan M.P. Occludin: structure, function and regulation. Adv. Drug. Deliv. Rev. 2005, 57:883-917.
24. Feldmann G., Mishra A., Hong S.M., Bisht S., Strock C.J., Ball D.W., Goggins M., Maitra A., Nelkin B.D. Inhibiting the cyclin-dependent kinase CDK5 blocks pancreatic cancer formation and progression through the suppression of Ras-Ral signaling. Can. Res. 2010, 70:4460-4469.
25. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 1993, 123:1777-1788.
26. Gupta, R., Brunak, S., 2002. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac. Symp. Biocomput., pp. 310-322.
27. Hart G.W., Greis K.D., Dong L.Y., Blomberg M.A., Chou T.Y., Jiang M.S., Roquemore E.P., Snow D.M., Kreppel L.K., Cole R.N., et al. O-linked N-acetylglucosamine: the " yin-yang" of Ser/Thr phosphorylation? Nuclear and cytoplasmic glycosylation. Adv. Exp. Med. Biol. 1995, 376:115-123.
28. Hessa T., Meindl-Beinker N.M., Bernsel A., Kim H., Sato Y., Lerch-Bader M., Nilsson I., White S.H., von Heijne G. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 2007, 450:1026-1030.
29. Jain S., Suzuki T., Seth A., Samak G., Rao R. Protein kinase Czeta phosphorylates occludin and promotes assembly of epithelial tight junctions. Biochem. J. 2011, 437:289-299.
30. Juretic D., Zoranic L., Zucic D. Basic charge clusters and predictions of membrane protein topology. J. Chem. Info. Comput. Sci. 2002, 42:620-632.
31. Kall L., Krogh A., Sonnhammer E.L. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucl. Acids Res. 2007, 35:W429-W432.
32. Kamemura K., Hart G.W. Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: a new paradigm for metabolic control of signal transduction and transcription. Prog. Nucl. Acid Res. Mol. Biol. 2003, 73:107-136.
33. Klabunde T., Hessler G. Drug design strategies for targeting G-protein-coupled receptors. Chembiochem: Eur. J., Chem. Biol. 2002, 3:928-944.
34. Koutsoudakis G., Kaul A., Steinmann E., Kallis S., Lohmann V., Pietschmann T., Bartenschlager R. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 2006, 80:5308-5320.
35. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157:105-132.
36. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
37. Lee N.P., Luk J.M. Hepatic tight junctions: from viral entry to cancer metastasis. World J. Gastroenterol. 2010, 16:289-295.
38. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science 1991, 252:1162-1164.
39. Mann M., Jensen O.N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21:255-261.
40. Marchiando A.M., Shen L., Graham W.V., Weber C.R., Schwarz B.T., Austin J.R., Raleigh D.R., Guan Y., Watson A.J., Montrose M.H., Turner J.R. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 2010, 189:111-126.
41. Mareel M., Leroy A. Clinical, cellular, and molecular aspects of cancer invasion. Physiol. Rev. 2003, 83:337-376.
42. Martin T.A., Mansel R.E., Jiang W.G. Loss of occludin leads to the progression of human breast cancer. Int. J. Mol. Med. 2010, 26:723-734.
43. McDonnell A.V., Jiang T., Keating A.E., Berger B. Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics 2006, 22:356-358.
44. McKenzie J.A.G., Riento K., Ridley A.J. Casein kinase Iε associates with and phosphorylates the tight junction protein occludin. FEBS Lett. 2006, 580:2388-2394.
45. Mee C.J., Farquhar M.J., Harris H.J., Hu K., Ramma W., Ahmed A., Maurel P., Bicknell R., Balfe P., McKeating J.A. Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor-dependent manner. Gastroenterology 2010, 138:1134-1142.
46. Meertens L., Bertaux C., Dragic T. Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J. Virol. 2006, 80:11571-11578.
47. Michta M.L., Hopcraft S.E., Narbus C.M., Kratovac Z., Israelow B., Sourisseau M., Evans M.J. Species-specific regions of occludin required for hepatitis C virus cell entry. J. Virol. 2010, JVI.01555-01510.
48. Mishra S., Ande S.R., Salter N.W. O-GlcNAc modification: why so intimately associated with phosphorylation?. Cell Commun. Signal 2011, 9:1.
49. Nugent, T., Ward, S., Jones, D.T., 2011. The MEMPACK alpha-helical transmembrane protein structure prediction server. Bioinformatics.
50. Obenauer J.C., Cantley L.C., Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 2003, 31:3635-3641.
51. Orban E., Szabo E., Lotz G., Kupcsulik P., Paska C., Schaff Z., Kiss A. Different expression of occludin and ZO-1 in primary and metastatic liver tumors. Pathol. Oncol. Res.: POR 2008, 14:299-306.
52. Owen D.M., Huang H., Ye J., Gale M. Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 2009, 394:99-108.
53. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A.J., Houghton M., Rosa D., Grandi G., Abrignani S. Binding of hepatitis C virus to CD81. Science 1998, 282:938-941.
54. 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.
55. Raleigh D.R., Boe D.M., Yu D., Weber C.R., Marchiando A.M., Bradford E.M., Wang Y., Wu L., Schneeberger E.E., Shen L., Turner J.R. Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J. Cell Biol. 2011, 193:565-582.
56. Rao R. Occludin phosphorylation in regulation of epithelial tight junctions. Ann. NY Acad Sci. 2009, 1165:62-68.
57. Saitou M., Fujimoto K., Doi Y., Itoh M., Fujimoto T., Furuse M., Takano H., Noda T., Tsukita S. Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J. Cell Biol. 1998, 141:397-408.
58. Samak G., Aggarwal S., Rao R.K. ERK is involved in EGF-mediated protection of tight junctions, but not adherens junctions, in acetaldehyde-treated Caco-2 cell monolayers. American journal of physiology. Gastr. Liver Physiol. 2011, 301:G50-59.
59. Scarselli E., Ansuini H., Cerino R., Roccasecca R.M., Acali S., Filocamo G., Traboni C., Nicosia A., Cortese R., Vitelli A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002, 21:5017-5025.
60. Severson E.A., Kwon M., Hilgarth R.S., Parkos C.A., Nusrat A. Glycogen Synthase Kinase 3 (GSK-3) influences epithelial barrier function by regulating occludin, claudin-1 and E-cadherin expression. Biochem. Biophys. Res. Commun. 2010, 397:592-597.
61. Simonovic I., Arpin M., Koutsouris A., Falk-Krzesinski H.J., Hecht G. Enteropathogenic Escherichia coli activates ezrin, which participates in disruption of tight junction barrier function. Infect Immun. 2001, 69:5679-5688.
62. Strock C.J., Park J.I., Nakakura E.K., Bova G.S., Isaacs J.T., Ball D.W., Nelkin B.D. Cyclin-dependent kinase 5 activity controls cell motility and metastatic potential of prostate cancer cells. Can. Res. 2006, 66:7509-7515.
63. Stuart R.O., Nigam S.K. Regulated assembly of tight junctions by protein kinase C. Proc. Natl. Acad Sci. USA 1995, 92:6072-6076.
64. Suzuki T., Elias B.C., Seth A., Shen L., Turner J.R., Giorgianni F., Desiderio D., Guntaka R., Rao R. PKC eta regulates occludin phosphorylation and epithelial tight junction integrity. Proc. Natl. Acad Sci. USA 2009, 106:61-66.
65. Tobioka H., Isomura H., Kokai Y., Tokunaga Y., Yamaguchi J., Sawada N. Occludin expression decreases with the progression of human endometrial carcinoma. Human Pathol. 2004, 35:159-164.
66. Tusnady G.E., Simon I. Topology prediction of helical transmembrane proteins: how far have we reached?. Curr. Protein Peptide Sci. 2010, 11:550-561.
67. Van Itallie C.M., Fanning A.S., Holmes J., Anderson J.M. Occludin is required for cytokine-induced regulation of tight junction barriers. J. Cell Sci. 2010, 123:2844-2852.
68. Zeidan Q., Hart G.W. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J. Cell Sci. 2010, 123:13-22.