Interferon Regulator Factor 8 (IRF8) limits ocular pathology during HSV-1 infection by restraining the activation and expansion of CD8+ T cells

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Sun, Lin ^a   St Leger, Anthony J ^a   Yu, Cheng Rong ^a   He, Chang ^a,c   Mahdi, Rashid M ^a   Chan, Chi Chao ^a   Wang, Hongsheng ^b   Morse, Herbert C ^b   Egwuagu, Charles E ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; CHEMOKINE RECEPTOR; INTEGRIN; INTERFERON REGULATORY FACTOR; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; EYE INFECTION; EYE INFLAMMATION; GENE DELETION; HERPES SIMPLEX VIRUS 1; INFLAMMATORY CELL; KERATITIS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; T LYMPHOCYTE ACTIVATION; TRIGEMINUS GANGLION; VIRAL CLEARANCE; WILD TYPE MOUSE; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; COMPLICATION; EYE; HERPES SIMPLEX; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS LOAD;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; EYE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; IMMUNOLOGIC MEMORY; INFLAMMATION; INTEGRINS; INTERFERON REGULATORY FACTORS; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; RECEPTORS, CHEMOKINE; VIRAL LOAD;

EID: 84969902721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155420     Document Type: Article

References (45)

1. Lohoff M, Mak TW. Roles of interferon-regulatory factors in T-helper-cell differentiation. Nature reviews Immunology. 2005; 5(2):125-35. doi: 10.1038/nri1552 PMID: 15688040.
2. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annual review of immunology. 2008; 26:535-84. doi: 10.1146/annurev.immunol.26.021607.090400 PMID: 18303999.
3. Wang H, Lee CH, Qi C, Tailor P, Feng J, Abbasi S, et al. IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood. 2008; 112(10):4028-38. doi: 10.1182/blood-2008-01-129049 PMID: 18799728; PubMed Central PMCID: PMC2581985.
4. Horiuchi M, Wakayama K, Itoh A, Kawai K, Pleasure D, Ozato K, et al. Interferon regulatory factor 8/interferon consensus sequence binding protein is a critical transcription factor for the physiological phenotype of microglia. Journal of neuroinflammation. 2012; 9:227. doi: 10.1186/1742-2094-9-227 PMID: 23020843; PubMed Central PMCID: PMC3546867.
5. Minten C, Terry R, Deffrasnes C, King NJ, Campbell IL. IFN regulatory factor 8 is a key constitutive determinant of the morphological and molecular properties of microglia in the CNS. PloS one. 2012; 7(11):e49851. doi: 10.1371/journal.pone.0049851 PMID: 23166780; PubMed Central PMCID: PMC3498170.
6. Nelson N, Kanno Y, Hong C, Contursi C, Fujita T, Fowlkes BJ, et al. Expression of IFN regulatory factor family proteins in lymphocytes. Induction of Stat-1 and IFN consensus sequence binding protein expression by T cell activation. Journal of immunology. 1996; 156(10):3711-20. PMID: 8621906.
7. Ouyang X, Zhang R, Yang J, Li Q, Qin L, Zhu C, et al. Transcription factor IRF8 directs a silencing programme for TH17 cell differentiation. Nature communications. 2011; 2:314. doi: 10.1038/ncomms1311 PMID: 21587231; PubMed Central PMCID: PMC3112536.
8. Yoshida Y, Yoshimi R, Yoshii H, Kim D, Dey A, Xiong H, et al. The transcription factor IRF8 activates integrin-mediated TGF-beta signaling and promotes neuroinflammation. Immunity. 2014; 40(2):187-98. doi: 10.1016/j.immuni.2013.11.022 PMID: 24485804; PubMed Central PMCID: PMC4105266.
9. Xu F, Schillinger JA, Sternberg MR, Johnson RE, Lee FK, Nahmias AJ, et al. Seroprevalence and coinfection with herpes simplex virus type 1 and type 2 in the United States, 1988-1994. The Journal of infectious diseases. 2002; 185(8):1019-24. doi: 10.1086/340041 PMID: 11930310.
10. Feldman LT, Ellison AR, Voytek CC, Yang L, Krause P, Margolis TP. Spontaneous molecular reactivation of herpes simplex virus type 1 latency in mice. Proc Natl Acad Sci U S A. 2002; 99(2):978-83. doi: 10.1073/pnas.022301899 PMID: 11773630; PubMed Central PMCID: PMC117416.
11. Khanna KM, Bonneau RH, Kinchington PR, Hendricks RL. Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity. 2003; 18(5):593-603. PMID: 12753737; PubMed Central PMCID: PMC2871305.
12. Rowe AM, Leger AJ St, Jeon S, Dhaliwal DK, Knickelbein JE, Hendricks RL. Herpes keratitis. Progress in retinal and eye research. 2013; 32:88-101. doi: 10.1016/j.preteyeres.2012.08.002 PMID: 22944008; PubMed Central PMCID: PMC3529813.
13. Liu X, Lee YS, Yu CR, Egwuagu CE. Loss of STAT3 in CD4+ T cells prevents development of experimental autoimmune diseases. Journal of immunology. 2008; 180(9):6070-6. PMID: 18424728; PubMed Central PMCID: PMC2435016.
14. Hayashi K, Hooper LC, Chin MS, Nagineni CN, Detrick B, Hooks JJ. Herpes simplex virus 1 (HSV-1) DNA and immune complex (HSV-1-human IgG) elicit vigorous interleukin 6 release from infected corneal cells via Toll-like receptors. The Journal of general virology. 2006; 87(Pt 8):2161-9. doi: 10.1099/vir.0.81772-0 PMID: 16847112.
15. Amadi-Obi A, Yu CR, Liu X, Mahdi RM, Clarke GL, Nussenblatt RB, et al. T(H)17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med. 2007; 13(6):711-8. PMID: 17496900.
16. Oh HM, Yu CR, Golestaneh N, Amadi-Obi A, Lee YS, Eseonu A, et al. STAT3 protein promotes T-cell survival and inhibits interleukin-2 production through up-regulation of Class O Forkhead transcription factors. J Biol Chem. 2011; 286(35):30888-97. doi: 10.1074/jbc.M111.253500 PMID: 21730069; PubMed Central PMCID: PMC3162449.
17. Lee YS, Amadi-Obi A, Yu CR, Egwuagu CE. Retinal cells suppress intraocular inflammation (uveitis) through production of interleukin-27 and interleukin-10. Immunology. 2011; 132(4):492-502. Epub 2011/02/08. doi: 10.1111/j.1365-2567.2010.03379.x PMID: 21294722; PubMed Central PMCID: PMC3075503.
18. Shrikant PA, Rao R, Li Q, Kesterson J, Eppolito C, Mischo A, et al. Regulating functional cell fates in CD8 T cells. Immunologic research. 2010; 46(1-3):12-22. doi: 10.1007/s12026-009-8130-9 PMID: 19859830.
19. Mosmann TR, Li L, Hengartner H, Kagi D, Fu W, Sad S. Differentiation and functions of T cell subsets. Ciba Foundation symposium. 1997; 204:148-54; discussion 54-8. PMID: 9107418.
20. Kim SH, Burton J, Yu CR, Sun L, He C, Wang H, et al. Dual Function of the IRF8 Transcription Factor in Autoimmune Uveitis: Loss of IRF8 in T Cells Exacerbates Uveitis, Whereas Irf8 Deletion in the Retina Confers Protection. Journal of immunology. 2015; 195(4):1480-8. doi: 10.4049/jimmunol.1500653 PMID: 26163590; PubMed Central PMCID: PMC4530071.
21. Decman V, Kinchington PR, Harvey SA, Hendricks RL. Gamma interferon can block herpes simplex virus type 1 reactivation from latency, even in the presence of late gene expression. Journal of virology. 2005; 79(16):10339-47. doi: 10.1128/JVI.79.16.10339-10347.2005 PMID: 16051826; PubMed Central PMCID: PMC1182646.
22. Leger AJ St, Peters B, Sidney J, Sette A, Hendricks RL. Defining the herpes simplex virus-specific CD8+ T cell repertoire in C57BL/6 mice. J Immunol. 2011; 186(7):3927-33. doi: 10.4049/jimmunol.1003735 PMID: 21357536; PubMed Central PMCID: PMC3308013.
23. Yu CR, Hayashi K, Lee YS, Mahdi RM, Shen de F, Chan CC, et al. Suppressor of cytokine signaling 1 (SOCS1) mitigates anterior uveitis and confers protection against ocular HSV-1 infection. Inflammation. 2015; 38(2):555-65. doi: 10.1007/s10753-014-9962-6 PMID: 24993154; PubMed Central PMCID: PMC4282977.
24. Frank GM, Lepisto AJ, Freeman ML, Sheridan BS, Cherpes TL, Hendricks RL. Early CD4(+) T cell help prevents partial CD8(+) T cell exhaustion and promotes maintenance of Herpes Simplex Virus 1 latency. J Immunol. 2010; 184(1):277-86. doi: 10.4049/jimmunol.0902373 PMID: 19949087; PubMed Central PMCID: PMC3298035.
25. Leger AJ St, Jeon S, Hendricks RL. Broadening the repertoire of functional herpes simplex virus type 1-specific CD8+ T cells reduces viral reactivation from latency in sensory ganglia. J Immunol. 2013; 191(5):2258-65. doi: 10.4049/jimmunol.1300585 PMID: 23878317; PubMed Central PMCID: PMC3779892.
26. Jeon S, Leger AJ St, Cherpes TL, Sheridan BS, Hendricks RL. PD-L1/B7-H1 regulates the survival but not the function of CD8+ T cells in herpes simplex virus type 1 latently infected trigeminal ganglia. J Immunol. 2013; 190(12):6277-86. doi: 10.4049/jimmunol.1300582 PMID: 23656736; PubMed Central PMCID: PMC3679223.
27. Lee W, Kim HS, Baek SY, Lee GR. Transcription factor IRF8 controls Th1-like regulatory T-cell function. Cellular & molecular immunology. 2015. doi: 10.1038/cmi.2015.72 PMID: 26166768.
28. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity. 2007; 27(2):281-95. doi: 10.1016/j.immuni.2007.07.010 PMID: 17723218; PubMed Central PMCID: PMC2034442.
29. Thimme R, Appay V, Koschella M, Panther E, Roth E, Hislop AD, et al. Increased expression of the NK cell receptor KLRG1 by virus-specific CD8 T cells during persistent antigen stimulation. Journal of virology. 2005; 79(18):12112-6. doi: 10.1128/JVI.79.18.12112-12116.2005 PMID: 16140789; PubMed Central PMCID: PMC1212638.
30. Tokoyoda K, Hauser AE, Nakayama T, Radbruch A. Organization of immunological memory by bone marrow stroma. Nat Rev Immunol. 2010; 10(3):193-200. doi: 10.1038/nri2727 PMID: 20154734.
31. Cui W, Liu Y, Weinstein JS, Craft J, Kaech SM. An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity. 2011; 35(5):792-805. doi: 10.1016/j.immuni.2011.09.017 PMID: 22118527; PubMed Central PMCID: PMC3431922.
32. Waight JD, Netherby C, Hensen ML, Miller A, Hu Q, Liu S, et al. Myeloid-derived suppressor cell development is regulated by a STAT/IRF-8 axis. The Journal of clinical investigation. 2013; 123(10):4464-78. doi: 10.1172/JCI68189 PMID: 24091328; PubMed Central PMCID: PMC3784535.
33. Freeman ML, Sheridan BS, Bonneau RH, Hendricks RL. Psychological stress compromises CD8+ T cell control of latent herpes simplex virus type 1 infections. Journal of immunology. 2007; 179(1):322-8. PMID: 17579052; PubMed Central PMCID: PMC2367250.
34. Ellis TN, Beaman BL. Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology. 2004; 112(1):2-12. doi: 10.1111/j.1365-2567.2004.01849.x PMID: 15096178; PubMed Central PMCID: PMC1782470.
35. Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood. 1992; 80(8):2012-20. PMID: 1382715.
36. Egwuagu CE, Li W, Yu CR, Che Mei Lin M, Chan CC, Nakamura T, et al. Interferon-gamma induces regression of epithelial cell carcinoma: critical roles of IRF-1 and ICSBP transcription factors. Oncogene. 2006; 25(26):3670-9. doi: 10.1038/sj.onc.1209402 PMID: 16462767.
37. Kanno Y, Kozak CA, Schindler C, Driggers PH, Ennist DL, Gleason SL, et al. The genomic structure of the murine ICSBP gene reveals the presence of the gamma interferon-responsive element, to which an ISGF3 alpha subunit (or similar) molecule binds. Molecular and cellular biology. 1993; 13(7):3951-63. PMID: 8321202; PubMed Central PMCID: PMC359937.
38. Wang H, Yan M, Sun J, Jain S, Yoshimi R, Abolfath SM, et al. A reporter mouse reveals lineage-specific and heterogeneous expression of IRF8 during lymphoid and myeloid cell differentiation. J Immunol. 2014; 193(4):1766-77. doi: 10.4049/jimmunol.1301939 PMID: 25024380; PubMed Central PMCID: PMC4119573.
39. Miyagawa F, Zhang H, Terunuma A, Ozato K, Tagaya Y, Katz SI. Interferon regulatory factor 8 integrates T-cell receptor and cytokine-signaling pathways and drives effector differentiation of CD8 T cells. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(30):12123-8. doi: 10.1073/pnas.1201453109 PMID: 22783014; PubMed Central PMCID: PMC3409775.
40. Holtschke T, Lohler J, Kanno Y, Fehr T, Giese N, Rosenbauer F, et al. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell. 1996; 87(2):307-17. PMID: 8861914.
41. Sawada S, Scarborough JD, Killeen N, Littman DR. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell. 1994; 77(6):917-29. PMID: 8004678.
42. Hayashi K, Hooper LC, Hooks JJ. Who (what) pays toll for the development of herpetic stromal keratitis (HSK). Seminars in ophthalmology. 2008; 23(4):229-34. doi: 10.1080/08820530802111408 PMID: 18584560.
43. Suryawanshi A, Veiga-Parga T, Rajasagi NK, Reddy PB, Sehrawat S, Sharma S, et al. Role of IL-17 and Th17 cells in herpes simplex virus-induced corneal immunopathology. Journal of immunology. 2011; 187(4):1919-30. doi: 10.4049/jimmunol.1100736 PMID: 21765013; PubMed Central PMCID: PMC3150378.
44. Tang Q, Hendricks RL. Interferon gamma regulates platelet endothelial cell adhesion molecule 1 expression and neutrophil infiltration into herpes simplex virus-infected mouse corneas. The Journal of experimental medicine. 1996; 184(4):1435-47. PMID: 8879215; PubMed Central PMCID: PMC2192815.
45. Zaid A, Mackay LK, Rahimpour A, Braun A, Veldhoen M, Carbone FR, et al. Persistence of skin-resident memory T cells within an epidermal niche. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111(14):5307-12. doi: 10.1073/pnas.1322292111 PMID: 24706879; PubMed Central PMCID: PMC3986170.