Surface plasmon resonance analysis of the binding of high-risk mucosal HPV E6 oncoproteins to the PDZ1 domain of the tight junction protein MAGI-1

Journal of Molecular Recognition

Volumn 24, Issue 4, 2011, Pages 511-523

  Fournane, Sadek ^a   Charbonnier, Sebastian ^a   Chapelle, Anne ^a   Kieffer, Bruno ^a   Orfanoudakis, Georges ^a   Travé, Gilles ^a   Masson, Murielle ^a   Nominé, Yves ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Biacore; HPV E6; MAGI 1; medium throughput screening; PDZ domain; protein peptide interaction; SPR

Indexed keywords

DNA BINDING PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 18; MAGI1 PROTEIN, HUMAN; NERVE CELL ADHESION MOLECULE; ONCOPROTEIN; REPRESSOR PROTEIN;

ARTICLE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SURFACE PLASMON RESONANCE;

CELL ADHESION MOLECULES, NEURONAL; DNA-BINDING PROTEINS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; ONCOGENE PROTEINS, VIRAL; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SURFACE PLASMON RESONANCE;

HUMAN PAPILLOMAVIRUS;

EID: 79953778055     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.1056     Document Type: Article

References (59)

1. Charbonnier S, Coutouly M, Kieffer B, Trave G, Atkinson RA,. 2006. 13C, 15N and 1H resonance assignment of the PDZ1 domain of MAGI-1 using QUASI. J. Biomol. NMR 36 (Suppl 1): 33. (Pubitemid 46909589)
2. Charbonnier S, Stier G, Orfanoudakis G, Kieffer B, Atkinson RA, Trave G,. 2008. Defining the minimal interacting regions of the tight junction protein MAGI-1 and HPV16 E6 oncoprotein for solution structure studies. Protein Expr. Purif. 60 (1): 64-73.
3. Chastre E, Abdessamad M, Kruglov A, Bruyneel E, Bracke M, Di Gioia Y, Beckerle MC, van Roy F, Kotelevets L,. 2009. TRIP6, a novel molecular partner of the MAGI-1 scaffolding molecule, promotes invasiveness. FASEB J. 23 (3): 916-928.
4. Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S,. 2003. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br. J. Cancer 88 (1): 63-73.
5. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H,. 2004. Classification of papillomaviruses. Virology 324 (1): 17-27. (Pubitemid 38737395)
6. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A,. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (3): 277-293.
7. Dobrosotskaya IY,. 2001. Identification of mNET1 as a candidate ligand for the first PDZ domain of MAGI-1. Biochem. Biophys. Res. Commun. 283 (4): 969-975. (Pubitemid 32924675)
8. Dobrosotskaya IY, James GL,. 2000. MAGI-1 interacts with beta-catenin and is associated with cell-cll adhesion structures. Biochem. Biophys. Res. Commun. 270 (3): 903-909. (Pubitemid 30444804)
9. Dobrosotskaya I, Guy RK, James GL,. 1997. MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein-protein interaction domains. J. Biol. Chem. 272 (50): 31589-31597. (Pubitemid 28013302)
10. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R,. 1996. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85 (7): 1067-1076. (Pubitemid 26231173)
11. Favre-Bonvin A, Reynaud C, Kretz-Remy C, Jalinot P,. 2005. Human papillomavirus type 18 E6 protein binds the cellular PDZ protein TIP-2/GIPC, which is involved in transforming growth factor beta signaling and triggers its degradation by the proteasome. J. Virol. 79 (7): 4229-4237. (Pubitemid 40388361)
12. Gianni S, Engstrom A, Larsson M, Calosci N, Malatesta F, Eklund L, Ngang CC, Travaglini-Allocatelli C, Jemth P,. 2005. The kinetics of PDZ domain-ligand interactions and implications for the binding mechanism. J. Biol. Chem. 280 (41): 34805-34812. (Pubitemid 41504614)
13. Glaunsinger BA, Lee SS, Thomas M, Banks L, Javier R,. 2000. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 19 (46): 5270-5280.
14. Hampson L, Li C, Oliver AW, Kitchener HC, Hampson IN,. 2004. The PDZ protein Tip-1 is a gain of function target of the HPV16 E6 oncoprotein. Int. J. Oncol. 25 (5): 1249-1256.
15. Handa K, Yugawa T, Narisawa-Saito M, Ohno S, Fujita M, Kiyono T,. 2007. E6AP-dependent degradation of DLG4/PSD95 by high-risk human papillomavirus type 18 E6 protein. J. Virol. 81 (3): 1379-1389. (Pubitemid 46167859)
16. Hirabayashi S, Tajima M, Yao I, Nishimura W, Mori H, Hata Y,. 2003. JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol. Cell. Biol. 23 (12): 4267-4282. (Pubitemid 36666429)
17. Jemth P, Gianni S,. 2007. PDZ domains: folding and binding. Biochemistry 46 (30): 8701-8708. (Pubitemid 47204435)
18. Jeong KW, Kim HZ, Kim S, Kim YS, Choe J,. 2007. Human papillomavirus type 16 E6 protein interacts with cystic fibrosis transmembrane regulator-associated ligand and promotes E6-associated protein-mediated ubiquitination and proteasomal degradation. Oncogene 26 (4): 487-499. (Pubitemid 46160963)
19. Jing M, Bohl J, Brimer N, Kinter M, Vande Pol SB,. 2007. Degradation of tyrosine phosphatase PTPN3 (PTPH1) by association with oncogenic human papillomavirus E6 proteins. J. Virol. 81 (5): 2231-2239.
20. Kang BS, Cooper DR, Devedjiev Y, Derewenda U, Derewenda ZS,. 2003. Molecular roots of degenerate specificity in syntenin's PDZ2 domain: reassessment of the PDZ recognition paradigm. Structure 11 (7): 845-853. (Pubitemid 36833270)
21. Karlsson R, Roos H, Bruno J, Stolz L,. 1997. Practical aspects concerning direct detection of low molecular weight analytes using BIACORE 2000. BIA. J. 18-21.
22. Keller R,. 2004. The computer aided resonance assignment tutorial. ISBN 3-85600-112-3, first edition. The online version can be downloaded from.
23. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, Ishibashi M,. 1997. Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. U.S.A. 94 (21): 11612-11616. (Pubitemid 27451047)
24. Kiyono T, Foster S, Koop J, McDougall J, Galloway D, Klingelhutz A,. 1998. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396 (6706): 84-88. (Pubitemid 28520454)
25. Kozlov G, Gehring K, Ekiel I,. 2000. Solution structure of the PDZ2 domain from human phosphatase hPTP1E and its interactions with C-terminal peptides from the Fas receptor. Biochemistry 39 (10): 2572-2580. (Pubitemid 30148909)
26. Lee SS, Weiss RS, Javier RT,. 1997. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. U.S.A. 94 (13): 6670-6675.
27. Lee SS, Glaunsinger B, Mantovani F, Banks L, Javier RT,. 2000. Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J. Virol. 74 (20): 9680-9693.
28. Liu Y, Henry GD, Hegde RS, Baleja JD,. 2007. Solution structure of the hDlg/SAP97 PDZ2 domain and its mechanism of interaction with HPV-18 papillomavirus E6 protein. Biochemistry 46 (38): 10864-10874. (Pubitemid 47463038)
29. Liu Y, Cherry JJ, Dineen JV, Androphy EJ, Baleja JD,. 2009. Determinants of stability for the E6 protein of papillomavirus type 16. J. Mol. Biol. 386 (4): 1123-1137.
30. Mulder FA, Schipper D, Bott R, Boelens R,. 1999. Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilis. J. Mol. Biol. 292 (1): 111-123. (Pubitemid 29425657)
31. Myszka DG,. 1999. Improving biosensor analysis. J. Mol. Recognit. 12 (5): 279-284. (Pubitemid 129708590)
32. Nakagawa S, Huibregtse JM,. 2000. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol. Cell. Biol. 20 (21): 8244-8253.
33. Narisawa-Saito M, Kiyono T,. 2007. Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci. 98 (10): 1505-1511. (Pubitemid 47308443)
34. Nguyen ML, Nguyen MM, Lee D, Griep AE, Lambert PF,. 2003. The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo. J. Virol. 77 (12): 6957-6964. (Pubitemid 36666888)
35. Nomine Y, Masson M, Charbonnier S, Zanier K, Ristriani T, Deryckere F, Sibler AP, Desplancq D, Atkinson RA, Weiss E, et al,. 2006. Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirus-mediated pathogenesis. Mol. Cell. 21 (5): 665-678. (Pubitemid 43290733)
36. Ohashi M, Sakurai M, Higuchi M, Mori N, Fukushi M, Oie M, Coffey RJ, Yoshiura K, Tanaka Y, Uchiyama M, et al,. 2004. Human T-cell leukemia virus type 1 Tax oncoprotein induces and interacts with a multi-PDZ domain protein, MAGI-3. Virology 320 (1): 52-62. (Pubitemid 38296714)
37. Ohno H, Hirabayashi S, Kansaku A, Yao I, Tajima M, Nishimura W, Ohnishi H, Mashima H, Fujita T, Omata M, et al,. 2003. Carom: a novel membrane-associated guanylate kinase-interacting protein with two SH3 domains. Oncogene 22 (52): 8422-8431. (Pubitemid 37523894)
38. Patrie KM, Drescher AJ, Goyal M, Wiggins RC, Margolis B,. 2001. The membrane-associated guanylate kinase protein MAGI-1 binds megalin and is present in glomerular podocytes. J. Am. Soc. Nephrol. 12 (4): 667-677. (Pubitemid 32246694)
39. Patrie KM, Drescher AJ, Welihinda A, Mundel P, Margolis B,. 2002. Interaction of two actin-binding proteins, synaptopodin and alpha-actinin-4, with the tight junction protein MAGI-1. J. Biol. Chem. 277 (33): 30183-30190.
40. Petit MM, Meulemans SM, Alen P, Ayoubi TA, Jansen E, Van de Ven WJ,. 2005. The tumor suppressor Scrib interacts with the zyxin-related protein LPP, which shuttles between cell adhesion sites and the nucleus. BMC Cell. Biol. 6 (1): 1.
41. Piotto M, Saudek V, Sklenar V,. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2 (6): 661-665.
42. Sainlos M, Iskenderian WS, Imperiali B,. 2009. A general screening strategy for peptide-based fluorogenic ligands: probes for dynamic studies of PDZ domain-mediated interactions. J. Am. Chem. Soc. 131 (19): 6680-6682.
43. Scopes RK,. 1974. Measurement of protein by spectrophotometry at 205nm. Anal. Biochem. 59 (1): 277-282.
44. Skelton NJ, Koehler MF, Zobel K, Wong WL, Yeh S, Pisabarro MT, Yin JP, Lasky LA, Sidhu SS,. 2003. Origins of PDZ domain ligand specificity. Structure determination and mutagenesis of the Erbin PDZ domain. J. Biol. Chem. 278 (9): 7645-7654. (Pubitemid 36800774)
45. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH, Crompton A, Chan AC, Anderson JM, Cantley LC,. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275 (5296): 73-77. (Pubitemid 27020310)
46. Spanos WC, Hoover A, Harris GF, Wu S, Strand GL, Anderson ME, Klingelhutz AJ, et al,. 2008. The PDZ binding motif of human papillomavirus type 16 E6 induces PTPN13 loss, which allows anchorage-independent growth and synergizes with ras for invasive growth. J. Virol. 82 (5): 2493-2500. (Pubitemid 351293550)
47. Stiffler MA, Chen JR, Grantcharova VP, Lei Y, Fuchs D, Allen JE, Zaslavskaia LA, MacBeath G,. 2007. PDZ domain binding selectivity is optimized accros the mouse proteome. Science 317: 364-369.
48. Storrs CH, Silverstein SJ,. 2007. PATJ, a tight junction-associated PDZ protein, is a novel degradation target of high-risk human papillomavirus E6 and the alternatively spliced isoform 18 E6. J. Virol. 81 (8): 4080-4090. (Pubitemid 46586903)
49. Thomas M, Glaunsinger B, Pim D, Javier R, Banks L,. 2001. HPV E6 and MAGUK protein interactions: determination of the molecular basis for specific protein recognition and degradation. Oncogene 20 (39): 5431-5439. (Pubitemid 32889479)
50. Thomas M, Laura R, Hepner K, Guccione E, Sawyers C, Lasky L, Banks L,. 2002. Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21 (33): 5088-5096.
51. Thomas M, Massimi P, Navarro C, Borg JP, Banks L,. 2005. The hScrib/Dlg apico-basal control complex is differentially targeted by HPV-16 and HPV-18 E6 proteins. Oncogene 24 (41): 6222-6230. (Pubitemid 43080045)
52. Thomas M, Narayan N, Pim D, Tomaic V, Massimi P, Nagasaka K, Kranjec C, Gammoh N, Banks L,. 2008a. Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27 (55): 7018-7030.
53. Thomas M, Dasgupta J, Zhang Y, Chen X, Banks L,. 2008b. Analysis of specificity determinants in the interactions of different HPV E6 proteins with their PDZ domain-containing substrates. Virology 376 (2): 371-378.
54. Tonikian R, Zhang Y, Sazinsky SL, Currell B, Yeh JH, Reva B, Held HA, Appleton BA, Evangelista M, Wu Y, et al,. 2008. A specificity map for the PDZ domain family. PLoS Biol. 6 (9): e239.
55. Valiente M, Andres-Pons A, Gomar B, Torres J, Gil A, Tapparel C, Antonarakis SE, Pulido R,. 2005. Binding of PTEN to specific PDZ domains contributes to PTEN protein stability and phosphorylation by microtubule-associated serine/threonine kinases. J. Biol. Chem. 280 (32): 28936-28943. (Pubitemid 41161339)
56. Zanier K, Charbonnier S, Baltzinger M, Nomine Y, Altschuh D, Trave G,. 2005. Kinetic analysis of the interactions of human papillomavirus E6 oncoproteins with the ubiquitin ligase E6AP using surface plasmon resonance. J. Mol. Biol. 349 (2): 401-412. (Pubitemid 40693758)
57. Zanier K, Nomine Y, Charbonnier S, Ruhlmann C, Schultz P, Schweizer J, Trave G,. 2007. Formation of well-defined soluble aggregates upon fusion to MBP is a generic property of E6 proteins from various human papillomavirus species. Protein Expr. Purif. 51 (1): 59-70. (Pubitemid 44822662)
58. Zhang Y, Dasgupta J, Ma RZ, Banks L, Thomas M, Chen XS,. 2007. Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein. J. Virol. 81 (7): 3618-3626. (Pubitemid 46456670)
59. zur Hausen H,. 1994. Molecular pathogenesis of cancer of the cervix and its causation by specific human papillomavirus types. Curr. Top. Microbiol. Immunol. 186: 131-156. (Pubitemid 24099089)