Association of Symptoms and Severity of Rift Valley Fever with Genetic Polymorphisms in Human Innate Immune Pathways

PLoS Neglected Tropical Diseases

Volumn 9, Issue 3, 2015, Pages

  Hise, Amy G ^a,b   Traylor, Zachary ^a   Hall, Noémi B ^c   Sutherland, Laura J ^a   Dahir, Saidi ^c   Ermler, Megan E ^a   Muiruri, Samuel ^c   Muchiri, Eric M ^c   Kazura, James W ^a   LaBeaud, A Desirée ^d,e   King, Charles H ^a   Stein, Catherine M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c Ministry of Public Health and Sanitation   (Kenya)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^e STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; INTERLEUKIN 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TICAM1 PROTEIN, HUMAN; TLR3 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 3; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CHILD; CLUSTER ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DNA EXTRACTION; EYE DISEASE; FEMALE; FEVER; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENOTYPE; HAPLOTYPE; HEMORRHAGIC FEVER; HUMAN; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALAISE; MALE; MENINGOENCEPHALITIS; PHLEBOTOMY; QUESTIONNAIRE; RIFT VALLEY FEVER; SEROLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; GENETICS; IMMUNOLOGY; INFANT; MIDDLE AGED; PRESCHOOL CHILD; RIFT VALLEY FEVER VIRUS; VERY ELDERLY; YOUNG ADULT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; FEMALE; GENOTYPE; HAPLOTYPES; HUMANS; IMMUNITY, INNATE; INFANT; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; TOLL-LIKE RECEPTOR 3; YOUNG ADULT;

EID: 84928782707     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003584     Document Type: Article

References (80)

1. CDC (2002) Rift Valley Fever. Viral Hemorrhagic Fevers Fact Sheets.
2. Isaacson M, (2001) Viral hemorrhagic fever hazards for travelers in Africa. Clin Infect Dis 33: 1707–1712. 11595975
3. WHO (2000) Rift Valley Fever. WHO Fact Sheet 207.
4. Woods CW, Karpati AM, Grein T, McCarthy N, Gaturuku P, et al. (2002) An outbreak of Rift Valley fever in Northeastern Kenya, 1997–98. Emerg Infect Dis 8: 138–144. 11897064
5. WHO (2007) Rift Valley Fever in Kenya and Somalia—update 3.
6. Linthicum KJ, Anyamba A, Tucker CJ, Kelley PW, Myers MF, et al. (1999) Climate and satellite indicators to forecast Rift Valley fever epidemics in Kenya. Science 285: 397–400. 10411500
7. LaBeaud AD, Ochiai Y, Peters CJ, Muchiri EM, King CH, (2007) Spectrum of Rift Valley fever virus transmission in Kenya: insights from three distinct regions. Am J Trop Med Hyg 76: 795–800. 17488893
8. LaBeaud AD, Sutherland LJ, Muiruri S, Muchiri EM, Gray LR, et al. (2011) Arbovirus prevalence in mosquitoes, Kenya. Emerg Infect Dis 17: 233–241. doi: 10.3201/eid1702.091666 21291594
9. King CH, Kahlon SS, Muiruri S, Labeaud AD, (2010) Facets of the Rift Valley fever outbreak in Northeastern Province, Kenya, 2006–2007. Am J Trop Med Hyg 82: 363. doi: 10.4269/ajtmh.2010.09-0800 20207854
10. LaBeaud AD, Muchiri EM, Ndzovu M, Mwanje MT, Muiruri S, et al. (2008) Interepidemic Rift Valley fever virus seropositivity, northeastern Kenya. Emerg Infect Dis 14: 1240–1246. doi: 10.3201/eid1408.080082 18680647
11. LaBeaud AD, Pfeil S, Muiruri S, Dahir S, Sutherland LJ, et al. (2015) Factors Associated with Severe Human Rift Valley Fever in Sangailu, Garissa County, Kenya. PLoS Negl Trop Dis In press.
12. Al-Hazmi A, Al-Rajhi AA, Abboud EB, Ayoola EA, Al-Hazmi M, et al. (2005) Ocular complications of Rift Valley fever outbreak in Saudi Arabia. Ophthalmology 112: 313–318. 15691569
13. Peters CJ, Liu CT, Anderson GW, Jr.Morrill JC, Jahrling PB, (1989) Pathogenesis of viral hemorrhagic fevers: Rift Valley fever and Lassa fever contrasted. Rev Infect Dis 11 Suppl 4: S743–749. 2665011
14. Kende M, Lupton HW, Rill WL, Gibbs P, Levy HB, et al. (1987) Ranking of prophylactic efficacy of poly(ICLC) against Rift Valley fever virus infection in mice by incremental relative risk of death. Antimicrob Agents Chemother 31: 1194–1198. 3631943
15. Kende M, Lupton HW, Rill WL, Levy HB, Canonico PG, (1987) Enhanced therapeutic efficacy of poly(ICLC) and ribavirin combinations against Rift Valley fever virus infection in mice. Antimicrob Agents Chemother 31: 986–990. 3662477
16. Frese M, Kochs G, Feldmann H, Hertkorn C, Haller O, (1996) Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J Virol 70: 915–923. 8551631
17. Ritter M, Bouloy M, Vialat P, Janzen C, Haller O, et al. (2000) Resistance to Rift Valley fever virus in Rattus norvegicus: genetic variability within certain 'inbred' strains. J Gen Virol 81: 2683–2688. 11038380
18. Sandrock M, Frese M, Haller O, Kochs G, (2001) Interferon-induced rat Mx proteins confer resistance to Rift Valley fever virus and other arthropod-borne viruses. J Interferon Cytokine Res 21: 663–668. 11576460
19. Anderson GW, Jr.Peters CJ, (1988) Viral determinants of virulence for Rift Valley fever (RVF) in rats. Microb Pathog 5: 241–250. 3266284
20. Anderson GW, Jr.Rosebrock JA, Johnson AJ, Jennings GB, Peters CJ, (1991) Infection of inbred rat strains with Rift Valley fever virus: development of a congenic resistant strain and observations on age-dependence of resistance. Am J Trop Med Hyg 44: 475–480. 2063951
21. Kahlon SS, Peters CJ, Leduc J, Muchiri EM, Muiruri S, et al. (2010) Severe Rift Valley fever may present with a characteristic clinical syndrome. Am J Trop Med Hyg 82: 371–375. doi: 10.4269/ajtmh.2010.09-0669 20207858
22. Takeda K, Akira S, (2001) Roles of Toll-like receptors in innate immune responses. Genes Cells 6: 733–742. 11554921
23. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730–737. 15208624
24. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, et al. (2004) The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101: 17264–17269. 15563593
25. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, et al. (2005) Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175: 2851–2858. 16116171
26. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19–28. 16039576
27. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A, (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206: 79–87. doi: 10.1084/jem.20081667 19139171
28. Ito M, Yanagi Y, Ichinohe T, (2012) Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog 8: e1002857. doi: 10.1371/journal.ppat.1002857 22916014
29. Lawrence TM, Hudacek AW, de Zoete MR, Flavell RA, Schnell MJ, (2013) Rabies virus is recognized by the NLRP3 inflammasome and activates interleukin-1beta release in murine dendritic cells. J Virol 87: 5848–5857. doi: 10.1128/JVI.00203-13 23487464
30. Triantafilou K, Kar S, Vakakis E, Kotecha S, Triantafilou M, (2013) Human respiratory syncytial virus viroporin SH: a viral recognition pathway used by the host to signal inflammasome activation. Thorax 68: 66–75. doi: 10.1136/thoraxjnl-2012-202182 23229815
31. Segovia J, Sabbah A, Mgbemena V, Tsai SY, Chang TH, et al. (2012) TLR2/MyD88/NF-kappaB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 7: e29695. doi: 10.1371/journal.pone.0029695 22295065
32. Ermler ME, Traylor Z, Patel K, Schattgen S, Vaneja SK, et al. (2014) Rift Valley fever virus infection induces activation of the NLRP3 inflammasome. Virology 449: 174–180. doi: 10.1016/j.virol.2013.11.015 24418550
33. Bieback K, Lien E, Klagge IM, Avota E, Schneider-Schaulies J, et al. (2002) Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J Virol 76: 8729–8736. 12163593
34. Finberg RW, Kurt-Jones EA, (2004) Viruses and Toll-like receptors. Microbes Infect 6: 1356–1360. 15596120
35. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, et al. (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 77: 4588–4596. 12663765
36. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, et al. (2000) Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 1: 398–401. 11062499
37. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA, (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll- like receptor 3. Nature 413: 732–738. 11607032
38. Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, et al. (2002) Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 3: 196–200. 11812998
39. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526–1529. 14976262
40. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740–745. 11130078
41. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, et al. (2004) Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci U S A 101: 5598–5603. 15034168
42. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A, (2003) Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 198: 513–520. 12900525
43. Krug A, Luker GD, Barchet W, Leib DA, Akira S, et al. (2004) Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103: 1433–1437. 14563635
44. Muzio M, Ni J, Feng P, Dixit VM, (1997) IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612–1615. 9374458
45. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, et al. (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2: 253–258. 9734363
46. Cao Z, Tanaka M, Regnier C, Rothe M, Yamit-hezi A, et al. (1999) NF-kappa B activation by tumor necrosis factor and interleukin-1. Cold Spring Harb Symp Quant Biol 64: 473–483. 11232324
47. Ye H, Arron JR, Lamothe B, Cirilli M, Kobayashi T, et al. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418: 443–447. 12140561
48. Gowen BB, Hoopes JD, Wong MH, Jung KH, Isakson KC, et al. (2006) TLR3 deletion limits mortality and disease severity due to Phlebovirus infection. J Immunol 177: 6301–6307. 17056560
49. Kende M, (1985) Prophylactic and therapeutic efficacy of poly(I,C)-LC against Rift Valley fever virus infection in mice. J Biol Response Mod 4: 503–511. 2416883
50. Ermler ME, Yerukhim E, Schriewer J, Schattgen S, Traylor Z, et al. (2013) RNA helicase signaling is critical for type i interferon production and protection against Rift Valley fever virus during mucosal challenge. J Virol 87: 4846–4860. doi: 10.1128/JVI.01997-12 23408632
51. Seth RB, Sun L, Chen ZJ, (2006) Antiviral innate immunity pathways. Cell Res 16: 141–147. 16474426
52. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981–988. 16127453
53. Kumar H, Kawai T, Kato H, Sato S, Takahashi K, et al. (2006) Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 203: 1795–1803. 16785313
54. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167–1172. 16177806
55. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727–740. 16153868
56. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101–105. 16625202
57. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, et al. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 103: 8459–8464. 16714379
58. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 5'-Triphosphate RNA is the ligand for RIG-I. Science 314: 994–997. 17038590
59. LaBeaud AD, Muiruri S, Sutherland LJ, Dahir S, Gildengorin G, et al. (2011) Postepidemic analysis of Rift Valley fever virus transmission in northeastern kenya: a village cohort study. PLoS Negl Trop Dis 5: e1265. doi: 10.1371/journal.pntd.0001265 21858236
60. International HapMap C (2003) The International HapMap Project. Nature 426: 789–796. 14685227
61. International HapMap C (2005) A haplotype map of the human genome. Nature 437: 1299–1320. 16255080
62. Frazer KA, Ballinger DG, Cox DR, Hinds DA, International HapMap C, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851–861. 17943122
63. Norusis M, (2009) Cluster analysis. SPSS Statistics 17- Statistical Procedures Companion. Upper Saddle River, NJ: Prentice Hall.
64. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–575. 17701901
65. Holliday EG, Smith AV, Cornes BK, Buitendijk GH, Jensen RA, et al. (2013) Insights into the genetic architecture of early stage age-related macular degeneration: a genome-wide association study meta-analysis. PLoS One 8: e53830. doi: 10.1371/journal.pone.0053830 23326517
66. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, et al. (2005) A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A 102: 7227–7232. 15870199
67. Davila S, Wright VJ, Khor CC, Sim KS, Binder A, et al. (2010) Genome-wide association study identifies variants in the CFH region associated with host susceptibility to meningococcal disease. Nat Genet 42: 772–776. doi: 10.1038/ng.640 20694013
68. Thakkinstian A, Han P, McEvoy M, Smith W, Hoh J, et al. (2006) Systematic review and meta-analysis of the association between complement factor H Y402H polymorphisms and age-related macular degeneration. Hum Mol Genet 15: 2784–2790. 16905558
69. Ng TK, Chen LJ, Liu DT, Tam PO, Chan WM, et al. (2008) Multiple gene polymorphisms in the complement factor h gene are associated with exudative age-related macular degeneration in chinese. Invest Ophthalmol Vis Sci 49: 3312–3317. doi: 10.1167/iovs.07-1517 18421087
70. Leveziel N, Zerbib J, Richard F, Querques G, Morineau G, et al. (2008) Genotype-phenotype correlations for exudative age-related macular degeneration associated with homozygous HTRA1 and CFH genotypes. Invest Ophthalmol Vis Sci 49: 3090–3094. doi: 10.1167/iovs.07-1540 18362109
71. Thompson IA, Liu B, Sen HN, Jiao X, Katamay R, et al. (2013) Association of complement factor h tyrosine 402 histidine genotype with posterior involvement in sarcoid-related uveitis. Am J Ophthalmol 155: 1068–1074 e1061. doi: 10.1016/j.ajo.2013.01.019 23497844
72. Gowen BB, Wong MH, Jung KH, Sanders AB, Mitchell WM, et al. (2007) TLR3 is essential for the induction of protective immunity against Punta Toro Virus infection by the double-stranded RNA (dsRNA), poly(I:C12U), but not Poly(I:C): differential recognition of synthetic dsRNA molecules. J Immunol 178: 5200–5208. 17404303
73. Moy RH, Gold B, Molleston JM, Schad V, Yanger K, et al. (2014) Antiviral autophagy restrictsRift Valley fever virus infection and is conserved from flies to mammals. Immunity 40: 51–65. doi: 10.1016/j.immuni.2013.10.020 24374193
74. Hertzog PJ, Hwang SY, Holland KA, Tymms MJ, Iannello R, et al. (1994) A gene on human chromosome 21 located in the region 21q22.2 to 21q22.3 encodes a factor necessary for signal transduction and antiviral response to type I interferons. J Biol Chem 269: 14088–14093. 8188689
75. de Weerd NA, Samarajiwa SA, Hertzog PJ, (2007) Type I interferon receptors: biochemistry and biological functions. J Biol Chem 282: 20053–20057. 17502368
76. Mogensen KE, Lewerenz M, Reboul J, Lutfalla G, Uze G, (1999) The type I interferon receptor: structure, function, and evolution of a family business. J Interferon Cytokine Res 19: 1069–1098. 10547147
77. Bouloy M, Janzen C, Vialat P, Khun H, Pavlovic J, et al. (2001) Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. J Virol 75: 1371–1377. 11152510
78. Song le H, Xuan NT, Toan NL, Binh VQ, Boldt AB, et al. (2008) Association of two variants of the interferon-alpha receptor-1 gene with the presentation of hepatitis B virus infection. Eur Cytokine Netw 19: 204–210. doi: 10.1684/ecn.2008.0137 19103527
79. He XX, Chang Y, Jiang HJ, Tang F, Meng FY, et al. (2010) Persistent effect of IFNAR-1 genetic polymorphism on the long-term pathogenesis of chronic HBV infection. Viral Immunol 23: 251–257. doi: 10.1089/vim.2009.0102 20565290
80. Welzel TM, Morgan TR, Bonkovsky HL, Naishadham D, Pfeiffer RM, et al. (2009) Variants in interferon-alpha pathway genes and response to pegylated interferon-Alpha2a plus ribavirin for treatment of chronic hepatitis C virus infection in the hepatitis C antiviral long-term treatment against cirrhosis trial. Hepatology 49: 1847–1858. doi: 10.1002/hep.22877 19434718