LCMV Glycosylation Modulates Viral Fitness and Cell Tropism

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Bonhomme, Cyrille J ^a   Knopp, Kristeene A ^a   Bederka, Lydia H ^a   Angelini, Megan M ^a   Buchmeier, Michael J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL ASSAY; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; EPITHELIUM CELL; GLYCOSYLATION; HUMAN; HUMAN CELL; LIFE CYCLE STAGE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; REPRODUCTIVE FITNESS; VIRAL TROPISM; VIRUS ATTACHMENT; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CELL LINE; CELLS, CULTURED; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGES; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; MUTATION; NEURONS; POLYSACCHARIDES; TROPISM; VIRAL PROTEINS;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

EID: 84872156367     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053273     Document Type: Article

References (65)

1. Lecompte E, ter Meulen J, Emonet S, Daffis S, Charrel RN, (2007) Genetic identification of Kodoko virus, a novel arenavirus of the African pigmy mouse (Mus Nannomys minutoides) in West Africa. Virology 364: 178-183.
2. Delgado S, Erickson BR, Agudo R, Blair PJ, Vallejo E, et al. (2008) Chapare virus, a newly discovered arenavirus isolated from a fatal hemorrhagic fever case in Bolivia. PLoS Pathog 4: e1000047.
3. Briese T, Paweska JT, McMullan LK, Hutchison SK, Street C, et al. (2009) Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 5: e1000455.
4. Salvato MS CJ, Buchmeier MJ, Charrel RN, Gonzalez JP, et al. (2005) Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press: 725.733.
5. Johnson KM, Wiebenga NH, Mackenzie RB, Kuns ML, Tauraso NM, et al. (1965) Virus Isolations from Human Cases of Hemorrhagic Fever in Bolivia. Proc Soc Exp Biol Med 118: 113-118.
6. Parodi AS, Greenway DJ, Rugiero HR, Frigerio M, De La Barrera JM, et al. (1958) [Concerning the epidemic outbreak in Junin]. Dia Med 30: 2300-2301.
7. Parodi AS, Rugiero HR, Greenway DJ, Mettler N, Martinez A, et al. (1959) [Isolation of the Junin virus (epidemic hemorrhagic fever) from the mites of the epidemic area (Echinolaelaps echidninus, Barlese)]. Prensa Med Argent 46: 2242-2244.
8. Lisieux T, Coimbra M, Nassar ES, Burattini MN, de Souza LT, et al. (1994) New arenavirus isolated in Brazil. Lancet 343: 391-392.
9. Tesh RB, Jahrling PB, Salas R, Shope RE, (1994) Description of Guanarito virus (Arenaviridae: Arenavirus), the etiologic agent of Venezuelan hemorrhagic fever. Am J Trop Med Hyg 50: 452-459.
10. Buckley SM, Casals J, (1970) Lassa fever, a new virus disease of man from West Africa. 3. Isolation and characterization of the virus. Am J Trop Med Hyg 19: 680-691.
11. Buckley SM, Casals J, Downs WG, (1970) Isolation and antigenic characterization of Lassa virus. Nature 227: 174.
12. Charrel RN, de Lamballerie X, Emonet S, (2008) Phylogeny of the genus Arenavirus. Curr Opin Microbiol 11: 362-368.
13. Bonthius DJ, Wright R, Tseng B, Barton L, Marco E, et al. (2007) Congenital lymphocytic choriomeningitis virus infection: spectrum of disease. Ann Neurol 62: 347-355.
14. Barton LL, Hyndman NJ, (2000) Lymphocytic choriomeningitis virus: reemerging central nervous system pathogen. Pediatrics 105: E35.
15. Amman BR, Pavlin BI, Albarino CG, Comer JA, Erickson BR, et al. (2007) Pet rodents and fatal lymphocytic choriomeningitis in transplant patients. Emerg Infect Dis 13: 719-725.
16. Fischer SA, Graham MB, Kuehnert MJ, Kotton CN, Srinivasan A, et al. (2006) Transmission of lymphocytic choriomeningitis virus by organ transplantation. N Engl J Med 354: 2235-2249.
17. Deibel R, Woodall JP, Decher WJ, Schryver GD, (1975) Lymphocytic choriomeningitis virus in man. Serologic evidence of association with pet hamsters. JAMA 232: 501-504.
18. Charrel RN, Retornaz K, Emonet S, Noel G, Chaumoitre K, et al. (2006) Acquired hydrocephalus caused by a variant lymphocytic choriomeningitis virus. Arch Intern Med 166: 2044-2046.
19. Emonet S, Retornaz K, Gonzalez JP, de Lamballerie X, Charrel RN, (2007) Mouse-to-human transmission of variant lymphocytic choriomeningitis virus. Emerg Infect Dis 13: 472-475.
20. Sevilla N, de la Torre JC, (2006) Arenavirus diversity and evolution: quasispecies in vivo. Curr Top Microbiol Immunol 299: 315-335.
21. Paweska JT, Sewlall NH, Ksiazek TG, Blumberg LH, Hale MJ, et al. (2009) Nosocomial outbreak of novel arenavirus infection, southern Africa. Emerg Infect Dis 15: 1598-1602.
22. Palacios G, Druce J, Du L, Tran T, Birch C, et al. (2008) A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med 358: 991-998.
23. Neuman BW, Adair BD, Burns JW, Milligan RA, Buchmeier MJ, et al. (2005) Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J Virol 79: 3822-3830.
24. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, et al. (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282: 2079-2081.
25. Borrow P, Oldstone MB, (1994) Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198: 1-9.
26. Di Simone C, Zandonatti MA, Buchmeier MJ, (1994) Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology 198: 455-465.
27. Di Simone C, Buchmeier MJ, (1995) Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209: 3-9.
28. York J, Dai D, Amberg SM, Nunberg JH, (2008) pH-induced activation of arenavirus membrane fusion is antagonized by small-molecule inhibitors. J Virol 82: 10932-10939.
29. Klewitz C, Klenk HD, ter Meulen J, (2007) Amino acids from both N-terminal hydrophobic regions of the Lassa virus envelope glycoprotein GP-2 are critical for pH-dependent membrane fusion and infectivity. J Gen Virol 88: 2320-2328.
30. Beyer WR, Popplau D, Garten W, von Laer D, Lenz O, (2003) Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J Virol 77: 2866-2872.
31. Wright KE, Spiro RC, Burns JW, Buchmeier MJ, (1990) Post-translational processing of the glycoproteins of lymphocytic choriomeningitis virus. Virology 177: 175-183.
32. Burns JW, Buchmeier MJ, (1991) Protein-protein interactions in lymphocytic choriomeningitis virus. Virology 183: 620-629.
33. Radoshitzky SR, Longobardi LE, Kuhn JH, Retterer C, Dong L,et al. Machupo virus glycoprotein determinants for human transferrin receptor 1 binding and cell entry. PLoS One 6: e21398.
34. Agnihothram SS, Dancho B, Grant KW, Grimes ML, Lyles DS, et al. (2009) Assembly of arenavirus envelope glycoprotein GPC in detergent-soluble membrane microdomains. J Virol 83: 9890-9900.
35. Helenius A, Aebi M, (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369.
36. Wyss DF, Wagner G, (1996) The structural role of sugars in glycoproteins. Curr Opin Biotechnol 7: 409-416.
37. Wright KE, Salvato MS, Buchmeier MJ, (1989) Neutralizing epitopes of lymphocytic choriomeningitis virus are conformational and require both glycosylation and disulfide bonds for expression. Virology 171: 417-426.
38. Sugawara K, Kitame F, Nishimura H, Nakamura K, (1988) Operational and topological analyses of antigenic sites on influenza C virus glycoprotein and their dependence on glycosylation. J Gen Virol 69 (Pt 3): 537-547.
39. Quinones-Kochs MI, Buonocore L, Rose JK, (2002) Role of N-linked glycans in a human immunodeficiency virus envelope glycoprotein: effects on protein function and the neutralizing antibody response. J Virol 76: 4199-4211.
40. Bonhomme CJ, Capul AA, Lauron EJ, Bederka LH, Knopp KA, et al. (2011) Glycosylation modulates arenavirus glycoprotein expression and function. Virology 409: 223-233.
41. Emonet SE, Urata S, de la Torre JC, (2011) Arenavirus reverse genetics: new approaches for the investigation of arenavirus biology and development of antiviral strategies. Virology 411: 416-425.
42. Hirano N, Fujiwara K, Hino S, Matumoto M, (1974) Replication and plaque formation of mouse hepatitis virus (MHV-2) in mouse cell line DBT culture. Arch Gesamte Virusforsch 44: 298-302.
43. Benoit ME, Tenner AJ Complement protein C1q-mediated neuroprotection is correlated with regulation of neuronal gene and microRNA expression. J Neurosci 31: 3459-3469.
44. Morgado P, Ong YC, Boothroyd JC, Lodoen MB Toxoplasma gondii induces B7-2 expression through activation of JNK signal transduction. Infect Immun 79: 4401-4412.
45. Sanchez AB, de la Torre JC, (2006) Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 350: 370-380.
46. Flatz L, Bergthaler A, de la Torre JC, Pinschewer DD, (2006) Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc Natl Acad Sci U S A 103: 4663-4668.
47. Battegay M, Cooper S, Althage A, Banziger J, Hengartner H, et al. (1991) Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J Virol Methods 33: 191-198.
48. Bowden TA, Crispin M, Graham SC, Harvey DJ, Grimes JM, et al. (2009) Unusual molecular architecture of the machupo virus attachment glycoprotein. J Virol 83: 8259-8265.
49. Abraham J, Corbett KD, Farzan M, Choe H, Harrison SC, (2010) Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol 17: 438-444.
50. Igonet S, Vaney MC, Vonhrein C, Bricogne G, Stura EA,et al. X-ray structure of the arenavirus glycoprotein GP2 in its postfusion hairpin conformation. Proc Natl Acad Sci U S A 108: 19967-19972.
51. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB, (1984) Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 160: 521-540.
52. Ahmed R, Oldstone MB, (1988) Organ-specific selection of viral variants during chronic infection. J Exp Med 167: 1719-1724.
53. Evans CF, Borrow P, de la Torre JC, Oldstone MB, (1994) Virus-induced immunosuppression: kinetic analysis of the selection of a mutation associated with viral persistence. J Virol 68: 7367-7373.
54. Sullivan BM, Emonet SF, Welch MJ, Lee AM, Campbell KP, et al. (2011) Point mutation in the glycoprotein of lymphocytic choriomeningitis virus is necessary for receptor binding, dendritic cell infection, and long-term persistence. Proc Natl Acad Sci U S A 108: 2969-2974.
55. Petrescu AJ, Milac AL, Petrescu SM, Dwek RA, Wormald MR, (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14: 103-114.
56. Eschli B, Zellweger RM, Wepf A, Lang KS, Quirin K, et al. (2007) Early antibodies specific for the neutralizing epitope on the receptor binding subunit of the lymphocytic choriomeningitis virus glycoprotein fail to neutralize the virus. J Virol 81: 11650-11657.
57. Welsh RM, O'Connell CM, Pfau CJ, (1972) Properties of defective lymphocytic choriomeningitis virus. J Gen Virol 17: 355-359.
58. van Opijnen T, Berkhout B, (2005) The host environment drives HIV-1 fitness. Rev Med Virol 15: 219-233.
59. Salvato M, Borrow P, Shimomaye E, Oldstone MB, (1991) Molecular basis of viral persistence: a single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic T-lymphocyte response and establishment of persistence. J Virol 65: 1863-1869.
60. Francois KO, Balzarini J, (2011) The highly conserved glycan at asparagine 260 of HIV-1 gp120 is indispensable for viral entry. J Biol Chem 286: 42900-42910.
61. Auwerx J, Francois KO, Covens K, Van Laethem K, Balzarini J, (2008) Glycan deletions in the HIV-1 gp120 V1/V2 domain compromise viral infectivity, sensitize the mutant virus strains to carbohydrate-binding agents and represent a specific target for therapeutic intervention. Virology 382: 10-19.
62. Balzarini J, (2007) Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat Rev Microbiol 5: 583-597.
63. Knoper RC, Ferrarone J, Yan Y, Lafont BA, Kozak CA, (2009) Removal of either N-glycan site from the envelope receptor binding domain of Moloney and Friend but not AKV mouse ecotropic gammaretroviruses alters receptor usage. Virology 391: 232-239.
64. Maisner A, Alvarez J, Liszewski MK, Atkinson DJ, Atkinson JP, et al. (1996) The N-glycan of the SCR 2 region is essential for membrane cofactor protein (CD46) to function as a measles virus receptor. J Virol 70: 4973-4977.
65. Melanson VR, Iorio RM, (2006) Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion. J Virol 80: 623-633.