Structures and Mechanisms of Nonsegmented, Negative-Strand RNA Virus Polymerases

Literature Cited

1. 1.

   Fodor E, Te Velthuis AJW. 2020. Structure and function of the influenza virus transcription and replication machinery. Cold Spring Harb. Perspect. Med. 10:9a038398
   [Google Scholar]
2. 2.

   Malet H, Williams HM, Cusack S, Rosenthal M. 2023. The mechanism of genome replication and transcription in bunyaviruses. PLOS Pathog. 19:e1011060
   [Google Scholar]
3. 3.

   Wandzik JM, Kouba T, Cusack S. 2021. Structure and function of influenza polymerase. Cold Spring Harb. . Perspect. Med. 11:9a038372
   [Google Scholar]
4. 4.

   Zhu Z, Fodor E, Keown JR. 2022. A structural understanding of influenza virus genome replication. Trends Microbiol. 31:3308–19
   [Google Scholar]
5. 5.

   Amarasinghe GK, Ayllon MA, Bao Y, Basler CF, Bavari S et al. 2019. Taxonomy of the order Mononegavirales: update 2019. Arch. Virol. 164:1967–80
   [Google Scholar]
6. 6.

   Ruigrok RW, Crepin T, Kolakofsky D. 2011. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 14:504–10
   [Google Scholar]
7. 7.

   Fearns R, Plemper RK. 2017. Polymerases of paramyxoviruses and pneumoviruses. Virus Res. 234:87–102
   [Google Scholar]
8. 8.

   Hume AJ, Muhlberger E. 2019. Distinct genome replication and transcription strategies within the growing filovirus family. J. Mol. Biol. 431:4290–320
   [Google Scholar]
9. 9.

   Kolakofsky D, Le Mercier P, Nishio M, Blackledge M, Crepin T, Ruigrok RWH 2021. Sendai virus and a unified model of mononegavirus RNA synthesis. Viruses 13:122466
   [Google Scholar]
10. 10.

    Noton SL, Fearns R. 2015. Initiation and regulation of paramyxovirus transcription and replication. Virology 479–480:545–54
    [Google Scholar]
11. 11.

    Whelan SP, Barr JN, Wertz GW. 2004. Transcription and replication of nonsegmented negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:61–119
    [Google Scholar]
12. 12.

    Gubbay O, Curran J, Kolakofsky D. 2001. Sendai virus genome synthesis and assembly are coupled: a possible mechanism to promote viral RNA polymerase processivity. J. Gen. Virol. 82:2895–903
    [Google Scholar]
13. 13.

    Abdella R, Aggarwal M, Okura T, Lamb RA, He Y. 2020. Structure of a paramyxovirus polymerase complex reveals a unique methyltransferase-CTD conformation. PNAS 117:4931–41
    [Google Scholar]
14. 14.

    Cao D, Gao Y, Roesler C, Rice S, D'Cunha P et al. 2020. Cryo-EM structure of the respiratory syncytial virus RNA polymerase. Nat. Commun. 11:368
    [Google Scholar]
15. 15.

    Gilman MSA, Liu C, Fung A, Behera I, Jordan P et al. 2019. Structure of the respiratory syncytial virus polymerase complex. Cell 179:193–204.e14
    [Google Scholar]
16. 16.

    Horwitz JA, Jenni S, Harrison SC, Whelan SPJ 2020. Structure of a rabies virus polymerase complex from electron cryo-microscopy. PNAS 117:2099–107
    [Google Scholar]
17. 17.

    Jenni S, Bloyet LM, Diaz-Avalos R, Liang B, Whelan SPJ et al. 2020. Structure of the vesicular stomatitis virus L protein in complex with its phosphoprotein cofactor. Cell Rep. 30:53–60.e5
    [Google Scholar]
18. 18.

    Liang B, Li Z, Jenni S, Rahmeh AA, Morin BM et al. 2015. Structure of the L protein of vesicular stomatitis virus from electron cryomicroscopy. Cell 162:314–27The first cryo-EM structure of an nsNSV polymerase, revealing the five characteristic domains.
    [Google Scholar]
19. 19.

    Pan J, Qian X, Lattmann S, El Sahili A, Yeo TH et al. 2020. Structure of the human metapneumovirus polymerase phosphoprotein complex. Nature 577:275–79
    [Google Scholar]
20. 20.

    Xie J, Wang L, Zhai G, Wu D, Lin Z et al. 2021. Structural architecture of a dimeric paramyxovirus polymerase complex. bioRxiv 2021.09.13.460081. https://doi.org/10.1101/2021.09.13.460081
21. 21.

    Yuan B, Peng Q, Cheng J, Wang M, Zhong J et al. 2022. Structure of the Ebola virus polymerase complex. Nature 610:394–401
    [Google Scholar]
22. 22.

    Liang B. 2020. Structures of the mononegavirales polymerases. J. Virol. 94:22e00175–20Another review article on the nsNSV polymerases that shows modeling of nsNSV polymerases onto other polymerase structures, identifying the channels in the polymerase.
    [Google Scholar]
23. 23.

    Te Velthuis AJW, Grimes JM, Fodor E 2021. Structural insights into RNA polymerases of negative-sense RNA viruses. Nat. Rev. Microbiol. 19:303–18
    [Google Scholar]
24. 24.

    Rahmeh AA, Schenk AD, Danek EI, Kranzusch PJ, Liang B et al. 2010. Molecular architecture of the vesicular stomatitis virus RNA polymerase. PNAS 107:20075–80The first negative-stain EM images of an nsNSV polymerase showing that it has globular domains that adopt different conformations.
    [Google Scholar]
25. 25.

    Bach S, Biedenkopf N, Grunweller A, Becker S, Hartmann RK. 2020. Hexamer phasing governs transcription initiation in the 3′-leader of Ebola virus. RNA 26:439–53
    [Google Scholar]
26. 26.

    le Mercier P, Kolakofsky D. 2019. Bipartite promoters and RNA editing of paramyxoviruses and filoviruses. RNA 25:279–85
    [Google Scholar]
27. 27.

    Vulliemoz D, Roux L. 2001.. “ Rule of six”: How does the Sendai virus RNA polymerase keep count?. J. Virol. 75:4506–18
    [Google Scholar]
28. 28.

    Weik M, Enterlein S, Schlenz K, Muhlberger E. 2005. The Ebola virus genomic replication promoter is bipartite and follows the rule of six. J. Virol. 79:10660–71
    [Google Scholar]
29. 29.

    Bloyet LM. 2021. The nucleocapsid of paramyxoviruses: structure and function of an encapsidated template. Viruses 13:122465
    [Google Scholar]
30. 30.

    Luo M, Terrell JR, McManus SA. 2020. Nucleocapsid structure of negative strand RNA virus. Viruses 12:8835
    [Google Scholar]
31. 31.

    Cowton VM, Fearns R. 2005. Evidence that the respiratory syncytial virus polymerase is recruited to nucleotides 1 to 11 at the 3′ end of the nucleocapsid and can scan to access internal signals. J. Virol. 79:11311–22
    [Google Scholar]
32. 32.

    Jordan PC, Liu C, Raynaud P, Lo MK, Spiropoulou CF et al. 2018. Initiation, extension, and termination of RNA synthesis by a paramyxovirus polymerase. PLOS Pathog. 14:e1006889
    [Google Scholar]
33. 33.

    Morin B, Rahmeh AA, Whelan SP. 2012. Mechanism of RNA synthesis initiation by the vesicular stomatitis virus polymerase. EMBO J. 31:1320–29
    [Google Scholar]
34. 34.

    Noton SL, Aljabr W, Hiscox JA, Matthews DA, Fearns R. 2014. Factors affecting de novo RNA synthesis and back-priming by the respiratory syncytial virus polymerase. Virology 462–463:318–27
    [Google Scholar]
35. 35.

    Shareef AM, Ludeke B, Jordan P, Deval J, Fearns R. 2021. Comparison of RNA synthesis initiation properties of non-segmented negative strand RNA virus polymerases. PLOS Pathog. 17:e1010151
    [Google Scholar]
36. 36.

    Smallwood S, Moyer SA. 1993. Promoter analysis of the vesicular stomatitis virus RNA polymerase. Virology 192:254–63
    [Google Scholar]
37. 37.

    Fearns R, Peeples ME, Collins PL. 2002. Mapping the transcription and replication promoters of respiratory syncytial virus. J. Virol. 76:1663–72
    [Google Scholar]
38. 38.

    Li T, Pattnaik AK. 1999. Overlapping signals for transcription and replication at the 3′ terminus of the vesicular stomatitis virus genome. J. Virol. 73:444–52
    [Google Scholar]
39. 39.

    Kao CC, Singh P, Ecker DJ. 2001. De novo initiation of viral RNA-dependent RNA synthesis. Virology 287:251–60
    [Google Scholar]
40. 40.

    van Dijk AA, Makeyev EV, Bamford DH. 2004. Initiation of viral RNA-dependent RNA polymerization. J. Gen. Virol. 85:1077–93
    [Google Scholar]
41. 41.

    Te Velthuis AJW, Robb NC, Kapanidis AN, Fodor E 2016. The role of the priming loop in influenza A virus RNA synthesis. Nat. Microbiol. 1:16029
    [Google Scholar]
42. 42.

    Butcher SJ, Grimes JM, Makeyev EV, Bamford DH, Stuart DI. 2001. A mechanism for initiating RNA-dependent RNA polymerization. Nature 410:235–40
    [Google Scholar]
43. 43.

    Appleby TC, Perry JK, Murakami E, Barauskas O, Feng J et al. 2015. Structural basis for RNA replication by the hepatitis C virus polymerase. Science 347:771–75
    [Google Scholar]
44. 44.

    Hong Z, Cameron CE, Walker MP, Castro C, Yao N et al. 2001. A novel mechanism to ensure terminal initiation by hepatitis C virus NS5B polymerase. Virology 285:6–11
    [Google Scholar]
45. 45.

    Ogino M, Gupta N, Green TJ, Ogino T. 2019. A dual-functional priming-capping loop of rhabdoviral RNA polymerases directs terminal de novo initiation and capping intermediate formation. Nucleic Acids Res. 47:299–309
    [Google Scholar]
46. 46.

    Cressey TN, Shareef AM, Kleiner VA, Noton SL, Byrne PO et al. 2022. Distinctive features of the respiratory syncytial virus priming loop compared to other non-segmented negative strand RNA viruses. PLOS Pathog. 18:e1010451
    [Google Scholar]
47. 47.

    Deflube LR, Cressey TN, Hume AJ, Olejnik J, Haddock E et al. 2019. Ebolavirus polymerase uses an unconventional genome replication mechanism. PNAS 116:8535–43
    [Google Scholar]
48. 48.

    Tremaglio CZ, Noton SL, Deflube LR, Fearns R. 2013. Respiratory syncytial virus polymerase can initiate transcription from position 3 of the leader promoter. J. Virol. 87:3196–207
    [Google Scholar]
49. 49.

    Noton SL, Cowton VM, Zack CR, McGivern DR, Fearns R. 2010. Evidence that the polymerase of respiratory syncytial virus initiates RNA replication in a nontemplated fashion. PNAS 107:10226–31
    [Google Scholar]
50. 50.

    Noton SL, Fearns R. 2011. The first two nucleotides of the respiratory syncytial virus antigenome RNA replication product can be selected independently of the promoter terminus. RNA 17:1895–906
    [Google Scholar]
51. 51.

    Arragain B, Durieux Trouilleton Q, Baudin F, Provaznik J, Azevedo N et al. 2022. Structural snapshots of La Crosse virus polymerase reveal the mechanisms underlying Peribunyaviridae replication and transcription. Nat. Commun. 13:902
    [Google Scholar]
52. 52.

    Kouba T, Drncova P, Cusack S. 2019. Structural snapshots of actively transcribing influenza polymerase. Nat. Struct. Mol. Biol. 26:460–70
    [Google Scholar]
53. 53.

    Wandzik JM, Kouba T, Karuppasamy M, Pflug A, Drncova P et al. 2020. A structure-based model for the complete transcription cycle of influenza polymerase. Cell 181:877–93.e21
    [Google Scholar]
54. 54.

    Arragain B, Effantin G, Gerlach P, Reguera J, Schoehn G et al. 2020. Pre-initiation and elongation structures of full-length La Crosse virus polymerase reveal functionally important conformational changes. Nat. Commun. 11:3590
    [Google Scholar]
55. 55.

    Braun MR, Deflube LR, Noton SL, Mawhorter ME, Tremaglio CZ, Fearns R. 2017. RNA elongation by respiratory syncytial virus polymerase is calibrated by conserved region V. PLOS Pathog. 13:e1006803Using site-directed mutagenesis and a small molecule inhibitor, this study shows that the capping domain can affect polymerase processivity.
    [Google Scholar]
56. 56.

    Cox RM, Toots M, Yoon JJ, Sourimant J, Ludeke B et al. 2018. Development of an allosteric inhibitor class blocking RNA elongation by the respiratory syncytial virus polymerase complex. J. Biol. Chem. 293:16761–77
    [Google Scholar]
57. 57.

    Ogino M, Green TJ, Ogino T. 2022. GDP polyribonucleotidyltransferase domain of vesicular stomatitis virus polymerase regulates leader-promoter escape and polyadenylation-coupled termination during stop-start transcription. PLOS Pathog. 18:e1010287
    [Google Scholar]
58. 58.

    Sourimant J, Lieber CM, Yoon JJ, Toots M, Govindarajan M et al. 2022. Orally efficacious lead of the AVG inhibitor series targeting a dynamic interface in the respiratory syncytial virus polymerase. Sci. Adv. 8:eabo2236
    [Google Scholar]
59. 59.

    Bach S, Demper JC, Klemm P, Schlereth J, Lechner M et al. 2021. Identification and characterization of short leader and trailer RNAs synthesized by the Ebola virus RNA polymerase. PLOS Pathog. 17:e1010002
    [Google Scholar]
60. 60.

    Colonno RJ, Banerjee AK. 1978. In vitro RNA transcription by the New Jersey serotype of vesicular stomatitis virus. II. Characterization of the leader RNA. J. Virol. 26:188–94
    [Google Scholar]
61. 61.

    Leppert M, Rittenhouse L, Perrault J, Summers DF, Kolakofsky D. 1979. Plus and minus strand leader RNAs in negative strand virus-infected cells. Cell 18:735–47
    [Google Scholar]
62. 62.

    Vidal S, Kolakofsky D. 1989. Modified model for the switch from Sendai virus transcription to replication. J. Virol. 63:1951–58
    [Google Scholar]
63. 63.

    Ogino T, Green TJ. 2019. RNA synthesis and capping by non-segmented negative strand RNA viral polymerases: lessons from a prototypic virus. Front. Microbiol. 10:1490
    [Google Scholar]
64. 64.

    Ogino T, Banerjee AK. 2007. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol. Cell 25:85–97Paper presenting the first description of the distinctive PRNTase capping mechanism used by nsNSV polymerases.
    [Google Scholar]
65. 65.

    Ogino T, Yadav SP, Banerjee AK. 2010. Histidine-mediated RNA transfer to GDP for unique mRNA capping by vesicular stomatitis virus RNA polymerase. PNAS 107:3463–68
    [Google Scholar]
66. 66.

    Liuzzi M, Mason SW, Cartier M, Lawetz C, McCollum RS et al. 2005. Inhibitors of respiratory syncytial virus replication target cotranscriptional mRNA guanylylation by viral RNA-dependent RNA polymerase. J. Virol. 79:13105–15
    [Google Scholar]
67. 67.

    Li J, Rahmeh A, Morelli M, Whelan SP. 2008. A conserved motif in region V of the large polymerase proteins of nonsegmented negative-sense RNA viruses that is essential for mRNA capping. J. Virol. 82:775–84
    [Google Scholar]
68. 68.

    Neubauer J, Ogino M, Green TJ, Ogino T. 2016. Signature motifs of GDP polyribonucleotidyltransferase, a non-segmented negative strand RNA viral mRNA capping enzyme, domain in the L protein are required for covalent enzyme-pRNA intermediate formation. Nucleic Acids Res. 44:330–41
    [Google Scholar]
69. 69.

    Paesen GC, Collet A, Sallamand C, Debart F, Vasseur JJ et al. 2015. X-ray structure and activities of an essential Mononegavirales L-protein domain. Nat. Commun. 6:8749Key paper presenting the X-ray crystal structure of the nsNSV methyltransferase and C-terminal domain dimer, and describing structure-directed functional analysis of the methyltransferase and the existence of an NTPase.
    [Google Scholar]
70. 70.

    Li J, Wang JT, Whelan SP. 2006. A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. PNAS 103:8493–98
    [Google Scholar]
71. 71.

    Martin B, Coutard B, Guez T, Paesen GC, Canard B et al. 2018. The methyltransferase domain of the Sudan ebolavirus L protein specifically targets internal adenosines of RNA substrates, in addition to the cap structure. Nucleic Acids Res. 46:7902–12
    [Google Scholar]
72. 72.

    Sutto-Ortiz P, Tcherniuk S, Ysebaert N, Abeywickrema P, Noel M et al. 2021. The methyltransferase domain of the respiratory syncytial virus L protein catalyzes cap N7 and 2′-O-methylation. PLOS Pathog. 17:e1009562
    [Google Scholar]
73. 73.

    Rahmeh AA, Li J, Kranzusch PJ, Whelan SP. 2009. Ribose 2′-O methylation of the vesicular stomatitis virus mRNA cap precedes and facilitates subsequent guanine-N-7 methylation by the large polymerase protein. J. Virol. 83:11043–50
    [Google Scholar]
74. 74.

    Ruedas JB, Perrault J. 2014. Putative domain-domain interactions in the vesicular stomatitis virus L polymerase protein appendage region. J. Virol. 88:14458–66
    [Google Scholar]
75. 75.

    Valle C, Martin B, Debart F, Vasseur JJ, Imbert I et al. 2020. The C-terminal domain of the Sudan Ebolavirus L protein is essential for RNA binding and methylation. J. Virol. 94:12e00520–20
    [Google Scholar]
76. 76.

    Valle C, Martin B, Ferron F, Roig-Zamboni V, Desmyter A et al. 2021. First insights into the structural features of Ebola virus methyltransferase activities. Nucleic Acids Res. 49:1737–48
    [Google Scholar]
77. 77.

    Tekes G, Rahmeh AA, Whelan SP. 2011. A freeze frame view of vesicular stomatitis virus transcription defines a minimal length of RNA for 5′ processing. PLOS Pathog. 7:e1002073
    [Google Scholar]
78. 78.

    Stillman EA, Whitt MA. 1999. Transcript initiation and 5′-end modifications are separable events during vesicular stomatitis virus transcription. J. Virol. 73:7199–209Paper showing that modifications at the 5′ end of the mRNA are dependent on the RNA sequence and that if the sequence at the 5′ end of the mRNA was altered, the polymerase aborted pre-mRNA synthesis, which can be attributed to lack of cap addition.
    [Google Scholar]
79. 79.

    Wang JT, McElvain LE, Whelan SP. 2007. Vesicular stomatitis virus mRNA capping machinery requires specific cis-acting signals in the RNA. J. Virol. 81:11499–506
    [Google Scholar]
80. 80.

    Ogino T, Kobayashi M, Iwama M, Mizumoto K. 2005. Sendai virus RNA-dependent RNA polymerase L protein catalyzes cap methylation of virus-specific mRNA. J. Biol. Chem. 280:4429–35
    [Google Scholar]
81. 81.

    Nishio M, Tsurudome M, Garcin D, Komada H, Ito M et al. 2011. Human parainfluenza virus type 2 L protein regions required for interaction with other viral proteins and mRNA capping. J. Virol. 85:725–32
    [Google Scholar]
82. 82.

    Ogino T. 2014. Capping of vesicular stomatitis virus pre-mRNA is required for accurate selection of transcription stop-start sites and virus propagation. Nucleic Acids Res. 42:12112–25
    [Google Scholar]
83. 83.

    Herman RC, Adler S, Lazzarini RA, Colonno RJ, Banerjee AK, Westphal H. 1978. Intervening polyadenylate sequences in RNA transcripts of vesicular stomatitis virus. Cell 15:587–96
    [Google Scholar]
84. 84.

    Herman RC, Schubert M, Keene JD, Lazzarini RA. 1980. Polycistronic vesicular stomatitis virus RNA transcripts. PNAS 77:4662–65
    [Google Scholar]
85. 85.

    Whelan SP, Barr JN, Wertz GW. 2000. Identification of a minimal size requirement for termination of vesicular stomatitis virus mRNA: implications for the mechanism of transcription. J. Virol. 74:8268–76Paper presenting evidence that the polymerase must elongate a certain distance from the gene start signal before it can recognize a gene end signal, consistent with it undergoing a conformational change following cap addition.
    [Google Scholar]
86. 86.

    Cartee TL, Megaw AG, Oomens AG, Wertz GW. 2003. Identification of a single amino acid change in the human respiratory syncytial virus L protein that affects transcriptional termination. J. Virol. 77:7352–60
    [Google Scholar]
87. 87.

    Juhasz K, Murphy BR, Collins PL. 1999. The major attenuating mutations of the respiratory syncytial virus vaccine candidate cpts530/1009 specify temperature-sensitive defects in transcription and replication and a non-temperature-sensitive alteration in mRNA termination. J. Virol. 73:5176–80
    [Google Scholar]
88. 88.

    Galloway SE, Wertz GW. 2008. S-adenosyl homocysteine-induced hyperpolyadenylation of vesicular stomatitis virus mRNA requires the methyltransferase activity of L protein. J. Virol. 82:12280–90
    [Google Scholar]
89. 89.

    Hunt DM, Hutchinson KL. 1993. Amino acid changes in the L polymerase protein of vesicular stomatitis virus which confer aberrant polyadenylation and temperature-sensitive phenotypes. Virology 193:786–93
    [Google Scholar]
90. 90.

    Hunt DM, Mehta R, Hutchinson KL. 1988. The L protein of vesicular stomatitis virus modulates the response of the polyadenylic acid polymerase to S-adenosylhomocysteine. J. Gen. Virol. 69:Part 102555–61
    [Google Scholar]
91. 91.

    Rose JK, Lodish HF, Brock ML. 1977. Giant heterogeneous polyadenylic acid on vesicular stomatitis virus mRNA synthesized in vitro in the presence of S-adenosylhomocysteine. J. Virol. 21:683–93Paper presenting the first evidence that perturbation of the methyltransferase domain can lead to hyperpolyadenylation, suggesting a link between the structure of the methyltransferase domain and mRNA release.
    [Google Scholar]
92. 92.

    Arnheiter H, Davis NL, Wertz G, Schubert M, Lazzarini RA. 1985. Role of the nucleocapsid protein in regulating vesicular stomatitis virus RNA synthesis. Cell 41:259–67
    [Google Scholar]
93. 93.

    Baker SC, Moyer SA. 1988. Encapsidation of Sendai virus genome RNAs by purified NP protein during in vitro replication. J. Virol. 62:834–38
    [Google Scholar]
94. 94.

    Blumberg BM, Leppert M, Kolakofsky D. 1981. Interaction of VSV leader RNA and nucleocapsid protein may control VSV genome replication. Cell 23:837–45
    [Google Scholar]
95. 95.

    Carrique L, Fan H, Walker AP, Keown JR, Sharps J et al. 2020. Host ANP32A mediates the assembly of the influenza virus replicase. Nature 587:638–43
    [Google Scholar]
96. 96.

    Cevik B, Smallwood S, Moyer SA. 2003. The L-L oligomerization domain resides at the very N-terminus of the Sendai virus L RNA polymerase protein. Virology 313:525–36
    [Google Scholar]
97. 97.

    Smallwood S, Moyer SA. 2004. The L polymerase protein of parainfluenza virus 3 forms an oligomer and can interact with the heterologous Sendai virus L, P and C proteins. Virology 318:439–50
    [Google Scholar]
98. 98.

    Trunschke M, Conrad D, Enterlein S, Olejnik J, Brauburger K, Muhlberger E. 2013. The L-VP35 and L-L interaction domains reside in the amino terminus of the Ebola virus L protein and are potential targets for antivirals. Virology 441:135–45
    [Google Scholar]
99. 99.

    Vulliemoz D, Roux L. 2002. Given the opportunity, the Sendai virus RNA-dependent RNA polymerase could as well enter its template internally. J. Virol. 76:7987–95
    [Google Scholar]
100. 100.

     Noton SL, Deflube LR, Tremaglio CZ, Fearns R. 2012. The respiratory syncytial virus polymerase has multiple RNA synthesis activities at the promoter. PLOS Pathog. 8:e1002980
     [Google Scholar]
101. 101.

     Chuang JL, Perrault J. 1997. Initiation of vesicular stomatitis virus mutant polR1 transcription internally at the N gene in vitro. J. Virol. 71:1466–75
     [Google Scholar]
102. 102.

     Emerson SU. 1982. Reconstitution studies detect a single polymerase entry site on the vesicular stomatitis virus genome. Cell 31:635–42
     [Google Scholar]
103. 103.

     Perrault J, Clinton GM, McClure MA. 1983. RNP template of vesicular stomatitis virus regulates transcription and replication functions. Cell 35:175–85
     [Google Scholar]
104. 104.

     Qanungo KR, Shaji D, Mathur M, Banerjee AK. 2004. Two RNA polymerase complexes from vesicular stomatitis virus-infected cells that carry out transcription and replication of genome RNA. PNAS 101:5952–57
     [Google Scholar]
105. 105.

     Whelan SP, Wertz GW. 2002. Transcription and replication initiate at separate sites on the vesicular stomatitis virus genome. PNAS 99:9178–83
     [Google Scholar]
106. 106.

     Cong J, Feng X, Kang H, Fu W, Wang Let al 2023. Structure of the Newcastle disease virus L protein in complex with tetrameric phosphoprotein. Nat. Commun 14:1324
     [Google Scholar]