A Mouse Model of Chronic West Nile Virus Disease

PLoS Pathogens

Volumn 12, Issue 11, 2016, Pages

  Graham, Jessica B ^a   Swarts, Jessica L ^a   Wilkins, Courtney ^b   Thomas, Sunil ^b   Green, Richard ^b   Sekine, Aimee ^b   Voss, Kathleen M ^b   Ireton, Renee C ^b   Mooney, Michael ^c   Choonoo, Gabrielle ^c   Miller, Darla R ^d   Treuting, Piper M ^e   Pardo Manuel de Villena, Fernando ^d   Ferris, Martin T ^d   McWeeney, Shannon ^c   Gale, Michael ^b   Lund, Jennifer M ^a,e  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; FLOW CYTOMETRY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; HISTOPATHOLOGY; IMMUNE RESPONSE; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; VIRUS INFECTION; WEST NILE VIRUS INFECTION; ANIMAL; CHRONIC DISEASE; DISEASE MODEL; DNA MICROARRAY; FEMALE; HUMAN; IMMUNOLOGY; REGULATORY T LYMPHOCYTE; WEST NILE FEVER; WEST NILE VIRUS;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; WEST NILE FEVER; WEST NILE VIRUS;

EID: 85002156930     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005996     Document Type: Article

References (45)

1. Colpitts TM, Conway MJ, Montgomery RR, Fikrig E, (2012) West Nile Virus: biology, transmission, and human infection. Clinical microbiology reviews25: 635–648. doi: 10.1128/CMR.00045-1223034323
2. Sejvar JJ, (2007) The long-term outcomes of human West Nile virus infection. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America44: 1617–1624.
3. Murray K, Walker C, Herrington E, Lewis JA, McCormick J, et al. (2010) Persistent infection with West Nile virus years after initial infection. J Infect Dis201: 2–4. doi: 10.1086/64873119961306
4. Daffis S, Samuel MA, Keller BC, Gale M, Jr.Diamond MS, (2007) Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog3: e106. doi: 10.1371/journal.ppat.003010617676997
5. Daffis S, Samuel MA, Suthar MS, Gale M, Jr.Diamond MS, (2008) Toll-like receptor 3 has a protective role against West Nile virus infection. Journal of virology82: 10349–10358. doi: 10.1128/JVI.00935-0818715906
6. Daffis S, Samuel MA, Suthar MS, Keller BC, Gale M, Jr.et al. (2008) Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. Journal of virology82: 8465–8475. doi: 10.1128/JVI.00918-0818562536
7. Suthar MS, Diamond MS, Gale M, Jr. (2013) West Nile virus infection and immunity. Nat Rev Microbiol11: 115–128. doi: 10.1038/nrmicro295023321534
8. Errett JS, Suthar MS, McMillan A, Diamond MS, Gale M, Jr. (2013) The essential, nonredundant roles of RIG-I and MDA5 in detecting and controlling West Nile virus infection. Journal of virology87: 11416–11425. doi: 10.1128/JVI.01488-1323966395
9. Keller BC, Fredericksen BL, Samuel MA, Mock RE, Mason PW, et al. (2006) Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. Journal of virology80: 9424–9434. doi: 10.1128/JVI.00768-0616973548
10. Samuel MA, Whitby K, Keller BC, Marri A, Barchet W, et al. (2006) PKR and RNase L contribute to protection against lethal West Nile Virus infection by controlling early viral spread in the periphery and replication in neurons. Journal of virology80: 7009–7019. doi: 10.1128/JVI.00489-0616809306
11. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, et al. (2010) IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog6: e1000757. doi: 10.1371/journal.ppat.100075720140199
12. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, et al. (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nature genetics36: 1133–1137. doi: 10.1038/ng1104-113315514660
13. Collaborative Cross C (2012) The genome architecture of the Collaborative Cross mouse genetic reference population. Genetics190: 389–401. doi: 10.1534/genetics.111.13263922345608
14. Threadgill DW, Miller DR, Churchill GA, de Villena FP, (2011) The collaborative cross: a recombinant inbred mouse population for the systems genetic era. ILAR journal / National Research Council, Institute of Laboratory Animal Resources52: 24–31.
15. Roberts A, Pardo-Manuel de Villena F, Wang W, McMillan L, Threadgill DW, (2007) The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics. Mammalian genome: official journal of the International Mammalian Genome Society18: 473–481.
16. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature477: 289–294. doi: 10.1038/nature1041321921910
17. Graham JB, Thomas S, Swarts J, McMillan AA, Ferris MT, et al. (2015) Genetic diversity in the collaborative cross model recapitulates human West Nile virus disease outcomes. MBio6: e00493–00415. doi: 10.1128/mBio.00493-1525944860
18. Appler KK, Brown AN, Stewart BS, Behr MJ, Demarest VL, et al. (2010) Persistence of West Nile virus in the central nervous system and periphery of mice. PLoS One5: e10649. doi: 10.1371/journal.pone.001064920498839
19. Courtney SC, Di H, Stockman BM, Liu H, Scherbik SV, et al. (2012) Identification of novel host cell binding partners of Oas1b, the protein conferring resistance to flavivirus-induced disease in mice. J Virol86: 7953–7963. doi: 10.1128/JVI.00333-1222623793
20. Simon-Chazottes D, Frenkiel MP, Montagutelli X, Guenet JL, Despres P, et al. (2011) Transgenic expression of full-length 2',5'-oligoadenylate synthetase 1b confers to BALB/c mice resistance against West Nile virus-induced encephalitis. Virology417: 147–153. doi: 10.1016/j.virol.2011.05.01821683973
21. Bauer M, Brakebusch C, Coisne C, Sixt M, Wekerle H, et al. (2009) Beta1 integrins differentially control extravasation of inflammatory cell subsets into the CNS during autoimmunity. Proc Natl Acad Sci U S A106: 1920–1925. doi: 10.1073/pnas.080890910619179279
22. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL, (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature420: 502–507. doi: 10.1038/nature0115212466842
23. Garg A, Barnes PF, Roy S, Quiroga MF, Wu S, et al. (2008) Mannose-capped lipoarabinomannan- and prostaglandin E2-dependent expansion of regulatory T cells in human Mycobacterium tuberculosis infection. Eur J Immunol38: 459–469. doi: 10.1002/eji.20073726818203140
24. Feruglio SL, Tonby K, Kvale D, Dyrhol-Riise AM, (2015) Early dynamics of T helper cell cytokines and T regulatory cells in response to treatment of active Mycobacterium tuberculosis infection. Clin Exp Immunol179: 454–465. doi: 10.1111/cei.1246825313008
25. Toor JS, Singh S, Sharma A, Arora SK, (2014) Mycobacterium tuberculosis modulates the gene interactions to activate the HIV replication and faster disease progression in a co-infected host. PLoS One9: e106815. doi: 10.1371/journal.pone.010681525198707
26. Chen X, Zhou B, Li M, Deng Q, Wu X, et al. (2007) CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol123: 50–59. doi: 10.1016/j.clim.2006.11.00917234458
27. Beiranvand E, Abediankenari S, Rezaei MS, Khani S, Sardari S, et al. (2014) Increased expression of forkhead box protein 3 gene of regulatory T cells in patients with active tuberculosis. Inflamm Allergy Drug Targets13: 330–334. 25198706
28. Tsai SL, Liaw YF, Chen MH, Huang CY, Kuo GC, (1997) Detection of type 2-like T-helper cells in hepatitis C virus infection: implications for hepatitis C virus chronicity. Hepatology25: 449–458. doi: 10.1002/hep.5102502339021963
29. Shoukry NH, Cawthon AG, Walker CM, (2004) Cell-mediated immunity and the outcome of hepatitis C virus infection. Annu Rev Microbiol58: 391–424. doi: 10.1146/annurev.micro.58.030603.12383615487943
30. Rehermann B, Nascimbeni M, (2005) Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol5: 215–229. doi: 10.1038/nri157315738952
31. Bolacchi F, Sinistro A, Ciaprini C, Demin F, Capozzi M, et al. (2006) Increased hepatitis C virus (HCV)-specific CD4+CD25+ regulatory T lymphocytes and reduced HCV-specific CD4+ T cell response in HCV-infected patients with normal versus abnormal alanine aminotransferase levels. Clin Exp Immunol144: 188–196. doi: 10.1111/j.1365-2249.2006.03048.x16634790
32. Manigold T, Racanelli V, (2007) T-cell regulation by CD4 regulatory T cells during hepatitis B and C virus infections: facts and controversies. Lancet Infect Dis7: 804–813. doi: 10.1016/S1473-3099(07)70289-X18045563
33. Wang JH, Layden TJ, Eckels DD, (2003) Modulation of the peripheral T-Cell response by CD4 mutants of hepatitis C virus: transition from a Th1 to a Th2 response. Hum Immunol64: 662–673. 12826368
34. Stoop JN, van der Molen RG, Baan CC, van der Laan LJ, Kuipers EJ, et al. (2005) Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. Hepatology41: 771–778. doi: 10.1002/hep.2064915791617
35. Xu D, Fu J, Jin L, Zhang H, Zhou C, et al. (2006) Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J Immunol177: 739–747. 16785573
36. Yang G, Liu A, Xie Q, Guo TB, Wan B, et al. (2007) Association of CD4+CD25+Foxp3+ regulatory T cells with chronic activity and viral clearance in patients with hepatitis B. Int Immunol19: 133–140. doi: 10.1093/intimm/dxl13017182968
37. Sugimoto K, Ikeda F, Stadanlick J, Nunes FA, Alter HJ, et al. (2003) Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection. Hepatology38: 1437–1448. doi: 10.1016/j.hep.2003.09.02614647055
38. Boettler T, Spangenberg HC, Neumann-Haefelin C, Panther E, Urbani S, et al. (2005) T cells with a CD4+CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection. J Virol79: 7860–7867. doi: 10.1128/JVI.79.12.7860-7867.200515919940
39. Rushbrook SM, Ward SM, Unitt E, Vowler SL, Lucas M, et al. (2005) Regulatory T cells suppress in vitro proliferation of virus-specific CD8+ T cells during persistent hepatitis C virus infection. J Virol79: 7852–7859. doi: 10.1128/JVI.79.12.7852-7859.200515919939
40. Cabrera R, Tu Z, Xu Y, Firpi RJ, Rosen HR, et al. (2004) An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection. Hepatology40: 1062–1071. doi: 10.1002/hep.2045415486925
41. Shrestha B, Diamond MS, (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol78: 8312–8321. doi: 10.1128/JVI.78.15.8312-8321.200415254203
42. Lanteri MC, O'Brien KM, Purtha WE, Cameron MJ, Lund JM, et al. (2009) Tregs control the development of symptomatic West Nile virus infection in humans and mice. J Clin Invest119: 3266–3277. doi: 10.1172/JCI3938719855131
43. Wang T, Welte T, (2013) Role of natural killer and Gamma-delta T cells in West Nile virus infection. Viruses5: 2298–2310. doi: 10.3390/v509229824061543
44. Welsh CE, Miller DR, Manly KF, Wang J, McMillan L, et al. (2012) Status and access to the Collaborative Cross population. Mamm Genome23: 706–712. doi: 10.1007/s00335-012-9410-622847377
45. Bottomly D, Wilmot B, McWeeney SK, (2014) oligoMask: A Framework for Assessing and Removing the Effect of Genetic Variants on Microarray Probes. R Journal6: 159–163.