Bacteria and bacterial envelope components enhance mammalian reovirus thermostability

PLoS Pathogens

Volumn 13, Issue 12, 2017, Pages

  Berger, Angela K ^a,b   Yi, Hong ^c   Kearns, Daniel B ^d   Mainou, Bernardo A ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

^c EMORY UNIVERSITY   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CHITIN; CHYMOTRYPSIN A; PHOSPHOTUNGSTIC ACID; ENDOTOXIN; ESCHERICHIA COLI ENDOTOXIN; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; N ACETYLGLUCOSAMINE; PEPTIDOGLYCAN; PHOTOPROTEIN; RECOMBINANT PROTEIN; RED FLUORESCENT PROTEIN; RNA; RNA, RECOMBINANT; TEICHOIC ACID;

AMYE GENE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL MEMBRANE; CELL CULTURE; COLON ADENOCARCINOMA; COLONY FORMING UNIT; CONFOCAL MICROSCOPY; ENDOCYTOSIS; ENVIRONMENTAL FACTOR; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GEL ELECTROPHORESIS; GENE LOCUS; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MAMMALIAN ORTHOREOVIRUS; MEMBRANE COMPONENT; NONHUMAN; POLIOMYELITIS VIRUS; PROTEIN EXPRESSION; TEMPERATURE STRESS; THERMOSTABILITY; TRANSMISSION ELECTRON MICROSCOPY; VIRION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; VIRUS RECOMBINANT; ANALOGS AND DERIVATIVES; CACO-2 CELL LINE; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECTS; ESCHERICHIA COLI K 12; GENETICS; HEAT; HELA CELL LINE; INTESTINE CELL; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; REOVIRIDAE; REOVIRUS INFECTION; RNA STABILITY; ULTRASTRUCTURE; VIROLOGY; VIRUS ATTACHMENT; VIRUS ENTRY;

ACETYLGLUCOSAMINE; BACILLUS SUBTILIS; CACO-2 CELLS; ENDOTOXINS; ENTEROCYTES; ESCHERICHIA COLI K12; GASTROINTESTINAL MICROBIOME; HELA CELLS; HOT TEMPERATURE; HUMANS; LIPOPOLYSACCHARIDES; LUMINESCENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDOGLYCAN; RECOMBINANT PROTEINS; REOVIRIDAE; REOVIRIDAE INFECTIONS; RNA; RNA STABILITY; TEICHOIC ACIDS; VIRION; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 85039904379     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006768     Document Type: Article

References (84)

1. Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR, The Evolution of Stomach Acidity and Its Relevance to the Human Microbiome. PloS one. 2015;10(7):e0134116. Epub 2015/07/30. doi: 10.1371/journal.pone.0134116 26222383.
2. Donaldson GP, Lee SM, Mazmanian SK, Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14(1):20–32. Epub 2015/10/27. doi: 10.1038/nrmicro3552 26499895.
3. Tropini C, Earle KA, Huang KC, Sonnenburg JL, The Gut Microbiome: Connecting Spatial Organization to Function. Cell host & microbe. 2017;21(4):433–42. Epub 2017/04/14. doi: 10.1016/j.chom.2017.03.010 28407481.
4. Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M, Yagita H, et al. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J Virol. 2014;88(12):6934–43. doi: 10.1128/JVI.00204-14 24696493.
5. Dermody TS, Parker J, Sherry B, Knipe DM, Howley PM, Orthoreoviruses. In: Fields Virology. 2. Sixth ed. Philadelphia: Lippincott Williams & Wilkins; 2013. p. 1304–46.
6. Greenberg HB, Estes MK, Rotaviruses: from pathogenesis to vaccination. Gastroenterology. 2009;136(6):1939–51. doi: 10.1053/j.gastro.2009.02.076 19457420.
7. Maclachlan NJ, Bluetongue: history, global epidemiology, and pathogenesis. Prev Vet Med. 2011;102(2):107–11. doi: 10.1016/j.prevetmed.2011.04.005 21570141.
8. Ouattara LA, Barin F, Barthez MA, Bonnaud B, Roingeard P, Goudeau A, et al. Novel human reovirus isolated from children with acute necrotizing encephalopathy. Emerging infectious diseases. 2011;17(8):1436–44. Epub 2011/08/02. doi: 10.3201/eid1708.101528 21801621.
9. Tai JH, Williams JV, Edwards KM, Wright PF, Crowe JE, Jr.Dermody TS, Prevalence of reovirus-specific antibodies in young children in Nashville, Tennessee. The Journal of infectious diseases. 2005;191(8):1221–4. Epub 2005/03/19. doi: 10.1086/428911 15776366.
10. Rosen L, Serologic grouping of reoviruses by hemagglutination-inhibition. Am J Hyg. 1960;71:242–9. 14438891.
11. Sabin AB, Reoviruses. A new group of respiratory and enteric viruses formerly classified as ECHO type 10 is described. Science New York, NY. 1959;130(3386):1387–9. 14440555.
12. Bouziat R, Hinterleitner R, Brown JJ, Stencel-Baerenwald JE, Ikizler M, Mayassi T, et al. Reovirus infection triggers inflammatory responses to dietary antigens and development of celiac disease. Science New York, NY. 2017;356(6333):44–50. doi: 10.1126/science.aah5298 28386004.
13. Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, Carter BD, et al. Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell host & microbe. 2009;5(1):59–71. doi: 10.1016/j.chom.2008.12.001 19154988.
14. Boehme KW, Guglielmi KM, Dermody TS, Reovirus nonstructural protein sigma1s is required for establishment of viremia and systemic dissemination. Proc Natl Acad Sci U S A. 2009;106(47):19986–91. Epub 2009/11/10. doi: 10.1073/pnas.0907412106 19897716.
15. Rubin DH, Eaton MA, Anderson AO, Reovirus infection in adult mice: the virus hemagglutinin determines the site of intestinal disease. Microb Pathog. 1986;1(1):79–87. Epub 1986/02/01. 2854595.
16. Amerongen HM, Wilson GA, Fields BN, Neutra MR, Proteolytic processing of reovirus is required for adherence to intestinal M cells. J Virol. 1994;68(12):8428–32. 7525989.
17. Boehme KW, Lai CM, Dermody TS, Mechanisms of reovirus bloodstream dissemination. Adv Virus Res. 2013;87:1–35. doi: 10.1016/B978-0-12-407698-3.00001-6 23809919.
18. Tyler KL, McPhee DA, Fields BN, Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science New York, NY. 1986;233(4765):770–4. Epub 1986/08/15. 3016895.
19. Rubin DH, Kornstein MJ, Anderson AO, Reovirus serotype 1 intestinal infection: a novel replicative cycle with ileal disease. J Virol. 1985;53(2):391–8. 2982027.
20. Barton ES, Connolly JL, Forrest JC, Chappell JD, Dermody TS, Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem. 2001;276(3):2200–11. Epub 2000/10/31. doi: 10.1074/jbc.M004680200 11054410.
21. Reiss K, Stencel JE, Liu Y, Blaum BS, Reiter DM, Feizi T, et al. The GM2 glycan serves as a functional coreceptor for serotype 1 reovirus. PLoS pathogens. 2012;8(12):e1003078. Epub 2012/12/14. doi: 10.1371/journal.ppat.1003078 23236285.
22. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, Schnell FJ, et al. Junction adhesion molecule is a receptor for reovirus. Cell. 2001;104(3):441–51. Epub 2001/03/10. S0092-8674(01)00231-8 [pii]. 11239401.
23. Campbell JA, Schelling P, Wetzel JD, Johnson EM, Forrest JC, Wilson GAR, et al. Junctional adhesion molecule a serves as a receptor for prototype and field-isolate strains of mammalian reovirus. Journal of virology. 2005;79(13):7967–78. doi: 10.1128/JVI.79.13.7967-7978.2005 15956543
24. Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS, Structure-function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment. J Biol Chem. 2003;278(48):48434–44. doi: 10.1074/jbc.M305649200 12966102.
25. Konopka-Anstadt JL, Mainou BA, Sutherland DM, Sekine Y, Strittmatter SM, Dermody TS, The Nogo receptor NgR1 mediates infection by mammalian reovirus. Cell host & microbe. 2014;15(6):681–91. doi: 10.1016/j.chom.2014.05.010 24922571.
26. Boulant S, Stanifer M, Kural C, Cureton DK, Massol R, Nibert ML, et al. Similar uptake but different trafficking and escape routes of reovirus virions and infectious subvirion particles imaged in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2013;24(8):1196–207. Epub 2013/02/22. doi: 10.1091/mbc.E12-12-0852 23427267.
27. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell. 2004;118(5):591–605. doi: 10.1016/j.cell.2004.08.017 15339664.
28. Maginnis MS, Forrest JC, Kopecky-Bromberg SA, Dickeson SK, Santoro SA, Zutter MM, et al. Beta1 integrin mediates internalization of mammalian reovirus. J Virol. 2006;80(6):2760–70. doi: 10.1128/JVI.80.6.2760-2770.2006 16501085.
29. Maginnis MS, Mainou BA, Derdowski A, Johnson EM, Zent R, Dermody TS, NPXY motifs in the beta1 integrin cytoplasmic tail are required for functional reovirus entry. J Virol. 2008;82(7):3181–91. doi: 10.1128/JVI.01612-07 18216114.
30. Mainou BA, Dermody TS, Transport to late endosomes is required for efficient reovirus infection. J Virol. 2012;86(16):8346–58. Epub 2012/06/08. doi: 10.1128/JVI.00100-12 22674975.
31. Mainou BA, Zamora PF, Ashbrook AW, Dorset DC, Kim KS, Dermody TS, Reovirus cell entry requires functional microtubules. mBio. 2013;4(4). Epub 2013/07/04. doi: 10.1128/mBio.00405-13 23820395.
32. Schulz WL, Haj AK, Schiff LA, Reovirus uses multiple endocytic pathways for cell entry. J Virol. 2012;86(23):12665–75. Epub 2012/09/14. doi: 10.1128/JVI.01861-12 22973022.
33. Baer GS, Dermody TS, Mutations in reovirus outer-capsid protein sigma3 selected during persistent infections of L cells confer resistance to protease inhibitor E64. J Virol. 1997;71(7):4921–8. Epub 1997/07/01. 9188554.
34. Ebert DH, Deussing J, Peters C, Dermody TS, Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J Biol Chem. 2002;277(27):24609–17. doi: 10.1074/jbc.M201107200 11986312.
35. Sturzenbecker LJ, Nibert M, Furlong D, Fields BN, Intracellular Digestion of Reovirus Particles Requires a Low Ph and Is an Essential Step in the Viral Infectious Cycle. Journal of virology. 1987;61(8):2351–61. WOS:A1987J239200001. 2885424
36. Maratos-Flier E, Goodman MJ, Murray AH, Kahn CR, Ammonium inhibits processing and cytotoxicity of reovirus, a nonenveloped virus. J Clin Invest. 1986;78(4):1003–7. doi: 10.1172/JCI112653 3760180.
37. Bodkin DK, Nibert ML, Fields BN, Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J Virol. 1989;63(11):4676–81. 2677401.
38. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science New York, NY. 2011;334(6053):249–52. doi: 10.1126/science.1211057 21998395.
39. Uchiyama R, Chassaing B, Zhang B, Gewirtz AT, Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. The Journal of infectious diseases. 2014;210(2):171–82. doi: 10.1093/infdis/jiu037 24436449.
40. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science New York, NY. 2014;346(6210):755–9. doi: 10.1126/science.1257147 25378626.
41. Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C, Chervonsky AV, et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science New York, NY. 2011;334(6053):245–9. doi: 10.1126/science.1210718 21998394.
42. Robinson CM, Jesudhasan PR, Pfeiffer JK, Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell host & microbe. 2014;15(1):36–46. doi: 10.1016/j.chom.2013.12.004 24439896.
43. Mainou BA, Ashbrook AW, Smith EC, Dorset DC, Denison MR, Dermody TS, Serotonin Receptor Agonist 5-Nonyloxytryptamine Alters the Kinetics of Reovirus Cell Entry. J Virol. 2015;89(17):8701–12. doi: 10.1128/JVI.00739-15 26109733.
44. Mainou BA, Dermody TS, Src kinase mediates productive endocytic sorting of reovirus during cell entry. J Virol. 2011;85(7):3203–13. Epub 2011/01/21. doi: 10.1128/JVI.02056-10 21248042.
45. Middleton JK, Severson TF, Chandran K, Gillian AL, Yin J, Nibert ML, Thermostability of reovirus disassembly intermediates (ISVPs) correlates with genetic, biochemical, and thermodynamic properties of major surface protein mu1. J Virol. 2002;76(3):1051–61. doi: 10.1128/JVI.76.3.1051-1061.2002 11773381.
46. Drayna D, Fields BN, Genetic studies on the mechanism of chemical and physical inactivation of reovirus. J Gen Virol. 1982;63 (Pt 1):149–59. doi: 10.1099/0022-1317-63-1-149 7175500.
47. Silhavy TJ, Kahne D, Walker S, The bacterial cell envelope. Cold Spring Harb Perspect Biol. 2010;2(5):a000414. doi: 10.1101/cshperspect.a000414 20452953.
48. Sah H, Stabilization of proteins against methylene chloride/water interface-induced denaturation and aggregation. J Control Release. 1999;58(2):143–51. Epub 1999/03/04. 10053187.
49. Chang BS, Mahoney RR, Enzyme thermostabilization by bovine serum albumin and other proteins: evidence for hydrophobic interactions. Biotechnol Appl Biochem. 1995;22 (Pt 2):203–14. Epub 1995/10/01. 7576258.
50. Reiter DM, Frierson JM, Halvorson EE, Kobayashi T, Dermody TS, Stehle T, Crystal structure of reovirus attachment protein sigma1 in complex with sialylated oligosaccharides. PLoS pathogens. 2011;7(8):e1002166. doi: 10.1371/journal.ppat.1002166 21829363.
51. Bass DM, Bodkin D, Dambrauskas R, Trier JS, Fields BN, Wolf JL, Intraluminal proteolytic activation plays an important role in replication of type 1 reovirus in the intestines of neonatal mice. J Virol. 1990;64(4):1830–3. 2157065.
52. Borsa J, Morash BD, Sargent MD, Copps TP, Lievaart PA, Szekely JG, Two modes of entry of reovirus particles into L cells. J Gen Virol. 1979;45(1):161–70. doi: 10.1099/0022-1317-45-1-161 521802.
53. Doyle JD, Danthi P, Kendall EA, Ooms LS, Wetzel JD, Dermody TS, Molecular determinants of proteolytic disassembly of the reovirus outer capsid. J Biol Chem. 2012;287(11):8029–38. Epub 2012/01/19. doi: 10.1074/jbc.M111.334854 22253447.
54. Anafu AA, Bowen CH, Chin CR, Brass AL, Holm GH, Interferon-inducible transmembrane protein 3 (IFITM3) restricts reovirus cell entry. J Biol Chem. 2013;288(24):17261–71. doi: 10.1074/jbc.M112.438515 23649619.
55. Kirchner E, Guglielmi KM, Strauss HM, Dermody TS, Stehle T, Structure of reovirus sigma1 in complex with its receptor junctional adhesion molecule-A. PLoS pathogens. 2008;4(12):e1000235. doi: 10.1371/journal.ppat.1000235 19079583.
56. Gentsch JR, Pacitti AF, Differential interaction of reovirus type 3 with sialylated receptor components on animal cells. Virology. 1987;161(1):245–8. 3672931.
57. Larson SM, Antczak JB, Joklik WK, Reovirus exists in the form of 13 particle species that differ in their content of protein sigma 1. Virology. 1994;201(2):303–11. doi: 10.1006/viro.1994.1295 8184540.
58. Nibert ML, Dermody TS, Fields BN, Structure of the reovirus cell-attachment protein: a model for the domain organization of sigma 1. J Virol. 1990;64(6):2976–89. 2335823.
59. Chappell JD, Prota AE, Dermody TS, Stehle T, Crystal structure of reovirus attachment protein sigma1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 2002;21(1–2):1–11. doi: 10.1093/emboj/21.1.1 11782420.
60. Weiner HL, Fields BN, Neutralization of reovirus: the gene responsible for the neutralization antigen. J Exp Med. 1977;146(5):1305–10. 925604.
61. Hutchings AB, Helander A, Silvey KJ, Chandran K, Lucas WT, Nibert ML, et al. Secretory immunoglobulin A antibodies against the sigma1 outer capsid protein of reovirus type 1 Lang prevent infection of mouse Peyer’s patches. J Virol. 2004;78(2):947–57. doi: 10.1128/JVI.78.2.947-957.2004 14694126.
62. Silvey KJ, Hutchings AB, Vajdy M, Petzke MM, Neutra MR, Role of immunoglobulin A in protection against reovirus entry into Murine Peyer’s patches. J Virol. 2001;75(22):10870–9. doi: 10.1128/JVI.75.22.10870-10879.2001 11602727.
63. Tan M, Jiang X, Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 2005;13(6):285–93. doi: 10.1016/j.tim.2005.04.004 15936661.
64. Miura T, Sano D, Suenaga A, Yoshimura T, Fuzawa M, Nakagomi T, et al. Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J Virol. 2013;87(17):9441–51. doi: 10.1128/JVI.01060-13 23804639.
65. Karst SM, Identification of a novel cellular target and a co-factor for norovirus infection—B cells & commensal bacteria. Gut Microbes. 2015;6(4):266–71. doi: 10.1080/19490976.2015.1052211 25997033.
66. Ross SR, Mouse mammary tumor virus molecular biology and oncogenesis. Viruses. 2010;2(9):2000–12. doi: 10.3390/v2092000 21274409.
67. Wilks J, Lien E, Jacobson AN, Fischbach MA, Qureshi N, Chervonsky AV, et al. Mammalian Lipopolysaccharide Receptors Incorporated into the Retroviral Envelope Augment Virus Transmission. Cell host & microbe. 2015;18(4):456–62. doi: 10.1016/j.chom.2015.09.005 26468748.
68. Karst SM, The influence of commensal bacteria on infection with enteric viruses. Nat Rev Microbiol. 2016;14(4):197–204. doi: 10.1038/nrmicro.2015.25 26853118.
69. Xu J, Zhang J, Lu X, Liang W, Zhang L, Kan B, O antigen is the receptor of Vibrio cholerae serogroup O1 El Tor typing phage VP4. J Bacteriol. 2013;195(4):798–806. Epub 2012/12/12. doi: 10.1128/JB.01770-12 23222721.
70. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, et al. The long-term stability of the human gut microbiota. Science New York, NY. 2013;341(6141):1237439. Epub 2013/07/06. doi: 10.1126/science.1237439 23828941.
71. Doyle JD, Stencel-Baerenwald JE, Copeland CA, Rhoads JP, Brown JJ, Boyd KL, et al. Diminished reovirus capsid stability alters disease pathogenesis and littermate transmission. PLoS pathogens. 2015;11(3):e1004693. doi: 10.1371/journal.ppat.1004693 25738608.
72. Drayna D, Fields BN, Activation and characterization of the reovirus transcriptase: genetic analysis. J Virol. 1982;41(1):110–8. 7086953.
73. Lin J, Lee LY, Roivainen M, Filman DJ, Hogle JM, Belnap DM, Structure of the Fab-labeled "breathing" state of native poliovirus. J Virol. 2012;86(10):5959–62. Epub 2012/03/09. doi: 10.1128/JVI.05990-11 22398295.
74. Thete D, Snyder AJ, Mainou BA, Danthi P, Reovirus mu1 Protein Affects Infectivity by Altering Virus-Receptor Interactions. J Virol. 2016;90(23):10951–62. doi: 10.1128/JVI.01843-16 27681135.
75. Dietrich MH, Ogden KM, Katen SP, Reiss K, Sutherland DM, Carnahan RH, et al. Structural Insights into Reovirus sigma1 Interactions with Two Neutralizing Antibodies. J Virol. 2017;91(4). doi: 10.1128/JVI.01621-16 27928010.
76. Virgin HWt, Mann MA, Fields BN, Tyler KL, Monoclonal antibodies to reovirus reveal structure/function relationships between capsid proteins and genetics of susceptibility to antibody action. J Virol. 1991;65(12):6772–81. 1719233.
77. Blutt SE, Conner ME, The gastrointestinal frontier: IgA and viruses. Front Immunol. 2013;4:402. Epub 2013/12/19. doi: 10.3389/fimmu.2013.00402 24348474.
78. Kobayashi T, Antar AA, Boehme KW, Danthi P, Eby EA, Guglielmi KM, et al. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell host & microbe. 2007;1(2):147–57. doi: 10.1016/j.chom.2007.03.003 18005692.
79. Virgin HWt, Bassel-Duby R, Fields BN, Tyler KL, Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol. 1988;62(12):4594–604. Epub 1988/12/01. 2460637.
80. Furlong DB, Nibert ML, Fields BN, Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol. 1988;62(1):246–56. Epub 1988/01/01. 3275434.
81. Smith RE, Zweerink HJ, Joklik WK, Polypeptide components of virions, top component and cores of reovirus type 3. Virology. 1969;39(4):791–810. Epub 1969/12/01. 0042-6822(69)90017-8 [pii]. 4311639.
82. Konkol MA, Blair KM, Kearns DB, Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J Bacteriol. 2013;195(18):4085–93. Epub 2013/07/10. doi: 10.1128/JB.00696-13 23836866.
83. Yasbin RE, Young FE, Transduction in Bacillus subtilis by bacteriophage SPP1. J Virol. 1974;14(6):1343–8. Epub 1974/12/01. 4214946.
84. Iskarpatyoti JA, Willis JZ, Guan J, Morse EA, Ikizler M, Wetzel JD, et al. A rapid, automated approach for quantitation of rotavirus and reovirus infectivity. Journal of virological methods. 2012;184(1–2):1–7. Epub 2012/04/03. doi: 10.1016/j.jviromet.2012.03.018 22465252.