Innate Immune Recognition of an AT-Rich Stem-Loop DNA Motif in the Plasmodium falciparum Genome

Immunity

Volumn 35, Issue 2, 2011, Pages 194-207

  Sharma, Shruti ^a   DeOliveira, Rosane B ^a   Kalantari, Parisa ^a   Parroche, Peggy ^a   Goutagny, Nadege ^a   Jiang, Zhaozhao ^a   Chan, Jennie ^a   Bartholomeu, Daniella C ^b   Lauw, Fanny ^a   Hall, J Perry ^c   Barber, Glen N ^d   Gazzinelli, Ricardo T ^a,b,e   Fitzgerald, Katherine A ^a   Golenbock, Douglas T ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c PFIZER INC   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN IRF3; PROTEIN IRF7; PROTEIN STING; PROTEIN TBK1; PROTOZOAL DNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; DNA DETERMINATION; GENOME; HUMAN; HUMAN CELL; INNATE IMMUNITY; MALARIA FALCIPARUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTOZOAL GENETICS; SIGNAL TRANSDUCTION;

ANIMALS; AT RICH SEQUENCE; DNA, PROTOZOAN; GENE EXPRESSION PROFILING; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; INTERFERON TYPE I; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDES; PLASMODIUM FALCIPARUM; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION;

EID: 80051880722     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.05.016     Document Type: Article

References (63)

1. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K., Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009, 10:1065-1072.
2. Adachi K., Tsutsui H., Kashiwamura S., Seki E., Nakano H., Takeuchi O., Takeda K., Okumura K., Van Kaer L., Okamura H., et al. Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. J. Immunol. 2001, 167:5928-5934.
3. Aucan C., Walley A.J., Hennig B.J., Fitness J., Frodsham A., Zhang L., Kwiatkowski D., Hill A.V. Interferon-alpha receptor-1 (IFNAR1) variants are associated with protection against cerebral malaria in the Gambia. Genes Immun. 2003, 4:275-282.
4. Baratin M., Roetynck S., Lépolard C., Falk C., Sawadogo S., Uematsu S., Akira S., Ryffel B., Tiraby J.G., Alexopoulou L., et al. Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 2005, 102:14747-14752.
5. Bonnard M., Mirtsos C., Suzuki S., Graham K., Huang J., Ng M., Itié A., Wakeham A., Shahinian A., Henzel W.J., et al. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 2000, 19:4976-4985.
6. Charrel-Dennis M., Latz E., Halmen K.A., Trieu-Cuot P., Fitzgerald K.A., Kasper D.L., Golenbock D.T. TLR-independent type I interferon induction in response to an extracellular bacterial pathogen via intracellular recognition of its DNA. Cell Host Microbe 2008, 4:543-554.
7. Chessler A.D., Ferreira L.R., Chang T.H., Fitzgerald K.A., Burleigh B.A. A novel IFN regulatory factor 3-dependent pathway activated by trypanosomes triggers IFN-beta in macrophages and fibroblasts. J. Immunol. 2008, 181:7917-7924.
8. Chiu Y.H., Macmillan J.B., Chen Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138:576-591.
9. Clark I.A., Alleva L.M., Mills A.C., Cowden W.B. Pathogenesis of malaria and clinically similar conditions. Clin. Microbiol. Rev. 2004, 17:509-539.
10. Cooper R.A., Papakrivos J., Lane K.D., Fujioka H., Lingelbach K., Wellems T.E. PfCG2, a Plasmodium falciparum protein peripherally associated with the parasitophorous vacuolar membrane, is expressed in the period of maximum hemoglobin uptake and digestion by trophozoites. Mol. Biochem. Parasitol. 2005, 144:167-176.
11. Der S.D., Zhou A., Williams B.R., Silverman R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 1998, 95:15623-15628.
12. deWalick S., Amante F.H., McSweeney K.A., Randall L.M., Stanley A.C., Haque A., Kuns R.D., MacDonald K.P., Hill G.R., Engwerda C.R. Cutting edge: Conventional dendritic cells are the critical APC required for the induction of experimental cerebral malaria. J. Immunol. 2007, 178:6033-6037.
13. Dixit E., Boulant S., Zhang Y., Lee A.S., Odendall C., Shum B., Hacohen N., Chen Z.J., Whelan S.P., Fransen M., et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010, 141:668-681.
14. Dostert C., Guarda G., Romero J.F., Menu P., Gross O., Tardivel A., Suva M.L., Stehle J.C., Kopf M., Stamenkovic I., et al. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE 2009, 4:e6510.
15. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S.M., Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4:491-496.
16. Foy E., Li K., Sumpter R., Loo Y.M., Johnson C.L., Wang C., Fish P.M., Yoneyama M., Fujita T., Lemon S.M., Gale M. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc. Natl. Acad. Sci. USA 2005, 102:2986-2991.
17. Franklin B.S., Rodrigues S.O., Antonelli L.R., Oliveira R.V., Goncalves A.M., Sales-Junior P.A., Valente E.P., Alvarez-Leite J.I., Ropert C., Golenbock D.T., Gazzinelli R.T. MyD88-dependent activation of dendritic cells and CD4(+) T lymphocytes mediates symptoms, but is not required for the immunological control of parasites during rodent malaria. Microbes Infect. 2007, 9:881-890.
18. Franklin B.S., Parroche P., Ataíde M.A., Lauw F., Ropert C., de Oliveira R.B., Pereira D., Tada M.S., Nogueira P., da Silva L.H., et al. Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc. Natl. Acad. Sci. USA 2009, 106:5789-5794.
19. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
20. Gazzinelli R.T., Ropert C., Campos M.A. Role of the Toll/interleukin-1 receptor signaling pathway in host resistance and pathogenesis during infection with protozoan parasites. Immunol. Rev. 2004, 201:9-25.
21. Goutagny N., Jiang Z., Tian J., Parroche P., Schickli J., Monks B.G., Ulbrandt N., Ji H., Kiener P.A., Coyle A.J., Fitzgerald K.A. Cell type-specific recognition of human metapneumoviruses (HMPVs) by retinoic acid-inducible gene I (RIG-I) and TLR7 and viral interference of RIG-I ligand recognition by HMPV-B1 phosphoprotein. J. Immunol. 2010, 184:1168-1179.
22. Griffith J.W., Sun T., McIntosh M.T., Bucala R. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J. Immunol. 2009, 183:5208-5220.
23. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 2008, 9:857-865.
24. Hänscheid T., Egan T.J., Grobusch M.P. Haemozoin: From melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect. Dis. 2007, 7:675-685.
25. Honda K., Taniguchi T. IRFs: Master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 2006, 6:644-658.
26. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
27. Hornung V., Ablasser A., Charrel-Dennis M., Bauernfeind F., Horvath G., Caffrey D.R., Latz E., Fitzgerald K.A. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009, 458:514-518.
28. Ishii K.J., Kawagoe T., Koyama S., Matsui K., Kumar H., Kawai T., Uematsu S., Takeuchi O., Takeshita F., Coban C., Akira S. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 2008, 451:725-729.
29. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455:674-678.
30. Ishikawa H., Ma Z., Barber G.N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009, 461:788-792.
31. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 6:981-988.
32. Khor C.C., Chapman S.J., Vannberg F.O., Dunne A., Murphy C., Ling E.Y., Frodsham A.J., Walley A.J., Kyrieleis O., Khan A., et al. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis. Nat. Genet. 2007, 39:523-528.
33. Koch O., Awomoyi A., Usen S., Jallow M., Richardson A., Hull J., Pinder M., Newport M., Kwiatkowski D. IFNGR1 gene promoter polymorphisms and susceptibility to cerebral malaria. J. Infect. Dis. 2002, 185:1684-1687.
34. Marchlik E., Thakker P., Carlson T., Jiang Z., Ryan M., Marusic S., Goutagny N., Kuang W., Askew G.R., Roberts V., et al. Mice lacking Tbk1 activity exhibit immune cell infiltrates in multiple tissues and increased susceptibility to LPS-induced lethality. J. Leukoc. Biol. 2010, 88:1171-1180.
35. Martin F.J., Gomez M.I., Wetzel D.M., Memmi G., O'Seaghdha M., Soong G., Schindler C., Prince A. Staphylococcus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J. Clin. Invest. 2009, 119:1931-1939.
36. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437:1167-1172.
37. Mockenhaupt F.P., Cramer J.P., Hamann L., Stegemann M.S., Eckert J., Oh N.R., Otchwemah R.N., Dietz E., Ehrhardt S., Schröder N.W., et al. Toll-like receptor (TLR) polymorphisms in African children: Common TLR-4 variants predispose to severe malaria. Proc. Natl. Acad. Sci. USA 2006, 103:177-182.
38. Naka I., Patarapotikul J., Hananantachai H., Tokunaga K., Tsuchiya N., Ohashi J. IFNGR1 polymorphisms in Thai malaria patients. Infect. Genet. Evol. 2009, 9:1406-1409.
39. Neill A.L., Hunt N.H. Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology 1992, 105:165-175.
40. O'Connell R.M., Saha S.K., Vaidya S.A., Bruhn K.W., Miranda G.A., Zarnegar B., Perry A.K., Nguyen B.O., Lane T.F., Taniguchi T., et al. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 2004, 200:437-445.
41. Panne D., Maniatis T., Harrison S.C. An atomic model of the interferon-beta enhanceosome. Cell 2007, 129:1111-1123.
42. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., Halmen K.A., Lamphier M., Olivier M., Bartholomeu D.C., et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. USA 2007, 104:1919-1924.
43. Pichyangkul S., Yongvanitchit K., Kum-arb U., Hemmi H., Akira S., Krieg A.M., Heppner D.G., Stewart V.A., Hasegawa H., Looareesuwan S., et al. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J. Immunol. 2004, 172:4926-4933.
44. Rathinam V.A., Jiang Z., Waggoner S.N., Sharma S., Cole L.E., Waggoner L., Vanaja S.K., Monks B.G., Ganesan S., Latz E., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 2010, 11:395-402.
45. Rayamajhi M., Humann J., Penheiter K., Andreasen K., Lenz L.L. Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J. Exp. Med. 2010, 207:327-337.
46. Roberts Z.J., Goutagny N., Perera P.Y., Kato H., Kumar H., Kawai T., Akira S., Savan R., van Echo D., Fitzgerald K.A., et al. The chemotherapeutic agent DMXAA potently and specifically activates the TBK1-IRF-3 signaling axis. J. Exp. Med. 2007, 204:1559-1569.
47. Rothenfusser S., Goutagny N., DiPerna G., Gong M., Monks B.G., Schoenemeyer A., Yamamoto M., Akira S., Fitzgerald K.A. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 2005, 175:5260-5268.
48. Sabbah A., Chang T.H., Harnack R., Frohlich V., Tominaga K., Dube P.H., Xiang Y., Bose S. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 2009, 10:1073-1080.
49. Saitoh T., Fujita N., Hayashi T., Takahara K., Satoh T., Lee H., Matsunaga K., Kageyama S., Omori H., Noda T., et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. USA 2009, 106:20842-20846.
50. Sanda C., Weitzel P., Tsukahara T., Schaley J., Edenberg H.J., Stephens M.A., McClintick J.N., Blatt L.M., Li L., Brodsky L., Taylor M.W. Differential gene induction by type I and type II interferons and their combination. J. Interferon Cytokine Res. 2006, 26:462-472.
51. Shimosato T., Kimura T., Tohno M., Iliev I.D., Katoh S., Ito Y., Kawai Y., Sasaki T., Saito T., Kitazawa H. Strong immunostimulatory activity of AT-oligodeoxynucleotide requires a six-base loop with a self-stabilized 5'-C...G-3' stem structure. Cell. Microbiol. 2006, 8:485-495.
52. Shio M.T., Eisenbarth S.C., Savaria M., Vinet A.F., Bellemare M.J., Harder K.W., Sutterwala F.S., Bohle D.S., Descoteaux A., Flavell R.A., Olivier M. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009, 5:e1000559.
53. Stetson D.B., Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006, 24:93-103.
54. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
55. Togbe D., Schofield L., Grau G.E., Schnyder B., Boissay V., Charron S., Rose S., Beutler B., Quesniaux V.F., Ryffel B. Murine cerebral malaria development is independent of toll-like receptor signaling. Am. J. Pathol. 2007, 170:1640-1648.
56. Unterholzner L., Keating S.E., Baran M., Horan K.A., Jensen S.B., Sharma S., Sirois C., Jin T., Xiao T., Fitzgerald K.A., et al. IFI16 is a novel innate immune sensor for cytoplasmic DNA. Nat. Immunol. 2010, 11:997-1004.
57. Vigário A.M., Belnoue E., Grüner A.C., Mauduit M., Kayibanda M., Deschemin J.C., Marussig M., Snounou G., Mazier D., Gresser I., Rénia L. Recombinant human IFN-alpha inhibits cerebral malaria and reduces parasite burden in mice. J. Immunol. 2007, 178:6416-6425.
58. Voisine C., Mastelic B., Sponaas A.M., Langhorne J. Classical CD11c+ dendritic cells, not plasmacytoid dendritic cells, induce T cell responses to Plasmodium chabaudi malaria. Int. J. Parasitol. 2010, 40:711-719.
59. Wu X., Gowda N.M., Kumar S., Gowda D.C. Protein-DNA Complex Is the Exclusive Malaria Parasite Component that Activates Dendritic Cells and Triggers Innate Immune Responses. J. Immunol. 2010, 184:4338-4348.
60. Xiao N., Eidenschenk C., Krebs P., Brandl K., Blasius A.L., Xia Y., Khovananth K., Smart N.G., Beutler B. The Tpl2 mutation Sluggish impairs type I IFN production and increases susceptibility to group B streptococcal disease. J. Immunol. 2009, 183:7975-7983.
61. Yoneyama M., Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 2009, 227:54-65.
62. Zhong B., Yang Y., Li S., Wang Y.Y., Li Y., Diao F., Lei C., He X., Zhang L., Tien P., Shu H.B. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008, 29:538-550.
63. Zhu J., Krishnegowda G., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: The requirement of extracellular signal-regulated kinase, p38, c-Jun N-terminal kinase and NF-kappaB pathways for the expression of proinflammatory cytokines and nitric oxide. J. Biol. Chem. 2005, 280:8617-8627.