Antimicrobial action of histone H2B in Escherichia coli: Evidence for membrane translocation and DNA-binding of a histone H2B fragment after proteolytic cleavage by outer membrane proteinase T

Biochimie

Volumn 90, Issue 11-12, 2008, Pages 1693-1702

  Kawasaki, Hiroaki ^a,b   Koyama, Takumi ^a   Conlon, J Michael ^c   Yamakura, Fumiyuki ^d   Iwamuro, Shawichi ^a  

^a TOHO UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^d JUNTENDO UNIVERSITY   (Japan)

Author keywords

Antimicrobial peptides; Frog skin; Histone H2B; Membrane penetration; OmpT

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE; HISTONE H2B; HYBRID PROTEIN; MALTOSE BINDING PROTEIN; PROTEINASE; PROTEINASE T; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERIOSTASIS; CONTROLLED STUDY; DNA BINDING; ESCHERICHIA COLI; MEMBRANE TRANSPORT; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROTEIN DEGRADATION;

ANIMALS; CARRIER PROTEINS; CLONING, MOLECULAR; DNA; ESCHERICHIA COLI; HISTONES; RANA ESCULENTA; RECOMBINANT FUSION PROTEINS; SKIN; SUBTILISINS;

ANURA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HYLIDAE; RHACOPHORUS SCHLEGELII;

EID: 55349100857     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2008.07.003     Document Type: Article

References (52)

1. Hoffmann J.A., Kafatos F.C., Janeway C.A., and Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science 284 (1999) 1313-1318
2. Hancock R.E. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1 (2001) 156-164
3. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
4. Harwig S.S., Tan L., Qu X.D., Cho Y., Eisenhauer P.B., and Lehrer R.I. Bactericidal properties of murine intestinal phospholipase A2. J. Clin. Invest. 95 (1995) 603-610
5. 2. J. Pept. Res. 66 (2005) 19-26
6. Conlon J.M., and Kim J.B. A protease inhibitor of the Kunitz family from skin secretions of the tomato frog, Dyscophus guineti (Microhylidae). Biochem. Biophys. Res. Commun. 279 (2000) 961-964
7. Tollin M., Bergman P., Svenberg T., Jörnvall H., Gudmundsson G.H., and Agerberth B. Antimicrobial peptides in the first line defence of human colon mucosa. Peptides 24 (2003) 523-530
8. Bergsson G., Agerberth B., Jörnavall H., and Gudmundsson G.H. Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). FEBS J. 272 (2005) 4960-4969
9. Parseghian M.H., and Luhrs K.A. Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem. Cell Biol. 84 (2006) 589-604
10. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., and Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 303 (2004) 1532-1535
11. Patat S.A., Carnegie R.B., Kingsbury C., Gross P.S., Chapman R., and Schey K.L. Antimicrobial activity of histones from hemocytes of the Pacific white shrimp. Eur. J. Biochem. 271 (2004) 4825-4833
12. Robinette D., Wada S., Arroll T., Levy M.G., Miller W.L., and Noga E.J. Antimicrobial activity in the skin of the channel catfish Ictalurus punctatus: characterization of broad-spectrum histone-like antimicrobial proteins. Cell. Mol. Life Sci. 54 (1998) 467-475
13. Richards R.C., O'Neil D.B., Thibault P., and Ewart K.V. Histone H1: an antimicrobial protein of Atlantic salmon (Salmo salar). Biochem. Biophys. Res. Commun. 284 (2001) 549-555
14. Noga E.J., Fan Z., and Silphaduang U. Histone-like proteins from fish are lethal to the parasitic dinoflagellate Amyloodinium ocellatum. Parasitology 123 (2001) 57-65
15. Fernandes J.M., Kemp G.D., Molle M.G., and Smith V.J. Anti-microbial properties of histone H2A from skin secretions of rainbow trout, Oncorhynchus mykiss. Biochem. J. 368 (2002) 611-620
16. Silphaduang U., Hincke M.T., Nys Y., and Mine Y. Antimicrobial proteins in chicken reproductive system. Biochem. Biophys. Res. Commun. 340 (2006) 648-655
17. Li G.H., Mine Y., Hincke M.T., and Nys Y. Isolation and characterization of antimicrobial proteins and peptide from chicken liver. J. Pept. Sci. 13 (2007) 368-378
18. Hiemstra P.S., Eisenhauer P.B., Harwig S.S., van den Barselaar M.T., van Furth R., and Lehrer R.I. Antimicrobial proteins of murine macrophages. Infect. Immun. 61 (1993) 3038-3046
19. Rose F.R., Bailey K., Keyte J.W., Chan W.C., Greenwood D., and Mahida Y.R. Potential role of epithelial cell-derived histone H1 proteins in innate antimicrobial defense in the human gastrointestinal tract. Infect. Immun. 66 (1998) 3255-3263
20. Kim H.S., Cho J.H., Park H.W., Yoon H., Kim M.S., and Kim S.C. Endotoxin-neutralizing antimicrobial proteins of the human placenta. J. Immunol. 168 (2002) 2356-2364
21. Howell S.J., Wilk D., Yadav S.P., and Bevins C.L. Antimicrobial polypeptides of the human colonic epithelium. Peptides 24 (2003) 1763-1770
22. Jacobsen F., Baraniskin A., Mertens J., Mittler D., Mohammadi-Tabrisi A., Schubert S., Soltau M., Lehnhardt M., Behnke B., Gatermann S., Steinau H.U., and Steinstraesser L. Activity of histone H1.2 in infected burn wounds. J. Antimicrob. Chemother. 55 (2005) 735-741
23. Park C.B., Kim M.S., and Kim S.C. A novel antimicrobial peptide from Bufo bufo gargarizans. Biochem. Biophys. Res. Commun. 218 (1996) 408-413
24. Park I.Y., Park C.B., Kim M.S., and Kim S.C. Parasin I, an antimicrobial peptide derived from histone H2A in the cat fish, Parasilurus asotus. FEBS Lett. 437 (1998) 258-262
25. Birkemo G.A., Lüders T., Andersen Ø., Nes I.F., and Nissen-Meyer J. Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Biochim. Biophys. Acta. 1646 (2003) 207-215
26. Lüders T., Birkemo G.A., Nissen-Meyer J., Andersen Ø., and Nes I.F. Proline conformation-dependent antimicrobial activity of a proline-rich histone H1 N-terminal peptide fragment isolated from the skin mucus of Atlantic salmon. Antimicrob. Agents Chemother. 49 (2005) 2399-2406
27. Frohm M., Gunne H., Bergman A.C., Agerberth B., Bergman T., Boman A., Lidén S., Jörnvall H., and Boman H.G. Biochemical and antibacterial analysis of human wound and blister fluid. Eur. J. Biochem. 237 (1996) 86-92
28. Park C.B., Kim H.S., and Kim S.C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting functions. Biochem. Biophys. Res. Commun. 244 (1998) 253-257
29. Park C.B., Yi K.S., Matsuzaki K., Kim M.S., and Kim S.C. Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 8245-8250
30. Kawasaki H., Isaacson T., Iwamuro S., and Conlon J.M. A protein with antimicrobial activity in the skin of Schlegel's green frog Rhacophorus schlegelii (Rhacophoridae) identified as histone H2B. Biochem. Biophys. Res. Commun. 312 (2003) 1082-1086
31. Barchiesi F., Colombo A.L., McGough D.A., and Rinaldi M.G. Comparative study of broth macrodilution and microdilution techniques for in vitro antifungal susceptibility testing of yeasts by using the National Committee for Clinical Laboratory Standard's proposed standards. J. Clin. Microbiol. 32 (1994) 2494-2500
32. Simmaco M., Mangoni M.L., Boman A., Barra D., and Boman H.G. Experimental infections of Rana esculenta with Aeromonas hydrophila: a molecular mechanism for the control of the normal flora. Scand. J. Immunol. 48 (1998) 357-363
33. Rosenbluh J., Hariton-Gazal E., Dagan A., Rottem S., Graessmann A., and Loyter A. Translocation of histone proteins across lipid bilayers and Mycoplasma membranes. J. Mol. Biol. 345 (2005) 387-400
34. Grodberg J., and Dunn J.J. ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170 (1988) 1245-1253
35. Cho J.H., Park I.Y., Kim H.S., Lee W.T., Kim M.S., and Kim S.C. Cathepsin D produces antimicrobial peptide parasin I from histone H2A in the skin mucosa of fish. FASEB J. 16 (2002) 429-431
36. Kim H.S., Yoon H., Minn I., Park C.B., Lee W.T., Zasloff M., and Kim S.C. Pepsin-mediated processing of the cytoplasmic histone H2A to strong antimicrobial peptide buforin I. J. Immunol. 165 (2000) 3268-3274
37. Leytus S.P., Bowles L.K., Konisky J., and Mangel W.F. Activation of plasminogen to plasmin by a protease associated with the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 1485-1489
38. Sugimura K. Mutant isolation and cloning of the gene encoding protease VII from Escherichia coli. Biochem. Biophys. Res. Commun. 153 (1988) 753-759
39. Baneyx F., and Georgiou G. In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172 (1990) 491-494
40. Grodberg J., Lundrigan M.D., Toledo D.L., Mangel W.F., and Dunn J.J. Complete nucleotide sequence and deduced amino acid sequence of the ompT gene of Escherichia coli K-12. Nucleic Acids Res. 16 (1988) 1209
41. Kukkonen M., and Korhonen T.K. The omptin family of enterobacterial surface proteases/adhesins: from housekeeping in Escherichia coli to systemic spread of Yersinia pestis. Int. J. Med. Microbiol. 294 (2004) 7-14
42. Hwang B.Y., Varadarajan N., Li H., Rodriguez S., Iverson B.L., and Georgiou G. Substrate specificity of the Escherichia coli outer membrane protease OmpP. J. Bacteriol. 189 (2007) 522-530
43. Vandeputte-Rutten L., Kramer R.A., Kroon J., Dekker N., Egmond M.R., and Gros P. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 20 (2001) 5033-5039
44. Stumpe S., and Bakker E.P. Requirement of a large K+-uptake capacity and of extracytoplasmic protease activity for protamine resistance of Escherichia coli. Arch. Microbiol. 167 (1997) 126-136
45. Stumpe S., Schmid R., Stephens D.L., Georgiou G., and Bakker E.P. Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J. Bacteriol. 180 (1998) 4002-4006
46. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3 (2005) 238-250
47. Kobayashi S., Takeshima K., Park C.B., Kim S.C., and Matsuzaki K. Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry 39 (2000) 8648-8654
48. Kobayashi S., Chikushi A., Tougu S., Imura Y., Nishida M., Yano Y., and Matsuzaki K. Membrane translocation mechanism of the antimicrobial peptide buforin 2. Biochemistry 43 (2004) 15610-15616
49. Stewart D.E., Sarkar A., and Wampler J.E. Occurrence and role of cis peptide bonds in protein structures. J. Mol. Biol. 214 (1990) 253-260
50. Augusto L.A., Decottignies P., Synguelakis M., Nicaise M., Le Maréchal P., and Chaby R. Histones: a novel class of lipopolysaccharide-binding molecules. Biochemistry 42 (2003) 3929-3938
51. Kawasaki H., Iwamuro S., Goto Y., Nielsen P.F., and Conlon J.M. Characterization of a hemolytic protein, identified as histone H4, from the skin of the Japanese tree frog Hyla japonica (Hylidae). Comp. Biochem. Physiol. B. 149 (2008) 120-125
52. Ohnuma A., Conlon J.M., Kawasaki H., and Iwamuro S. Developmental and triiodothyronine-induced expression of genes encoding preprotemporins in the skin of Tago's brown frog Rana tagoi. Gen. Comp. Endocrinol. 146 (2006) 242-250