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Attachment and Cell Entry of Mammalian Orthoreovirus

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Reoviruses: Entry, Assembly and Morphogenesis

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 309))

Abstract

Mammalian orthoreoviruses (reoviruses) serve as a tractable model system for studies of viral pathogenesis. Reoviruses infect virtually all mammals, but cause disease only in the very young. Prototype strains of the three reovirus serotypes differ in pathogenesis following infection of newborn mice. Reoviruses are nonenveloped, icosahedral particles that consist of ten segments of double-stranded RNA encapsidated within two protein shells, the inner core and outer capsid. High-resolution structures of individual components of the reovirus outer capsid and a single viral receptor have been solved and provide insight into the functions of these molecules in viral attachment, entry, and pathogenesis. Attachment of reovirus to target cells is mediated by the reovirus σ1 protein, a filamentous trimer that projects from the outer capsid. Junctional adhesion molecule-A is a serotype-independent receptor for reovirus, and sialic acid is a coreceptor for serotype 3 strains. After binding to receptors on the cell surface, reovirus is internalized via receptor-mediated endocytosis. Internalization is followed by stepwise disassembly of the viral outer capsid in the endocytic compartment. Uncoating events, which require acidic pH and endocytic proteases, lead to removal of major outer-capsid protein σ3, resulting in exposure of membrane-penetration mediator μ1 and a conformational change in attachment protein σ1. After penetration of endosomes by uncoated particles, the transcriptionally active viral core is released into the cytoplasm, where replication proceeds. Despite major advances in defining reovirus attachment and entry mechanisms, many questions remain. Ongoing research is aimed at understanding serotype-dependent differences in reovirus tropism, viral cell-entry pathways, the individual and corporate roles of acidic pH and proteases in viral entry, and μ1 function in membrane penetration.

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References

  1. Amerongen HM, Wilson GAR, Fields BN, Neutra MR (1994) Proteolytic processing of reovirus is required for adherence to intestinal M cells. JVirol 68:8428–8432

    CAS  Google Scholar 

  2. Arrate MP, Rodriguez JM, Tran TM, Brock TA, Cunningham SA (2001) Cloning of human junctional adhesion molecule 3 (JAM3) and its identification as the JAM2 counter-receptor. J Biol Chem 276:45826–45832

    Article  PubMed  CAS  Google Scholar 

  3. Baer GS, Dermody TS (1997) Mutations in reovirus outer-capsid protein σ3 selected during persistent infections of L cells confer resistance to protease inhibitor E64. J Virol 71:4921–4928

    PubMed  CAS  Google Scholar 

  4. Baer GS, Ebert DH, Chung CJ, Erickson AH, Dermody TS (1999) Mutant cells selected during persistent reovirus infection do not express mature cathepsin L and do not support reovirus disassembly. J Virol 73:9532–9543

    PubMed  CAS  Google Scholar 

  5. Balda MS, Matter K (2000) Transmembrane proteins of tight junctions. Semin Cell Dev Biol 11:281–289

    Article  PubMed  CAS  Google Scholar 

  6. Barrett AJ, Kembhavi AA, Brown MA, Kirschke H, Knight CG, Tamai M, Hanada K (1982) L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem J 201:189–198

    PubMed  CAS  Google Scholar 

  7. 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

    Article  PubMed  CAS  Google Scholar 

  8. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, Schnell F, Nusrat A, Parkos CA, Dermody TS (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104:441–451

    Article  PubMed  CAS  Google Scholar 

  9. Barton ES, Youree BE, Ebert DH, Forrest JC, Connolly JL, Valyi-Nagy T, Washington K, Wetzel JD, Dermody TS (2003) Utilization of sialic acid as a coreceptor is required for reovirus-induced biliary disease. J Clin Invest 111:1823–1833

    Article  PubMed  CAS  Google Scholar 

  10. Bass DM, Bodkin D, Dambrauskas R, Trier JS, Fields BN, Wolf JL (1990) Intra-luminal proteolytic activation plays an important role in replication of type 1 reovirus in the intestines of neonatal mice. J Virol 64:1830–1833

    PubMed  CAS  Google Scholar 

  11. Bassel-Duby R, Spriggs DR, Tyler KL, Fields BN (1986) Identification of attenuating mutations on the reovirus type 3 S1 double-stranded RNA segment with a rapid sequencing technique. J Virol 60:64–67

    PubMed  CAS  Google Scholar 

  12. Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, Bartfai T, Dejana E, Brockhaus M (2000) Homophilic interaction of junctional adhesion molecule. J Biol Chem 275:30970–30976

    Article  PubMed  CAS  Google Scholar 

  13. Bazzoni G, Martinez-Estrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E (2000) Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem 275:20520–20526

    Article  PubMed  CAS  Google Scholar 

  14. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323

    Article  PubMed  CAS  Google Scholar 

  15. Bodkin DK, Nibert ML, Fields BN (1989) Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J Virol 63:4676–4681

    PubMed  CAS  Google Scholar 

  16. Bond JS, Butler PE (1987) Intracellular proteases. Ann Rev Biochem 56:333–364

    Article  PubMed  CAS  Google Scholar 

  17. Borsa J, Morash BD, Sargent MD, Copps TP, Lievaart PA, Szekely JG (1979) Two modes of entry of reovirus particles into L cells. J Gen Virol 45:161–170

    PubMed  CAS  Google Scholar 

  18. Borsa J, Sargent MD, Lievaart PA, Copps TP (1981)Reovirus: evidence for a second step in the intracellular uncoating and transcriptase activation process. Virology 111:191–200

    Article  PubMed  CAS  Google Scholar 

  19. Bousarghin L, Touze A, Sizaret PY, Coursaget P (2003) Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol 77:3846–3850

    Article  PubMed  CAS  Google Scholar 

  20. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43

    Article  PubMed  CAS  Google Scholar 

  21. Canning WM, Fields BN (1983) Ammonium chloride prevents lytic growth of reovirus and helps to establish persistent infection in mouse L cells. Science 219:987–988

    Article  PubMed  CAS  Google Scholar 

  22. Carson M (1987) Ribbon models of macromolecules. J Mol Graph 5:103–106

    Article  CAS  Google Scholar 

  23. Cera MR, Del Prete A, Vecchi A, Corada M, Martin-Padura I, Motoike T, Tonetti P, Bazzoni G, Vermi W, Gentili F, Bernasconi S, Sato TN, Mantovani A, Dejana E (2004) Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J Clin Invest 114:729–738

    Article  PubMed  CAS  Google Scholar 

  24. Chandran K, Farsetta DL, Nibert ML (2002) Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein μ1 mediates membrane disruption. J Virol 76:9920–9933

    Article  PubMed  CAS  Google Scholar 

  25. Chandran K, Nibert ML(1998)Protease cleavage of reovirus capsid protein μ1/μ1C is blocked by alkyl sulfate detergents, yielding a new type of infectious subvirion particle. J Virol 762:467–475

    Google Scholar 

  26. Chandran K, Parker JS, Ehrlich M, Kirchhausen T, Nibert ML (2003) The delta region of outer-capsid protein μ1 undergoes conformational change and release from reovirus particles during cell entry. J Virol 77:13361–13375

    Article  PubMed  CAS  Google Scholar 

  27. Chandran K, Walker SB, Chen Y, Contreras CM, Schiff LA, Baker TS, Nibert ML (1999) In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3. J Virol 73:3941–3950

    PubMed  CAS  Google Scholar 

  28. Chapman HA, Riese RJ, Shi GP (1997) Emerging roles for cysteine proteases in human biology. Annu Rev Physiol 59:63–88

    Article  PubMed  CAS  Google Scholar 

  29. 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

    Article  PubMed  CAS  Google Scholar 

  30. 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 μ1. J Virol 71:1834–1841

    PubMed  CAS  Google Scholar 

  31. Chappell JD, Prota A, Dermody TS, Stehle T (2002) Crystal structure of reovirus attachment protein μ1 reveals evolutionary relationship to adenovirus fiber. EMBO J 21:1–11

    Article  PubMed  CAS  Google Scholar 

  32. Clarke P, Meintzer SM, Gibson S, Widmann C, Garrington TP, Johnson GL, Tyler KL (2000) Reovirus-induced apoptosis is mediated by TRAIL. J Virol 74:8135–8139

    Article  PubMed  CAS  Google Scholar 

  33. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM (2001) The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci U S A 98:15191–15196

    Article  PubMed  CAS  Google Scholar 

  34. Connolly JL, Barton ES, Dermody TS (2001) Reovirus binding to cell surface sialic acid potentiates virus-induced apoptosis. J Virol 75:4029–4039

    Article  PubMed  CAS  Google Scholar 

  35. Connolly JL, Dermody TS (2002) Virion disassembly is required for apoptosis induced by reovirus. J Virol 76:1632–1641

    Article  PubMed  CAS  Google Scholar 

  36. Connolly JL, Rodgers SE, Clarke P, Ballard DW, Kerr LD, Tyler KL, Dermody TS (2000) Reovirus-induced apoptosis requires activation of transcription factor NF-κB. J Virol 74:2981–2989

    Article  PubMed  CAS  Google Scholar 

  37. Cunningham SA, Arrate MP, Rodriguez JM, Bjercke RJ, Vanderslice P, Morris AP, Brock TA (2000) A novel protein with homology to the junctional adhesion molecule. Characterization of leukocyte interactions. J Biol Chem 275:34750–34756

    Article  PubMed  CAS  Google Scholar 

  38. DeBiasi R, Edelstein C, Sherry B, Tyler K(2001) Calpain inhibition protects against virus-induced apoptotic myocardial injury. J Virol 75:351–361

    Article  PubMed  CAS  Google Scholar 

  39. DelMaschio A, De Luigi A, Martin-Padura I, Brockhaus M, Bartfai T, Fruscella P, Adorini L, Martino G, Furlan R, De Simoni MG, Dejana E (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

    Article  PubMed  Google Scholar 

  40. Denisova E, Dowling W, LaMonica R, Shaw R, Scarlata S, Ruggeri F, Mackow ER (1999) Rotavirus capsid protein VP5* permeabilizes membranes. J Virol 73:3147–3153

    PubMed  CAS  Google Scholar 

  41. Dermody TS (1998) Molecular mechanisms of persistent infection by reovirus. In: Tyler KL, Oldstone MBA (eds), Curr TopicsMicro Immunol, vol. 233. Reoviruses, II Cytopathogenicity and pathogenesis. Springer-Verlag, Berlin Heidelberg, New York, pp 1–22

    Google Scholar 

  42. Dermody TS, Nibert ML, Bassel-Duby R, Fields BN (1990) A σ1 region important for hemagglutination by serotype 3 reovirus strains. J Virol 64:5173–5176

    PubMed  CAS  Google Scholar 

  43. Dermody TS, Nibert ML, Bassel-Duby R, Fields BN (1990) Sequence diversity in S1 genes and S1 translation products of 11 serotype 3 reovirus strains. J Virol 64:4842–4850

    PubMed  CAS  Google Scholar 

  44. Dermody TS, Nibert ML, Wetzel JD, Tong X, Fields BN (1993) Cells and viruses with mutations affecting viral entry are selected during persistent infections of L cells with mammalian reoviruses. J Virol 67:2055–2063

    PubMed  CAS  Google Scholar 

  45. Dichter MA, Weiner HL (1984) Infection of neuronal cell cultures with reovirus mimics in vitro patterns of neurotropism. Ann Neurol 16:603–610

    Article  PubMed  CAS  Google Scholar 

  46. Dryden KA, Wang G, Yeager M, Nibert ML, Coombs KM, Furlong DB, Fields BN, Baker TS (1993) Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J Cell Biol 122:1023–1041

    Article  PubMed  CAS  Google Scholar 

  47. Dryden KA, Farsetta DL, Wang G, Keegan JM, Fields BN, Baker TS, Nibert ML (1998) Internal structures containing transcriptase-related proteins in top component particles of mammalian orthoreovirus. Virology 245:33–46

    Article  PubMed  CAS  Google Scholar 

  48. Duncan R, Lee PWK (1994) Localization of two protease-sensitive regions separating distinct domains in the reovirus cell-attachment protein sigma 1. Virology 203:149–152

    Article  PubMed  CAS  Google Scholar 

  49. Duncan R, Horne D, Strong JE, Leone G, Pon RT, Yeung MC, Lee PWK (1991) Conformational and functional analysis of the C-terminal globular head of the reovirus cell attachment protein. Virology 182:810–819

    Article  PubMed  CAS  Google Scholar 

  50. Ebert DH, Deussing J, Peters C, Dermody TS (2002) Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J Biol Chem 277:24609–24617

    Article  PubMed  CAS  Google Scholar 

  51. Ebert DH, Kopecky-Bromberg SA, Dermody TS (2004) Cathepsin B is inhibited in mutant cells selected during persistent reovirus infection. J Biol Chem 279:3837–3851

    Article  PubMed  CAS  Google Scholar 

  52. Ebert DH, Wetzel JD, Brumbaugh DE, Chance SR, Stobie LE, Baer GS, Dermody TS (2001) Adaptation of reovirus to growth in the presence of protease inhibitor E64 segregates with a mutation in the carboxy terminus of viral outer-capsid protein σ3. J Virol 75:3197–3206

    Article  PubMed  CAS  Google Scholar 

  53. Ebnet K, Schulz CU, Meyer Zu Brickwedde MK, Pendl GG, Vestweber D (2000) Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 275:27979–27988

    PubMed  CAS  Google Scholar 

  54. Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer Zu Brickwedde MK, Ohno S, Vestweber D (2001) The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J 20:3738–3748

    Article  PubMed  CAS  Google Scholar 

  55. Ebnet K, Suzuki A, Ohno S, Vestweber D (2004) Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 117:19–29

    Article  PubMed  CAS  Google Scholar 

  56. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrincoated pits. Cell 118:591–605

    Article  PubMed  CAS  Google Scholar 

  57. Estes MK, Graham DY, Mason BB (1981) Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J Virol 39:879–888

    PubMed  CAS  Google Scholar 

  58. Fleeton M, Contractor N, Leon F, Wetzel JD, Dermody TS, Kelsall B (2004) Peyer’s patch dendritic cells process viral antigen from apoptotic epithelial cells in the intestine of reovirus-infected mice. J Exp Med 200:235–245

    Article  PubMed  CAS  Google Scholar 

  59. 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

    Article  PubMed  CAS  Google Scholar 

  60. Fraser RDB, Furlong DB, Trus BL, Nibert ML, Fields BN, Steven AC (1990) Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. JVirol 64:2990–3000

    CAS  Google Scholar 

  61. 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

    PubMed  CAS  Google Scholar 

  62. Gal S, Gottesman MM (1986) The major excreted protein (MEP) of transformed mouse cells and cathepsin L have similar protease specificity. Biochem Biophys Res Commun 139:156–162

    Article  PubMed  CAS  Google Scholar 

  63. Gal S, Willingham MC, Gottesman MM (1985) Processing and lysosomal localization of a glycoprotein whose secretion is transformation stimulated. J Cell Biol 100:535–544

    Article  PubMed  CAS  Google Scholar 

  64. Gentsch JR, Pacitti AF (1985) Effect of neuraminidase treatment of cells and effect of soluble glycoproteins on type 3 reovirus attachment to murine L cells. J Virol 56:356–364

    PubMed  CAS  Google Scholar 

  65. Gentsch JR, Pacitti AF (1987) Differential interaction of reovirus type 3 with sialylated receptor components on animal cells. Virology 161:245–248

    Article  PubMed  CAS  Google Scholar 

  66. Georgi A, Mottola-Hartshorn C, Warner A, Fields B, Chen LB (1990) Detection of individual fluorescently labeled reovirions in living cells. Proc Natl Acad Sci U S A 87:6579–6583

    Article  PubMed  CAS  Google Scholar 

  67. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG (1998) Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618–1620

    Google Scholar 

  68. Golden JW, Bahe JA, Lucas WT, Nibert ML, Schiff LA (2004) Cathepsin S supports acid-independent infection by some reoviruses. J Biol Chem 279:8547–8557

    Article  PubMed  CAS  Google Scholar 

  69. Gottesman MM, Sobel ME (1980) Tumor promoters and Kirsten sarcoma virus increase synthesis of a secreted glycoprotein by regulating levels of translatable mRNA. Cell 19:449–455

    Article  PubMed  CAS  Google Scholar 

  70. Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S (2002) Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem 277:455–461

    Article  PubMed  CAS  Google Scholar 

  71. Helander A, Silvey KJ, Mantis NJ, Hutchings AB, Chandran K, Lucas WT, Nibert ML, Neutra MR (2003) The viral sigma1 protein and glycoconjugates containing alpha2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J Virol 77:7964–7977

    Article  PubMed  CAS  Google Scholar 

  72. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S (2001) Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 154:491–497

    Article  PubMed  CAS  Google Scholar 

  73. Jané-Valbuena J, Nibert ML, Spencer SM, Walker SB, Baker TS, Chen Y, Centonze VE, Schiff LA (1999) Reovirus virion-like particles obtained by recoating infectious subvirion particles with baculovirus-expressedσ3 protein: an approach for analyzing σ3 functions during virus entry. J Virol 73:2963–2973

    PubMed  Google Scholar 

  74. Jané-Valbuena J, Breun LA, Schiff LA, Nibert ML (2002) Sites and determinants of early cleavages in the proteolytic processing pathway of reovirus surface protein sigma3. J Virol 76:5184–5197

    Article  PubMed  CAS  Google Scholar 

  75. Kaye KM, Spriggs DR, Bassel-Duby R, Fields BN, Tyler KL (1986) Genetic basis for altered pathogenesis of an immune-selected antigenic variant of reovirus type 3 Dearing. J Virol 59:90–97

    PubMed  CAS  Google Scholar 

  76. Kido H, Towatari T, Niwa Y, Okumura Y, Beppu Y (1996) Cellular proteases involved in the pathogenicity of human immunodeficiency and influenza viruses. Adv Exp Med Biol 389:233–240

    PubMed  CAS  Google Scholar 

  77. Kido H, Murakami M, Oba K, Chen Y, Towatari T (1999) Cellular proteinases trigger the infectivity of the influenza A and Sendai viruses. Mol Cells 9:235–244

    PubMed  CAS  Google Scholar 

  78. Kirschke H, Langner J, Wiederanders B, Ansorge S, Bohley P (1977) Cathepsin L. A new proteinase from rat-liver lysosomes. Eur J Biochem 74:293–301

    Article  PubMed  CAS  Google Scholar 

  79. Kirschke H, Wiederanders B, Bromme D, Rinne A (1989) Cathepsin S from bovine spleen. Purification, distribution, intracellular localization and action on proteins. Biochem J 264:467–473

    PubMed  CAS  Google Scholar 

  80. Kostrewa D, Brockhaus M, D’Arcy A, Dale GE, Nelboeck P, Schmid G, Mueller F, Bazzoni G, Dejana E, Bartfai T, Winkler FK, Hennig M (2001) X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J 20:4391–4398

    Article  PubMed  CAS  Google Scholar 

  81. Kothandaraman S, Hebert MC, Raines RT, Nibert ML(1998) No role for pepstatin-A-sensitive acidic proteinases in reovirus infections of L or MDCK cells. Virology 251:264–272

    Article  PubMed  CAS  Google Scholar 

  82. Lechner F, Sahrbacher U, Suter T, Frei K, Brockhaus M, Koedel U, Fontana A(2000) Antibodies to the junctional adhesion molecule cause disruption of endothelial cells and do not prevent leukocyte influx into the meninges after viral or bacterial infection. J Infect Dis 182:978–982

    Article  PubMed  CAS  Google Scholar 

  83. Lee PW, Hayes EC, Joklik WK (1981) Protein σ1 is the reovirus cell attachment protein. Virology 108:156–163

    Article  PubMed  CAS  Google Scholar 

  84. Leone G, Duncan R, Lee PWK(1991) Trimerization of the reovirus cell attachment protein (σ1) induces conformational changes in σ1 necessary for its cell-binding function. Virology 184:758–761

    Article  PubMed  CAS  Google Scholar 

  85. Lerner AM, Cherry JD, Finland M (1963) Haemagglutination with reoviruses. Virology 19:58–65

    Article  PubMed  CAS  Google Scholar 

  86. Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC (2002) Structure of the reovirus membrane-penetration protein, μ1, in a complex with is protector protein, σ3. Cell 108:283–295

    Article  PubMed  CAS  Google Scholar 

  87. Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Ponchet M, Parkos CA (2000) Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 113:2363–2374

    PubMed  CAS  Google Scholar 

  88. Mach L, Stuwe K, Hagen A, Ballaun C, Glossl J (1992) Proteolytic processing and glycosylation of cathepsin B. The role of the primary structure of the latent precursor and of the carbohydrate moiety for cell-type-specific molecular forms of the enzyme. Biochem J 282:577–582

    PubMed  CAS  Google Scholar 

  89. Mann MA, Knipe DM, Fischbach GD, Fields BN (2002) Type 3 reovirus neuroinvasion after intramuscular inoculation: direct invasion of nerve terminals and age-dependent pathogenesis. Virology 303:222–231

    Article  PubMed  CAS  Google Scholar 

  90. Maratos-Flier E, Goodman MJ, Murray AH, Kahn CR (1986) Ammonium inhibits processing and cytotoxicity of reovirus, a nonenveloped virus. J Clin Invest 78:617–625

    Google Scholar 

  91. Martinez CG, Guinea R, Benavente J, Carrasco L (1996) The entry of reovirus into L cells is dependent on vacuolar proton-ATPase activity. J Virol 70:576–579

    PubMed  CAS  Google Scholar 

  92. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (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

    Article  PubMed  CAS  Google Scholar 

  93. Mason RW (1989) Interaction of lysosomal cysteine proteinases with alpha-2-macroglobulin: conclusive evidence for the endopeptidase activities of cathepsins B and H. Arch Biochem Biophys 273:367–374

    Article  PubMed  CAS  Google Scholar 

  94. Matlin KS, Reggio HV, Helenius A, Simons K (1982) Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91:601–613

    Article  Google Scholar 

  95. Maxfield FR (1982) Weak bases and ionophores rapidly and reversibly raise the pH in endocytic vesicles in cultured mouse fibroblasts. J Cell Biol 95:676–681

    Article  PubMed  CAS  Google Scholar 

  96. McCrae MA, Joklik WK (1978) The nature of the polypeptide encoded by each of the ten double-stranded RNA segments of reovirus type 3. Virology 89:578–593

    Article  PubMed  CAS  Google Scholar 

  97. Metcalf P, Cyrklaff M, Adrian M (1991) The 3-dimensional structure of reovirus obtained by cryoelectron microscopy. EMBO J 10:3129–3136

    PubMed  CAS  Google Scholar 

  98. Mizuochi T, Yee ST, Kasai M, Kakiuchi T, Muno D, Kominami E (1994) Both cathepsin B and cathepsin D are necessary for processing of ovalbumin as well as for degradation of class II MHC invariant chain. Immunol Let 43:189–193

    Article  CAS  Google Scholar 

  99. Morrison LA, Sidman RL, Fields BN (1991) Direct spread of reovirus from the intestinal lumen to the central nervous system through vagal autonomic nerve fibers. Proc Natl Acad Sci U S A 88:3852–3856

    Article  PubMed  CAS  Google Scholar 

  100. Mustoe TA, Ramig RF, Sharpe AH, Fields BN (1978) Genetics of reovirus: identification of the dsRNA segments encoding the polypeptides of the μ and σ size classes. Virology 89:594–604

    Article  PubMed  CAS  Google Scholar 

  101. Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos JA, Ploegh H, Peters C, Rudensky AY (1998) Cathespin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280:450–453

    Article  PubMed  CAS  Google Scholar 

  102. Nason E, Wetzel J, Mukherjee S, Barton E, Prasad B, Dermody T (2001) A monoclonal antibody specific for reovirus outer-capsid protein σ3 inhibits σ1-mediated hemagglutination by steric hindrance. J Virol 75:6625–6634

    Article  PubMed  CAS  Google Scholar 

  103. Nibert ML, Fields BN (1992) A carboxy-terminal fragment of protein μ1/μ1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66:6408–6418

    PubMed  CAS  Google Scholar 

  104. Nibert ML, Schiff LA (2001) Reoviruses and their replication. In: Knipe DM, Howley PM (eds) Fields virology, 4th edn. Lippincott Williams Wilkins, Philadelphia, pp 1679–1728

    Google Scholar 

  105. Nibert ML, Furlong DB, Fields BN (1991) Mechanisms of viral pathogenesis: distinct forms of reoviruses and their roles during replication in cells and host. J Clin Invest 88:727–734

    Article  PubMed  CAS  Google Scholar 

  106. Nibert ML, Schiff LA, Fields BN (1991) Mammalian reoviruses contain a myristoylated structural protein. J Virol 65:1960–1967

    PubMed  CAS  Google Scholar 

  107. Nibert ML, Chappell JD, Dermody TS (1995) Infectious subvirion particles of reovirus type 3 Dearing exhibit a loss in infectivity and contain a cleaved σ1 protein. J Virol 69:5057–5067

    PubMed  CAS  Google Scholar 

  108. Nibert ML, Odegard AL, Agosto MA, Chandran K, Schiff LA (2005) Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J Mol Biol 345:461–474

    Article  PubMed  CAS  Google Scholar 

  109. Oberhaus SM, Smith RL, Clayton GH, Dermody TS, Tyler KL (1997) Reovirus infection and tissue injury in the mouse central nervous system are associated with apoptosis. J Virol 71:2100–2106

    PubMed  CAS  Google Scholar 

  110. Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, Nibert ML (2004) Putative autocleavage of outer capsid protein σ1, allowing release of myristoylated peptide σ1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78:8732–8745

    Article  PubMed  CAS  Google Scholar 

  111. Ohkuma S, Poole B (1978) Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A 75:3327–3331

    Article  PubMed  CAS  Google Scholar 

  112. Olland AM, Jané-Valbuena J, Schiff LA, Nibert ML, Harrison SC (2001) Structure of the reovirus outer capsid and dsRNA-binding protein σ3 at 1.8 Å resolution. EMBO J 20:979–989

    Article  PubMed  CAS  Google Scholar 

  113. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C (2002) JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 3:151–158

    Article  PubMed  CAS  Google Scholar 

  114. Ozaki H, Ishii K, Horiuchi H, Arai H, Kawamoto T, Okawa K, Iwamatsu A, Kita T (1999) Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol 163:553–557

    PubMed  CAS  Google Scholar 

  115. Paul RW, Lee PWK (1987) Glycophorin is the reovirus receptor on human erythrocytes. Virology 159:94–101

    Article  PubMed  CAS  Google Scholar 

  116. Paul RW, Choi AH, Lee PWK (1989) The α-anomeric form of sialic acid is the minimal receptor determinant recognized by reovirus. Virology 172:382–385

    Article  PubMed  CAS  Google Scholar 

  117. Prota AE, Campbell JA, Schelling P, Forrest JC, Peters TR, Watson MJ, Aurrand-Lions M, Imhof B, Dermody TS, Stehle T (2003) Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc Natl Acad Sci U S A 100:5366–5371

    Article  PubMed  CAS  Google Scholar 

  118. Riese RJ, Wolf PR, Bromme D, Natkin LR, Villadangos JA, Ploegh HL, Chapman HA (1996) Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4:357–366

    Article  PubMed  CAS  Google Scholar 

  119. Rodgers SE, Barton ES, Oberhaus SM, Pike B, Gibson CA, Tyler KL, Dermody TS (1997) Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bcl-2. J Virol 71:2540–2546

    PubMed  CAS  Google Scholar 

  120. Rosen L (1960) Serologic grouping of reovirus by hemagglutination-inhibition. Am J Hyg 71:242–249

    PubMed  CAS  Google Scholar 

  121. Rowan AD, Mason P, Mach L, Mort JS (1992) Rat procathepsin B. Proteolytic processing to the mature form in vitro. J Biol Chem 267:15993–15999

    PubMed  CAS  Google Scholar 

  122. Rubin DH, Weiner DB, Dworkin C, Greene MI, Maul GG, Williams WV (1992) Receptor utilization by reovirus type 3: distinct binding sites on thymoma and fibroblast cell lines result in differential compartmentalization of virions. Microb Pathog 12:351–365

    Article  PubMed  CAS  Google Scholar 

  123. Rubin DH, Wetzel JD, Williams WV, Cohen JA, Dworkin C, Dermody TS (1992) Binding of type 3 reovirus by a domain of the σ1 protein important for hemagglutination leads to infection of murine erythroleukemia cells. J Clin Invest 90:2536–2542

    PubMed  CAS  Google Scholar 

  124. Rust MJ, Lakadamyali M, Zhang F, Zhuang X (2004) Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11:567–573

    Article  PubMed  CAS  Google Scholar 

  125. Ryan RE, Sloane BF, Sameni M, Wood PL (1995) Microglial cathepsin B: an immunological examination of cellular and secreted species. J Neurochem 65:1035–1045

    Article  PubMed  CAS  Google Scholar 

  126. Sabin AB (1959) Reoviruses: a new group of respiratory and enteric viruses formerly classified as ECHO type 10 is described. Science 130:1387–1389

    Article  PubMed  CAS  Google Scholar 

  127. Sagik B, Puck T, Levine S (1954) Quantitative aspects of the spontaneous elution of influenza virus from red cells. J Exp Med 99:251–260

    Article  PubMed  CAS  Google Scholar 

  128. Salminen A, Gottesman MM (1990) Inhibitor studies indicate that active cathepsin L is probably essential to its own processing in cultured fibroblasts. Biochem J 272:39–44

    PubMed  CAS  Google Scholar 

  129. Sieczkarski SB, Whittaker GR (2002) Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 76:10455–10464

    Article  PubMed  CAS  Google Scholar 

  130. Smith RE, Zweerink HJ, Joklik WK (1969) Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39:791–810

    Article  PubMed  CAS  Google Scholar 

  131. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH, Crompton A, Chan AC, Anderson JM, Cantley LC (1997) Recognition of unique carboxylterminal motifs by distinct PDZ domains. Science 275:73–77

    Article  PubMed  CAS  Google Scholar 

  132. Spear PG (2002) Viral interactions with receptors in cell junctions and effects on junctional stability. Dev Cell 3:462–464

    Article  PubMed  CAS  Google Scholar 

  133. Spriggs DR, Fields BN (1982) Attenuated reovirus type 3 strains generated by selection of haemagglutinin antigenic variants. Nature 297:68–70

    Article  PubMed  CAS  Google Scholar 

  134. Spriggs DR, Bronson RT, Fields BN (1983) Hemagglutinin variants of reovirus type 3 have altered central nervous system tropism. Science 220:505–507

    Article  PubMed  CAS  Google Scholar 

  135. 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

    Article  PubMed  CAS  Google Scholar 

  136. Stehle T, Dermody TS (2004) Structural similarities in the cellular receptors used by adenovirus and reovirus. Viral Immunol 17:129–143

    Article  PubMed  CAS  Google Scholar 

  137. Stiasny K, Allison SL, Marchler-Bauer A, Kunz C, Heinz FX (1996) Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. J Virol 70:8142–8147

    PubMed  CAS  Google Scholar 

  138. Strong JE, Leone G, Duncan R, Sharma RK, Lee PW (1991) Biochemical and biophysical characterization of the reovirus cell attachment protein sigma 1: evidence that it is a homotrimer. Virology 184:23–32

    Article  PubMed  CAS  Google Scholar 

  139. Sturzenbecker LJ, Nibert ML, Furlong DB, Fields BN (1987) Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J Virol 61:2351–2361

    PubMed  CAS  Google Scholar 

  140. Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K, Satoh A, Nishioka H, Aoki J, Nomoto A, Mizoguchi A, Takai Y (1999) Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol 145:539–549

    Article  PubMed  CAS  Google Scholar 

  141. Tardieu M, Weiner HL (1982) Viral receptors on isolated murine and human ependymal cells. Science 215:419–421

    Article  PubMed  CAS  Google Scholar 

  142. Tardieu M, Powers ML, Weiner HL (1983) Age-dependent susceptibility to reovirus type 3 encephalitis: role of viral and host factors. Ann Neurol 13:602–607

    Article  PubMed  CAS  Google Scholar 

  143. Tosteson MT, Nibert ML, Fields BN (1993) Ion channels induced in lipid bilayers by subvirion particles of the nonenveloped mammalian reoviruses. Proc Natl Acad Sci U S A 90:10549–10552

    Article  PubMed  CAS  Google Scholar 

  144. Tsukita S, Furuse M, Itoh M (1999) Structural and signalling molecules come together at tight junctions. Curr Opin Cell Biol 11:628–633

    Article  PubMed  CAS  Google Scholar 

  145. Turner DL, Duncan R, Lee PW (1992) Site-directed mutagenesis of the C-terminal portion of reovirus protein σ1: evidence for a conformation-dependent receptor binding domain. Virology 186:219–227

    Article  PubMed  CAS  Google Scholar 

  146. Tyler KL (2001) Mammalian reoviruses. In: Knipe DM, Howley PM (eds) Fields virology, 4th edn. Lippincott Williams Wilkins, Philadelphia, pp 1729–1945

    Google Scholar 

  147. Tyler KL, McPhee DA, Fields BN (1986) Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science 233:770–774

    Article  PubMed  CAS  Google Scholar 

  148. Tyler KL, Squier MK, Rodgers SE, Schneider SE, Oberhaus SM, Grdina TA, Cohen JJ, Dermody TS (1995) Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein σ1. J Virol 69:6972–6979

    PubMed  CAS  Google Scholar 

  149. Ullmer C, Schmuck K, Figge A, Lubbert H (1998) Cloning and characterization of MUPP1, a novel PDZ domain protein. FEBS Lett 424:63–68

    Article  PubMed  CAS  Google Scholar 

  150. 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

    Article  PubMed  CAS  Google Scholar 

  151. Virgin HW, Tyler KL, Dermody TS (1997) Reovirus. In: Nathanson N (ed) Viral pathogenesis. Lippincott-Raven, New York, pp 669–699

    Google Scholar 

  152. Warner MS, Geraghty RJ, Martinez WM, Montgomery RI, Whitbeck JC, Xu R, Eisenberg RJ, Cohen GH, Spear PG (1998) A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179–189

    Article  PubMed  CAS  Google Scholar 

  153. Weiner HL, Drayna D, Averill DR Jr, Fields BN (1977) Molecular basis of reovirus virulence: role of the S1 gene. Proc Natl Acad Sci U S A 74:5744–5748

    Article  PubMed  CAS  Google Scholar 

  154. Weiner HL, Ault KA, Fields BN (1980) Interaction of reovirus with cell surface receptors. I. Murine and human lymphocytes have a receptor for the hemagglutinin of reovirus type 3. J Immunol 124:2143–2148

    PubMed  CAS  Google Scholar 

  155. Weiner HL, Powers ML, Fields BN (1980) Absolute linkage of virulence and central nervous system tropism of reoviruses to viral hemagglutinin. J InfectDis 141:609–616

    CAS  Google Scholar 

  156. Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, Wiley DC (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333:426–431

    Article  PubMed  CAS  Google Scholar 

  157. Wetzel JD, Wilson GJ, Baer GS, Dunnigan LR, Wright JP, Tang DSH, Dermody TS (1997) Reovirus variants selected during persistent infections of L cells contain mutations in the viral S1 and S4 genes and are altered in viral disassembly. J Virol 71:1362–1369

    PubMed  CAS  Google Scholar 

  158. 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

    Article  PubMed  CAS  Google Scholar 

  159. Wilson GJ, Wetzel JD, Puryear W, Bassel-Duby R, Dermody TS (1996) Persistent reovirus infections of L cells select mutations in viral attachment protein σ1 that alter oligomer stability. J Virol 70:6598–6606

    PubMed  CAS  Google Scholar 

  160. Wilson GJ, Nason EL, Hardy CS, Ebert DH, Wetzel JD, Prasad BVV, Dermody TS (2002) A single mutation in the carboxy terminus of reovirus outer-capsid protein σ3 confers enhanced kinetics of σ3 proteolysis, resistance to inhibitors of viral disassembly, and alterations in σ3 structure. J Virol 76:9832–9843

    Article  PubMed  CAS  Google Scholar 

  161. Wilson JH, Luftig RB, Wood WB (1970) Interaction of bacteriophage T4 tail fiber components with a lipopolysaccharide fraction from Escherichia coli. J Mol Biol 51:423–434

    Article  PubMed  CAS  Google Scholar 

  162. Wolf JL, Rubin DH, Finberg R, Kaufman RS, Sharpe AH, Trier JS, Fields BN(1981) Intestinal M cells: a pathway of entry of reovirus into the host. Science 212:471–472

    Article  PubMed  CAS  Google Scholar 

  163. Yoon M, Spear PG (2002) Disruption of adherens junctions liberates nectin-1 to serve as receptor for herpes simplex virus and pseudorabies virus entry. J Virol 76:7203–7208

    Article  PubMed  CAS  Google Scholar 

  164. Zahraoui A, Louvard D, Galli T (2000) Tight junction, a platform for trafficking and signaling protein complexes. J Cell Biol 151:F31–F36

    Article  PubMed  CAS  Google Scholar 

  165. Campbell JA, Schelling P, Wetzel JD, Johnson EM, Forrest JC, Wilson GA, Aurrand-Lions M, Imhof BA, Stehle T, Dermody TS (2005) Junctional adhesion molecule a serves as a receptor for prototype and field-isolate strains of mammalian reovirus. J Virol 79:7967–778

    Article  PubMed  CAS  Google Scholar 

  166. Clark KM, Wetzel JD, Gu Y, Ebert DH, McAbee SA, Stoneman EK, Baer GS, Zhu Y, Wilson GJ, Prasad BVV, Dermody TS (2006) Reovirus variants selected for resistance to ammonium chloride have mutations in viral outer capsid protein σ3. J Virol 80:671–681

    Article  PubMed  CAS  Google Scholar 

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Guglielmi, K.M., Johnson, E.M., Stehle, T., Dermody, T.S. (2006). Attachment and Cell Entry of Mammalian Orthoreovirus. In: Roy, P. (eds) Reoviruses: Entry, Assembly and Morphogenesis. Current Topics in Microbiology and Immunology, vol 309. Springer, Berlin, Heidelberg . https://doi.org/10.1007/3-540-30773-7_1

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