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Volume 99, Issue 2

The use of novel epitope-tagged arenaviruses reveals that Rab5c-positive endosomal membranes are targeted by the LCMV matrix protein Free

Abstract

We report the development of recombinant New World (Junín; JUNV) and Old World (lymphocytic choriomeningitis virus; LCMV) mammarenaviruses that encode an HA-tagged matrix protein (Z). These viruses permit the robust affinity purification of Z from infected cells or virions, as well as the detection of Z by immunofluorescent microscopy. Importantly, the HA-tagged viruses grow with wild-type kinetics in a multi-cycle growth assay. Using these viruses, we report a novel description of JUNV Z localization in infected cells, as well as the first description of colocalization between LCMV Z and the GTPase Rab5c. This latter result, when combined with our previous findings that LCMV genome and glycoprotein also colocalize with Rab5c, suggest that LCMV may target Rab5c-positive membranes for preassembly of virus particles prior to budding. The recombinant viruses reported here will provide the field with new tools to better study Z protein functionality and identify key Z protein interactions with host machinery.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): arenavirus , HA epitope tag , Junín (JUNV) , lymphocytic choriomeningitis (LCMV) , Matrix protein (Z) and Rab5c
© 2018 The Authors
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/content/journal/jgv/10.1099/jgv.0.001004
2018-02-01
2024-04-24
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References

  1. Maiztegui JI. Clinical and epidemiological patterns of Argentine haemorrhagic fever. Bull World Health Organ 1975; 52:567–575[PubMed]
     [Google Scholar]
  2. Salazar-Bravo J, Ruedas LA, Yates TL. Mammalian reservoirs of arenaviruses. In Oldstone MA. (editor) Arenaviruses I (Current Topics in Microbiology and Immunology Berlin Heidelberg: Springer; 2002 pp. 25–63
     [Google Scholar]
  3. Childs JE, Glass GE, Korch GW, Ksiazek TG, Leduc JW. Lymphocytic choriomeningitis virus infection and house mouse (Mus musculus) distribution in urban Baltimore. Am J Trop Med Hyg 1992; 47:27–34 [View Article][PubMed]
     [Google Scholar]
  4. Keenlyside RA, McCormick JB, Webb PA, Smith E, Elliott L et al. Case-control study of Mastomys natalensis and humans in Lassa virus-infected households in Sierra Leone. Am J Trop Med Hyg 1983; 32:829–837 [View Article][PubMed]
     [Google Scholar]
  5. Meyer BJ, de La Torre JC, Southern PJ. Arenaviruses: genomic RNAs, transcription, and replication. In Oldstone MA. (editor) Arenaviruses I (Current Topics in Microbiology and Immunology) Berlin Heidelberg: Springer; 2002 pp. 139–157
     [Google Scholar]
  6. Fehling SK, Lennartz F, Strecker T. Multifunctional nature of the arenavirus RING finger protein Z. Viruses 2012; 4:2973–3011 [View Article][PubMed]
     [Google Scholar]
  7. Djavani M, Lukashevich IS, Sanchez A, Nichol ST, Salvato MS. Completion of the Lassa fever virus sequence and identification of a RING finger open reading frame at the L RNA 5' End. Virology 1997; 235:414–418 [View Article][PubMed]
     [Google Scholar]
  8. Schlie K, Maisa A, Freiberg F, Groseth A, Strecker T et al. Viral protein determinants of Lassa virus entry and release from polarized epithelial cells. J Virol 2010; 84:3178–3188 [View Article][PubMed]
     [Google Scholar]
  9. Capul AA, Perez M, Burke E, Kunz S, Buchmeier MJ et al. Arenavirus Z-glycoprotein association requires Z myristoylation but not functional RING or late domains. J Virol 2007; 81:9451–9460 [View Article][PubMed]
     [Google Scholar]
  10. Strecker T, Eichler R, Meulen J, Weissenhorn W, Dieter Klenk H et al. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 2003; 77:10700–10705 [View Article][PubMed]
     [Google Scholar]
  11. Perez M, Craven RC, de La Torre JC. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci USA 2003; 100:12978–12983 [View Article][PubMed]
     [Google Scholar]
  12. Eichler R, Strecker T, Kolesnikova L, ter Meulen J, Weissenhorn W et al. Characterization of the Lassa virus matrix protein Z: electron microscopic study of virus-like particles and interaction with the nucleoprotein (NP). Virus Res 2004; 100:249–255 [View Article][PubMed]
     [Google Scholar]
  13. Ziegler CM, Eisenhauer P, Kelly JA, Dang LN, Beganovic V et al. A proteomic survey of Junín virus interactions with human proteins reveals host factors required for arenavirus replication. J Virol 2017JVI.01565-17 [View Article][PubMed]
     [Google Scholar]
  14. Ziegler CM, Eisenhauer P, Bruce EA, Weir ME, King BR et al. The lymphocytic choriomeningitis virus matrix protein PPXY late domain drives the production of defective interfering particles. PLoS Pathog 2016; 12:e1005501 [View Article][PubMed]
     [Google Scholar]
  15. Fehling SK, Noda T, Maisner A, Lamp B, Conzelmann KK et al. The microtubule motor protein KIF13A is involved in intracellular trafficking of the Lassa virus matrix protein Z. Cell Microbiol 2013; 15:315–334 [View Article][PubMed]
     [Google Scholar]
  16. Flatz L, Bergthaler A, de La Torre JC, Pinschewer DD. Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc Natl Acad Sci USA 2006; 103:4663–4668 [View Article][PubMed]
     [Google Scholar]
  17. Emonet SF, Seregin AV, Yun NE, Poussard AL, Walker AG et al. Rescue from cloned cDNAs and in vivo characterization of recombinant pathogenic Romero and live-attenuated Candid #1 strains of Junin virus, the causative agent of Argentine hemorrhagic fever disease. J Virol 2011; 85:1473–1483 [View Article][PubMed]
     [Google Scholar]
  18. Ziegler CM, Eisenhauer P, Bruce EA, Beganovic V, King BR et al. A novel phosphoserine motif in the LCMV matrix protein Z regulates the release of infectious virus and defective interfering particles. J Gen Virol 2016; 97:2084–2089 [View Article][PubMed]
     [Google Scholar]
  19. King BR, Hershkowitz D, Eisenhauer PL, Weir ME, Ziegler CM et al. A map of the arenavirus nucleoprotein-host protein interactome reveals that Junín virus selectively impairs the antiviral activity of double-stranded RNA-activated protein kinase (PKR). J Virol 2017; 91:e00763-17 [View Article]
     [Google Scholar]
  20. Welsh RM, Pfau CJ. Determinants of lymphocytic choriomeningitis interference. J Gen Virol 1972; 14:177–187 [View Article][PubMed]
     [Google Scholar]
  21. Huang AS, Baltimore D. Defective viral particles and viral disease processes. Nature 1970; 226:325–327 [View Article][PubMed]
     [Google Scholar]
  22. Ortiz-Riaño E, Cheng BY, de La Torre JC, Martínez-Sobrido L. The C-terminal region of lymphocytic choriomeningitis virus nucleoprotein contains distinct and segregable functional domains involved in NP-Z interaction and counteraction of the type I interferon response. J Virol 2011; 85:13038–13048 [View Article][PubMed]
     [Google Scholar]
  23. Shtanko O, Imai M, Goto H, Lukashevich IS, Neumann G et al. A role for the C terminus of Mopeia virus nucleoprotein in its incorporation into Z protein-induced virus-like particles. J Virol 2010; 84:5415–5422 [View Article][PubMed]
     [Google Scholar]
  24. Perez M, Greenwald DL, de La Torre JC. Myristoylation of the RING finger Z protein is essential for arenavirus budding. J Virol 2004; 78:11443–11448 [View Article][PubMed]
     [Google Scholar]
  25. Strecker T, Maisa A, Daffis S, Eichler R, Lenz O et al. The role of myristoylation in the membrane association of the Lassa virus matrix protein Z. Virol J 2006; 3:93 [View Article][PubMed]
     [Google Scholar]
  26. García CC, Ellenberg PC, Artuso MC, Scolaro LA, Damonte EB. Characterization of Junín virus particles inactivated by a zinc finger-reactive compound. Virus Res 2009; 143:106–113 [View Article][PubMed]
     [Google Scholar]
  27. Fan L, Briese T, Lipkin WI. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J Virol 2010; 84:1785–1791 [View Article][PubMed]
     [Google Scholar]
  28. Loureiro ME, Wilda M, Levingston Macleod JM, D'Antuono A, Foscaldi S et al. Molecular determinants of Arenavirus Z protein homo-oligomerization and L polymerase binding. J Virol 2011JVI.05691-05611
     [Google Scholar]
  29. Baird NL, York J, Nunberg JH. Arenavirus infection induces discrete cytosolic structures for RNA replication. J Virol 2012; 86:11301–11310 [View Article][PubMed]
     [Google Scholar]
  30. Levingston Macleod JM, D'Antuono A, Loureiro ME, Casabona JC, Gomez GA et al. Identification of two functional domains within the arenavirus nucleoprotein. J Virol 2011; 85:2012–2023 [View Article][PubMed]
     [Google Scholar]
  31. Groseth A, Wolff S, Strecker T, Hoenen T, Becker S. Efficient budding of the tacaribe virus matrix protein z requires the nucleoprotein. J Virol 2010; 84:3603–3611 [View Article][PubMed]
     [Google Scholar]
  32. King BR, Kellner S, Eisenhauer PL, Bruce EA, Ziegler CM et al. Visualization of the lymphocytic choriomeningitis mammarenavirus (LCMV) genome reveals the early endosome as a possible site for genome replication and viral particle pre-assembly. J Gen Virol 2017; 98:2454–2460 [View Article][PubMed]
     [Google Scholar]
  33. Randow F, Sale JE. Retroviral transduction of DT40. Subcell Biochem 2006; 40:383–386[PubMed]
     [Google Scholar]
  34. Panda D, Das A, Dinh PX, Subramaniam S, Nayak D et al. RNAi screening reveals requirement for host cell secretory pathway in infection by diverse families of negative-strand RNA viruses. Proc Natl Acad Sci USA 2011; 108:19036–19041 [View Article][PubMed]
     [Google Scholar]
  35. Rojek JM, Kunz S. Cell entry by human pathogenic arenaviruses. Cell Microbiol 2008; 10:828–835 [View Article][PubMed]
     [Google Scholar]
  36. Pasqual G, Rojek JM, Masin M, Chatton JY, Kunz S. Old world arenaviruses enter the host cell via the multivesicular body and depend on the endosomal sorting complex required for transport. PLoS Pathog 2011; 7:e1002232 [View Article][PubMed]
     [Google Scholar]
  37. Quirin K, Eschli B, Scheu I, Poort L, Kartenbeck J et al. Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 2008; 378:21–33 [View Article][PubMed]
     [Google Scholar]
  38. Amorim MJ, Bruce EA, Read EK, Foeglein A, Mahen R et al. A Rab11- and microtubule-dependent mechanism for cytoplasmic transport of influenza A virus viral RNA. J Virol 2011; 85:4143–4156 [View Article][PubMed]
     [Google Scholar]
  39. Momose F, Sekimoto T, Ohkura T, Jo S, Kawaguchi A et al. Apical transport of influenza A virus ribonucleoprotein requires Rab11-positive recycling endosome. PLoS One 2011; 6:e21123 [View Article][PubMed]
     [Google Scholar]
  40. Eisfeld AJ, Kawakami E, Watanabe T, Neumann G, Kawaoka Y. RAB11A is essential for transport of the influenza virus genome to the plasma membrane. J Virol 2011; 85:6117–6126 [View Article][PubMed]
     [Google Scholar]
  41. Chou YY, Heaton NS, Gao Q, Palese P, Singer RH et al. Colocalization of different influenza viral RNA segments in the cytoplasm before viral budding as shown by single-molecule sensitivity FISH analysis. PLoS Pathog 2013; 9:e1003358 [View Article][PubMed]
     [Google Scholar]
  42. Lakdawala SS, Wu Y, Wawrzusin P, Kabat J, Broadbent AJ et al. Influenza a virus assembly intermediates fuse in the cytoplasm. PLoS Pathog 2014; 10:e1003971 [View Article][PubMed]
     [Google Scholar]
  43. Bruce EA, Digard P, Stuart AD. The Rab11 pathway is required for influenza A virus budding and filament formation. J Virol 2010; 84:5848–5859 [View Article][PubMed]
     [Google Scholar]
  44. Dansako H, Hiramoto H, Ikeda M, Wakita T, Kato N. Rab18 is required for viral assembly of hepatitis C virus through trafficking of the core protein to lipid droplets. Virology 2014; 462-463:166–174 [View Article][PubMed]
     [Google Scholar]
  45. Salloum S, Wang H, Ferguson C, Parton RG, Tai AW. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog 2013; 9:e1003513 [View Article][PubMed]
     [Google Scholar]
  46. Goñi SE, Borio CS, Romano FB, Rota RP, Pilloff MG et al. Expression and purification of Z protein from Junín virus. J Biomed Biotechnol 2010; 2010:1–14 [View Article][PubMed]
     [Google Scholar]
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The use of novel epitope-tagged arenaviruses reveals that Rab5c-positive endosomal membranes are targeted by the LCMV matrix protein
J. Gen. Virol. 99, 187 (2018); https://doi.org/10.1099/jgv.0.001004
/content/journal/jgv/10.1099/jgv.0.001004
/content/journal/jgv/10.1099/jgv.0.001004
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