Cytosolic sensing of extracellular self-DNA transported into monocytes by the antimicrobial peptide LL37

Blood

Volumn 120, Issue 18, 2012, Pages 3699-3707

  Chamilos, Georgios ^a,e,f   Gregorio, Josh ^a   Meller, Stephan ^a   Lande, Roberto ^b,c   Kontoyiannis, Dimitrios P ^a   Modlin, Robert L ^d   Gilliet, Michel ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CRETE   (Greece)

^f INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ALPHA INTERFERON; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DOUBLE STRANDED DNA; INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; TANK BINDING KINASE 1; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; DENDRITIC CELL; DNA SEQUENCE; DNA TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; METHYLATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84868573547     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-01-401364     Document Type: Article

References (39)

1. Theofilopoulos AN, Baccala R, Beutler B, Kono DH. Type I interferons (alpha/beta) in immunity and autpimmunity. Annu Rev Immunol. 2005;23:307-336. (Pubitemid 40563172)
2. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity . 2006;25(3):373-381. (Pubitemid 44354218)
3. Santini SM, Lapenta C, Logozzi M, et al. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J Exp Med. 2000;191(10):1777-1788. (Pubitemid 30331574)
4. Luft T, Pang KC, Thomas E, et al. Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol. 1998;161(4):1947-1953. (Pubitemid 28387618)
5. Hornung V, Latz E. Intracellular DNA recognition. Nat Rev Immunol. 2010;10(2):123-130.
6. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 2008;8(8):594-606.
7. Takaoka A, Wang Z, Choi MK, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune responses. Nature. 2007; 448(7152):501-505. (Pubitemid 47123520)
8. Wang Z, Choi MK, Ban T, et al. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc Natl Acad Sci U S A. 2008;105(14):5477-5482. (Pubitemid 351753888)
9. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell. 2009;7(3):576-591.
10. Unterholzner L, Keating SE, Baran M, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol. 2010;11(11):997-1004.
11. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol. 2011;12(10):959-965.
12. Ishii KJ, Coban C, Kato H, et al.AToll-like receptor-independent antiviral response induced by doublestranded B-form DNA. Nat Immunol. 2006;7(1):40-48. (Pubitemid 41823867)
13. Stetson DB, Medzhitov R. Recognition of cytosolic DNA activates IRF3-dependent innate immune responses. Immunity. 2006;24(1):93-103. (Pubitemid 43077203)
14. Ishii KJ, Kawagoe T, Koyama S, et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature. 2008;451(7179):725-729. (Pubitemid 351220566)
15. Miyahira AK, Shahangian A, Hwang S, Sun R, Cheng G. TANK-binding kinase-1 plays an important role during in vitro and in vivo type I IFN responses to DNA virus infections. J Immunol. 2009;182(4):2248-2257.
16. Zhang X, Brann TW, Zhou M, et al. Cutting edge: Ku70 is a novel cytosolic DNA sensor that induces type III rather than type I IFN. J Immunol. 2011;186(8):4541-4545.
17. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783-801. (Pubitemid 43261452)
18. Lande R, Gregorio J, Facchinetti V, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature. 2007;449(7162):564- 569. (Pubitemid 47525141)
19. Gregorio J, Meller S, Conrad C. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med. 2010;207(13):2921-2930.
20. Lande R, Ganguly D, Facchinetti V, et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med. 2011;3(73):73ra19
21. Okabe Y, Kawane K, Akira S, Taniguchi T, Nagata S. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med. 2005;202(10):1333-1339. (Pubitemid 41668736)
22. Boule MW, Broughton C, Mackay F, Akira S, Marshak-Rothstein A, Rifkin IR. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J Exp Med. 2004;199(12):1631-1640. (Pubitemid 38821996)
23. Decker P, Singh-Jasuja H, Haager S, Kotter I, Rammensee HG. Nucleosome, the main autoantigen in systemic lupus erythematosus, induces direct dendritic cell activation via a MyD88-independent pathway: consequences on inflammation. J Immunol. 2005;174(6):3326-3334. (Pubitemid 40354036)
24. Moller A, Nordheim A, Kozlowski SA, Patel DJ, Rich A. Bromination stabilizes poly (dC-dG) in the Z-DNA form under low-salt conditions. Biochemistry. 1984;23(1):54-62.
25. Kadowaki N, Ho S, Antonenko S, et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med. 2001;194(6):863-869. (Pubitemid 32983021)
26. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem. 1991;266(26):17707-1712.
27. Kuznik A, Bencina M, Svajger U, Jeras M, Rozman B, Jerala R. Mechanism of endosomal TLR inhibition by antimalarial drugs ans imidazoquinolines. J Immunol. 2001;186(8):4794-4804.
28. Krieg AM. CpG motifs in bacterial DNA and their immune effects. Ann Rev Immunol. 2002;20:709-760. (Pubitemid 34293438)
29. Verpooten D, Ma Y, Hou S, Yan Z, He BJ. Control of TANK-binding kinase-1-mediated signaling by the gamma(1)34.5 protein of herpes simplex virus 1. J Biol Chem. 2009;284(1):1097-1105.
30. Howell MD, Wollenberg A, Gallo RL, et al. Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol. 2006;117(4):836-841.
31. Sandgren S, Wittrup A, Cheng F, et al. The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis. J Biol Chem. 2004;279(17):17951-17956. (Pubitemid 38568102)
32. Yang D, Chen Q, Schmidt AP, et al. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med. 2000;192(7):1069-1074.
33. Wong KL, Chen W, Balakrishnan T, Toh YX, Fink K, Wong SC. Susceptibility and response of human monocyte subsets to primary dengue virus infection. PLoS One. 2012;7(5):e36435.
34. El-Sayed A, Khalil A, Koruge K, Futaki S, Harashima H. Octaarginine- and octalysine-modified nanoparticles have different modes of endosomal escape. J Biol Chem. 2008;283:23450-23461.
35. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol. 2004;22:181-215. (Pubitemid 38680422)
36. Ong PY, Ohtake T, Brandt C, et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med. 2002;347(15):1151-1160.
37. Howell MD, Jones JF, Kisich KO, Streib JE, Gallo R, Leung DY. Selective killing of vaccinia virus by LL37: implications for eczema vaccinatum. J Immunol. 2004;172(3):1763-1767. (Pubitemid 38116824)
38. Howell MD, Gallo RL, Boguniewicz M, et al. Cytokine milieu of atopic dermatitis skin subverts the immune response to vaccinia virus. Immunity. 2006;24(3):341-348.
39. Hochrein H, Schlatter B, O'Keeffe M, et al. Herpes simplex virus type-1 IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc Natl Acad Sci U S A. 2004;101(31):11416-11421. (Pubitemid 39038361)