Type III interferon is a critical regulator of innate antifungal immunity

Science Immunology

Volumn 2, Issue 16, 2017, Pages

  Espinosa, Vanessa ^a   Dutta, Orchi ^a,b   McElrath, Constance ^a,b,d   Du, Peicheng ^c   Chang, Yun Juan ^c   Cicciarelli, Bryan ^d   Pitler, Amy ^d   Whitehead, Ian ^d   Obar, Joshua J ^e   Durbin, Joan E ^a,d   Kotenko, Sergei V ^a,d   Rivera, Amariliz ^a,d  

^a Rutgers The State University of New Jersey   (United States)

^b University of Medicine and Dentistry of New Jersey   (United States)

^c UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CCR2 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR2; CYTOKINE RECEPTOR; IFNLR1 PROTEIN, HUMAN; IFNLR1 PROTEIN, MOUSE; INTERFERON; INTERFERON RECEPTOR; INTERFERON TYPE III;

ADAPTIVE IMMUNITY; ANIMAL; ASPERGILLUS FUMIGATUS; CELL LINE; DEFICIENCY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MONOCYTE; MOUSE; NEUTROPHIL; PATHOGENICITY; SYSTEMIC MYCOSIS;

ADAPTIVE IMMUNITY; ANIMALS; ASPERGILLUS FUMIGATUS; CELL LINE; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; INTERFERON-ALPHA; INTERFERONS; INVASIVE FUNGAL INFECTIONS; MICE; MONOCYTES; NEUTROPHILS; RECEPTORS, CCR2; RECEPTORS, CYTOKINE; RECEPTORS, INTERFERON;

EID: 85032796421     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aan5357     Document Type: Article

References (40)

1. C. F. Nathan, H. W. Murray, M. E. Wiebe, B. Y. Rubin, Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158, 670–689 (1983).
2. A. N. Theofilopoulos, R. Baccala, B. Beutler, D. H. Kono, Type I interferons (/) in immunity and autoimmunity. Annu. Rev. Immunol. 23, 307–336 (2005).
3. G. M. Boxx, G. Cheng, The roles of type I interferon in bacterial infection. Cell Host Microbe 19, 760–769 (2016).
4. Z. G. Ramirez-Ortiz, C. K. Lee, J. P. Wang, L. Boon, C. A. Specht, S. M. Levitz, A nonredundant role for plasmacytoid dendritic cells in host defense against the human fungal pathogen Aspergillus fumigatus. Cell Host Microbe 9, 415–424 (2011).
5. S. V. Kotenko, G. Gallagher, V. V. Baurin, A. Lewis-Antes, M. Shen, N. K. Shah, J. A. Langer, F. Sheikh, H. Dickensheets, R. P. Donnelly, IFN-s mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4, 69–77 (2003).
6. P. Sheppard, W. Kindsvogel, W. Xu, K. Henderson, S. Schlutsmeyer, T. E. Whitmore, R. Kuestner, U. Garrigues, C. Birks, J. Roraback, C. Ostrander, D. Dong, J. Shin, S. Presnell, B. Fox, B. Haldeman, E. Cooper, D. Taft, T. Gilbert, F. J. Grant, M. Tackett, W. Krivan, G. McKnight, C. Clegg, D. Foster, K. M. Klucher, IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4, 63–68 (2003).
7. S. Crotta, S. Davidson, T. Mahlakoiv, C. J. Desmet, M. R. Buckwalter, M. L. Albert, P. Staeheli, A. Wack, Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenza-infected airway epithelia. PLOS Pathog. 9, e1003773 (2013).
8. J.-D. Lin, N. Feng, A. Sen, M. Balan, H.-C. Tseng, C. McElrath, S. V. Smirnov, J. Peng, L. L. Yasukawa, R. K. Durbin, J. E. Durbin, H. B. Greenberg, S. V. Kotenko, Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLOS Pathog. 12, e1005600 (2016).
9. T. J. Nice, M. T. Baldridge, B. T. McCune, J. M. Norman, H. M. Lazear, M. Artyomov, M. S. Diamond, H. W. Virgin, Interferon- cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347, 269–273 (2015).
10. K. Blazek, H. L. Eames, M. Weiss, A. J. Byrne, D. Perocheau, J. E. Pease, S. Doyle, F. McCann, R. O. Williams, I. A. Udalova, IFN- resolves inflammation via suppression of neutrophil infiltration and IL-1 production. J. Exp. Med. 212, 845–853 (2015).
11. J. Pott, T. Mahlakõiv, M. Mordstein, C. U. Duerr, T. Michiels, S. Stockinger, P. Staeheli, M. W. Hornef, IFN- determines the intestinal epithelial antiviral host defense. Proc. Natl. Acad. Sci. U.S.A. 108, 7944–7949 (2011).
12. I. E. Galani, V. Triantafyllia, E. E. Eleminiadou, O. Koltsida, A. Stavropoulos, M. Manioudaki, D. Thanos, S. E. Doyle, S. V. Kotenko, K. Thanopoulou, E. Andreakos, Interferon- mediates non-redundant front-line antiviral protection against influenza virus infection without compromising host fitness. Immunity 46, 875–890.e6 (2017).
13. S. D. Willger, S. Puttikamonkul, K.-H. Kim, J. B. Burritt, N. Grahl, L. J. Metzler, R. Barbuch, M. Bard, C. B. Lawrence, R. A. Cramer Jr., A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus. PLOS Pathog. 4, e1000200 (2008).
14. S. V. Kotenko, J. E. Durbin, Contribution of type III interferons to antiviral immunity: Location, location, location. J. Biol. Chem. 292, 7295–7303 (2017).
15. G. D. Brown, D. W. Denning, N. A. R. Gow, S. M. Levitz, M. G. Netea, T. C. White, Hidden killers: Human fungal infections. Sci. Transl. Med. 4, 165rv113 (2012).
16. J.-P. Latgè, Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12, 310–350 (1999).
17. P. E. Verweij, A. Chowdhary, W. J. G. Melchers, J. F. Meis, Azole resistance in Aspergillus fumigatus: Can we retain the clinical use of mold-active antifungal azoles? Clin. Infect. Dis. 62, 362–368 (2016).
18. B. H. Segal, Aspergillosis. N. Engl. J. Med. 360, 1870–1884 (2009).
19. V. Espinosa, A. Rivera, First line of defense: Innate cell-mediated control of pulmonary aspergillosis. Front. Microbiol. 7, 272 (2016).
20. F. Lanternier, S. Cypowyj, C. Picard, J. Bustamante, O. Lortholary, J.-L. Casanova, A. Puel, Primary immunodeficiencies underlying fungal infections. Curr. Opin. Pediatr. 25, 736–747 (2013).
21. J. D. Pollock, D. A. Williams, M. A. C. Gifford, L. L. Li, X. Du, J. Fisherman, S. H. Orkin, C. M. Doerschuk, M. C. Dinauer, Mouse model of X–linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat. Genet. 9, 202–209 (1995).
22. V. Espinosa, A. Jhingran, O. Dutta, S. Kasahara, R. Donnelly, P. Du, J. Rosenfeld, I. Leiner, C.-C. Chen, Y. Ron, T. M. Hohl, A. Rivera, Inflammatory monocytes orchestrate innate antifungal immunity in the lung. PLOS Pathog. 10, e1003940 (2014).
23. A. K. Caffrey, M. M. Lehmann, J. M. Zickovich, V. Espinosa, K. M. Shepardson, C. P. Watschke, K. M. Hilmer, A. Thammahong, B. M. Barker, A. Rivera, R. A. Cramer, J. J. Obar, IL-1 signaling is critical for leukocyte recruitment after pulmonary Aspergillus fumigatus challenge. PLOS Pathog. 11, e1004625 (2015).
24. A. Åhlin, G. Elinder, J. Palmblad, Dose-dependent enhancements by interferon- on functional responses of neutrophils from chronic granulomatous disease patients. Blood 89, 3396–3401 (1997).
25. K. B. Boyle, L. R. Stephens, P. T. Hawkins, Activation of the neutrophil NADPH oxidase by Aspergillus fumigatus. Ann. N. Y. Acad. Sci. 1273, 68–73 (2012).
26. M. J. Chusid, P. G. Sohnle, J. N. Fink, M. L. Shea, A genetic defect of granulocyte oxidative metabolism in a man with disseminated aspergillosis. J. Lab. Clin. Med. 97, 730–738 (1981).
27. E. L. Falcone, S. M. Holland, Invasive fungal infection in chronic granulomatous disease: Insights into pathogenesis and management. Curr. Opin. Infect. Dis. 25, 658–669 (2012).
28. M. J. Grimm, R. R. Vethanayagam, N. G. Almyroudis, C. G. Dennis, A. N. H. Khan, A. C. D’Auria, K. L. Singel, B. A. Davidson, P. R. Knight, T. S. Blackwell, T. M. Hohl, M. K. Mansour, J. M. Vyas, M. Röhm, C. F. Urban, T. Kelkka, R. Holmdahl, B. H. Segal, Monocyte- and macrophage-targeted NADPH oxidase mediates antifungal host defense and regulation of acute inflammation in mice. J. Immunol. 190, 4175–4184 (2013).
29. J. G. Liese, A. Jansson, T. Petropoulou, S. Kloos, B. H. Belohradsky, V. Jendrossek, M. Gahr, Chronic granulomatous disease in adults. Lancet 347, 220–223 (1996).
30. D. E. Morgenstern, M. A. C. Gifford, L. L. Li, C. M. Doerschuk, M. C. Dinauer, Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J. Exp. Med. 185, 207–218 (1997).
31. B. Philippe, O. Ibrahim-Granet, M. C. Prévost, M. A. Gougerot-Pocidalo, M. Sanchez Perez, A. Van der Meeren, J. P. Latgé, Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect. Immun. 71, 3034–3042 (2003).
32. N. Ank, H. West, C. Bartholdy, K. Eriksson, A. R. Thomsen, S. R. Paludan, Lambda interferon (IFN-), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J. Virol. 80, 4501–4509 (2006).
33. R. K. Durbin, S. V. Kotenko, J. E. Durbin, Interferon induction and function at the mucosal surface. Immunol. Rev. 255, 25–39 (2013).
34. A. Broggi, Y. Tan, F. Granucci, I. Zanoni, IFN- suppresses intestinal inflammation by non-translational regulation of neutrophil function. Nat. Immunol. 2017, 10.1038/ni.3821 (2017).
35. E. Passegué, E. F. Wagner, I. L. Weissman, JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119, 431–443 (2004).
36. J. A. Van Ziffle, C. A. Lowell, Neutrophil-specific deletion of Syk kinase results in reduced host defense to bacterial infection. Blood 114, 4871–4882 (2009).
37. T. M. Hohl, A. Rivera, L. Lipuma, A. Gallegos, C. Shi, M. Mack, E. G. Pamer, Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6, 470–481 (2009).
38. N. V. Serbina, T. M. Hohl, M. Cherny, E. G. Pamer, Selective expansion of the monocytic lineage directed by bacterial infection. J. Immunol. 183, 1900–1910 (2009).
39. P. J. Klover, W. J. Muller, G. W. Robinson, R. M. Pfeiffer, D. Yamaji, L. Hennighausen, Loss of STAT1 from mouse mammary epithelium results in an increased Neu-induced tumor burden. Neoplasia 12, 899–905 (2010).
40. +-T-cell responses to live and heat-inactivated Aspergillus fumigatus conidia. Infect. Immun. 73, 7170–7179 (2005).