Uncovering viral protein-protein interactions and their role in arenavirus life cycle

Viruses

Volumn 4, Issue 9, 2012, Pages 1651-1667

  Loureiro, Maria Eugenia ^a   D'Antuono, Alejandra ^a   Macleod, Jesica M Levingston ^b   López, Nora ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Protein protein interaction; Tacaribe virus; Viral RNA synthesis; Virus assembly

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; FATTY ACID BINDING PROTEIN; VIRUS NUCLEOPROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARENAVIRUS; ENZYME ACTIVE SITE; LIFE CYCLE; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW; RNA SYNTHESIS; VIRION; VIRUS ASSEMBLY; VIRUS EXPRESSION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS REPLICATION;

ARENAVIRUS; PROTEIN INTERACTION MAPS; VIRAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

ARENAVIRIDAE; ARENAVIRUS; TACARIBE VIRUS;

EID: 84866992574     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4091651     Document Type: Review

References (82)

1. Geisbert, T.W.; Jahrling, P.B. Exotic emerging viral diseases: progress and challenges. Nat. Med. 2004, 10, S110-121.
2. García, C.; Sepulveda, C.; Damonte, E.B. Novel therapeutic targets for arenavirus hemorrhagic fevers. Future Virology 2011, 6, 27-44.
3. Charrel, R.N.; de Lamballerie, X.; Emonet, S. Phylogeny of the genus Arenavirus. Curr. Opin. Microbiol. 2008, 11, 362-368.
4. Martínez-Peralta, L.A.; Coto, C.E.; Weissenbacher, M.C. The Tacaribe complex: the close relationship between a pathogenic (Junin) anda nonpathogenic (Tacaribe) arenavirus. In The Arenaviridae; Salvato, M.S. (ed.); Plenum Press: New York, N. Y, USA, 1993, pp. 281-296.
5. Franze-Fernández, M.T.; Iapalucci, S.; López, N.; Rossi, C. Subgenomic RNAs of Tacaribe virus. In The Arenaviridae; Salvato, M.S. (ed.); Plenum Press: New York, N. Y, USA. 1993, pp. 113-132
6. Buchmeier, M.J.; de La Torre, J.C.; Peters, C.J. Arenaviridae: The viruses and their replication. In Fields Virology, 5th ed.; Knipe, D.M. et al. (ed.); Lippincott Williams & Wilkins, Philadelphia, PA, U.S.A., 2007; Volume 2; pp. 1791-1828.
7. Kolakofsky, D.; Garcin, D. The unusual mechanism of arenavirus RNA synthesis. In The Arenaviridae; M. S. Salvato (ed.); Plenum Press: New York, N. Y, U.S.A., 1993, pp. 103-112
8. Lopez, N.; Franze-Fernandez, M.T. A single stem-loop structure in Tacaribe arenavirus intergenic region is essential for transcription termination but is not required for a correct initiation of transcription and replication. Virus Res. 2007, 124, 237-244.
9. Iapalucci, S.; Lopez, N.; Franze-Fernandez, M.T. The 3' end termini of the Tacaribe arenavirus subgenomic RNAs. Virology 1991, 182, 269-278.
10. Hass, M.; Westerkofsky, M.; Muller, S.; Becker-Ziaja, B.; Busch, C.; Gunther, S. Mutational analysis of the Lassa virus promoter. J. Virol. 2006, 80, 12414-12419.
11. Perez, M.; de la Torre, J.C. Characterization of the genomic promoter of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 2003, 77, 1184-1194.
12. Kranzusch, P.J.; Schenk, A.D.; Rahmeh, A.A.; Radoshitzky, S.R.; Bavari, S.; Walz, T.; Whelan, S.P. Assembly of a functional Machupo virus polymerase complex. Proc. Natl. Acad. Sci. U S A 2010, 107, 20069-20074.
13. Iapalucci, S.; Lopez, N.; Rey, O.; Zakin, M.M.; Cohen, G.N.; Franze-Fernandez, M.T. The 5' region of Tacaribe virus L RNA encodes a protein with a potential metal binding domain. Virology 1989, 173, 357-361.
14. Salvato, M.S.; Shimomaye, E.M. The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 1989, 173, 1-10.
15. Borden, K.L. RING domains: master builders of molecular scaffolds? J. Mol. Biol. 2000, 295, 1103-1112.
16. Campbell Dwyer, E.J.; Lai, H.; MacDonald, R.C.; Salvato, M.S.; Borden, K.L. The lymphocytic choriomeningitis virus RING protein Z associates with eukaryotic initiation factor 4E and selectively represses translation in a RING-dependent manner. J. Virol. 2000, 74, 3293-3300.
17. Kentsis, A.; Dwyer, E.C.; Perez, J.M.; Sharma, M.; Chen, A.; Pan, Z.Q.; Borden, K.L. The RING domains of the promyelocytic leukemia protein PML and the arenaviral protein Z repress translation by directly inhibiting translation initiation factor eIF4E. J. Mol. Biol. 2001, 312, 609-623.
18. Volpon, L.; Osborne, M.J.; Capul, A.A.; de la Torre, J.C.; Borden, K.L. Structural characterization of the Z RING-eIF4E complex reveals a distinct mode of control for eIF4E. Proc. Natl. Acad. Sci. U S A 2010, 107, 5441-5446.
19. Borden, K.L.; Campbell Dwyer, E.J.; Salvato, M.S. An arenavirus RING (zinc-binding) protein binds the oncoprotein promyelocyte leukemia protein (PML) and relocates PML nuclear bodies to the cytoplasm. J. Virol. 1998, 72, 758-766.
20. Borden, K.L.; Campbell Dwyer, E.J.; Carlile, G.W.; Djavani, M.; Salvato, M.S. Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J. Virol. 1998, 72, 3819-3826.
21. Topcu, Z.; Mack, D.L.; Hromas, R.A.; Borden, K.L. The promyelocytic leukemia protein PML interacts with the proline-rich homeodomain protein PRH: a RING may link hematopoiesis and growth control. Oncogene 1999, 18, 7091-7100.
22. Djavani, M.; Topisirovic, I.; Zapata, J.C.; Sadowska, M.; Yang, Y.; Rodas, J.; Lukashevich, I.S.; Bogue, C.W.; Pauza, C.D.; Borden, K.L.; Salvato, M.S. The proline-rich homeodomain (PRH/HEX) protein is down-regulated in liver during infection with lymphocytic choriomeningitis virus. J. Virol. 2005, 79, 2461-2473.
23. Fan, L.; Briese, T.; Lipkin, W.I. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J. Virol. 2010, 84, 1785-1791.
24. Salvato, M.S. Molecular biology of the prototype arenavirus, lymphocytic choriomeningitis virus. In The Arenaviridae; Salvato, M.S. (ed.); Plenum Press: New York, N. Y, U.S.A., 1993, pp. 133-156.
25. Iapalucci, S.; Chernavsky, A.; Rossi, C.; Burgin, M.J.; Franze-Fernandez, M.T. Tacaribe virus gene expression in cytopathic and non-cytopathic infections. Virology 1994, 200, 613-622.
26. Lopez, N.; Jacamo, R.; Franze-Fernandez, M.T. Transcription and RNA replication of Tacaribe virus genome and antigenome analogs require N and L proteins: Z protein is an inhibitor of these processes. J. Virol. 2001, 75, 12241-12251.
27. Lee, K.J.; Novella, I.S.; Teng, M.N.; Oldstone, M.B.; de La Torre, J.C., NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs. J. Virol. 2000, 74, 3470-3477.
28. Cornu, T.I.; de la Torre, J.C. RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J. Virol. 2001, 75, 9415-9426.
29. Hass, M.; Golnitz, U.; Muller, S.; Becker-Ziaja, B.; Gunther, S. Replicon system for Lassa virus. J. Virol. 2004, 78, 13793-13803.
30. Kranzusch, P.J.; Whelan, S.P. Arenavirus Z protein controls viral RNA synthesis by locking a polymerase-promoter complex. Proc. Natl. Acad. Sci. U S A 2011, 108, 19743-19748.
31. Jacamo, R.; Lopez, N.; Wilda, M.; Franze-Fernandez, M.T. Tacaribe virus Z protein interacts with the L polymerase protein to inhibit viral RNA synthesis. J. Virol. 2003, 77, 10383-10393.
32. Loureiro, M.E.; Wilda, M.; Levingston Macleod, J.M.; D'Antuono, A.; Foscaldi, S.; Marino Buslje, C.; Lopez, N. Molecular determinants of arenavirus Z protein homo-oligomerization and L polymerase binding. J. Virol. 2011, 85, 12304-12314.
33. Muller, R.; Poch, O.; Delarue, M.; Bishop, D.H.; Bouloy, M. Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J. Gen. Virol. 1994, 75, 1345-1352.
34. Ferrer-Orta, C.; Arias, A.; Escarmis, C.; Verdaguer, N. A comparison of viral RNA-dependent RNA polymerases. Curr. Opin. Struct. Biol. 2006, 16, 27-34.
35. Hass, M.; Lelke, M.; Busch, C.; Becker-Ziaja, B.; Gunther, S. Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome. J. Virol. 2008, 82, 10207-10217.
36. Vieth, S.; Torda, A.E.; Asper, M.; Schmitz, H.; Gunther, S. Sequence analysis of L RNA of Lassa virus. Virology 2004, 318, 153-168.
37. Brunotte, L.; Lelke, M.; Hass, M.; Kleinsteuber, K.; Becker-Ziaja, B.; Gunther, S. Domain structure of Lassa virus L protein. J. Virol. 2011, 85, 324-333.
38. Morin, B.; Coutard, B.; Lelke, M.; Ferron, F.; Kerber, R.; Jamal, S.; Frangeul, A.; Baronti, C.; Charrel, R.; de Lamballerie, X.; Vonrhein, C.; Lescar, J.; Bricogne, G.; Gunther, S.; Canard, B. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog. 2010, 6, e1001038.
39. Lelke, M.; Brunotte, L.; Busch, C.; Gunther, S. An N-terminal region of Lassa virus L protein plays a critical role in transcription but not replication of the virus genome. J. Virol. 2010, 84, 1934-1944.
40. Wilda, M.; Lopez, N.; Casabona, J.C.; Franze-Fernandez, M.T. Mapping of the Tacaribe arenavirus Z-protein binding sites on the L protein identified both amino acids within the putative polymerase domain and a region at the N terminus of L that are critically involved in binding. J. Virol. 2008, 82, 11454-11460.
41. Sanchez, A.B.; de la Torre, J.C. Genetic and biochemical evidence for an oligomeric structure of the functional L polymerase of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 2005, 79, 7262-7268.
42. Kerber, R.; Rieger, T.; Busch, C.; Flatz, L.; Pinschewer, D.D.; Kummerer, B.M.; Gunther, S. Cross-species analysis of the replication complex of Old World arenaviruses reveals two Nucleoprotein sites involved in L protein function. J. Virol. 2010, 85, 12518-12528.
43. Levingston Macleod, J.M.; D'Antuono, A.; Loureiro, M.E.; Casabona, J.C.; Gomez, G.A.; Lopez, N. Identification of two functional domains within the arenavirus nucleoprotein. J. Virol. 2011, 85, 2012-2023.
44. Ortiz-Riaño, E.; Cheng, B.Y.; de la Torre, J.C.; Martinez-Sobrido, L. Self-association of lymphocytic choriomeningitis virus nucleoprotein is mediated by its N-terminal region and is not required for its anti-interferon function. J. Virol. 2012, 86, 3307-3317.
45. Qi, X.; Lan, S.; Wang, W.; Schelde, L.M.; Dong, H.; Wallat, G.D.; Ly, H.; Liang, Y.; Dong, C. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 2010, 468, 779-783.
46. Brunotte, L.; Kerber, R.; Shang, W.; Hauer, F.; Hass, M.; Gabriel, M.; Lelke, M.; Busch, C.; Stark, H.; Svergun, D.I.; Betzel, C.; Perbandt, M.; Günther, S. Structure of the Lassa virus nucleoprotein revealed by X-ray crystallography, small-angle X-ray scattering, and electron microscopy. J. Biol. Chem. 2011, 286, 38748-38756.
47. Hastie, K.M.; Liu, T.; Li, S.; King, L.B.; Ngo, N.; Zandonatti, M.A.; Woods, V.L., Jr.; de la Torre, J.C.; Saphire, E.O. Crystal structure of the Lassa virus nucleoprotein-RNA complex reveals a gating mechanism for RNA binding. Proc. Natl. Acad. Sci. U S A 2011, 108, 19365-19370.
48. Albertini, A.A.; Schoehn, G.; Weissenhorn, W.; Ruigrok, R.W. Structural aspects of rabies virus replication. Cell. Mol. Life. Sci. 2008, 65, 282-294.
49. Ruigrok, R.W.; Crepin, T.; Kolakofsky, D. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 2012, 14, 504-510.
50. Ferron, F.; Li, Z.; Danek, E.I.; Luo, D.; Wong, Y.; Coutard, B.; Lantez, V.; Charrel, R.; Canard, B.; Walz, T.; Lescar, J. The hexamer structure of Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog. 2011, 7, e1002030.
51. Salvato, M.S.; Schweighofer, K.J.; Burns, J.; Shimomaye, E.M. Biochemical and immunological evidence that the 11 kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res. 1992, 22, 185-198.
52. Perez, M.; Craven, R.C.; de la Torre, J.C. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. U S A 2003, 100, 12978-12983.
53. Strecker, T.; Eichler, R.; Meulen, J.; Weissenhorn, W.; Dieter Klenk, H.; Garten, W.; Lenz, O. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J. Virol. 2003, 77, 10700-10705.
54. Urata, S.; Noda, T.; Kawaoka, Y.; Yokosawa, H.; Yasuda, J. Cellular factors required for Lassa virus budding. J. Virol. 2006, 80, 4191-4195.
55. Strecker, T.; Maisa, A.; Daffis, S.; Eichler, R.; Lenz, O.; Garten, W. The role of myristoylation in the membrane association of the Lassa virus matrix protein Z. Virol. J. 2006, 3, 93.
56. Perez, M.; Greenwald, D.L.; de la Torre, J.C. Myristoylation of the RING finger Z protein is essential for arenavirus budding. J. Virol. 2004, 78, 11443-11448.
57. Eichler, R.; Strecker, T.; Kolesnikova, L.; ter Meulen, J.; Weissenhorn, W.; Becker, S.; Klenk, H.D.; Garten, W.; Lenz, O. 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.
58. Casabona, J.C.; Levingston Macleod, J.M.; Loureiro, M.E.; Gomez, G.A.; Lopez, N. The RING domain and the L79 residue of Z protein are involved in both the rescue of nucleocapsids and the incorporation of glycoproteins into infectious chimeric arenavirus-like particles. J. Virol. 2009, 83, 7029-7039.
59. Levingston Macleod, J.M.; Casabona, J.C.; Gómez, G.; Loureiro, E.; Wilda, M.; López, N. Mapping of interacting domains between the nucleoprotein and Z matrix protein of New World Arenaviruses. XIV International Conference on Negative Strand Viruses. Brugge, Belgium, June 20-25, 2010; Abstract 80, pp. 87.
60. Capul, A.A.; de la Torre, J.C.; Buchmeier, M.J. Conserved residues in Lassa fever virus Z protein modulate viral infectivity at the level of the ribonucleoprotein. J. Virol. 2011, 85, 3172-3178.
61. Urata, S.; Yasuda, J.; de la Torre, J.C. The Z protein of the New World arenavirus Tacaribe virus has bona fide budding activity that does not depend on known late domain motifs. J. Virol. 2009, 83, 12651-12655.
62. 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.
63. Shtanko, O.; Watanabe, S.; Jasenosky, L.D.; Watanabe, T.; Kawaoka, Y. ALIX/AIP1 is required for NP incorporation into Mopeia virus Z-induced virus-like particles. J. Virol. 2011, 85, 3631-3641.
64. Ortiz-Riaño, E.; Cheng, B.Y.; de la Torre, J.C.; Martinez-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.
65. Shtanko, O.; Imai, M.; Goto, H.; Lukashevich, I.S.; Neumann, G.; Watanabe, T.; Kawaoka, Y. 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.
66. Nunberg, J.H.; York, J. The curious case of arenavirus entry, and its inhibition. Viruses 2012, 4, 83-101.
67. Mittler, E.; Kolesnikova, L.; Strecker, T.; Garten, W.; Becker, S. Role of the transmembrane domain of Marburg virus surface protein GP in assembly of the viral envelope. J. Virol. 2007, 81, 3942-3948.
68. Checkley, M.A.; Luttge, B.G.; Freed, E.O. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J. Mol. Biol. 2011, 410, 582-608.
69. Capul, A.A.; Perez, M.; Burke, E.; Kunz, S.; Buchmeier, M.J.; de la Torre, J.C. Arenavirus Z-glycoprotein association requires Z myristoylation but not functional RING or late domains. J. Virol. 2007, 81, 9451-9460.
70. Schlie, K.; Maisa, A.; Freiberg, F.; Groseth, A.; Strecker, T.; Garten, W. Viral protein determinants of Lassa virus entry and release from polarized epithelial cells. J. Virol. 2010, 84, 3178-3188.
71. Davis, M.R.; Jiang, J.; Zhou, J.; Freed, E.O.; Aiken, C. A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J. Virol. 2006, 80, 2405-2417.
72. Okumura, A.; Harty, R.N. Rabies virus assembly and budding. Adv. Virus Res. 2011, 79, 23-32.
73. Hartlieb, B.; Weissenhorn, W. Filovirus assembly and budding. Virology 2006, 344, 64-70.
74. Kentsis, A.; Gordon, R.E.; Borden, K.L. Self-assembly properties of a model RING domain. Proc. Natl. Acad. Sci. U S A 2002, 99, 667-672.
75. Cornu, T.I.; Feldmann, H.; de la Torre, J.C. Cells expressing the RING finger Z protein are resistant to arenavirus infection. J. Virol. 2004, 78, 2979-2983.
76. Parisi, G.; Echave, J.; Ghiringhelli, D.; Romanowski, V. Computational characterisation of potential RNA-binding sites in arenavirus nucleocapsid proteins. Virus Genes 1996, 13, 247-254.
77. Urata, S.; de la Torre, J.C. Arenavirus budding. Adv. Virol. 2011, 2011, 180326.
78. Lan, S.; McLay Schelde, L.; Wang, J.; Kumar, N.; Ly, H.; Liang, Y. Development of infectious clones for virulent and avirulent Pichinde viruses: a model virus to study arenavirus-induced hemorrhagic fevers. J. Virol. 2009, 83, 6357-6362.
79. Albariño, C.G.; Bergeron, E.; Erickson, B.R.; Khristova, M.L.; Rollin, P.E.; Nichol, S.T. Efficient reverse genetics generation of infectious Junin viruses differing in glycoprotein processing. J. Virol. 2009, 83, 5606-5614.
80. Flatz, L.; Bergthaler, A.; de la Torre, J.C.; Pinschewer, D.D. Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc. Natl. Acad. Sci. U S A 2006, 103, 4663-4668.
81. Sanchez, A.B.; de la Torre, J.C. Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 2006, 350, 370-380.
82. Emonet, S.F.; Seregin, A.V.; Yun, N.E.; Poussard, A.L.; Walker, A.G.; de la Torre, J.C.; Paessler, S. 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.