Buforins: Histone H2A-derived antimicrobial peptides from toad stomach

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 8, 2009, Pages 1564-1569

  Cho, Ju Hyun ^a   Sung, Bong Hyun ^b   Kim, Sun Chang ^b  

^a Gyeongsang National University   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Antimicrobial peptide; Buforin; Histone H2A; Proline hinge; Structure activity

Indexed keywords

BUFORIN; CECROPIN; HISTONE H2A; MELITTIN; PEPSIN A; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIMICROBIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; BACILLUS SUBTILIS; BACTERIAL PERITONITIS; BACTERICIDAL ACTIVITY; BIOFILM; CANDIDA ALBICANS; CELL MEMBRANE PERMEABILITY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; DRUG POTENCY; ESCHERICHIA COLI; INNATE IMMUNITY; MEDICAL RESEARCH; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN SECRETION; PSEUDOMONAS PUTIDA; REVIEW; SACCHAROMYCES CEREVISIAE; SALMONELLA TYPHIMURIUM; SEPSIS; SEPTIC SHOCK; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS; STOMACH GLAND; STOMACH MUCOSA; STREPTOCOCCUS MUTANS; STRUCTURE ACTIVITY RELATION; TOAD;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BUFONIDAE; HUMANS; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; PROTEINS; STOMACH;

ANURA; BUFO GARGARIZANS;

EID: 67649406168     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.10.025     Document Type: Review

References (92)

1. Nicolas P., and Mor A. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 49 (1995) 277-304
2. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
3. Kagnoff M.F., and Eckmann L. Epithelial cells as sensors for microbial infection. J. Clin. Invest. 100 (1997) 6-10
4. Gallo R.L., and Huttner K.M. Antimicrobial peptides: an emerging concept in cutaneous biology. J. Invest. Dermatol. 111 (1998) 739-743
5. Nascimento A.C., Fontes W., Sebben A., and Castro M.S. Antimicrobial peptides from anurans skin secretions. Prot. Peptide Letters 10 (2003) 227-238
6. Pukala T.L., Bowie J.H., Maselli V.M., Musgrave I.F., and Tyler M.J. Host-defence peptides from the glandular secretions of amphibians: structure and activity. Nat. Prod. Rep. 23 (2006) 368-393
7. Barra D., and Simmaco M. Amphibian skin: a promising resource for antimicrobial peptides. Trends Biotechnol. 13 (1995) 205-209
8. Hancock R.E., and Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24 (2006) 1551-1557
9. Hancock R.E., and Scott M.G. The role of antimicrobial peptides in animal defenses. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8856-8861
10. Boman H.G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13 (1995) 61-92
11. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3 (2005) 238-250
12. Shai Y. Mode of action of membrane active antimicrobial peptides. Biopolymers 66 (2002) 236-248
13. Matsuzaki K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462 (1999) 1-10
14. Shai Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462 (1999) 55-70
15. Mookherjee N., and Hancock R.E. Cationic host defence peptides: innate immune regulatory peptides as a novel approach for treating infections. Cell. Mol. Life Sci. 64 (2007) 922-933
16. Yang D., Biragyn A., Kwak L.W., and Oppenheim J.J. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol. 23 (2002) 291-296
17. Bals R., and Wilson J.M. Cathelicidins-a family of multifunctional antimicrobial peptides. Cell. Mol. Life Sci. 60 (2003) 711-720
18. 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
19. 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
20. 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 cellular functions. Biochem. Biophys. Res. Commun. 244 (1998) 253-257
21. Kim H.S., Park C.B., Kim M.S., and Kim S.C. cDNA cloning and characterization of buforin I, an antimicrobial peptide: a cleavage product of histone H2A. Biochem. Biophys. Res. Commun. 229 (1996) 381-387
22. 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
23. Hirsch J.G. Bactericidal action of histone. J. Exp. Med. 108 (1958) 925-944
24. Miller T.E., and Watson D.W. Biochemical characterization of the antimicrobial histone released by deoxyribonuclease and lactic acid. Proc. Soc. Exp. Biol. Med. 131 (1969) 339-342
25. 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
26. Bevins C.L. Antimicrobial peptides as agents of mucosal immunity. Ciba Found. Symp. 186 (1994) 250-260 discussion 261-259
27. Huttner K.M., and Bevins C.L. Antimicrobial peptides as mediators of epithelial host defense. Pediatr. Res. 45 (1999) 785-794
28. Wehkamp J., Schauber J., and Stange E.F. Defensins and cathelicidins in gastrointestinal infections. Curr. Opin. Gastroenterol. 23 (2007) 32-38
29. Birkemo G.A., Luders T., Andersen O., 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
30. 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
31. Li C., Song L., Zhao J., Zhu L., Zou H., Zhang H., Wang H., and Cai Z. Preliminary study on a potential antibacterial peptide derived from histone H2A in hemocytes of scallop Chlamys farreri. Fish Shellfish Immunol. 22 (2007) 663-672
32. Luders T., Birkemo G.A., Nissen-Meyer J., Andersen O., 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
33. Fernandes J.M., Molle G., Kemp G.D., and Smith V.J. Isolation and characterisation of oncorhyncin II, a histone H1-derived antimicrobial peptide from skin secretions of rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol. 28 (2004) 127-138
34. Kawasaki H., Isaacson T., Iwamuro S., and Conlon J.M. A protein with antimicrobial activity in the skin of Schlegel's green tree frog Rhacophorus schlegelii (Rhacophoridae) identified as histone H2B. Biochem. Biophys. Res. Commun. 312 (2003) 1082-1086
35. 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
36. Patrzykat A., Zhang L., Mendoza V., Iwama G.K., and Hancock R.E. Synergy of histone-derived peptides of coho salmon with lysozyme and flounder pleurocidin. Antimicrob. Agents Chemother. 45 (2001) 1337-1342
37. 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
38. 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
39. Park I.Y., Park C.B., Kim M.S., and Kim S.C. Parasin I, an antimicrobial peptide derived from histone H2A in the catfish, Parasilurus asotus. FEBS Lett. 437 (1998) 258-262
40. 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
41. Cho J.H., Park I.Y., Kim M.S., and Kim S.C. Matrix metalloproteinase 2 is involved in the regulation of the antimicrobial peptide parasin I production in catfish skin mucosa. FEBS Lett. 531 (2002) 459-463
42. Yi G.S., Park C.B., Kim S.C., and Cheong C. Solution structure of an antimicrobial peptide buforin II. FEBS Lett. 398 (1996) 87-90
43. 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
44. 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
45. 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
46. Uyterhoeven E.T., Butler C.H., Ko D., and Elmore D.E. Investigating the nucleic acid interactions and antimicrobial mechanism of buforin II. FEBS Lett. 582 (2008) 1715-1718
47. Otvos Jr. L., O I., Rogers M.E., Consolvo P.J., Condie B.A., Lovas S., Bulet P., and Blaszczyk-Thurin M. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39 (2000) 14150-14159
48. Kragol G., Lovas S., Varadi G., Condie B.A., Hoffmann R., and Otvos Jr. L. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40 (2001) 3016-3026
49. Giacometti A., Cirioni O., Ghiselli R., Goffi L., Mocchegiani F., Riva A., Scalise G., and Saba V. Polycationic peptides as prophylactic agents against methicillin-susceptible or methicillin-resistant Staphylococcus epidermidis vascular graft infection. Antimicrob. Agents Chemother. 44 (2000) 3306-3309
50. Giacometti A., Cirioni O., Barchiesi F., Del Prete M.S., and Scalise G. Antimicrobial activity of polycationic peptides. Peptides 20 (1999) 1265-1273
51. Giacometti A., Cirioni O., Del Prete M.S., Barchiesi F., Fortuna M., Drenaggi D., and Scalise G. In vitro activities of membrane-active peptides alone and in combination with clinically used antimicrobial agents against Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 44 (2000) 1716-1719
52. Giacometti A., Cirioni O., Del Prete M.S., Barchiesi F., Paggi A.M., Petrelli E., and Scalise G. Comparative activities of polycationic peptides and clinically used antimicrobial agents against multidrug-resistant nosocomial isolates of Acinetobacter baumannii. J. Antimicrob. Chemother. 46 (2000) 807-810
53. Giacometti A., Cirioni O., Del Prete M.S., Paggi A.M., D'Errico M.M., and Scalise G. Combination studies between polycationic peptides and clinically used antibiotics against Gram-positive and Gram-negative bacteria. Peptides 21 (2000) 1155-1160
54. Giacometti A., Cirioni O., Del Prete M.S., Barchiesi F., Fineo A., and Scalise G. Activity of buforin II alone and in combination with azithromycin and minocycline against Cryptosporidium parvum in cell culture. J. Antimicrob. Chemother. 47 (2001) 97-99
55. Giacometti A., Cirioni O., Barchiesi F., Del Prete M.S., Fortuna M., Caselli F., and Scalise G. In vitro susceptibility tests for cationic peptides: comparison of broth microdilution methods for bacteria that grow aerobically. Antimicrob. Agents Chemother. 44 (2000) 1694-1696
56. Giacometti A., Cirioni O., Del Prete M.S., Barchiesi F., and Scalise G. Short-term exposure to membrane-active antibiotics inhibits Cryptosporidium parvum infection in cell culture. Antimicrob. Agents Chemother. 44 (2000) 3473-3475
57. Garcia G.E., Moorad D.R., and Gordon R.K. Buforin I, a natural peptide, inhibits botulinum neurotoxin B activity in vitro. J. Appl. Toxicol. 19 Suppl 1 (1999) S19-22
58. Chu A.J., Chen B.M., Lin H., and Beydoun S. Antimicrobial peptide buforin I inhibits tissue factor-initiated coagulation. Arch. Biochem. Biophys. 392 (2001) 3-7
59. Jerala R., and Porro M. Endotoxin neutralizing peptides. Curr. Top. Med. Chem. 4 (2004) 1173-1184
60. Rosenfeld Y., and Shai Y. Lipopolysaccharide (Endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim. Biophys. Acta 1758 (2006) 1513-1522
61. Ghiselli R., Giacometti A., Cirioni O., Mocchegiani F., Viticchi C., Scalise G., and Saba V. Cationic peptides combined with betalactams reduce mortality from peritonitis in experimental rat model. J. Surg. Res. 108 (2002) 107-111
62. Giacometti A., Cirioni O., Ghiselli R., Mocchegiani F., Del Prete M.S., Viticchi C., Kamysz W., E L.E., Saba V., and Scalise G. Potential therapeutic role of cationic peptides in three experimental models of septic shock. Antimicrob. Agents Chemother. 46 (2002) 2132-2136
63. Giacometti A., Cirioni O., Ghiselli R., Orlando F., Mocchegiani F., D'Amato G., Silvestri C., Riva A., Del Prete M.S., Saba V., and Scalise G. Antiendotoxin activity of antimicrobial peptides and glycopeptides. J. Chemother. 15 (2003) 129-133
64. Hoskin D.W., and Ramamoorthy A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 1778 (2008) 357-375
65. Papo N., and Shai Y. Host defense peptides as new weapons in cancer treatment. Cell. Mol. Life Sci. 62 (2005) 784-790
66. Papo N., Seger D., Makovitzki A., Kalchenko V., Eshhar Z., Degani H., and Shai Y. Inhibition of tumor growth and elimination of multiple metastases in human prostate and breast xenografts by systemic inoculation of a host defense-like lytic peptide. Cancer Res. 66 (2006) 5371-5378
67. Papo N., Braunstein A., Eshhar Z., and Shai Y. Suppression of human prostate tumor growth in mice by a cytolytic d-, l-amino acid peptide: membrane lysis, increased necrosis, and inhibition of prostate-specific antigen secretion. Cancer Res. 64 (2004) 5779-5786
68. Papo N., and Shai Y. New lytic peptides based on the D,L-amphipathic helix motif preferentially kill tumor cells compared to normal cells. Biochemistry 42 (2003) 9346-9354
69. Papo N., Shahar M., Eisenbach L., and Shai Y. A novel lytic peptide composed of dl-amino acids selectively kills cancer cells in culture and in mice. J. Biol. Chem. 278 (2003) 21018-21023
70. Sharma S.V. Melittin resistance: a counterselection for ras transformation. Oncogene 7 (1992) 193-201
71. Moore A.J., Devine D.A., and Bibby M.C. Preliminary experimental anticancer activity of cecropins. Pept. Res. 7 (1994) 265-269
72. Cruciani R.A., Barker J.L., Zasloff M., Chen H.C., and Colamonici O. Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 3792-3796
73. Takeshima K., Chikushi A., Lee K.K., Yonehara S., and Matsuzaki K. Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J. Biol. Chem. 278 (2003) 1310-1315
74. Lee H.S., Park C.B., Kim J.M., Jang S.A., Park I.Y., Kim M.S., Cho J.H., and Kim S.C. Mechanism of anticancer activity of buforin IIb, a histone H2A-derived peptide. Cancer Lett. 271 (2008) 47-55
75. Hanai N., Nakamura K., and Shitara K. Recombinant antibodies against ganglioside expressed on tumor cells. Cancer Chemother. Pharmacol. 46 Suppl (2000) S13-17
76. Bitton R.J., Guthmann M.D., Gabri M.R., Carnero A.J., Alonso D.F., Fainboim L., and Gomez D.E. Cancer vaccines: an update with special focus on ganglioside antigens. Oncol. Rep. 9 (2002) 267-276
77. Lehrer R.I., Lichtenstein A.K., and Ganz T. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu. Rev. Immunol. 11 (1993) 105-128
78. Coates A., Hu Y., Bax R., and Page C. The future challenges facing the development of new antimicrobial drugs. Nat. Rev. Drug Discov. 1 (2002) 895-910
79. Gordon Y.J., Romanowski E.G., and McDermott A.M. A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Curr. Eye Res. 30 (2005) 505-515
80. McPhee J.B., Scott M.G., and Hancock R.E. Design of host defence peptides for antimicrobial and immunity enhancing activities. Comb. Chem. High Throughput Screen. 8 (2005) 257-272
81. Meng H., and Kumar K. Antimicrobial activity and protease stability of peptides containing fluorinated amino acids. J. Am. Chem. Soc. 129 (2007) 15615-15622
82. Hancock R.E., and Lehrer R. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16 (1998) 82-88
83. Ingham A.B., and Moore R.J. Recombinant production of antimicrobial peptides in heterologous microbial systems. Biotechnol. Appl. Biochem. 47 (2007) 1-9
84. Lee J.H., Minn I., Park C.B., and Kim S.C. Acidic peptide-mediated expression of the antimicrobial peptide buforin II as tandem repeats in Escherichia coli. Protein Expr. Purif. 12 (1998) 53-60
85. Lee J.H., Kim M.S., Cho J.H., and Kim S.C. Enhanced expression of tandem multimers of the antimicrobial peptide buforin II in Escherichia coli by the DEAD-box protein and trxB mutant. Appl. Microbiol. Biotechnol. 58 (2002) 790-796
86. Kim J.M., Jang S.A., Yu B.J., Sung B.H., Cho J.H., and Kim S.C. High-level expression of an antimicrobial peptide histonin as a natural form by multimerization and furin-mediated cleavage. Appl. Microbiol. Biotechnol. 78 (2008) 123-130
87. Chong S., Mersha F.B., Comb D.G., Scott M.E., Landry D., Vence L.M., Perler F.B., Benner J., Kucera R.B., Hirvonen C.A., Pelletier J.J., Paulus H., and Xu M.Q. Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene 192 (1997) 271-281
88. Mathys S., Evans T.C., Chute I.C., Wu H., Chong S., Benner J., Liu X.Q., and Xu M.Q. Characterization of a self-splicing mini-intein and its conversion into autocatalytic N- and C-terminal cleavage elements: facile production of protein building blocks for protein ligation. Gene 231 (1999) 1-13
89. Ingham A.B., Sproat K.W., Tizard M.L., and Moore R.J. A versatile system for the expression of nonmodified bacteriocins in Escherichia coli. J. Appl. Microbiol. 98 (2005) 676-683
90. Morassutti C., De Amicis F., Bandiera A., and Marchetti S. Expression of SMAP-29 cathelicidin-like peptide in bacterial cells by intein-mediated system. Protein Expr. Purif. 39 (2005) 160-168
91. Diao H., Guo C., Lin D., and Zhang Y. Intein-mediated expression is an effective approach in the study of beta-defensins. Biochem. Biophys. Res. Commun. 357 (2007) 840-846
92. Chen Y.Q., Zhang S.Q., Li B.C., Qiu W., Jiao B., Zhang J., and Diao Z.Y. Expression of a cytotoxic cationic antibacterial peptide in Escherichia coli using two fusion partners. Protein Expr. Purif. 57 (2008) 303-311