Diminished Reovirus Capsid Stability Alters Disease Pathogenesis and Littermate Transmission

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages

  Doyle, Joshua D ^a   Stencel Baerenwald, Jennifer E ^a   Copeland, Courtney A ^a   Rhoads, Jillian P ^a   Brown, Judy J ^a   Boyd, Kelli L ^a   Atkinson, James B ^a   Dermody, Terence S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; CAPSID PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DYSKINESIA; FLACCID PARALYSIS; HEAT TOLERANCE; HISTOLOGY; LETHALITY; LUCIFERASE ASSAY; METASTASIS; MOUSE; MUTATION; NEWBORN; NONHUMAN; PLAQUE ASSAY; REOVIRIDAE; SEIZURE; TENDON REFLEX; VIRUS CAPSID; VIRUS LOAD; VIRUS MYOCARDITIS; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; GENETICS; MAMMALIAN ORTHOREOVIRUS; METABOLISM; VIRION; VIRUS ASSEMBLY;

ANIMALIA; MAMMALIA; MIRIDAE; MUS; ORTHOREOVIRUS;

ANIMALS; CAPSID; CAPSID PROTEINS; MICE; MUTATION; ORTHOREOVIRUS, MAMMALIAN; VIRION; VIRUS ASSEMBLY;

EID: 84926442797     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004693     Document Type: Article

References (88)

1. Stein BS, Engleman EG, (1991) Mechanism of HIV-1 entry into CD4+ T cells. Adv Exp Med Biol 300: 71–86; discussion 87–96. 1685857
2. Stein BS, Gowda SD, Lifson JD, Penhallow RC, Bensch KG, et al. (1987) pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 49: 659–668. 3107838
3. Wahlberg JM, Bron R, Wischut J, Garoff H, (1992) Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J Virol 66: 7309–7318. 1433520
4. Gibbons DL, Vaney MC, Roussel A, Vigouroux A, Reilly B, et al. (2004) Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427: 320–325. 14737160
5. Glomb-Reinmund S, Kielian M, (1998) The role of low pH and disulfide shuffling in the entry and fusion of Semliki Forest virus and Sindbis virus. Virology 248: 372–381. 9721245
6. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM, (2005) Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308: 1643–1645. 15831716
7. Takada A, Robison C, Goto H, Sanchez A, Murti KG, et al. (1997) A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A 94: 14764–14769. 9405687
8. Wilson IA, Skehel JJ, Wiley DC, (1981) Structure of the hemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289: 366–373. 7464906
9. Bullough PA, Hughson FM, Skehel JJ, Wiley DC, (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37–43. 8072525
10. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS, (2005) Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci USA 102: 9288–9293. 15964978
11. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA, (2006) Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc Natl Acad Sci U S A 103: 17903–17908. 17093041
12. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS, (2006) Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439: 38–44. 16397490
13. Colston EM, Racaniello VR, (1995) Poliovirus variants selected on mutant receptor-expressing cells identify capsid residues that expand receptor recognition. J Virol 69: 4823–4829. 7609049
14. Belnap DM, Filman DJ, Trus BL, Cheng N, Booy FP, et al. (2000) Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J Virol 74: 1342–1354. 10627545
15. Fricks CE, Hogle JM, (1990) Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol 64: 1934–1945. 2157861
16. Tosteson MT, Chow M, (1997) Characterization of the ion channels formed by poliovirus in planar lipid membranes. J Virol 71: 507–511. 8985378
17. 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. 9036860
18. Louis N, Fender P, Barge A, Kitts P, Chroboczek J, (1994) Cell-binding domain of adenovirus serotype 2 fiber. J Virol 68: 4104–4106. 8189552
19. Lonberg-Holm K, Lonberg-Holm K, Philipson L, (1981) Attachment of animal viruses to cells: An introduction. In: Virus Receptors. London: Chapman & Hall. pp. 3–20.
20. Greber UF, Willetts M, Webster P, Helenius A, (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75: 477–486. 8221887
21. Greber UF, Webster P, Weber JM, Helenius A, (1996) The role of the adenovirus protease on virus entry into cells. EMBO 15: 1766–1777. 8617221
22. Rosen L, (1962) Reoviruses in animals other than man. Annals of the New York Academy of Science 101: 461–465. 13974842
23. Scott FW, Kahn DE, Gillespie JH, (1970) Feline reovirus: isolation, characterization, and pathogenicity of a feline reovirus. Am J Vet Res 31: 11–20. 4313157
24. Cox P, Griffith M, Angles M, Deere D, Ferguson C, (2005) Concentrations of pathogens and indicators in animal feces in the Sydney watershed. Appl Environ Microbiol 71: 5929–5934. 16204506
25. Wolf JL, Rubin DH, Finberg R, Kaufman RS, Sharpe AH, et al. (1981) Intestinal M cells: a pathway of entry of reovirus into the host. Science 212: 471–472. 6259737
26. Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M, et al. (2014) Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J Virol 88: 6934–6943. doi: 10.1128/JVI.00204-14 24696493
27. Antar AAR, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, et al. (2009) Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5: 59–71. doi: 10.1016/j.chom.2008.12.001 19154988
28. Boehme KW, Guglielmi KM, Dermody TS, (2009) Reovirus nonstructural protein s1s is required for establishment of viremia and systemic dissemination. Proc Natl Acad Sci USA 106: 19986–19991. doi: 10.1073/pnas.0907412106 19897716
29. Weiner HL, Drayna D, Averill DR, JrFields BN, (1977) Molecular basis of reovirus virulence: role of the S1 gene. Proc Natl Acad of Sci USA 74: 5744–5748. 271999
30. 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 of Sci USA 88: 3852–3856. 1850838
31. 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. 3016895
32. Barton ES, Youree BE, Ebert DH, Forrest JC, Connolly JL, et al. (2003) Utilization of sialic acid as a coreceptor is required for reovirus-induced biliary disease. J Clin Invest 111: 1823–1833. 12813018
33. Tyler KL, Sokol RJ, Oberhaus SM, Le M, Karrer FM, et al. (1998) Detection of reovirus RNA in hepatobiliary tissues from patients with extrahepatic biliary atresia and choledochal cysts. Hepatology 27: 1475–1482. 9620316
34. Glaser JH, Balistreri WF, Morecki R, (1984) Role of reovirus type 3 in persistent infantile cholestasis. J Pediatr 15: 912–915.
35. Morecki R, Glaser JH, Cho S, Balistreri WF, Horwitz MS, (1982) Biliary atresia and reovirus type 3 infection. N Engl J Med 307: 481–484. 6285193
36. Richardson SC, Bishop RF, Smith AL, (1994) Reovirus serotype 3 infection in infants with extrahepatic biliary atresia or neonatal hepatitis. J Gastroenterol Hepatol 9: 264–268. 8054525
37. Coffey MC, Strong JE, Forsyth PA, Lee PW, (1998) Reovirus therapy of tumors with activated Ras pathway. Science 282: 1332–1334. 9812900
38. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW, (2004) Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc Natl Acad Sci USA 101: 11099–11104. 15263068
39. Hashiro G, Loh PC, Yau JT, (1977) The preferential cytotoxicity of reovirus for certain transformed cell lines. Arch Virol 54: 307–315. 562142
40. Lerner AM, Cherry JD, Finland M, (1963) Haemagglutination with reoviruses. Virology 19: 58–65. 13929839
41. Dermody TS, Nibert ML, Bassel-Duby R, Fields BN, (1990) A s1 region important for hemagglutination by serotype 3 reovirus strains. J Virol 64: 5173–5176. 2398540
42. 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. 11239401
43. Chappell JD, Prota A, Dermody TS, Stehle T, (2002) Crystal structure of reovirus attachment protein s1 reveals evolutionary relationship to adenovirus fiber. EMBO Journal 21: 1–11. 11782420
44. Kirchner E, Guglielmi KM, Strauss HM, Dermody TS, Stehle T, (2008) Structure of reovirus s1 in complex with its receptor junctional adhesion molecule-A. PLoS Pathog 4: e1000235. doi: 10.1371/journal.ppat.1000235 19079583
45. 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. 17452315
46. Maginnis MS, Forrest JC, Kopecky-Bromberg SA, Dickeson SK, Santoro SA, et al. (2006) b1 integrin mediates internalization of mammalian reovirus. J Virol 80: 2760–2770. 16501085
47. Mainou BA, Dermody TS, (2012) Transport to late endosomes is required for efficient reovirus infection. J Virol 86: 8346–8358. doi: 10.1128/JVI.00100-12 22674975
48. Mohamed MM, Sloane BF, (2006) Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev: Cancer 6: 764–775. 16990854
49. 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. 11986312
50. Nibert ML, Fields BN, (1992) A carboxy-terminal fragment of protein m1/m1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66: 6408–6418. 1328674
51. Chandran K, Parker JS, Ehrlich M, Kirchhausen T, Nibert ML, (2003) The delta region of outer-capsid protein m1 undergoes conformational change and release from reovirus particles during cell entry. J Virol 77: 13361–13375. 14645591
52. Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, et al. (2004) Putative autocleavage of outer capsid protein m1, allowing release of myristoylated peptide m1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78: 8732–8745. 15280481
53. Nibert ML, Odegard AL, Agosto MA, Chandran K, Schiff LA, (2005) Putative autocleavage of reovirus m1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J Mol Biol 345: 461–474. 15581891
54. Chandran K, and Max L. Nibert. In Vitro Membrane Permeabilization by Mammalian Reovirus ISVPs is Accompanied by Dramatic Changes in Particle Structure and Enzymatic Activities; 2001; Madison, WI.
55. Baer GS, Dermody TS, (1997) Mutations in reovirus outer-capsid protein s3 selected during persistent infections of L cells confer resistance to protease inhibitor E64. J Virol 71: 4921–4928. 9188554
56. Wetzel JD, Wilson GJ, Baer GS, Dunnigan LR, Wright JP, et al. (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. 8995660
57. Ebert DH, Wetzel JD, Brumbaugh DE, Chance SR, Stobie LE, et al. (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 s3. J Virol 75: 3197–3206. 11238846
58. Clark KM, Wetzel JD, Gu Y, Ebert DH, McAbee SA, et al. (2006) Reovirus variants selected for resistance to ammonium chloride have mutations in viral outer-capsid protein s3. J Virol 80: 671–681. 16378970
59. Kobayashi T, Antar AAR, Boehme KW, Danthi P, Eby EA, et al. (2007) A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1: 147–157. 18005692
60. Doyle JD, Danthi P, Kendall EA, Ooms LS, Wetzel JD, et al. (2012) Molecular determinants of proteolytic disassembly of the reovirus outer capsid. J Biol Chem 287: 8029–8038. doi: 10.1074/jbc.M111.334854 22253447
61. Kedl R, Schmechel S, Schiff L, (1995) Comparative sequence analysis of the reovirus S4 genes from 13 serotype 1 and serotype 3 field isolates. J Virol 69: 552–559. 7527088
62. Weiner HL, Powers ML, Fields BN, (1980) Absolute linkage of virulence and central nervous system tropism of reoviruses to viral hemagglutinin. J Infect Dis 141: 609–616. 6989930
63. Goody RJ, Schittone SA, Tyler KL, (2008) Experimental reovirus-induced acute flaccid paralysis and spinal motor neuron cell death. J Neuropathol Exp Neuro 67: 231–239. doi: 10.1097/NEN.0b013e31816564f0 18344914
64. Bodkin DK, Fields BN, (1989) Growth and survival of reovirus in intestinal tissue: role of the L2 and S1 genes. J Virol 63: 1188–1193. 2915380
65. Keroack M, Fields BN, (1986) Viral shedding and transmission between hosts determined by reovirus L2 gene. Science 232: 1635–1638. 3012780
66. Nibert ML, Chappell JD, Dermody TS, (1995) Infectious subvirion particles of reovirus type 3 Dearing exhibit a loss in infectivity and contain a cleaved s1 protein. J Virol 69: 5057–5067. 7609075
67. Chappell JD, Barton ES, Smith TH, Baer GS, Duong DT, et al. (1998) Cleavage susceptibility of reovirus attachment protein s1 during proteolytic disassembly of virions is determined by a sequence polymorphism in the s1 neck. J Virol 72: 8205–8213. 9733863
68. Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC, (2002) Structure of the reovirus membrane-penetration protein, m1, in a complex with its protector protein, s3. Cell 108: 283–295. 11832217
69. Bokiej M, Ogden KM, Ikizler M, Reiter DM, Stehle T, et al. (2012) Optimum length and flexibility of reovirus attachment protein s1 are required for efficient viral infection. J Virol 86: 10270–10280. doi: 10.1128/JVI.01338-12 22811534
70. Sherry B, Schoen FJ, Wenske E, Fields BN, (1989) Derivation and characterization of an efficiently myocarditic reovirus variant. J Virol 63: 4840–4849. 2552157
71. Sherry B, Li XY, Tyler KL, Cullen JM, Virgin HW, (1993) Lymphocytes protect against and are not required for reovirus-induced myocarditis. J Virol 67: 6119–6124. 8396673
72. Sherry B, Baty CJ, Blum MA, (1996) Reovirus-induced acute myocarditis in mice correlates with viral RNA synthesis rather than generation of infectious virus in cardiac myocytes. J Virol 70: 6709–6715. 8794307
73. Sherry B, Fields BN, (1989) The reovirus M1 gene, encoding a viral core protein, is associated with the myocarditic phenotype of a reovirus variant. J Virol 63: 4850–4856. 2552158
74. Lu HH, Yang CF, Murdin AD, Klein MH, Harber JJ, et al. (1994) Mouse neurovirulence determinants of poliovirus type 1 strain LS-a map to the coding regions of capsid protein VP1 and proteinase 2Apro. J Virol 68: 7507–7515. 7933134
75. 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. 7233831
76. 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. 2885424
77. Wilson GJ, Nason EL, Hardy CS, Ebert DH, Wetzel JD, et al. (2002) A single mutation in the carboxy terminus of reovirus outer-capsid protein s3 confers enhanced kinetics of s3 proteolysis, resistance to inhibitors of viral disassembly, and alterations in s3 structure. J Virol 76: 9832–9843. 12208961
78. Boehme KW, Frierson JM, Konopka JL, Kobayashi T, Dermody TS, (2011) The reovirus s1s protein is a determinant of hematogenous but not neural virus dissemination in mice. J Virol 85: 11781–11790. doi: 10.1128/JVI.02289-10 21917967
79. Holm GH, Pruijssers AJ, Li L, Danthi P, Sherry B, et al. (2010) Interferon regulatory factor 3 attenuates reovirus myocarditis and contributes to viral clearance. J Virol 84: 6900–6908. doi: 10.1128/JVI.01742-09 20463082
80. Frierson JM, Pruijssers AJ, Konopka JL, Reiter DM, Abel TW, et al. (2012) Utilization of sialylated glycans as coreceptors enhances the neurovirulence of serotype 3 reovirus. J Virol 86: 13164–13173. doi: 10.1128/JVI.01822-12 23035227
81. Sherry B, Torres J, Blum MA, (1998) Reovirus induction of and sensitivity to beta interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J Virol 72: 1314–1323. 9445032
82. Tai JH, Williams JV, Edwards KM, Wright PF, Crowe JE, et al. (2005) Prevalence of reovirus-specific antibodies in young children in Nashville, Tennessee. J Infect Dis191: 1221–1224.
83. Kobayashi T, Ooms LS, Ikizler M, Chappell JD, Dermody TS, (2010) An improved reverse genetics system for mammalian orthoreoviruses. Virology 2: 194–200.
84. Tyler KL, Bronson RT, Byers KB, Fields BN, (1985) Molecular basis of viral neurotropism: experimental reovirus infection. Neurology 35: 88–92. 2981418
85. Virgin HW, IVBassel-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. 2460637
86. Wetzel JD, Chappell JD, Fogo AB, Dermody TS, (1997) Efficiency of viral entry determines the capacity of murine erythroleukemia cells to support persistent infections by mammalian reoviruses. J Virol 71: 299–306. 8985350
87. Holm GH, Zurney J, Tumilasci V, Danthi P, Hiscott J, et al. (2007) Retinoic acid-inducible gene-I and interferon-b promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J Biol Chem 282: 21953–21961. 17540767
88. Richardson BA, Overbaugh J, (2005) Basic statistical considerations in virological experiments. J Virol 79: 669–676. 15613294