LL-37 peptide enhancement of signal transduction by toll-like receptor 3 is regulated by pH identification of a peptide antagonist of LL-37

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27614-27624

  Singh, Divyendu ^a   Vaughan, Robert ^a   Kao, C Cheng ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; BACTERIOPHAGES; CELL SIGNALING; LIGHT SCATTERING; OLIGOMERIZATION; OLIGOMERS; PEPTIDES; RNA;

CELL-BASED; COLOCALIZATION; DOUBLE-STRANDED RNA (DSRNA); HUMAN EPITHELIAL CELLS; LIGHT SCATTERING SPECTROSCOPY; PH-DEPENDENT; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4;

SIGNAL TRANSDUCTION;

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 29; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CATHEPSIN; DOUBLE STRANDED RNA; POLYPEPTIDE ANTIBIOTIC AGENT; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; PEPTIDE; TLR3 PROTEIN, HUMAN;

ACIDIFICATION; ARTICLE; CONTROLLED STUDY; DRUG HALF LIFE; DYNAMIC LIGHT SCATTERING SPECTROSCOPY; ENDOSOME; ENZYME LOCALIZATION; ENZYME REGULATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; OLIGOMERIZATION; PH; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; SPECTROSCOPY; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; UPREGULATION;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; ENDOSOMES; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PEPTIDES; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

EID: 84907484277     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.582973     Document Type: Article

References (35)

1. Sorensen, O. E., Follin, P., Johnsen, A. H., Calafat, J., Tjabringa, G. S., Hiemstra, P. S., and Borregaard, N. (2001) Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97, 3951-3959
2. Doss, M., White, M. R., Tecle, T., and Hartshorn, K. L. (2010) Human defensins and LL-37 in mucosal immunity. J. Leukoc. Biol. 87, 79-92
3. Lande, R, Ganguly, D., Facchinetti, V., Frasca, L., Conrad, C., Gregorio, J., Meller, S., Chamilos, G., Sebasigari, R., Riccieri, V., Bassett, R., Amuro, H., Fukuhara, S., Ito, T., Liu, Y. J., and Gilliet, M. (2011) Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transi. Med. 3, 73ra19
4. Kim, S. K., Park, S., and Lee, E. S. (2010) Toll-like receptors and antimicrobial peptides expressions of psoriasis: correlation with serum vitamin D level. J. Korean Med. Sci. 25, 1506-1512
5. Gambichler, T., Kobus, S., Kobus, A., Tigges, C., Scola, N., Altmeyer, P., Kreuter, A., Bechara, F. G., and Skrygan, M. (2011) Expression of antimicrobial peptides and proteins in etanercept-treated psoriasis patients. Regul. Pept. 167, 163-166
6. Goleva, E., Searing, D. A., Jackson, L. P., Richers, B. N., and Leung, D. Y. (2012) Steroid requirements and immune associations with vitamin D are stronger in children than adults with asthma. J. Allergy Clin. Immunol. 129, 1243-1251
7. Sun, J., Dahlén, B., Agerberth, B., and Haeggström, J. Z. (2013) The antimicrobial peptide LL-37 induces synthesis and release of cysteinyl leukotrienes from human eosinophils: implications for asthma. Allergy 68, 304-311
8. Rohde, G., Message, S. D., Haas, J. J., Kebadze, T., Parker, H., Laza-Stanca, V., Khaitov, M. R., Kon, O. M., Stanciu, L. A., Mallia, P., Edwards, M. R., and Johnston, S. L. (2014) CxC-chemokines and antimicrobial peptides in rhinovirus-induced experimental asthma exacerbations. Clin. Exp. Allergy 44, 930-939
9. Dombrowski, Y., and Schauber, J. (2012) Cathelicidin LL-37: a defense molecule with a potential role in psoriasis pathogenesis. Exp. Dermatol. 21, 327-330
10. Lai, Y., Adhikarakunnathu, S., Bhardwaj, K., Ranjith-Kumar, C. T., Wen, Y., Jordan, J. L., Wu, L. H., Dragnea, B., San Mateo, L., and Kao, C. C. (2011) LL37 and cationic peptides enhance TLR3 signaling by viral doublestranded RNAs. PLoS ONE 6, e26632
11. Lai, Y., Yi, G., Chen, A., Bhardwaj, K., Tragesser, B. J., Rodrigo, A., Valverde, Zlotnick, A., Mukhopadhyay, S., Ranjith-Kumar, C. T., and Kao, C. C. (2011) Viral double-strand RNA-binding proteins can enhance innate immune signaling by toll-like Receptor 3. PLoS ONE 6, e25837
12. Li, G., Domenico, J., Jia, Y., Lucas, J. J., and Gelfand, E. W. (2009) NF-κB-dependent induction of cathelicidin-related antimicrobial peptide in murine mast cells by lipopolysaccharide. Int. Arch. Allergy Immunol. 150, 122-132
13. Wan, M., van der Does, A. M., Tang, X., Lindbom, L., Agerberth, B., and Haeggström, J. Z. (2014) Antimicrobial peptide LL-37 promotes bacterial phagocytosis by human macrophages. J. Leukoc. Biol. 95, 971-981
14. Phelps, M. A., Foraker, A. B., Gao, W., Dalton, J. T., and Swaan, P. W. (2004) A novel rhodamine-riboflavin conjugate probe exhibits distinct fluorescence resonance energy transfer that enables riboflavin trafficking and subcellular localization studies. Mol. Pharm. 1, 257-266
15. Johansson, J., Gudmundsson, G. H., Rottenberg, M. E., Berndt, K. D., and Agerberth, B. (1998) Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem. 273, 3718-3724
16. Boite, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232
17. Sekar, R. B., and Periasamy, A. (2003) Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J. Cell Biol. 160, 629-633
18. Singh, D., Qi, R., Jordan, J. L., San Mateo, L., and Kao, C. C. (2013) The human antimicrobial peptide LL-37, but not the mouse ortholog, mCRAMP, can stimulate signaling by poly(I:C) through a FPRL1-dependent pathway. J. Biol. Chem. 288, 8258-8268
19. Vaughan, R., Fan, B., You, J. S., and Kao, C. C. (2012) Identification and functional characterization of the nascent RNA contacting residues of the hepatitis C virus RNA-dependent RNA polymerase. RNA 18, 1541-1552
20. Ranjith-Kumar, C. T., Duffy, K. E., Jordan, J. L., Eaton-Bassiri, A., Vaughan, R., Hoose, S. A., Lamb, R. J., Sarisky, R. T., and Kao, C. C. (2008) Single-stranded oligonucleotides can inhibit cytokine production induced by human toll-like receptor 3. Mol. Cell. Biol. 28, 4507-4519
21. Leonard, J. N., Chirlando, R., Asians, J., Bell, J. K., Mar guiles, D. H., Davies, D. R., and Segal, D. M. (2008) The TLR3 signaling complex forms by cooperative receptor dimerization. Proc. Natl. Acad. Sci. U.S.A. 105, 258-263
22. Oren, Z., Lerman, J. C., Gudmundsson, G. H., Agerberth, B., and Shai, Y. (1999) Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem. J. 341, 501-513
23. Xhindoli, D., Pacor, S., Guida, F., Antcheva, N., and Tossi, A. (2014) Native oligomerization determines the mode of action and biological activities of human cathelicidin LL-37. Biochem. J. 457, 263-275
24. Ewald, S. E., Engel, A., Lee, J., Wang, M., Bogyo, M., and Barton, G. M. (2011) Nucleic acid recognition by Toil-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 208, 643-651
25. Sepulveda, F. E., Maschalidi, S., Colisson, R., Heslop, L., Ghirelli, C., Sakka, E., Lennon-Duménil, A. M., Amigorena, S., Cabanie, L., and Manoury, B. (2009) Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 31, 737-748
26. Lu, K., Ye, W., Zhou, L., Collins, L. B., Chen, X., Gold, A., Ball, L. M., and Swenberg, J. A. (2010) Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers. J. Am. Chem. Soc. 132, 3388-3399
27. Pérez-Vargas J., Vaughan, R. C., Houser, C., Hastie, K. M., Kao, C. C., and Nemerow, G. R. (2014) Isolation and characterization of the DNA and protein binding activities of adenovirus core protein V. J. Virol. 88, 9287-9296
28. Forgac, M. (2007) Vacuolar ATP ases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929
29. Limmon, G. V., Arredouani, M., McCann, K. L., Corn Minor, R. A., Kobzik, L., and Imani, F. (2008) Scavenger receptor class-A is a novel cell surface receptor for double-stranded RNA. FASEB J. 22, 159-167
30. Takiguchi, T., Morizane, S., Yamamoto, T., Kajita, A., Ikeda, K., and Iwatsuki, K. (2014) Cathelicidin antimicrobial peptide LL-37 augments IFN-ß expression and anti-viral activity induced by double-stranded RNA in keratinocytes. Br. J. Dermatol. 10.1111/bjd.12942
31. de Bouteiller, O., Merck, E., Hasan, U. A., Hubac, S., Benguigui, B., Trinchieri, G., Bates, E. E., and Caux, C. (2005) Recognition of double-stranded RNA by human Toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH. J. Biol. Chem. 280, 38133-38145
32. Kuznik, A., Bencina, M., Svajger, U., Jeras, M., Rozman, B., and Jerala, R. (2011) Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J. Immunol. 186, 4794-4804
33. Garcia-Cattaneo, A., Gobert, F. X., Müller, M., Toscano, F., Flores, M., Lescure, A., Del Nery, E., and Benaroch, P. (2012) Cleavage of Toll-like receptor 3 by cathepsins B and H is essential for signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 9053-9058
34. Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y.H., Homey, B., Cao, W., Wang, Y. H., Su, B., Nestle, F. O., Zal, T., Mellman, I., Schröder, J. M., Liu, Y. J., and Gilliet, M. (2007) Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449, 564-569
35. Martin, T. J. (2014) Bone biology and anabolic therapies for bone: current status and future prospects. J. Bone Metab. 21, 8 -20