Interferon (IFN)-λ takes the helm: Immunomodulatory roles of type III IFNs

Frontiers in Immunology

Volumn 8, Issue NOV, 2017, Pages

  Zanoni, Ivan ^a,b   Granucci, Francesca ^b   Broggi, Achille ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Bacterial infections; Dendritic cells; Fungal infection; Interferon lambda; Natural killer cells; Neutrophils; Type III interferon; Viral infection

Indexed keywords

INTERFERON; INTERFERON LAMBDA; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; JANUS KINASE; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CELL MATURATION; CELL MIGRATION; CYTOKINE PRODUCTION; DENDRITIC CELL; EXTRACELLULAR TRAP; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; MACROPHAGE; NATURAL KILLER CELL; NEUTROPHIL; PHAGOCYTOSIS; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS LOAD;

EID: 85035335577     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01661     Document Type: Review

References (65)

1. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci (1957) 147:258-67. doi:10.1098/rspb.1957.0049
2. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol (2003) 4:69-77. doi:10.1038/ni875
3. 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
4. Fox BA, Sheppard PO, O'Hara PJ. The role of genomic data in the discovery, annotation and evolutionary interpretation of the interferon-lambda family. PLoS One (2009) 4:e4933. doi:10.1371/journal.pone.0004933
5. Kotenko SV. IFN-λs. Curr Opin Immunol (2011) 23:583-90. doi:10.1016/j.coi.2011.07.007
6. Odendall C, Kagan JC. The unique regulation and functions of type III interferons in antiviral immunity. Curr Opin Virol (2015) 12:47-52. doi:10.1016/j.coviro.2015.02.003
7. 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
8. Lazear HM, Nice TJ, Diamond MS. Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity (2015) 43:15-28. doi:10.1016/j.immuni.2015.07.001
9. Odendall C, Voak AA, Kagan JC. Type III IFNs are commonly induced by bacteria-sensing TLRs and reinforce epithelial barriers during infection. J Immunol (2017) 199:3270-9. doi:10.4049/jimmunol.1700250
10. 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 monocyte-derived dendritic cells. Eur J Immunol (2004) 34:796-805. doi:10.1002/eji.200324610
11. Bierne H, Travier L, Mahlakõiv T, Tailleux L, Subtil A, Lebreton A, et al. Activation of type III interferon genes by pathogenic bacteria in infected epithelial cells and mouse placenta. PLoS One (2012) 7:e39080. doi:10.1371/journal.pone.0039080
12. Mahlakõiv T, Hernandez P, Gronke K, Diefenbach A, Staeheli P. Leukocyte-derived IFN-α/β and epithelial IFN-λ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog (2015) 11:e1004782. doi:10.1371/journal.ppat.1004782
13. Sato S, Li K, Kameyama T, Hayashi T, Ishida Y, Murakami S, et al. The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity (2015) 42:123-32. doi:10.1016/j.immuni.2014.12.016
14. 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) 15:717-26. doi:10.1038/ni.2915
15. Sommereyns C, Paul S, Staeheli P, Michiels T. IFN-lambda (IFN-λ) 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
16. Baldridge MT, Lee S, Brown JJ, McAllister N, Urbanek K, Dermody TS, et al. Expression of Ifnlr1 on intestinal epithelial cells is critical to the antiviral effects of IFN-lambda against norovirus and reovirus. J Virol (2017) 13:91(7). doi:10.1128/JVI.02079-16
17. Lin J-D, Feng N, Sen A, Balan M, Tseng H-C, McElrath C, et al. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLoS Pathog (2016) 12:e1005600. doi:10.1371/journal.ppat.1005600
18. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM, Artyomov M, et al. Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science (2015) 347:269-73. doi:10.1126/science.1258100
19. Galani IE, Triantafyllia V, Eleminiadou E-E, Koltsida O, Stavropoulos A, Manioudaki M, et al. Interferon-λ mediates non-redundant front-line antiviral protection against influenza virus infection without compromising host fitness. Immunity (2017) 46:875-90.e6. doi:10.1016/j.immuni.2017.04.025
20. Broggi A, Tan Y, Granucci F, Zanoni I. IFN-λ suppresses intestinal inflammation by non-translational regulation of neutrophil function. Nat Immunol (2017) 18:1084-93. doi:10.1038/ni.3821
21. 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) 212:845-53. doi:10.1084/jem.20140995
22. Chrysanthopoulou A, Kambas K, Stakos D, Mitroulis I, Mitsios A, Vidali V, et al. Interferon lambda1/IL-29 and inorganic polyphosphate are novel regulators of neutrophil-driven thromboinflammation. J Pathol (2017) 243:111-22. doi:10.1002/path.4935
23. Lasfar A, de laTorre A, Abushahba W, Cohen-Solal KA, Castaneda I, Yuan Y, et al. Concerted action of IFN-a and IFN-λ induces local NK cell immunity and halts cancer growth. Oncotarget (2016) 7:49259-67. doi:10.18632/oncotarget.10272
24. Wang Y, Li T, Chen Y, Wei H, Sun R, Tian Z. Involvement of NK cells in IL-28B-mediated immunity against influenza virus infection. J Immunol (2017) 199:1012-20. doi:10.4049/jimmunol.1601430
25. Koltsida O, Hausding M, Stavropoulos A, Koch S, Tzelepis G, Ubel C, et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med (2011) 3:348-61. doi:10.1002/emmm.201100142
26. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med (2013) 210:1283-99. doi:10.1084/jem.20122220
27. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol (2011) 11:519-31. doi:10.1038/nri3024
28. Campbell EL, Bruyninckx WJ, Kelly CJ, Glover LE, McNamee EN, Bowers BE, et al. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity (2014) 40:66-77. doi:10.1016/j.immuni.2013.11.020
29. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol (2012) 5:354-66. doi:10.1038/mi.2012.24
30. Espinosa V, Dutta O, McElrath C, Du P, Chang Y-J, Cicciarelli B, et al. Type III interferon is a critical regulator of innate antifungal immunity. Sci Immunol (2017) 2:eaan5357. doi:10.1126/sciimmunol.aan5357
31. Kambas K, Mitroulis I, Apostolidou E, Girod A, Chrysanthopoulou A, Pneumatikos I, et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS One (2012) 7:e45427. doi:10.1371/journal.pone.0045427
32. Meager A, Visvalingam K, Dilger P, Bryan D, Wadhwa M. Biological activity of interleukins-28 and-29: comparison with type I interferons. Cytokine (2005) 31:109-18. doi:10.1016/j.cyto.2005.04.003
33. Rauch I, Rosebrock F, Hainzl E, Heider S, Majoros A, Wienerroither S, et al. Noncanonical effects of IRF9 in intestinal inflammation: more than type I and type III interferons. Mol Cell Biol (2015) 35:2332-43. doi:10.1128/MCB.01498-14
34. Chiriac M, Günther C, Becker C, Siebler J, Neurath M. IL-28-dependent activation of epithelial STAT1 drives epithelial wound healing in inflammatory bowel disease. Gastroenterology (2017) 152:S90. doi:10.1016/S0016-5085(17)30650-9
35. Yang J-Y, Kim M-S, Kim E, Cheon JH, Lee Y-S, Kim Y, et al. Enteric viruses ameliorate gut inflammation via toll-like receptor 3 and toll-like receptor 7-mediated interferon-β production. Immunity (2016) 44:889-900. doi:10.1016/j.immuni.2016.03.009
36. Sun L, Nava GM, Stappenbeck TS. Host genetic susceptibility, dysbiosis and viral triggers in IBD. Curr Opin Gastroenterol (2011) 27:321-7. doi:10.1097/MOG.0b013e32834661b4
37. Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY, Keller BC, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell (2015) 160:447-60. doi:10.1016/j.cell.2015.01.002
38. Mennechet FJD, Uzé G. Interferon-λ-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood (2006) 107:4417-23. doi:10.1182/blood-2005-10-4129
39. Jordan WJ, Eskdale J, Srinivas S, Pekarek V. Human interferon lambda-1 (IFN-1/IL-29) modulates the Th1/Th2 response. Genes Immun (2007) 8:254-61. doi:10.1038/sj.gene.6364382
40. Finotti G, Tamassia N, Cassatella MA. Interferon-λs and plasmacytoid dendritic cells: a close relationship. Front Immunol (2017) 8:e74. doi:10.3389/fimmu.2017.01015
41. Megjugorac NJ, Gallagher GE, Gallagher G. IL-4 enhances IFN-λ1 (IL-29) production by plasmacytoid DCs via monocyte secretion of IL-1Ra. Blood (2010) 15:4185-90. doi:10.1182/blood-2009-09-246157
42. Liu F, Liu C, Hu X, Shang Y, Wu L. MicroRNA-21: a positive regulator for optimal production of type I and type III interferon by plasmacytoid dendritic cells. Front Immunol (2017) 8:947. doi:10.3389/fimmu.2017.00947
43. 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
44. Finotti G, Tamassia N, Calzetti F, Fattovich G, Cassatella MA. Endogenously produced TNF-a 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
45. Finotti G, Tamassia N, Cassatella MA. Synergistic production of TNFa and IFNa by human pDCs incubated with IFNλ3 and IL-3. Cytokine (2016) 86:124-31. doi:10.1016/j.cyto.2016.08.005
46. Morrow MP, Pankhong P, Laddy DJ, Schoenly KA, Yan J, Cisper N, et al. Comparative ability of IL-12 and IL-28B to regulate Treg populations and enhance adaptive cellular immunity. Blood (2009) 113:5868-77. doi:10.1182/blood-2008-11-190520
47. Krämer B, Eisenhardt M, Glässner A. Do λ-IFNs IL28A and IL28B act on human natural killer cells? Proc Natl Acad Sci U S A (2011) 108:E519-20. doi:10.1073/pnas.1108850108
48. Gardiner CM, Morrison MH, Dring MM. Reply to Krämer et al.: Human natural killer (NK) cell inhibition by IL28A. Proc Natl Acad Sci U S A (2011) 108:E521-2. doi:10.1073/pnas.1109288108
49. Morrison MH, Keane C, Quinn LM, Kelly A, O'Farrelly C, Bergin C, et al. IFNL cytokines do not modulate human or murine NK cell functions. Hum Immunol (2014) 75:996-1000. doi:10.1016/j.humimm.2014.06.016
50. Souza-Fonseca-Guimaraes F, Young A, Mittal D, Martinet L, Bruedigam C, Takeda K, et al. NK cells require IL-28R for optimal in vivo activity. Proc Natl Acad Sci U S A (2015) 112:E2376. doi:10.1073/pnas.1424241112
51. Granucci F, Zanoni I, Pavelka N, van Dommelen SLH, Andoniou CE, Belardelli F, et al. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J Exp Med (2004) 200:287-95. doi:10.1084/jem.20040370
52. Granucci F, Zanoni I, Ricciardi-Castagnoli P. Central role of dendritic cells in the regulation and deregulation of immune responses. Cell Mol Life Sci (2008) 65:1683-97. doi:10.1007/s00018-008-8009-2
53. Zanoni I, Spreafico R, Bodio C, Di Gioia M, Cigni C, Broggi A, et al. IL-15 cis presentation is required for optimal NK cell activation in lipopolysaccharide-mediated inflammatory conditions. Cell Rep (2013) 4:1235-49. doi:10.1016/j.celrep.2013.08.021
54. Mingozzi F, Spreafico R, Gorletta T, Cigni C, Di Gioia M, Caccia M, et al. Prolonged contact with dendritic cells turns lymph node-resident NK cells into anti-tumor effectors. EMBO Mol Med (2016) 8:1039-51. doi:10.15252/emmm.201506164
55. Ferlazzo G, Pack M, Thomas D, Paludan C, Schmid D, Strowig T, et al. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci U S A (2004) 101:16606-11. doi:10.1073/pnas.0407522101
56. Ferlazzo G, Morandi B, D'Agostino A, Meazza R, Melioli G, Moretta A, et al. The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells. Eur J Immunol (2003) 33:306-13. doi:10.1002/immu.200310004
57. Jaeger BN, Donadieu J, Cognet C, Bernat C, Ordoñez-Rueda D, Barlogis V, et al. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med (2012) 209:565-80. doi:10.1084/jem.20111908
58. Costantini C, Cassatella MA. The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol (2011) 89:221-33. doi:10.1189/jlb.0510250
59. Muneo N, Tagawa M, Iwata F, Suzuki T, Nakamura A, Okada M, et al. IL-28 elicits antitumor responses against murine fibrosarcoma. J Immunol (2007) 178:5086-98. doi:10.4049/jimmunol.178.8.5086
60. Zhang S, Kodys K, Li K, Szabo G. Human type 2 myeloid dendritic cells produce interferon-λ and amplify interferon-a in response to hepatitis C virus infection. Gastroenterology (2013) 144:414-25.e7. doi:10.1053/j.gastro.2012.10.034
61. de Groen RA, Groothuismink ZMA, Liu BS, Boonstra A. IFN-λ is able to augment TLR-mediated activation and subsequent function of primary human B cells. J Leukoc Biol (2015) 98:623-30. doi:10.1189/jlb.3A0215-041RR
62. Wang X, Wang H, Liu M-Q, Li J-L, Zhou R-H, Zhou Y, et al. IFN-λ inhibits drug-resistant HIV infection of macrophages. Front Immunol (2017) 8:210. doi:10.3389/fimmu.2017.00210
63. Hou W, Wang X, Ye L, Zhou L, Yang ZQ, Riedel E, et al. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J Virol (2009) 83:3834-42. doi:10.1128/JVI.01773-08
64. Liu B-S, Janssen HLA, Boonstra A. IL-29 and IFNa differ in their ability to modulate IL-12 production by TLR-activated human macrophages and exhibit differential regulation of the IFNλ receptor expression. Blood (2011) 117:2385-95. doi:10.1182/blood-2010-07-298976
65. Witte K, Gruetz G, Volk H-D, Looman AC, Asadullah K, Sterry W, et al. Despite IFN-λ 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