Structure of reovirus σ1 in complex with its receptor junctional adhesion molecule-A

PLoS Pathogens

Volumn 4, Issue 12, 2008, Pages

  Kirchner, Eva ^a   Guglielmi, Kristen M ^b   Strauss, Holger M ^c   Dermody, Terence S ^b   Stehle, Thilo ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Gesellschaft für Kolloidanalytik GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HOMODIMER; IMMUNOGLOBULIN; IMMUNOGLOBULIN RECEPTOR; JUNCTIONAL ADHESION MOLECULE A; REOVIRUS ATTACHMENT PROTEIN DELTA 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; CELL ADHESION MOLECULE; JUNCTIONAL ADHESION MOLECULE A , HUMAN; JUNCTIONAL ADHESION MOLECULE-A , HUMAN; SIGMA 1 PROTEIN, REOVIRUS;

ARTICLE; BINDING SITE; BIOPHYSICS; CELL ADHESION; CELL CULTURE; CELL SURFACE; CRYSTAL STRUCTURE; DIMERIZATION; DISSOCIATION CONSTANT; FEMALE; GEL PERMEATION CHROMATOGRAPHY; GENETICS; HUMAN; HUMAN CELL; LIGAND BINDING; MAMMALIAN ORTHOREOVIRUS; NONHUMAN; PLANT GROWTH; PLASMID; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN STRUCTURE; ULTRACENTRIFUGATION; VIRUS ATTACHMENT; VIRUS MORPHOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; HELA CELL; METABOLISM; PH; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY;

MAMMALIA; ORTHOREOVIRUS;

BINDING SITES; CAPSID PROTEINS; CELL ADHESION MOLECULES; CRYSTALLOGRAPHY, X-RAY; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULINS; MODELS, MOLECULAR; ORTHOREOVIRUS, MAMMALIAN; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE;

EID: 58149263468     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000235     Document Type: Article

References (66)

1. Albelda SM (1991) Endothelial and epithelial cell adhesion molecules. Am J Respir Cell Mol Biol 4: 195-203.
2. Vogelmann R, Amieva MR, Falkow S, Nelson WJ (2004) Breaking into the epithelial apical-junctional complex-news from pathogen hackers. Curr Opin Cell Biol 16: 86-93.
3. Wang J, Springer TA (1998) Structural specializations of immunoglobulin superfamily members for adhesion to integrins and viruses. Immunol Rev 163: 197-215.
4. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, et al. (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104: 441-451.
5. Makino A, Shimojima M, Miyazawa T, Kato K, Tohya Y, et al. (2006) Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J Virol 80: 4482-4490.
6. Schiff LA, Nibert ML, Tyler KL (2007) Orthoreoviruses and their replication. In: Knipe DM, Howley PM, eds (2007) Fields Virology. Fifth ed. Philadelphia: Lippincott Williams & Wilkins. pp 1853-1915.
7. Kobayashi T, Antar AAR, Boehme KW, Danthi P, Eby EA, et al. (2007) Plasmid-based reverse genetics for animal double-stranded RNA viruses. Cell Host Microbe 1: 147-157.
8. Fraser RDB, Furlong DB, Trus BL, Nibert ML, Fields BN, et al. (1990) Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J Virol 64: 2990-3000.
9. Furlong DB, Nibert ML, Fields BN (1988) Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol 62: 246-256.
10. Stewart PL, Burnett RM, Cyrklaff M, Fuller SD (1991) Image reconstruction reveals the complex molecular organization of adenovirus. Cell 67: 145-154.
11. Chappell JD, Duong JL, Wright BW, Dermody TS (2000) Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J Virol 74: 8472-8479.
12. Chappell JD, Gunn VL, Wetzel JD, Baer GS, Dermody TS (1997) Mutations in type 3 reovirus that determine binding to sialic acid are contained in the fibrous tail domain of viral attachment protein σ1. J Virol 71: 1834-1841.
13. Schelling P, Guglielmi KM, Kirchner E, Paetzold B, Dermody TS, et al. (2007) The reovirus σ1 aspartic acid sandwich: a trimerization motif poised for conformational change. J Biol Chem 282: 11582-11589.
14. Chappell JD, Prota A, Dermody TS, Stehle T (2002) Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J 21: 1-11.
15. van Raaij MJ, Mitraki A, Lavigne G, Cusack S (1999) A triple β-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature 401: 935-938.
16. Merckel MC, Huiskonen JT, Bamford DH, Goldman A, Tuma R (2005) The structure of the bacteriophage PRD1 spike sheds light on the evolution of viral capsid architecture. Mol Cell 18: 161-170.
17. Guardado CP, Fox GC, Hermo Parrado XL, Llamas-Saiz AL, Costas C, et al. (2005) Structure of the carboxy-terminal receptor-binding domain of avian reovirus fibre sigmaC. J Mol Biol 354: 137-149.
18. Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, et al. (2000) Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 113: 2363-2374.
19. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, et al. (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142: 117-127.
20. Williams LA, Martin-Padura I, Dejana E, Hogg N, Simmons DL (1999) Identification and characterisation of human junctional adhesion molecule (JAM). Mol Immunol 36: 1175-1188.
21. Del Maschio A, De Luigi A, Martin-Padura I, Brockhaus M, Bartfai T, et al. (1999) Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J Exp Med 190: 1351-1356.
22. Woodfin A, Reichel CA, Khandoga A, Corada M, Voisin MB, et al. (2007) JAM-A mediates neutrophil transmigration in a stimulus-specific manner in vivo: evidence for sequential roles for JAM-A and PECAM-1 in neutrophil transmigration. Blood 110: 1848-1856.
23. Kostrewa D, Brockhaus M, D'Arcy A, Dale GE, Nelboeck P, et al. (2001) X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J 20: 4391-4398.
24. Prota AE, Campbell JA, Schelling P, Forrest JC, Peters TR, et al. (2003) Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc Natl Acad Sci USA 100: 5366-5371.
25. van Raaij MJ, Chouin E, van der Zandt H, Bergelson JM, Cusack S (2000) Dimeric structure of the coxsackievirus and adenovirus receptor D1 domain at 1.7 A resolution. Structure 8: 1147-1155.
26. Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS (2003) Structure-function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J Biol Chem 278: 48434-48444.
27. Guglielmi KM, Kirchner E, Holm GH, Stehle T, Dermody TS (2007) Reovirus binding determinants in junctional adhesion molecule-A. J Biol Chem 282: 17930-17940.
28. Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497.
29. Rodgers DW (1994) Cryocrystallography. Structure 2: 1135-1140.
30. Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, et al. (2000) Homophilic interaction of junctional adhesion molecule. J Biol Chem 275: 30970-30976.
31. Barton ES, Connolly JL, Forrest JC, Chappell JD, Dermody TS (2001) Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 276: 2200-2211.
32. Campbell JA, Shelling P, Wetzel JD, Johnson EM, Wilson GAR, et al. (2005) Junctional adhesion molecule-A serves as a receptor for prototype and field-isolate strains of mammalian reovirus. J Virol 79: 7967-7978.
33. Kleywegt GJ, Jones TA (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D Biol Crystallogr 50: 178-185.
34. Guglielmi KM, Johnson EM, Stehle T, Dermody TS (2006) Attachment and cell entry of mammalian orthoreovirus. Curr Top Microbiol Immunol 309: 1-38.
35. Wu E, Pache L, Von Seggern DJ, Mullen TM, Mikyas Y, et al. (2003) Flexibility of the adenovirus fiber is required for efficient receptor interaction. J Virol 77: 7225-7235.
36. Stehle T, Dermody TS (2003) Structural evidence for common functions and ancestry of the reovirus and adenovirus attachment proteins. Rev Med Virol 13: 123-132.
37. Stehle T, Dermody TS (2004) Structural similarities in the cellular receptors used by adenovirus and reovirus. Viral Immunol 17: 129-143.
38. Bewley MC, Springer K, Zhang YB, Freimuth P, Flanagan JM (1999) Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286: 1579-1583.
39. Kirby I, Davison E, Beavil AJ, Soh CP, Wickham TJ, et al. (2000) Identification of contact residues and definition of the CAR-binding site of adenovirus type 5 fiber protein. J Virol 74: 2804-2813.
40. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, et al. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
41. He Y, Chipman PR, Howitt J, Bator CM, Whitt MA, et al. (2001) Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nat Struct Biol 8: 874-878.
42. Ossiboff RJ, Parker JS (2007) Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. J Virol 81: 13608-13621.
43. Bhella D, Gatherer D, Chaudhry Y, Pink R, Goodfellow IG (2008) Structural insights into calicivirus attachment and uncoating. J Virol 82: 8051-8058.
44. Mercier GT, Campbell JA, Chappell JD, Stehle T, Dermody TS, et al. (2004) A chimeric adenovirus vector encoding reovirus attachment protein σ1 targets cells expressing junctional adhesion molecule 1. Proc Natl Acad Sci USA 101: 6188-6193.
45. Forsyth P, Roldan G, George D, Wallace C, Palmer CA, et al. (2008) A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 16: 627-632.
46. Liu TC, Kirn D (2007) Systemic efficacy with oncolytic virus therapeutics: clinical proof-of-concept and future directions. Cancer Res 67: 429-432.
47. Norman KL, Lee PW (2000) Reovirus as a novel oncolytic agent. J Clin Invest 105: 1035-1038.
48. Parato KA, Senger D, Forsyth PA, Bell JC (2005) Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 5: 965-976.
49. Wilcox ME, Yang W, Senger D, Rewcastle NB, Morris DG, et al. (2001) Reovirus as an oncolytic agent against experimental human malignant gliomas. J Natl Cancer Inst 93: 903-912.
50. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing antibody. Nature 393: 648-659.
51. Bella J, Kolatkar PR, Marlor CW, Greve JM, Rossmann MG (1998) The structure of the two amino-terminal domains of human ICAM-1 suggests how it functions as a rhinovirus receptor and as an LFA-1 integrin ligand. Proceedings of the National Academy of Sciences 95: 4140-4145.
52. Miller J, Knorr R, Ferrone M, Houdei R, Carron CP, et al. (1995) Intercellular adhesion molecule-1 dimerization and its consequences for adhesion mediated by lymphocyte function associated-1. J Exp Med 182: 1231-1241.
53. Wu H, Kwong PD, Hendrickson WA (1997) Dimeric association and segmental variability in the structure of human CD4. Nature 387: 527-530.
54. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, et al. (2008) Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15: 567-572.
55. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763.
56. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921.
57. Emsley P, Cowtan K (2004) Coot: model building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
58. Kleywegt GJ, Jones TA (1994) Halloween - masks and bones. In: Bailey S, Hubbard R, Waller D, eds (1994) From first map to final model. Warrington (UK): SERC Daresbury Laboratory. pp 59-66.
59. Gamblin SJ, Rodgers DW, Stehle T (1996) Improving electron density maps calculated from weak or anisotropic data. Proceedings of the CCP4 Study Weekend. Daresbury, UK: Daresbury Laboratory. pp 160-163.
60. DeLano WL (2002) The PyMOL Molecular Graphics System. San Carlos, USA: DeLano Scientific.
61. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
62. Virgin HW IV, Bassel-Duby R, Fields BN, Tyler KL (1988) Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol 62: 4594-4604.
63. Ishii K, Ueda Y, Matsuo K, Matsuura Y, Kitamura T, et al. (2002) Structural analysis of vaccinia virus DIs strain: application as a new replication-deficient viral vector. Virology 302: 433-444.
64. Lerner MG, Carlson HA (2006) APBS plugin for PyMOL. Ann Arbor: University of Michigan.
65. Brünger AT (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472-475.
66. Brändén C-I, Jones TA (1990) Between objectivity and subjectivity. Nature 343: 687-689.