Interferon-λs and plasmacytoid dendritic cells: A close relationship

Frontiers in Immunology

Volumn 8, Issue AUG, 2017, Pages

  Finotti, Giulia ^a   Tamassia, Nicola ^a   Cassatella, Marco A ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85027978642     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01015     Document Type: Article

References (76)

1. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, et al. Nomenclature of monocytes and dendritic cells in blood. Blood (2010) 116:e74–80. doi:10.1182/blood-2010-02-258558
2. Lee J, Breton G, Oliveira TYK, Zhou YJ, Aljoufi A, Puhr S, et al. Restricted dendritic cell and monocyte progenitors in human cord blood and bone marrow. J Exp Med (2015) 212:385–99. doi:10.1084/jem.20141442
3. Collin M, Mcgovern N, Haniffa M. Human dendritic cell subsets. Immunology (2013) 140:22–30. doi:10.1111/imm.12117
4. Swiecki M, Colonna M. The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol (2015) 15:471–85. doi:10.1038/nri3865
5. Liu Y-J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol (2005) 23:275–306. doi:10.1146/annurev.immunol.23.021704.115633
6. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science (1999) 284:1835–7. doi:10.1016/S0887-7963(00)80131-5
7. Kadowaki N, Antonenko S, Lau JY-N, Liu Y-J. Natural interferon α/β– producing cells link innate and adaptive immunity. J Exp Med (2000) 192:219–26. doi:10.1084/jem.192.2.219
8. Ito T, Kanzler H, Duramad O, Cao W, Liu Y-J. Specialization, kinetics, and repertoire of type 1 interferon responses by human plasmacytoid predendritic cells. Blood (2006) 107:2423–31. doi:10.1182/blood-2005-07-2709
9. Dzionek A, Inagaki Y, Okawa K, Nagafune J, Röck J, Sohma Y, et al. Plasmacytoid dendritic cells: from specific surface markers to specific cellular functions. Hum Immunol (2002) 63:1133–48. doi:10.1016/S0198-8859(02)00752-8
10. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med (1997) 185:1101–11. doi:10.1084/jem.185.6.1101
11. Penna G, Vulcano M, Sozzani S, Adorini L. Differential migration behavior and chemokine production by myeloid and plasmacytoid dendritic cells. Hum Immunol (2002) 63:1164–71. doi:10.1016/S0198-8859(02)00755-3
12. Sozzani S, Vermi W, Del Prete A, Facchetti F. Trafficking properties of plasmacytoid dendritic cells in health and disease. Trends Immunol (2010) 31:270–7. doi:10.1016/j.it.2010.05.004
13. Decalf J, Fernandes S, Longman R, Ahloulay M, Audat F, Lefrerre F, et al. Plasmacytoid dendritic cells initiate a complex chemokine and cytokine network and are a viable drug target in chronic HCV patients. J Exp Med (2007) 204:2423–37. doi:10.1084/jem.20070814
14. Mathan TS, Figdor CG, Buschow SI. Human plasmacytoid dendritic cells: from molecules to intercellular communication network. Front Immunol (2013) 4:372. doi:10.3389/fimmu.2013.00372
15. Gilliet M, Cao W, Liu Y-J. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol (2008) 8:594–606. doi:10.1038/nri2358
16. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol (2014) 32:513–45. doi:10.1146/annurev-immunol-032713-120231
17. Trinchieri G. Type I interferon: friend or foe? J Exp Med (2010) 207:2053–63. doi:10.1084/jem.20101664
18. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol (2015) 15:87–103. doi:10.1038/ nri3787
19. Villadangos JA, Young L. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity (2008) 29:352–61. doi:10.1016/j.immuni.2008.09.002
20. Soumelis V, Liu YJ. From plasmacytoid to dendritic cell: morphological and functional switches during plasmacytoid pre-dendritic cell differentiation. Eur J Immunol (2006) 36:2286–92. doi:10.1002/eji.200636026
21. Piqueras B, Connolly J, Freitas H, Palucka AK, Banchereau J. Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood (2006) 107:2613–8. doi:10.1182/blood-2005-07-2965
22. Kohrgruber N, Halanek N, Gröger M, Winter D, Rappersberger K, Schmitt-Egenolf M, et al. Survival, maturation, and function of CD11c- and CD11c+ peripheral blood dendritic cells are differentially regulated by cytokines. J Immunol (1999) 163:3250–9.
23. Lepelletier Y, Zollinger R, Ghirelli C, Raynaud F, Hadj-Slimane R, Cappuccio A, et al. Toll-like receptor control of glucocorticoid-induced apoptosis in human plasmacytoid predendritic cells (pDCs). Blood (2010) 116:3389–97. doi:10.1182/blood-2010-05-282913
24. Fonteneau J-F, Gilliet M, Larsson M, Dasilva I, Münz C, Liu Y-J, et al. Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood (2003) 101:3520–6. doi:10.1182/blood-2002-10-3063
25. Coccia EM, Severa M, Giacomini E, Monneron D, Remoli ME, Julkunen I, et al. Viral infection and toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and mono-cyte-derived dendritic cells. Eur J Immunol (2004) 34:796–805. doi:10.1002/ eji.200324610
26. Megjugorac NJ, Gallagher GE, Gallagher G. Modulation of human plasmacytoid DC function by IFN-lambda1 (IL-29). J Leukoc Biol (2009) 86:1359–63. doi:10.1189/jlb.0509347
27. Yin Z, Dai J, Deng J, Sheikh F, Natalia M, Shih T, et al. Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells. J Immunol (2012) 189:2735–45. doi:10.4049/jimmunol.1102038
28. Hillyer P, Mane VP, Schramm LM, Puig M, Verthelyi D, Chen A, et al. Expression profiles of human interferon-alpha and interferon-lambda subtypes are ligand- and cell-dependent. Immunol Cell Biol (2012) 90:774–83. doi:10.1038/icb.2011.109
29. Murata K, Sugiyama M, Kimura T, Yoshio S, Kanto T, Kirikae I, et al. Ex vivo induction of IFN-λ3 by a TLR7 agonist determines response to Peg-IFN/ Ribavirin therapy in chronic hepatitis C patients. J Gastroenterol (2014) 49:126–37. doi:10.1007/s00535-013-0814-1
30. Zhang S, Kodys K, Li K, Szabo G. Human type 2 myeloid dendritic cells produce interferon-λ and amplify interferon-α in response to hepatitis C virus infection. Gastroenterology (2013) 144:414–25.e7. doi:10.1053/j.gastro.2012.10.034
31. Florentin J, Aouar B, Dental C, Thumann C, Firaguay G, Gondois-Rey F, et al. HCV glycoprotein E2 is a novel BDCA-2 ligand and acts as an inhibitor of IFN production by plasmacytoid dendritic cells. Blood (2012) 120:4544–51. doi:10.1182/blood-2012-02-413286
32. Yoshio S, Kanto T, Kuroda S, Matsubara T, Higashitani K, Kakita N, et al. Human blood dendritic cell antigen 3 (BDCA3)(+) dendritic cells are a potent producer of interferon-λ in response to hepatitis C virus. Hepatology (2013) 57:1705–15. doi:10.1002/hep.26182
33. Prokunina-Olsson L, Muchmore B, Tang W, Pfeiffer RM, Park H, Dickensheets H, et al. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat Genet (2013) 45:164–71. doi:10.1038/ng.2521
34. Donnelly RP, Kotenko SV. Interferon-lambda: a new addition to an old family. J Interferon Cytokine Res (2010) 30:555–64. doi:10.1089/jir.2010.0078
35. Syedbasha M, Egli A. Interferon Lambda: modulating immunity in infectious diseases. Front Immunol (2017) 8:119. doi:10.3389/fimmu.2017.00119
36. Kotenko SV, Durbin JE. Contribution of type III interferons to antiviral immunity: location, location, location. J Biol Chem (2017) 292:7295–303. doi:10.1074/jbc.R117.777102
37. Lazear H, Nice T, Diamond M. Interferon-λ: immune functions at Barrier surfaces and beyond. Immunity (2015) 43:15–28. doi:10.1016/j.immuni.2015.07.001
38. Stiff A, Carson W. Investigations of interferon-lambda for the treatment of cancer. J Innate Immun (2015) 7:243–50. doi:10.1159/000370113
39. de Weerd NA, Nguyen T. The interferons and their receptors-distribution and regulation. Immunol Cell Biol (2012) 90:483–91. doi:10.1038/icb.2012.9
40. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol (2003) 4:69–77. doi:10.1038/ni875
41. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol (2003) 4:63–8. doi:10.1038/ni873
42. Sommereyns C, Paul S, Staeheli P, Michiels T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog (2008) 4:e1000017. doi:10.1371/journal.ppat.1000017
43. Robek MD, Boyd BS, Chisari FV. Lambda interferon inhibits hepatitis B and C virus replication. J Virol (2005) 79:3851–4. doi:10.1128/JVI.79.6.3851-3854.2005
44. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature (2009) 461:798–801. doi:10.1038/nature08463
45. Diegelmann J, Beigel F, Zitzmann K, Kaul A, Göke B, Auernhammer CJ, et al. Comparative analysis of the lambda-interferons IL-28A and IL-29 regarding their transcriptome and their antiviral properties against hepatitis C virus. PLoS One (2010) 5:e15200. doi:10.1371/journal.pone.0015200
46. Pagliaccetti NE, Robek MD. Interferon-lambda in the immune response to hepatitis B virus and hepatitis C virus. J Interferon Cytokine Res (2010) 30:585–90. doi:10.1089/jir.2010.0060
47. Zhang L, Jilg N, Shao R-X, Lin W, Fusco DN, Zhao H, et al. IL28B inhibits hepatitis C virus replication through the JAK-STAT pathway. J Hepatol (2011) 55:289–98. doi:10.1016/j.jhep.2010.11.019
48. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature (2009) 461:399–401. doi:10.1038/nature08309
49. Suppiah V, Moldovan M, Ahlenstiel G, Berg T, Weltman M, Abate ML, et al. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet (2009) 41:1100–4. doi:10.1038/ng.447
50. Tanaka Y, Nishida N, Sugiyama M, Kurosaki M, Matsuura K, Sakamoto N, et al. Genome-wide association of IL28B with response to pegylated inter-feron-alpha and ribavirin therapy for chronic hepatitis C. Nat Genet (2009) 41:1105–9. doi:10.1038/ng.449
51. Muir AJ, Arora S, Everson G, Flisiak R, George J, Ghalib R, et al. A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection. J Hepatol (2014) 61:1238–46. doi:10.1016/j.jhep.2014.07.022
52. Ank N, Iversen MB, Bartholdy C, Staeheli P, Hartmann R, Jensen UB, et al. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J Immunol (2008) 180:2474–85. doi:10.4049/ jimmunol.180.4.2474
53. Witte K, Gruetz G, Volk H-D, Looman AC, Asadullah K, Sterry W, et al. Despite IFN-lambda receptor expression, blood immune cells, but not keratinocytes or melanocytes, have an impaired response to type III interferons: implications for therapeutic applications of these cytokines. Genes Immun (2009) 10:702–14. doi:10.1038/gene.2009.72
54. Finotti G, Tamassia N, Calzetti F, Fattovich G, Cassatella MA. Endogenously produced TNF-α contributes to the expression of CXCL10/IP-10 in IFN-λ3-activated plasmacytoid dendritic cells. J Leukoc Biol (2016) 99:107–19. doi:10.1189/jlb.3VMA0415-144R
55. Kelly A, Robinson MW, Roche G, Biron CA, O'Farrelly C, Ryan EJ. Immune cell profiling of IFN-λ response shows pDCs express highest level of IFN-λR1 and are directly responsive via the JAK-STAT pathway. J Interferon Cytokine Res (2016) 36:671–80. doi:10.1089/jir.2015.0169
56. Pekarek V, Srinivas S, Eskdale J, Gallagher G. Interferon lambda-1 (IFN-lambda1/IL-29) induces ELR(-) CXC chemokine mRNA in human peripheral blood mononuclear cells, in an IFN-gamma-independent manner. Genes Immun (2007) 8:177–80. doi:10.1038/sj.gene.6364372
57. Jordan WJ, Eskdale J, Boniotto M, Rodia M, Kellner D, Gallagher G. Modulation of the human cytokine response by interferon lambda-1 (IFN-λ1/ IL-29). Genes Immun (2007) 8:13–20. doi:10.1038/sj.gene.6364348
58. Davidson S, McCabe TM, Crotta S, Gad HH, Hessel EM, Beinke S, et al. IFNλ is a potent anti-influenza therapeutic without the inflammatory side effects of IFNα treatment. EMBO Mol Med (2016) 8:1099–112. doi:10.15252/ emmm.201606413
59. Finotti G, Tamassia N, Cassatella MA. Synergistic production of TNFα and IFNα by human pDCs incubated with IFNλ3 and IL-3. Cytokine (2016) 86:124–31. doi:10.1016/j.cyto.2016.08.005
60. O'Connor KS, Ahlenstiel G, Suppiah V, Schibeci S, Ong A, Leung R, et al. IFNL3 mediates interaction between innate immune cells: implications for hepatitis C virus pathogenesis. Innate Immun (2014) 20:598–605. doi:10.1177/1753425913503385
61. Marcello T, Grakoui A, Barba-Spaeth G, Machlin ES, Kotenko SV, MacDonald MR, et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology (2006) 131:1887–98. doi:10.1053/j.gastro.2006.09.052
62. Bolen CR, Ding S, Robek MD, Kleinstein SH. Dynamic expression profiling of type I and type III interferon-stimulated hepatocytes reveals a stable hierarchy of gene expression. Hepatology (2014) 59:1262–72. doi:10.1002/ hep.26657
63. Jilg N, Lin W, Hong J, Schaefer EA, Wolski D, Meixong J, et al. Kinetic differences in the induction of interferon stimulated genes by interferon-α and interleukin 28B are altered by infection with hepatitis C virus. Hepatology (2014) 59:1250–61. doi:10.1002/hep.26653
64. Odendall C, Dixit E, Stavru F, Bierne H, Franz KM, Durbin AF, et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat Immunol (2014) 15:717–28. doi:10.1038/ni.2915
65. Lee SJ, Kim WJ, Moon SK. Role of the p38 MAPK signaling pathway in mediating interleukin-28A-induced migration of UMUC-3 cells. Int J Mol Med (2012) 30:945–52. doi:10.3892/ijmm.2012.1064
66. Pervolaraki K, Stanifer ML, Münchau S, Renn LA, Albrecht D, Kurzhals S, et al. Type I and type III interferons display different dependency on mitogen-activated protein kinases to mount an antiviral state in the human gut. Front Immunol (2017) 8:459. doi:10.3389/fimmu.2017.00459
67. Kotenko SV, Langer JA. Full house: 12 receptors for 27 cytokines. Int Immunopharmacol (2004) 4:593–608. doi:10.1016/j.intimp.2004. 01.003
68. Wolk K, Witte K, Witte E, Raftery M, Kokolakis G, Philipp S, et al. IL-29 is produced by TH17 cells and mediates the cutaneous antiviral competence in psoriasis. Sci Transl Med (2013) 5:204ra129. doi:10.1126/scitranslmed. 3006245
69. Wu Q, Yang Q, Lourenco E, Sun H, Zhang Y. Interferon-lambda1 induces peripheral blood mononuclear cell-derived chemokines secretion in patients with systemic lupus erythematosus: its correlation with disease activity. Arthritis Res Ther (2011) 13:R88. doi:10.1186/ar3363
70. Oon S, Wilson NJ, Wicks I. Targeted therapeutics in SLE: emerging strategies to modulate the interferon pathway. Clin Transl Immunology (2016) 5:e79. doi:10.1038/cti.2016.26
71. Blazek K, Eames HL, Weiss M, Byrne AJ, Perocheau D, Pease JE, et al. IFN-λ resolves inflammation via suppression of neutrophil infiltration and IL-1β production. J Exp Med (2015) 212(6):845. doi:10.1084/jem. 20140995
72. Koch S, Finotto S. Role of interferon-λ in allergic asthma. J Innate Immun (2015) 7:224–30. doi:10.1159/000369459
73. Lasfar A, Zloza A, Cohen-Solal KA. IFN-lambda therapy: current status and future perspectives. Drug Discov Today (2016) 21:167–71. doi:10.1016/j. drudis.2015.10.021
74. Vermi W, Soncini M, Melocchi L, Sozzani S, Facchetti F. Plasmacytoid dendritic cells and cancer. J Leukoc Biol (2011) 90:681–90. doi:10.1189/jlb.0411190
75. Riboldi E, Daniele R, Cassatella MA, Sozzani S, Bosisio D. Engagement of BDCA-2 blocks TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. Immunobiology (2009) 214:868–76. doi:10.1016/j.imbio.2009.06.016
76. Lasfar A, Gogas H, Zloza A, Kaufman HL, Kirkwood JM. IFN-λ cancer immunotherapy: new kid on the block. Immunotherapy (2016) 8:877–88. doi:10.2217/imt-2015-0021