Induction of interferon-λ contributes to TLR3 and RIG-I activation-mediated inhibition of herpes simplex virus type 2 replication in human cervical epithelial cells

Molecular Human Reproduction

Volumn 21, Issue 12, 2015, Pages 917-929

  Zhou, Li ^a   Li, Jie Liang ^b   Zhou, Yu ^b   Liu, Jin Biao ^a   Zhuang, Ke ^a   Gao, Jian Feng ^a   Liu, Shi ^a   Sang, Ming ^a,c   Wu, Jian Guo ^a   Ho, Wen Zhe ^a,b  

^a WUHAN UNIVERSITY   (China)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HUBEI UNIVERSITY OF MEDICINE   (China)

Author keywords

Herpes simplex virus type 2; Human cervical epithelial cells; Interferon stimulated genes; Interferon ; Retinoic acid inducible gene I; Toll like receptor 3

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; 2',5' OLIGOADENYLATE SYNTHETASE 1; DOUBLE STRANDED RNA; INTERFERON; INTERFERON LAMBDA; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERFERON STIMULATED GENE 56 PROTEIN; INTERLEUKIN 10 RECEPTOR BETA; MYXOVIRUS RESISTANCE PROTEIN A; RETINOIC ACID INDUCIBLE PROTEIN I; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; VIRUS PROTEIN; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; TLR3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; E6E7 CELL LINE; END1 CELL LINE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; GENITAL TRACT INFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HERPES SIMPLEX VIRUS 2 INFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UTERINE CERVIX EPITHELIUM; VIRUS INHIBITION; VIRUS REPLICATION; WESTERN BLOTTING; GENETICS; METABOLISM; PHYSIOLOGY; PROSPECTIVE STUDY; VIROLOGY;

DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; EPITHELIAL CELLS; HERPESVIRUS 2, HUMAN; HUMANS; POLY I-C; PROSPECTIVE STUDIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; VIRUS REPLICATION;

EID: 84949970204     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gav058     Document Type: Article

References (56)

1. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001;413:732-738.
2. Ank N, Paludan SR. Type III IFNs: new layers of complexity in innate antiviral immunity. Biofactors 2009;35:82-87.
3. Ank N,West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 2006;80:4501-4509.
4. Ashkar AA, Yao XD, Gill N, Sajic D, Patrick AJ, Rosenthal KL. Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J Infect Dis 2004;190:1841-1849.
5. Azulay-Debby H, Edry E, Melamed D. CpG DNA stimulates autoreactive immature B cells in the bone marrow. Eur J Immunol 2007;37:1463-1475.
6. Barton GM, Medzhitov R. Toll-like receptors and their ligands. Curr Top Microbiol Immunol 2002;270:81-92.
7. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, Stark GR. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 2007;6:975-990.
8. Cannella F, Scagnolari C, Selvaggi C, Stentella P, Recine N, Antonelli G, Pierangeli A. Interferon lambda 1 expression in cervical cells differs between low-risk and high-risk human papillomavirus-positive women. Med Microbiol Immunol 2014;203:177-184.
9. Chan T, Barra NG, Lee AJ, Ashkar AA. Innate and adaptive immunity against herpes simplex virus type 2 in the genital mucosa. J Reprod Immunol 2011; 88:210-218.
10. Chao CT, Chen YC, Chiang CK, Huang JW, Hu FC, Fang CC, Chang CC, Yen CJ. Sequence variants of peroxisome proliferator-activated receptor-gamma gene and the clinical courses of patients with end-stage renal disease. Dis Markers 2015;2015:763459.
11. Cheng K, Wang X, Yin H. Small-molecule inhibitors of the TLR3/dsRNA complex. J Am Chem Soc 2011;133:3764-3767.
12. Chiang C, Beljanski V, Yin K, Olagnier D, Ben Yebdri F, Steel C, Goulet ML, DeFilippis VR, Streblow DN, Haddad EK et al. Sequence-specific modifications enhance the broad spectrum antiviral response activated by RIG-I agonists. J Virol 2015;89:8011-8025.
13. Dasgupta G, BenMohamed L. Of mice and not humans: how reliable are animal models for evaluation of herpes CD8(+)-T cell-epitopes-based immunotherapeutic vaccine candidates? Vaccine 2011;29:5824-5836.
14. Doyle SE, Schreckhise H, Khuu-Duong K, Henderson K, Rosler R, Storey H, Yao L, Liu H, Barahmand-pour F, Sivakumar P et al. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 2006;44:896-906.
15. DrannikAG,NagK, SallenaveJM,Rosenthal KL.Antiviral activityof trappin-2and elafin in vitro and in vivo against genital herpes. J Virol 2013;87:7526-7538.
16. Duerst RJ, Morrison LA. Herpes simplex virus 2 virion host shutoff protein interferes with type I interferon production and responsiveness. Virology 2004;322:158-167.
17. Fichorova RN, Rheinwald JG, Anderson DJ. Generation of papillomavirusimmortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol Reprod 1997;57:847-855.
18. Fichorova RN, Cronin AO, Lien E, Anderson DJ, Ingalls RR. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J Immunol 2002; 168:2424-2432.
19. Fife KH, Warren TJ, Justus SE, Heitman CK. An international, randomized, double-blind, placebo-controlled, study of valacyclovir for the suppression of herpes simplex virus type 2 genital herpes in newly diagnosed patients. Sex Transm Dis 2008;35:668-673.
20. Finlay BB, McFadden G. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 2006;124:767-782.
21. Fujita T, Onoguchi K, Onomoto K, Hirai R, Yoneyama M. Triggering antiviral response by RIG-I-related RNA helicases. Biochimie 2007;89:754-760.
22. Funami K, SasaiM,OhbaY,Oshiumi H, SeyaT,MatsumotoM. Spatiotemporal mobilizationofToll/IL-1 receptor domain-containing adaptormolecule-1 in response to dsRNA. J Immunol 2007;179:6867-6872.
23. Gill N, Deacon PM, Lichty B, Mossman KL, Ashkar AA. Induction of innate immunity against herpes simplex virus type 2 infection via local delivery of Toll-like receptor ligands correlates with beta interferon production. J Virol 2006;80:9943-9950.
24. Gill N, Davies EJ, Ashkar AA. The role of toll-like receptor ligands/agonists in protection against genital HSV-2 infection. Am J Reprod Immunol 2008; 59:35-43.
25. Govender Y, Avenant C, Verhoog NJ, Ray RM, Grantham NJ, Africander D, Hapgood JP. The injectable-only contraceptive medroxyprogesterone acetate, unlike norethisterone acetate and progesterone, regulates inflammatory genes in endocervical cells via the glucocorticoid receptor. PLoS One 2014;9:e96497.
26. Harle P, Sainz B Jr, Carr DJ, HalfordWP. The immediate-early protein, ICP0, is essential for the resistance of herpes simplex virus to interferon-alpha/ beta. Virology 2002;293:295-304.
27. Herbst-Kralovetz MM, Pyles RB. Quantification of poly(I:C)-mediated protection against genital herpes simplex virus type 2 infection. J Virol 2006;80:9988-9997.
28. Hertz CJ,WuQ, Porter EM, Zhang YJ,Weismuller KH,Godowski PJ, GanzT, Randell SH, Modlin RL. Activation of Toll-like receptor 2 on human tracheobronchial epithelial cells induces the antimicrobial peptide human beta defensin-2. J Immunol 2003;171:6820-6826.
29. Hijazi K, Cuppone AM, Smith K, Stincarelli MA, Ekeruche-Makinde J, De Falco G, Hold GL, Shattock R, Kelly CG, Pozzi G et al. Expression of genes for drug transporters in the human female genital tract and modulatory effect of antiretroviral drugs. PLoS One 2015;10:e0131405.
30. Hou W, Wang X, Ye L, Zhou L, Yang ZQ, Riedel E, Ho WZ. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J Virol 2009;83:3834-3842.
31. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002;20:197-216.
32. Katze MG, He Y, GaleMJr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2002;2:675-687.
33. Kaushic C, Ashkar AA, Reid LA, Rosenthal KL. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 2003;77:4558-4565.
34. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003;4:69-77.
35. Li J, Ye L,Wang X, Hu S, HoW. Induction of interferon-Lambda contributes to Toll-like receptor 3-mediated herpes simplex virus type 1 inhibition in astrocytes. J Neurosci Res 2012;90:399-406.
36. Lin HD, Lin FJ, Chiang TY, Lee TW. The complete mitochondrial genome sequence of Metzia formosae (Cypriniformes, Cyprinidae). Mitochondrial DNA 2015;26:257-258.
37. Melroe GT, DeLuca NA, Knipe DM. Herpes simplex virus 1 has multiple mechanisms for blocking virus-induced interferon production. J Virol 2004;78:8411-8420.
38. Murphy JA, Duerst RJ, Smith TJ, Morrison LA. Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J Virol 2003; 77:9337-9345.
39. Nazli A, Yao XD, Smieja M, Rosenthal KL, Ashkar AA, Kaushic C. Differential induction of innate anti-viral responses by TLR ligands against Herpes simplex virus, type 2, infection in primary genital epithelium of women. Antiviral Res 2009;81:103-112.
40. Pletnev S, Magracheva E, Kozlov S, Tobin G, Kotenko SV, Wlodawer A, Zdanov A. Characterization of the recombinant extracellular domains of human interleukin-20 receptors and their complexes with interleukin-19 and interleukin-20. Biochemistry 2003;42:12617-12624.
41. Roizman B, Taddeo B. The strategy of herpes simplex virus replication and takeover of the host cell. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B,Whitley R, Yamanishi K (eds). Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Cambridge: Cambridge University Press, 2007.
42. SatheA, ReddyKV. TLR9 and RIG-I signaling in human endocervical epithelial cells modulates inflammatory responses of macrophages and dendritic cells in vitro. PLoS One 2014;9:e83882.
43. Schaefer TM, Desouza K, Fahey JV, BeagleyKW, Wira CR. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004;112:428-436.
44. Shao Q, XuW, Guo Q, Yan L, Rui L, Liu J, Zhao Y, Li Z. RIG-I from waterfowl and mammals differ in their abilities to induce antiviral responses against influenza A viruses. J Gen Virol 2015;96:277-287.
45. Smith MF Jr, Mitchell A, Li G, Ding S, Fitzmaurice AM, Ryan K, Crowe S, Goldberg JB. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J Biol Chem 2003; 278:32552-32560.
46. Sperling RS, Fife KH, Warren TJ, Dix LP, Brennan CA. The effect of daily valacyclovir suppression on herpes simplex virus type 2 viral shedding in HSV-2 seropositive subjects without a history of genital herpes. Sex Transm Dis 2008;35:286-290.
47. Verhoog NJ, Du Toit A, Avenant C, Hapgood JP. Glucocorticoidindependent repression of tumor necrosis factor (TNF) alpha-stimulated interleukin (IL)-6 expression by the glucocorticoid receptor: a potential mechanism for protection against an excessive inflammatory response. J Biol Chem 2011;286:19297-19310.
48. Wen G, Chen C, Guo J, Zhang Z, Shang Y, Shao H, Luo Q, Yang J,Wang H, Wang H et al. Development of a novel thermostable Newcastle disease virus vaccine vector for expression of a heterologous gene. J Gen Virol 2015;96:1219-1228.
49. Wira CR, Grant-Tschudy KS, Crane-Godreau MA. Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am J Reprod Immunol 2005;53:65-76.
50. Xing J, Ni L,Wang S,WangK, LinR,Zheng C.Herpes simplex virus 1-encoded tegument proteinVP16abrogates the productionofbeta interferon(IFN) by inhibiting NF-kappaB activation and blocking IFN regulatory factor 3 to recruit its coactivator CBP. J Virol 2013;87:9788-9801.
51. Yao XD, Rosenthal KL. Herpes simplex virus type 2 virion host shutoff protein suppresses innate dsRNA antiviral pathways in human vaginal epithelial cells. J Gen Virol 2011;92:1981-1993.
52. Zhang X, Chentoufi AA, Dasgupta G, Nesburn AB, Wu M, Zhu X, Carpenter D, Wechsler SL, You S, BenMohamed L. A genital tract peptide epitope vaccine targeting TLR-2 efficiently induces local and systemic CD8+ T cells and protects against herpes simplex virus type 2 challenge. Mucosal Immunol 2009;2:129-143.
53. ZhangX,Dervillez X,ChentoufiAA, BadakhshanT, Bettahi I, Benmohamed L. Targeting the genital tract mucosa with a lipopeptide/recombinant adenovirus prime/boost vaccine induces potent and long-lasting CD8+ T cell immunity against herpes: importance of MyD88. J Immunol 2012; 189:4496-4509.
54. Zhang X, Liang Z, Yin X, Shao X. Proteomic analysis of the occlusion derived virus of Clostera anachoreta granulovirus. J Gen Virol 2015;96:2394-2404.
55. Zhou L, Wang X, Wang YJ, Zhou Y, Hu S, Ye L, Hou W, Li H, Ho WZ. Activation of toll-like receptor-3 induces interferon-lambda expression in human neuronal cells. Neuroscience 2009a;159:629-637
56. Zhou Y, Ye L,WanQ, Zhou L,Wang X, Li J, Hu S, Zhou D,HoW. Activation of Toll-like receptors inhibits herpes simplex virus-1 infection of human neuronal cells. J Neurosci Res 2009b;87:2916-2925.