IL-17A promotes macrophage effector mechanisms against trypanosoma cruzi by trapping parasites in the endolysosomal compartment

Immunobiology

Volumn 218, Issue 6, 2013, Pages 910-923

  Erdmann, Hanna ^a,b   Roßnagel, Caroline ^a   Böhme, Julia ^a,b   Iwakura, Yoichiro ^c   Jacobs, Thomas ^d   Schaible, Ulrich E ^a   Hölscher, Christoph ^a,b  

^a RESEARCH CENTER BORSTEL   (Germany)

^b Cluster of Excellence Inflammation at Interfaces   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

^d BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

Cytokines; Intracellular parasite; Macrophages; Mice; Trypanosoma cruzi

Indexed keywords

ACTIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 17; INTERLEUKIN 23;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PHAGOCYTOSIS; CELL STIMULATION; CELLULAR IMMUNITY; CHAGAS DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DNA SEQUENCE; EFFECTOR CELL; ENDOLYSOSOMAL COMPARTMENT; ENZYME ACTIVITY; FEMALE; HOST PARASITE INTERACTION; HOST RESISTANCE; IN VITRO STUDY; IN VIVO STUDY; INFECTION RESISTANCE; INTERNALIZATION; INTRACELLULAR SPACE; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TH1 CELL; TRYPANOSOMA CRUZI;

ANIMALS; CELL LINE; CELLS, CULTURED; ENDOSOMES; FEMALE; HOST-PARASITE INTERACTIONS; INTERLEUKIN-17; INTERLEUKIN-23 SUBUNIT P19; LYSOSOMES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PARASITEMIA; PHAGOCYTOSIS; SURVIVAL RATE; TRYPANOSOMA CRUZI;

EID: 84876304890     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.10.005     Document Type: Article

References (51)

1. Aggarwal S., Ghilardi N., Xie M.H., de Sauvage F.J., Gurney A.L. Interleukin-23 promotes a distinct CD4T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 2003, 278:1910.
2. Andrews N.W., Whitlow M.B. Secretion by Trypanosoma cruzi of a hemolysin active at low pH. Mol. Biochem. Parasitol. 1989, 33:249.
3. Andrews N.W., Abrams C.K., Slatin S.L., Griffiths G. A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 1990, 61:1277.
4. Burleigh B.A., Andrews N.W. The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu. Rev. Microbiol. 1995, 49:175.
5. Chen L., Watanabe T., Watanabe H., Sendo F. Neutrophil depletion exacerbates experimental Chagas' disease in BALB/c, but protects C57BL/6 mice through modulating the Th1/Th2 dichotomy in different directions. Eur. J. Immunol. 2001, 31:265.
6. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S.A., Gorman D., Kastelein R.A., Sedgwick J.D. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744.
7. da Matta Guedes P.M., Gutierrez F.R., Maia F.L., Milanezi C.M., Silva G.K., Pavanelli W.R., Silva J.S. IL-17 produced during Trypanosoma cruzi infection plays a central role in regulating parasite-induced myocarditis. PLoS Negl. Trop. Dis. 2010, 4:e604.
8. de Meirelles M.N., de Araujo Jorge T.C., de Souza W. Interaction of Trypanosoma cruzi with macrophages in vitro: dissociation of the attachment and internalization phases by low temperature and cytochalasin B. Z. Parasitenkd. 1982, 68:7.
9. Dubin P.J., Kolls J.K. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 292:L519.
10. Fossiez F., Djossou O., Chomarat P., Flores-Romo L., Ait-Yahia S., Maat C., Pin J.J., Garrone P., Garcia E., Saeland S., Blanchard D., Gaillard C., Das Mahapatra B., Rouvier E., Golstein P., Banchereau J., Lebecque S. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 1996, 183:2593.
11. Gazzinelli R.T., Oswald I.P., Hieny S., James S.L., Sher A. The microbicidal activity of interferon-gamma-treated macrophages against Trypanosoma cruzi involves an l-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-beta. Eur. J. Immunol. 1992, 22:2501.
12. Ghilardi N., Kljavin N., Chen Q., Lucas S., Gurney A.L., De Sauvage F.J. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 2004, 172:2827.
13. Gillooly D.J., Simonsen A., Stenmark H. Phosphoinositides and phagocytosis. J. Cell Biol. 2001, 155:15.
14. Gomes J.A., Bahia-Oliveira L.M., Rocha M.O., Martins-Filho O.A., Gazzinelli G., Correa-Oliveira R. Evidence that development of severe cardiomyopathy in human Chagas' disease is due to a Th1-specific immune response. Infect. Immun. 2003, 71:1185.
15. Happel K.I., Dubin P.J., Zheng M., Ghilardi N., Lockhart C., Quinton L.J., Odden A.R., Shellito J.E., Bagby G.J., Nelson S., Kolls J.K. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 2005, 202:761.
16. Holscher C., Kohler G., Muller U., Mossmann H., Schaub G.A., Brombacher F. Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase. Infect. Immun. 1998, 66:1208.
17. Huang W., Na L., Fidel P.L., Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 2004, 190:624.
18. Huang F., Kao C.Y., Wachi S., Thai P., Ryu J., Wu R. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J. Immunol. 2007, 179:6504.
19. Hunter C.A., Slifer T., Araujo F. Interleukin-12-mediated resistance to Trypanosoma cruzi is dependent on tumor necrosis factor alpha and gamma interferon. Infect. Immun. 1996, 64:2381.
20. Hwang S.Y., Kim J.Y., Kim K.W., Park M.K., Moon Y., Kim W.U., Kim H.Y. IL-17 induces production of IL-6 and IL-8 in rheumatoid arthritis synovial fibroblasts via NF-kappaB- and PI3-kinase/Akt-dependent pathways. Arthritis Res. Ther. 2004, 6:R120.
21. Ishigame H., Kakuta S., Nagai T., Kadoki M., Nambu A., Komiyama Y., Fujikado N., Tanahashi Y., Akitsu A., Kotaki H., Sudo K., Nakae S., Sasakawa C., Iwakura Y. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30:108.
22. Kelly M.N., Kolls J.K., Happel K., Schwartzman J.D., Schwarzenberger P., Combe C., Moretto M., Khan I.A. Interleukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect. Immun. 2005, 73:617.
23. Kipnis T.L., Calich V.L., da Silva W.D. Active entry of bloodstream forms of Trypanosoma cruzi into macrophages. Parasitology 1979, 78:89.
24. Lemmers A., Moreno C., Gustot T., Marechal R., Degre D., Demetter P., de Nadai P., Geerts A., Quertinmont E., Vercruysse V., Le Moine O., Deviere J. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 2009, 49:646.
25. Lieberman L.A., Cardillo F., Owyang A.M., Rennick D.M., Cua D.J., Kastelein R.A., Hunter C.A. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J. Immunol. 2004, 173:1887.
26. Lin Y., Ritchea S., Logar A., Slight S., Messmer M., Rangel-Moreno J., Guglani L., Alcorn J.F., Strawbridge H., Park S.M., Onishi R., Nyugen N., Walter M.J., Pociask D., Randall T.D., Gaffen S.L., Iwakura Y., Kolls J.K., Khader S.A. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009, 31:799.
27. May R.C., Machesky L.M. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 2001, 114:1061.
28. Miyazaki Y., Hamano S., Wang S., Shimanoe Y., Iwakura Y., Yoshida H. IL-17 is necessary for host protection against acute-phase Trypanosoma cruzi infection. J. Immunol. 2010, 185:1150-1157.
29. Monteiro A.C., Schmitz V., Morrot A., de Arruda L.B., Nagajyothi F., Granato A., Pesquero J.B., Muller-Esterl W., Tanowitz H.B., Scharfstein J. Bradykinin B2 Receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses. PLoS Pathog. 2007, 3:e185.
30. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., Sedgwick J.D., Cua D.J. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 2003, 198:1951.
31. Nakae S., Komiyama Y., Nambu A., Sudo K., Iwase M., Homma I., Sekikawa K., Asano M., Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002, 17:375.
32. Nogueira N., Cohn Z. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J. Exp. Med. 1976, 143:1402.
33. O'Connor W., Kamanaka M., Booth C.J., Town T., Nakae S., Iwakura Y., Kolls J.K., Flavell R.A. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 2009, 10:603.
34. Oka K., Sawamura T., Kikuta K., Itokawa S., Kume N., Kita T., Masaki T. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9535.
35. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., Zonin F., Vaisberg E., Churakova T., Liu M., Gorman D., Wagner J., Zurawski S., Liu Y., Abrams J.S., Moore K.W., Rennick D., de Waal-Malefyt R., Hannum C., Bazan J.F., Kastelein R.A. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715.
36. Reiling N., Holscher C., Fehrenbach A., Kroger S., Kirschning C.J., Goyert S., Ehlers S. Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J. Immunol. 2002, 169:3480.
37. Schenkman S., Robbins E.S., Nussenzweig V. Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infect. Immun. 1991, 59:645.
38. Shin O.S., Miller L.S., Modlin R.L., Akira S., Uematsu S., Hu L.T. Downstream signals for MyD88-mediated phagocytosis of Borrelia burgdorferi can be initiated by TRIF and are dependent on PI3K. J. Immunol. 2009, 183:491.
39. Silverpil E., Glader P., Hansson M., Linden A. Impact of Interleukin-17 on macrophage phagocytosis of apoptotic neutrophils and particles. Inflammation 2011, 34:1-9.
40. Souza P.E., Rocha M.O., Menezes C.A., Coelho J.S., Chaves A.C., Gollob K.J., Dutra W.O. Trypanosoma cruzi infection induces differential modulation of costimulatory molecules and cytokines by monocytes and T cells from patients with indeterminate and cardiac Chagas' disease. Infect. Immun. 2007, 75:1886.
41. Tachado S.D., Samrakandi M.M., Cirillo J.D. Non-opsonic phagocytosis of Legionella pneumophila by macrophages is mediated by phosphatidylinositol 3-kinase. PLoS ONE 2008, 3:e3324.
42. Tardieux I., Webster P., Ravesloot J., Boron W., Lunn J.A., Heuser J.E., Andrews N.W. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 1992, 71:1117.
43. Tomlinson S., Vandekerckhove F., Frevert U., Nussenzweig V. The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology 1995, 110(Pt 5):547.
44. Tosello Boari J., Amezcua Vesely M.C., Bermejo D.A., Ramello M.C., Montes C.L., Cejas H., Gruppi A., Acosta Rodriguez E.V. IL-17RA signaling reduces inflammation and mortality during Trypanosoma cruzi infection by recruiting suppressive IL-10-producing neutrophils. PLoS Pathog. 2012, 8:e1002658.
45. Tyler K.M., Engman D.M. The life cycle of Trypanosoma cruzi revisited. Int. J. Parasitol. 2001, 31:472.
46. Vespa G.N., Cunha F.Q., Silva J.S. Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro. Infect. Immun. 1994, 62:5177.
47. Woolsey A.M., Sunwoo L., Petersen C.A., Brachmann S.M., Cantley L.C., Burleigh B.A. Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J. Cell Sci. 2003, 116:3611.
48. Wu Q., Martin R.J., Rino J.G., Breed R., Torres R.M., Chu H.W. IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect. 2007, 9:78.
49. Ye P., Rodriguez F.H., Kanaly S., Stocking K.L., Schurr J., Schwarzenberger P., Oliver P., Huang W., Zhang P., Zhang J., Shellito J.E., Bagby G.J., Nelson S., Charrier K., Peschon J.J., Kolls J.K. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 2001, 194:519.
50. Zhang S., Kim C.C., Batra S., McKerrow J.H., Loke P. Delineation of diverse macrophage activation programs in response to intracellular parasites and cytokines. PLoS Negl. Trop. Dis. 2010, 4:e648.
51. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., Ouyang W. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007, 445:648.