Processing of human toll-like receptor 7 by furin-like proprotein convertases is required for its accumulation and activity in endosomes

Immunity

Volumn 39, Issue 4, 2013, Pages 711-721

  Hipp, Madeleine M ^a   Shepherd, Dawn ^a   Gileadi, Uzi ^a   Aichinger, Michael C ^a   Kessler, Benedikt M ^b   Edelmann, Mariola J ^b   Essalmani, Rachid ^c   Seidah, Nabil G ^c   Reisesousa, Caetano ^d   Cerundolo, Vincenzo ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CALCIUM; FURIN; INTERLEUKIN 12P40; INTERLEUKIN 8; PROPROTEIN CONVERTASE 1; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ARTICLE; CONFOCAL MICROSCOPY; CYTOKINE RELEASE; CYTOLYSIS; DENDRITIC CELL; ENDOSOME; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR CLONING; PHAGOSOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AUTOIMMUNITY; CELL LINE; ENDOSOMES; FEEDBACK, PHYSIOLOGICAL; FURIN; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; LENTIVIRUS; MACROPHAGES; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE; PROPROTEIN CONVERTASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; QUINOLINES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7;

EID: 84885766791     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.09.004     Document Type: Article

References (45)

1. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
2. Alexander B. Anticoagulant therapy with coumarin congeners. Action and guidelines. Am. J. Med. 1962, 33:679-691.
3. Bell J.K., Mullen G.E.D., Leifer C.A., Mazzoni A., Davies D.R., Segal D.M. Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol. 2003, 24:528-533.
4. Blasius A.L., Beutler B. Intracellular toll-like receptors. Immunity 2010, 32:305-315.
5. Brinkmann M.M., Spooner E., Hoebe K., Beutler B., Ploegh H.L., Kim Y.-M. The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J.Cell Biol. 2007, 177:265-275.
6. Decroly E., Wouters S., Di Bello C., Lazure C., Ruysschaert J.M., Seidah N.G. Identification of the paired basic convertases implicated in HIV gp160 processing based on invitro assays and expression in CD4(+) cell lines. J.Biol. Chem. 1996, 271:30442-30450.
7. Demaison C., Parsley K., Brouns G., Scherr M., Battmer K., Kinnon C., Grez M., Thrasher A.J. High-level transduction and gene expression in hematopoietic repopulating cells using a human imunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum. Gene Ther. 2002, 13:803-813.
8. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
9. Diebold S.S., Massacrier C., Akira S., Paturel C., Morel Y., Reis e Sousa C. Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides. Eur. J. Immunol. 2006, 36:3256-3267.
10. Ewald S.E., Lee B.L., Lau L., Wickliffe K.E., Shi G.P., Chapman H.A., Barton G.M. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008, 456:658-662.
11. Ewald S.E., Engel A., Lee J., Wang M., Bogyo M., Barton G.M. Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J.Exp. Med. 2011, 208:643-651.
12. Fugère M., Limperis P.C., Beaulieu-Audy V., Gagnon F., Lavigne P., Klarskov K., Leduc R., Day R. Inhibitory potency and specificity of subtilase-like pro-protein convertase (SPC) prodomains. J.Biol. Chem. 2002, 277:7648-7656.
13. Govindaraj R.G., Manavalan B., Basith S., Choi S. Comparative analysis of species-specific ligand recognition in Toll-like receptor 8 signaling: a hypothesis. PLoS ONE 2011, 6:e25118.
14. Hallenberger S., Bosch V., Angliker H., Shaw E., Klenk H.D., Garten W. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 1992, 360:358-361.
15. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
16. Honda K., Ohba Y., Yanai H., Negishi H., Mizutani T., Takaoka A., Taya C., Taniguchi T. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 2005, 434:1035-1040.
17. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
18. Kagan J.C. Signaling organelles of the innate immune system. Cell 2012, 151:1168-1178.
19. Kanno A., Yamamoto C., Onji M., Fukui R., Saitoh S., Motoi Y., Shibata T., Matsumoto F., Muta T., Miyake K. Essential role for Toll-like receptor 7 (TLR7)-unique cysteines in an intramolecular disulfide bond, proteolytic cleavage and RNA sensing. Int. Immunol. 2013, 25:413-422.
20. Kim Y.M., Brinkmann M.M., Paquet M.E., Ploegh H.L. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 2008, 452:234-238.
21. Komiyama T., Coppola J.M., Larsen M.J., van Dort M.E., Ross B.D., Day R., Rehemtulla A., Fuller R.S. Inhibition of furin/proprotein convertase-catalyzed surface and intracellular processing by small molecules. J.Biol. Chem. 2009, 284:15729-15738.
22. Krug A. Nucleic acid recognition receptors in autoimmunity. Handb. Exp. Pharmacol. 2008, 183:129-151.
23. Leadbetter E.A., Rifkin I.R., Hohlbaum A.M., Beaudette B.C., Shlomchik M.J., Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002, 416:603-607.
24. Lee B.L., Moon J.E., Shu J.H., Yuan L., Newman Z.R., Schekman R., Barton G.M. UNC93B1 mediates differential trafficking of endosomal TLRs. Elife 2013, 2:e00291.
25. Logeat F., Bessia C., Brou C., LeBail O., Jarriault S., Seidah N.G., Israël A. The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc. Natl. Acad. Sci. USA 1998, 95:8108-8112.
26. Malfait A.-M., Arner E.C., Song R.-H., Alston J.T., Markosyan S., Staten N., Yang Z., Griggs D.W., Tortorella M.D. Proprotein convertase activation of aggrecanases in cartilage insitu. Arch. Biochem. Biophys. 2008, 478:43-51.
27. Maschalidi S., Hässler S., Blanc F., Sepulveda F.E., Tohme M., Chignard M., van Endert P., Si-Tahar M., Descamps D., Manoury B. Asparagine endopeptidase controls anti-influenza virus immune responses through TLR7 activation. PLoS Pathog. 2012, 8:e1002841.
28. Mohty M., Vialle-Castellano A., Nunes J.A., Isnardon D., Olive D., Gaugler B. IFN-alpha skews monocyte differentiation into Toll-like receptor 7-expressing dendritic cells with potent functional activities. J.Immunol. 2003, 171:3385-3393.
29. Molloy S.S., Bresnahan P.A., Leppla S.H., Klimpel K.R., Thomas G. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J.Biol. Chem. 1992, 267:16396-16402.
30. Nie G.Y., Li Y., Minoura H., Findlay J.K., Salamonsen L.A. Specific and transient up-regulation of proprotein convertase 6 at the site of embryo implantation and identification of a unique transcript in mouse uterus during early pregnancy. Biol. Reprod. 2003, 68:439-447.
31. Nour N., Basak A., Chrétien M., Seidah N.G. Structure-function analysis of the prosegment of the proprotein convertase PC5A. J.Biol. Chem. 2003, 278:2886-2895.
32. Park B., Brinkmann M.M., Spooner E., Lee C.C., Kim Y.-M., Ploegh H.L. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 2008, 9:1407-1414.
33. Pirher N., Ivicak K., Pohar J., Bencina M., Jerala R. A second binding site for double-stranded RNA in TLR3 and consequences for interferon activation. Nat. Struct. Mol. Biol. 2008, 15:761-763.
34. Rousselet E., Benjannet S., Hamelin J., Canuel M., Seidah N.G. The proprotein convertase PC7: unique zymogen activation and trafficking pathways. J.Biol. Chem. 2011, 286:2728-2738.
35. Rousselet E., Benjannet S., Marcinkiewicz E., Asselin M.C., Lazure C., Seidah N.G. Proprotein convertase PC7 enhances the activation of the EGF receptor pathway through processing of the EGF precursor. J.Biol. Chem. 2011, 286:9185-9195.
36. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G.B., Wagner H., Bauer S. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 2004, 34:2541-2550.
37. Salvas A., Benjannet S., Reudelhuber T.L., Chrétien M., Seidah N.G. Evidence for proprotein convertase activity in the endoplasmic reticulum/early Golgi. FEBS Lett. 2005, 579:5621-5625.
38. Sasai M., Linehan M.M., Iwasaki A. Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 2010, 329:1530-1534.
39. Seidah N.G., Mayer G., Zaid A., Rousselet E., Nassoury N., Poirier S., Essalmani R., Prat A. The activation and physiological functions of the proprotein convertases. Int. J. Biochem. Cell Biol. 2008, 40:1111-1125.
40. Sepulveda F.E., Maschalidi S., Colisson R., Heslop L., Ghirelli C., Sakka E., Lennon-Duménil A.M., Amigorena S., Cabanie L., Manoury B. Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 2009, 31:737-748.
41. Shlomchik M.J. Activating systemic autoimmunity: B's, T's, and tolls. Curr. Opin. Immunol. 2009, 21:626-633.
42. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., Mudd S., Mann N., Sovath S., Goode J., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 2006, 7:156-164.
43. Takahashi S., Kasai K., Hatsuzawa K., Kitamura N., Misumi Y., Ikehara Y., Murakami K., Nakayama K. A mutation of furin causes the lack of precursor-processing activity in human colon carcinoma LoVo cells. Biochem. Biophys. Res. Commun. 1993, 195:1019-1026.
44. Zarkik S., Decroly E., Wattiez R., Seidah N.G., Burny A., Ruysschaert J.M. Comparative processing of bovine leukemia virus envelope glycoprotein gp72 by subtilisin/kexin-like mammalian convertases. FEBS Lett. 1997, 406:205-210.
45. Zhong M., Munzer J.S., Basak A., Benjannet S., Mowla S.J., Decroly E., Chrétien M., Seidah N.G. The prosegments of furin and PC7 as potent inhibitors of proprotein convertases. Invitro and exvivo assessment of their efficacy and selectivity. J.Biol. Chem. 1999, 274:33913-33920.