CD8α dendritic cells drive establishment of HSV-1 latency

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Mott, Kevin R ^a   Allen, Sariah J ^a   Zandian, Mandana ^a   Konda, Bindu ^b   Sharifi, Behrooz G ^b   Jones, Clinton ^c   Wechsler, Steven L ^d   Town, Terrence ^e   Ghiasi, Homayon ^a  

^a BURNS AND ALLEN RESEARCH INSTITUTE   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8ALPHA ANTIGEN; CD8 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL TRANSFER; CONTROLLED STUDY; DENDRITIC CELL; EYE INFECTION; HERPES SIMPLEX VIRUS 1; INNATE IMMUNITY; MOUSE; NONHUMAN; PHENOTYPE; TRIGEMINUS GANGLION; VIRUS LATENCY; ADOPTIVE TRANSFER; ANIMAL; C3H MOUSE; C57BL MOUSE; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PROCEDURES; RECURRENT DISEASE; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD8; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HERPESVIRUS 1, HUMAN; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; RECURRENCE; TRIGEMINAL GANGLION; VIRUS LATENCY;

EID: 84898843954     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093444     Document Type: Article

References (71)

1. Dawson CR (1984) Ocular herpes simplex virus infections. Clin Dermatol 2: 56-66.
2. Barron BA, Gee L, Hauck WW, Kurinij N, Dawson CR, et al. (1994) Herpetic Eye Disease Study. A controlled trial of oral acyclovir for herpes simplex stromal keratitis. Ophthalmology 101: 1871-1882.
3. Wilhelmus KR, Dawson CR, Barron BA, Bacchetti P, Gee L, et al. (1996) Risk factors for herpes simplex virus epithelial keratitis recurring during treatment of stromal keratitis or iridocyclitis. Herpetic Eye Disease Study Group. Br J Ophthalmol 80: 969-972. (Pubitemid 26413698)
4. Oh JO, Kimura SJ, Ostler HB, Dawson CR, Smolin G (1976) Oculogenital transmission of type 2 herpes simplex virus in adults. Surv Ophthalmol 21: 106-109.
5. Pavan-Langston D (1983) Ocular viral infections. Med Clin North Am 67: 973-990.
6. Corey L (1994) The current trend in genital herpes. Progress in prevention. Sex Transm Dis 21: S38-S44.
7. Gordon YJ (1990) Pathogenesis and latency of herpes simplex virus type 1 (HSV-1): an ophthalmologist's view of the eye as a model for the study of the virus- host relationship. Adv Exp Med Biol 278: 205-209.
8. Kaufman HE, Azcuy AM, Varnell ED, Sloop GD, Thompson HW, et al. (2005) HSV-1 DNA in tears and saliva of normal adults. Invest Ophthalmol Vis Sci 46: 241-247. (Pubitemid 40041203)
9. Steiner I (1996) Human herpes viruses latent infection in the nervous system. Immunol Rev 152: 157-173.
10. Doymaz MZ, Rouse BT (1992) Herpetic stromal keratitis: an immunopathologic disease mediated by CD4+ T lymphocytes. Invest Ophthalmol Vis Sci 33: 2165-2173.
11. Liu T, Khanna KM, Chen X, Fink DJ, Hendricks RL (2000) CD8(+) T cells can block herpes simplex virus type 1 (HSV-1) reactivation from latency in sensory neurons. J Exp Med 191: 1459-1466. (Pubitemid 30257343)
12. Khanna KM, Bonneau RH, Kinchington PR, Hendricks RL (2003) Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18: 593-603. (Pubitemid 36588577)
13. Allen SJ, Hamrah P, Gate DM, Mott KR, Mantopoulos D, et al. (2011) The role of LAT in increased CD8+ T cell exhaustion in trigeminal ganglia of mice latently infected with herpes simplex virus type 1. J Virol 85: 4184-4197.
14. Mott KR, Bresee CJ, Allen SJ, BenMohamed L, Wechsler SL, et al. (2009) Level of herpes simplex virus type 1 latency correlates with severity of corneal scarring and exhaustion of CD8+ T cells in trigeminal ganglia of latently infected mice. J Virol 83: 2246-2254.
15. Mott KR, Ghiasi H (2008) Role of dendritic cells in enhancement of herpes simplex virus type 1 latency and reactivation in vaccinated mice. Clin Vaccine Immunol 15: 1859-1867.
16. Tailor P, Tamura T, Morse HC, 3rd, Ozato K (2008) The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood 111: 1942-1945. (Pubitemid 351451503)
17. Fung-Leung WP, Schilham MW, Rahemtulla A, Kundig TM, Vollenweider M, et al. (1991) CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 65: 443-449. (Pubitemid 121002054)
18. Osorio Y, Ghiasi H (2003) Comparison of adjuvant efficacy of herpes simplex virus type 1 recombinant viruses expressing TH1 and TH2 cytokine genes. J Virol 77: 5774-5783. (Pubitemid 36538970)
19. Perng GC, Dunkel EC, Geary PA, Slanina SM, Ghiasi H, et al. (1994) The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. J Virol 68: 8045-8055. (Pubitemid 24362693)
20. Crooks ME, Littman DR (1994) Disruption of T lymphocyte positive and negative selection in mice lacking the CD8 beta chain. Immunity 1: 277-285.
21. Gilliet M, Boonstra A, Paturel C, Antonenko S, Xu XL, et al. (2002) The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J Exp Med 195: 953-958. (Pubitemid 34286765)
22. Balkhi MY, Latchumanan VK, Singh B, Sharma P, Natarajan K (2004) Cross-regulation of CD86 by CD80 differentially regulates T helper responses from Mycobacterium tuberculosis secretory antigen-activated dendritic cell subsets. J Leukoc Biol 75: 874-883. (Pubitemid 38580068)
23. Ahmed R, King CC, Oldstone MB (1987) Virus-lymphocyte interaction: T cells of the helper subset are infected with lymphocytic choriomeningitis virus during persistent infection in vivo. J Virol 61: 1571-1576. (Pubitemid 17069750)
24. Mott KR, Underhill D, Wechsler SL, Town T, Ghiasi H (2009) A role for the JAK-STAT1 pathway in blocking replication of HSV-1 in dendritic cells and macrophages. Virol J 6: 56.
25. Mott KR, Perng GC, Osorio Y, Kousoulas KG, Ghiasi H (2007) A Recombinant Herpes Simplex Virus Type 1 Expressing Two Additional Copies of gK Is More Pathogenic than Wild-Type Virus in Two Different Strains of Mice. J Virol 81: 12962-12972. (Pubitemid 350156934)
26. Mott KR, Osorio Y, Brown DJ, Morishige N, Wahlert A, et al. (2007) The corneas of naive mice contain both CD4+ and CD8+ T cells. Mol Vis 13: 1802-1812. (Pubitemid 47520913)
27. Braaten DC, McClellan JS, Messaoudi I, Tibbetts SA, McClellan KB, et al. (2006) Effective control of chronic gamma-herpesvirus infection by unconventional MHC Class Ia-independent CD8 T cells. PLoS Pathog 2: e37.
28. Rock DL, Nesburn AB, Ghiasi H, Ong J, Lewis TL, et al. (1987) Detection of latency-related viral RNAs in trigeminal ganglia of rabbits latently infected with herpes simplex virus type 1. J Virol 61: 3820-3826. (Pubitemid 18011480)
29. Dobson AT, Margolis TP, Sedarati F, Stevens JG, Feldman LT (1990) A latent, nonpathogenic HSV-1-derived vector stably expresses beta- galactosidase in mouse neurons. Neuron 5: 353-360. (Pubitemid 20294985)
30. Zamoyska R (1994) The CD8 coreceptor revisited: one chain good, two chains better. Immunity 1: 243-246.
31. Lombardi V, Speak AO, Kerzerho J, Szely N, Akbari O (2012) CD8alpha(+)beta(-) and CD8alpha(+)beta(+) plasmacytoid dendritic cells induce Foxp3(+) regulatory T cells and prevent the induction of airway hyper-reactivity. Mucosal Immunol 5: 432-443.
32. Devine L, Kieffer LJ, Aitken V, Kavathas PB (2000) Human CD8 beta, but not mouse CD8 beta, can be expressed in the absence of CD8 alpha as a beta beta homodimer. J Immunol 164: 833-838. (Pubitemid 30043707)
33. Gorman SD, Sun YH, Zamoyska R, Parnes JR (1988) Molecular linkage of the Ly-3 and Ly-2 genes. Requirement of Ly-2 for Ly-3 surface expression. J Immunol 140: 3646-3653.
34. Aliberti J, Schulz O, Pennington DJ, Tsujimura H, Reis e Sousa C, et al. (2003) Essential role for ICSBP in the in vivo development of murine CD8alpha+ dendritic cells. Blood 101: 305-310. (Pubitemid 36025923)
35. Turcotte K, Gauthier S, Mitsos LM, Shustik C, Copeland NG, et al. (2004) Genetic control of myeloproliferation in BXH-2 mice. Blood 103: 2343-2350. (Pubitemid 38326256)
36. Stevens JG (1989) Human herpesviruses: a consideration of the latent state. Microbiol Rev 53: 318-332.
37. Wechsler SL, Nesburn AB, Watson R, Slanina S, Ghiasi H (1988) Fine mapping of the major latency-related RNA of herpes simplex virus type 1 in humans. J Gen Virol 69: 3101-3106. (Pubitemid 19026486)
38. Fraser NW, Valyi-Nagy T (1993) Viral, neuronal and immune factors which may influence herpes simplex virus (HSV) latency and reactivation. Microb Pathog 15: 83-91.
39. Mott KR, UnderHill D, Wechsler SL, Ghiasi H (2008) Lymphoid-related CD11c+CD8a+ dendritic cells are involved in enhancing HSV-1 latency. J Virol 82: 9870-9879.
40. Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7: 19-30. (Pubitemid 46020824)
41. Belz GT, Nutt SL (2012) Transcriptional programming of the dendritic cell network. Nat Rev Immunol 12: 101-113.
42. den Haan JM, Lehar SM, Bevan MJ (2000) CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192: 1685-1696.
43. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, et al. (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111. (Pubitemid 46196991)
44. Belz GT, Smith CM, Eichner D, Shortman K, Karupiah G, et al. (2004) Cutting edge: conventional CD8alpha(+) dendritic cells are generally involved in priming CTL immunity to viruses. J Immunol 172: 1996-2000. (Pubitemid 38182342)
45. Belz GT, Behrens GM, Smith CM, Miller JF, Jones C, et al. (2002) The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med 196: 1099-1104. (Pubitemid 35231768)
46. Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y, et al. (2002) The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 195: 1289-1302. (Pubitemid 34564331)
47. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, et al. (2007) Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 207: 1247-1260.
48. Allenspach EJ, Lemos MP, Porrett PM, Turka LA, Laufer TM (2008) Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity 29: 795-806.
49. Maldonado-Lopez R, Moser M (2001) Dendritic cell subsets and the regulation of Th1/Th2 responses. Semin Immunol 13: 275-282. (Pubitemid 32744578)
50. den Haan JM, Bevan MJ (2002) Constitutive versus activation-dependent cross-presentation of immune complexes by CD8(+) and CD8(-) dendritic cells in vivo. J Exp Med 196: 817-827.
51. Kawamura K, Kadowaki N, Kitawaki T, Uchiyama T (2006) Virus-stimulated plasmacytoid dendritic cells induce CD4+ cytotoxic regulatory T cells. Blood 107: 1031-1038. (Pubitemid 43156302)
52. Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL (2012) Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 86: 6792-6803.
53. Zhou Y, Callendret B, Xu D, Brasky KM, Feng Z, et al. (2012) Dominance of the CD4(+) T helper cell response during acute resolving hepatitis A virus infection. J Exp Med 209: 1481-1492.
54. Lee HK, Zamora M, Linehan MM, Iijima N, Gonzalez D, et al. (2009) Differential roles of migratory and resident DCs in T cell priming after mucosal or skin HSV-1 infection. J Exp Med 206: 359-370.
55. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
56. Schnorrer P, Behrens GM, Wilson NS, Pooley JL, Smith CM, et al. (2006) The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U S A 103: 10729-10734. (Pubitemid 44078044)
57. Alaniz RC, Sandall S, Thomas EK, Wilson CB (2004) Increased dendritic cell numbers impair protective immunity to intracellular bacteria despite augmenting antigen-specific CD8(+) T lymphocyte responses. J Immunol 172: 3725-3735. (Pubitemid 38337957)
58. Edelson BT, Bradstreet TR, Hildner K, Carrero JA, Frederick KE, et al. (2011) CD8alpha(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 35: 236-248.
59. Engelmayer J, Larsson M, Subklewe M, Chahroudi A, Cox WI, et al. (1999) Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J Immunol 163: 6762-6768.
60. Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM (1998) Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 72: 2733-2737. (Pubitemid 28175508)
61. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
62. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, et al. (2000) Human skin Langerhans cells are targets of dengue virus infection. Nature Medicine 6: 816-820. (Pubitemid 30469433)
63. Paroli M, Schiaffella E, Di Rosa F, Barnaba V (2000) Persisting viruses and autoimmunity. J Neuroimmunol 107: 201-204. (Pubitemid 30347428)
64. Ganguly D, Haak S, Sisirak V, Reizis B (2013) The role of dendritic cells in autoimmunity. Nat Rev Immunol 13: 566-577.
65. Kautz-Neu K, Noordegraaf M, Dinges S, Bennett CL, John D, et al. (2011) Langerhans cells are negative regulators of the anti-Leishmania response. J Exp Med 208: 885-891.
66. Frank GM, Buela KA, Maker DM, Harvey SA, Hendricks RL (2012) Early responding dendritic cells direct the local NK response to control herpes simplex virus 1 infection within the cornea. J Immunol 188: 1350-1359.
67. Kobelt D, Lechmann M, Steinkasserer A (2003) The interaction between dendritic cells and herpes simplex virus-1. Curr Top Microbiol Immunol 276: 145-161. (Pubitemid 36538351)
68. Salio M, Cella M, Suter M, Lanzavecchia A (1999) Inhibition of dendritic cell maturation by herpes simplex virus. Eur J Immunol 29: 3245-3253. (Pubitemid 29484215)
69. Kruse M, Rosorius O, Kratzer F, Stelz G, Kuhnt C, et al. (2000) Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J Virol 74: 7127-7136. (Pubitemid 30470697)
70. Stefanidou M, Ramos I, Mas Casullo V, Trepanier JB, Rosenbaum S, et al. (2013) HSV-2 Prevents Dendritic Cell Maturation, Induces Apoptosis and Triggers Release of Pro-inflammatory Cytokines: Potential Links to HSV-HIV Synergy. J Virol 87: 1443-1453.
71. Liu T, Khanna KM, Carriere BN, Hendricks RL (2001) Gamma interferon can prevent herpes simplex virus type 1 reactivation from latency in sensory neurons. J Virol 75: 11178-11184. (Pubitemid 33031584)