Production of CXC and CC Chemokines by Human Antigen-Presenting Cells in Response to Lassa Virus or Closely Related Immunogenic Viruses, and in Cynomolgus Monkeys with Lassa Fever

PLoS Neglected Tropical Diseases

Volumn 8, Issue 1, 2014, Pages 37-

  Pannetier, Delphine ^a,b   Reynard, Stéphanie ^a,c   Russier, Marion ^a,c   Carnec, Xavier ^d   Baize, Sylvain ^a,c  

^a Institut Pasteur   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE LYON   (France)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; BETA CHEMOKINE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 3; RANTES; NUCLEOPROTEIN; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFECTION CONTROL; LASSA FEVER; LASSA VIRUS; MACACA FASCICULARIS; MALE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS NEUTRALIZATION; ANIMAL; ANIMAL DISEASE; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PRIMATE DISEASE; SECRETION (PROCESS);

ANIMALS; ANTIGEN-PRESENTING CELLS; CHEMOKINES, CC; CHEMOKINES, CXC; HUMANS; IMMUNE EVASION; LASSA FEVER; LASSA VIRUS; MALE; NUCLEOPROTEINS; PRIMATE DISEASES; VIRAL PROTEINS;

EID: 84893734414     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002637     Document Type: Article

References (64)

1. McCormick JB, Webb PA, Krebs JW, Johnson KM, Smith ES, (1987) A prospective study of the epidemiology and ecology of Lassa fever. J Infect Dis 155: 437-444.
2. McCormick JB, King IJ, Webb PA, Scribner CL, Craven RB, et al. (1986) Lassa Fever. Effective therapy with ribavirin. New Eng J Med 314: 20-26.
3. Sogoba N, Feldmann H, Safronetz D, (2012) Lassa Fever in West Africa: Evidence for an Expanded Region of Endemicity. Zoonoses and Public Health 59: 43-47.
4. Lenz O, ter Meulen J, Klenk H-D, Seidah NG, Garten W, (2001) The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc Natl Acad Sci USA 98: 12701-12705.
5. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, et al. (1998) Identification of α-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282: 2079-2081.
6. Buchmeier MJ, de la Torre J-C, Peters CJ (2007) Arenaviridae: the viruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, et al., editors. Fields virology. 5th ed. Philadelphia: Lippincott Williams & Wilkins. pp. 1791-1827.
7. Cornu TI, de la Torre JC, (2001) RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J Virol 75: 9415-9426.
8. Perez M, Craven RC, de la Torre JC, (2003) The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci USA 100: 12978-12983.
9. Strecker T, Eichler R, ter Meulen J, Weissenhorn W, Klenk H-D, et al. (2003) Lassa virus Z protein is a matrix protein sufficient for the release of virus-like particles. J Virol 77: 10700-10705.
10. Baize S, Kaplon J, Faure C, Pannetier D, Georges-Courbot MC, et al. (2004) Lassa virus infection of dendritic cells and macrophages is productive but fails to activate cells. J Immunol 172: 2861-2869.
11. Hensley L, Smith M, Geisbert J, Fritz E, Daddario-DiCaprio K, et al. (2011) Pathogenesis of lassa fever in cynomolgus macaques. Virology Journal 8: 205.
12. Mahanty S, Hutchinson K, Agarwal S, Mcrae M, Rollin PE, et al. (2003) Cutting Edge: impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J Immunol 170: 2797-2801.
13. Walker DH, Johnson KM, Lange JV, Gardner JJ, Kiley MP, et al. (1982) Experimental infection of Rhesus monkeys with Lassa virus and a closely related Arenavirus, Mozambique virus. J Infect Dis 146: 360-368.
14. Walker DH, McCormick JB, Johnson KM, Webb PA, Komba-Kono G, et al. (1982) Pathologic and virologic study of fatal Lassa fever in man. Am J Pathol 107: 349-356.
15. Johnson KM, McCormick JB, Webb PA, Smith ES, Elliott LH, et al. (1987) Clinical virology of Lassa fever in hospitalized patients. J Infect Dis 155: 456-463.
16. Pinschewer DD, Perez M, Jeetendra E, Bächi T, Horvath E, et al. (2004) Kinetics of protective antibodies are determined by the viral surface antigen. J Clin Invest 114: 988-993.
17. Baize S, Marianneau P, Loth P, Reynard S, Journeaux A, et al. (2009) Early and strong immune responses are associated with control of viral replication and recovery in Lassa virus-infected cynomolgus monkeys. J Virol 83: 5890-5903.
18. ter Meulen J, Badusche M, Kuhnt K, Doetze A, Satoguina J, et al. (2000) Characterization of human CD4+ T cell clones recognizing conserved and variable epitopes of the Lassa virus nucleoprotein. J Virol 74: 2186-2192.
19. ter Meulen J, Badusche M, Satoguina J, Strecker T, Lenz O, et al. (2004) Old and New world arenaviruses share a highly conserved epitope in the fusion domain of the glycoprotein 2, which is recognized by Lassa virus-specific human CD4+ T-cell clones. Virology 321: 134-143.
20. Bowen MD, Peters CJ, Nichol ST, (1997) Phylogenetic analysis of the Arenaviridae: patterns of virus evolution and evidence for cospeciation between Arenaviruses and their rodent hosts. Molec Phylogen Evol 8: 301-316.
21. Ruo SL, Mitchell SW, Kiley MP, Roumillat LF, Fisher-Hoch SP, et al. (1991) Antigenic relatedness between arenaviruses defined at the epitope level by monoclonal antibodies. J Gen Virol 72: 549-555.
22. Wulff H, McIntosh B, Hamner D, Johnson K, (1977) Isolation of an arenavirus closely related to Lassa virus from Mastomys natalensis in south-east Africa. Bull World Health Organ 55: 441-444.
23. Kiley MP, Lange JV, Johnson KM, (1979) Protection of rhesus monkeys from Lassa virus by immunisation with closely related arenavirus. Lancet 2: 738-745.
24. Baize S, Pannetier D, Faure C, Marianneau P, Marendat I, et al. (2006) Role of interferons in the control of Lassa virus replication in human dendritic cells and macrophages. Microb Infect 8: 1193-1422.
25. Pannetier D, Faure C, Georges-Courbot MC, Deubel V, Baize S, (2004) Human macrophages, but not dendritic cells, are activated and produce type I interferons in response to Mopeia virus infection. J Virol 78: 10516-10524.
26. Pannetier D, Reynard S, Russier M, Journeaux A, Tordo N, et al. (2011) Human dendritic cells infected with the non-pathogenic Mopeia virus induce stronger T-cell responses than with Lassa virus. J Virol 85: 8293-8306.
27. Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO, (2011) Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3′ to 5′ exonuclease activity essential for immune suppression. Proceedings of the National Academy of Sciences 108: 2396-2401.
28. Qi X, Lan S, Wang W, Schelde LM, Dong H, et al. (2010) Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468: 779-785.
29. Habjan M, Andersson I, Klingström J, Schümann M, Martin A, et al. (2008) Processing of Genome 5′ Termini as a Strategy of Negative-Strand RNA Viruses to Avoid RIG-I-Dependent Interferon Induction. PLoS ONE 3: e2032.
30. Martinez-Sobrido L, Emonet S, Giannakas P, Cubitt B, Garcia-Sastre A, et al. (2009) Identification of Amino Acid Residues Critical for the Anti-Interferon Activity of the Nucleoprotein of the Prototypic Arenavirus Lymphocytic Choriomeningitis Virus. J Virol 83: 11330-11340.
31. Carnec X, Baize S, Reynard S, Diancourt L, Caro V, et al. (2011) Lassa virus nucleoprotein mutants generated by reverse genetics induce robust type I IFN response in human dendritic cells and macrophages. J Virol 85: 12093-12097.
32. Pythoud C, Rodrigo WWSI, Pasqual G, Rothenberger S, Martínez-Sobrido L, et al. (2012) Arenavirus Nucleoprotein Targets Interferon Regulatory Factor-Activating Kinase IKKε. Journal of Virology 86: 7728-7738.
33. Rodrigo WWSI, Ortiz-Riaño E, Pythoud C, Kunz S, de la Torre JC, et al. (2012) Arenavirus Nucleoproteins Prevent Activation of Nuclear Factor Kappa B. Journal of Virology 86: 8185-8197.
34. Moser B, Loetscher P, (2001) Lymphocyte traffic control by chemokines. Nature Immunol 2: 123-128.
35. Deshmane S, Kremlev S, Amini S, Sawaya B, (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29: 313-326.
36. Sung Jung H, Zhang H, Moseman EA, Alvarez D, Iannacone M, et al. (2012) Chemokine Guidance of Central Memory T Cells Is Critical for Antiviral Recall Responses in Lymph Nodes. Cell 150: 1249-1263.
37. Wack A, Openshaw P, O'Garra A, (2011) Contribution of cytokines to pathology and protection in virus infection. Current Opinion in Virology 1: 184-195.
38. Liu M, Guo S, Hibbert JM, Jain V, Singh N, et al. (2011) CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine & Growth Factor Reviews 22: 121-130.
39. Mahanty S, Bausch DG, Thomas RL, Goba A, Bah A, et al. (2001) Low levels of interleukin-8 and interferon-inducible protein-10 in serum are associated with fatal infections in acute Lassa fever. J Infect Dis 183: 1713-1721.
40. Lukashevich IS, Maryankova R, Vladyko AS, Nashkevic N, Koleda S, et al. (1999) Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-α gene expression. J Med Virol 59: 552-560.
41. Djavani MM, Crasta OR, Zapata JC, Fei Z, Folkerts O, et al. (2007) Early Blood Profiles of Virus Infection in a Monkey Model for Lassa Fever. J Virol 81: 7960-7973.
42. Günther S, Emmerich P, Laue T, Kühle O, Asper M, et al. (2000) Imported Lassa fever in Germany: molecular characterization of a new Lassa virus strain. Emerg Infect Dis 6: 466-476.
43. Russier M, Reynard S, Tordo N, Baize S, (2012) NK cells are early activated by Lassa and Mopeia virus-infected human macrophages, but do not mediate virus suppression. Eur J Immunol 42: 1822-1832.
44. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686.
45. Cook D, Beck M, Coffman T, Kirby S, Sheridan J, et al. (1995) Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science 269: 1583-1585.
46. Lin C-L, Suri RM, Rahdon RA, Austyn JM, Roake JA, (1998) Dendritic cell chemotaxis and transendothelial migration are induced by distinct chemokines and are regulated on maturation. Eur J Immunol 28: 4114-4122.
47. Xu LL, Warren MK, Rose WL, Gong W, Wang JM, (1996) Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. Journal of Leukocyte Biology 60: 365-371.
48. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, et al. (2006) Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interactions. Nature 440: 890-895.
49. Schall TJ, Bacon K, Camp RDR, Kaspari JW, Goeddel DV, (1993) Human macrophage inflammatory protein α (MIP-1α) and MIP-1β chemokines attract distinct populations of lymphocytes. J Exp Med 177: 1821-1825.
50. Taub DD, Conlon K, Lloyd AR, Oppenheim JJ, Kelvin DJ, (1993) Preferential migration of activated CD4+ and CD8+ T cells in response to MIP-1α and MIP-1β. Science 260: 355-358.
51. Taub DD, Proost P, Murphy WJ, Anver M, Longo DL, et al. (1995) Monocyte chemotactic protein-1 (MCP-1),-2, and-3 are chemotactic for human T lymphocytes. J Clin Invest 95: 1370-1376.
52. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, et al. (1996) Chemokine receptor specific for IP10 and Mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 184: 963-969.
53. Inngjerdingen M, Damaj B, Maghazachi AA, (2001) Expression and regulation of chemokine receptors in human natural killer cells. Blood 97: 367-375.
54. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, et al. (2002) IFN-γ-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168: 3195-3204.
55. Foley JF, Yu C-R, Solow R, Yacobucci M, Peden KWC, et al. (2005) Roles for CXC chemokine ligand 10 and 11 in recruiting CD4+ T cells to HIV-1-infected monocyte-derived macrophages, dendritic cells, and lymph nodes. J Immunol 174: 4892-4900.
56. Lande R, Giacomini E, Grassi T, Remoli ME, Iona E, et al. (2003) IFN-αβ released by Mycobacterium tuberculosis-infected human dendritic cells induces the expression of CXCL10: selective recruitment of NK and activated T cells. J Immunol 170: 1174-1182.
57. Taub DD, Sayers TJ, Carter CRD, Ortaldo JR, (1995) α and β chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol 155: 3877-3888.
58. Whiting D, Hsieh G, Yun JJ, Banerji A, Yao W, et al. (2004) Chemokine monokine induced by IFN-γ/CXC chemokine ligand 9 stimulates T lymphocyte proliferation and effector cytokine production. J Immunol 172: 7417-7424.
59. Hsieh M-F, Lai S-L, Chen J-P, Sung J-M, Lin Y-L, et al. (2006) Both CXCR3 and CXCL10/IFN-inducible protein 10 are required for resistance to primary infection by dengue virus. J Immunol 177: 1855-1863.
60. Christensen JE, de Lemos C, Moos T, Christensen JP, Thomsen AR, (2006) CXCL10 is the key ligand for CXCR3 on CD8+ effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J Immunol 176: 4235-4243.
61. Malhotra S, Yen JY, Honko AN, Garamszegi S, Caballero IS, et al. (2013) Transcriptional Profiling of the Circulating Immune Response to Lassa Virus in an Aerosol Model of Exposure. PLoS Negl Trop Dis 7: e2171.
62. Groom JR, Luster AD, (2011) CXCR3 ligands: Redundant, collaborative and antagonistic functions. Immunol Cell Biol 89: 207-215.
63. Macal M, Lewis Gavin M, Kunz S, Flavell R, Harker James A, et al. (2012) Plasmacytoid Dendritic Cells Are Productively Infected and Activated through TLR-7 Early after Arenavirus Infection. Cell Host Microbe 11: 617-630.
64. Martinez-Sobrido L, Giannakas P, Cubitt B, Garcia-Sastre A, de La Torre JC, (2007) Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J Virol 81: 12696-12703.