Influence of specific amino acid side-chains on the antimicrobial activity and structure of bovine lactoferrampin

Biochemistry and Cell Biology

Volumn 90, Issue 3, 2012, Pages 362-377

  Haney, Evan F ^a   Nazmi, Kamran ^b   Bolscher, Jan G M ^b   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Antimicrobial peptide; Lactoferrampin; Lipid binding; Membrane interactions; Solution structure

Indexed keywords

AMINO ACID RESIDUES; AMPHIPATHIC; ANTI-MICROBIAL ACTIVITY; ANTIMICROBIAL PEPTIDE; BI-LAYER; C-TERMINAL REGIONS; IRON-BINDING PROTEIN; ISOTHERMAL TITRATION CALORIMETRY; LACTOFERRAMPIN; LACTOFERRIN; LIPID BINDING; MEMBRANE BINDING; MEMBRANE INSERTION; N-TERMINAL HELIX; PEPTIDE FOLDING; SEQUENCE ANALYSIS; SIDE-CHAINS; SOLUTION STRUCTURES;

AMINO ACIDS; DIFFERENTIAL SCANNING CALORIMETRY; DRUG INTERACTIONS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PHOSPHOLIPIDS; POLYPEPTIDES;

MAMMALS;

AMINO ACID; LACTOFERRAMPIN; PEPTIDE; PEPTIDE F 278 G; PEPTIDE G 279 A; PEPTIDE G 279 P; PEPTIDE K 273 G; PEPTIDE LFAMPB 265 284; PEPTIDE LFAMPB 268 284; PEPTIDE W 268 G; PEPTIDE W 268 G F 278 G; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; CIRCULAR DICHROISM; COMPARATIVE STUDY; DIFFERENTIAL SCANNING CALORIMETRY; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE DAMAGE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTI-BACTERIAL AGENTS; CALORIMETRY, DIFFERENTIAL SCANNING; CATTLE; ERYTHROCYTES; ESCHERICHIA COLI; HEMOLYSIS; HUMANS; LACTOFERRIN; MICELLES; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHATIDYLGLYCEROLS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SODIUM DODECYL SULFATE; STREPTOCOCCUS SANGUIS; THERMODYNAMICS; UNILAMELLAR LIPOSOMES;

BOVINAE; MAMMALIA;

EID: 84861414217     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/o11-057     Document Type: Article

References (50)

1. Adão R. Nazmi K. Bolscher J.G. Bastos M. 2011. C-and N-truncated antimicrobial peptides from LFampin 265-284: biophysical versus microbiology results. J. Pharm. Bioallied Sci. 3 (1): 60-69. 10.4103/0975-7406.76467 21430955
2. Adlerova L. Bartoskova A. Faldyna M. 2008. Lactoferrin: a review. Vet. Med. (Praha), 53: 457-468.
3. Ames, B.N. 1966. Assay of inorganic phosphate, total phosphate and phosphatases. In Methods in enzymology. Edited by E.F. Neufeld and V. Ginsberg. Academic Press, New York. pp. 115-118.
4. Andrushchenko V.V. Aarabi M.H. Nguyen L.T. Prenner E.J. Vogel H.J. 2008. Thermodynamics of the interactions of tryptophan-rich cathelicidin antimicrobial peptides with model and natural membranes. Biochim. Biophys. Acta, 1778 (4): 1004-1014. 10.1016/j.bbamem.2007.12.022 18222168
5. Arndt-Jovin D.J. Jovin T.M. 1989. Fluorescence labeling and microscopy of DNA. Methods Cell Biol. 30: 417-448. 10.1016/S0091-679X(08)60989-9 2467179
6. Aurora R. Rose G.D. 1998. Helix capping. Protein Sci. 7 (1): 21-38. 9514257
7. Bellamy W. Takase M. Yamauchi K. Wakabayashi H. Kawase K. Tomita M. 1992. Identification of the bactericidal domain of lactoferrin. Biochim. Biophys. Acta, 1121 (1-2): 130-136. 10.1016/0167-4838(92)90346-F 1599934
8. Brogden K.A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 (3): 238-250. 10.1038/nrmicro1098 15703760
9. Brünger A.T. Adams P.D. Clore G.M. Delano W.L. Gros P. Grosse-Kunstleve R.W. et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (5): 905-921. 10.1107/S0907444998003254 9757107
10. Cevik I.U. Dalkara T. 2003. Intravenously administered propidium iodide labels necrotic cells in the intact mouse brain after injury. Cell Death Differ. 10 (8): 928-929. 10.1038/sj.cdd.4401250 12868000
11. Chakrabartty A. Kortemme T. Baldwin R.L. 1994. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci. 3 (5): 843-852. 10.1002/pro.5560030514 8061613
12. Chan D.I. Prenner E.J. Vogel H.J. 2006. Tryptophan-and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta, 1758 (9): 1184-1202. 10.1016/j.bbamem.2006.04.006 16756942
13. Chen H.C. Brown J.H. Morell J.L. Huang C.M. 1988. Synthetic magainin analogues with improved antimicrobial activity. FEBS Lett. 236 (2): 462-466. 10.1016/0014-5793(88)80077-2 3410055
14. Delaglio F. Grzesiek S. Vuister G.W. Zhu G. Pfeifer J. Bax A. 1995. Nmrpipe'a multidimensional spectral processing system based on unix pipes. J. Biomol. NMR, 6 (3): 277-293. 10.1007/BF00197809 8520220
15. Epand R.M. Vogel H.J. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta, 1462 (1-2): 11-28. 10.1016/S0005-2736(99)00198-4 10590300
16. Flores-Villaseñor H. Canizalez-Román A. Reyes-Lopez M. Nazmi K. de la Garza.M. Zazueta-Beltrán J. et al. 2010. Bactericidal effect of bovine lactoferrin, LFcin, LFampin and LFchimera on antibiotic-resistant Staphylococcus aureus and Escherichia coli. Biometals, 23 (3): 569-578. 10.1007/s10534-010-9306-4 20195887
17. Gifford J.L. Hunter H.N. Vogel H.J. 2005. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell. Mol. Life Sci. 62 (22): 2588-2598. 10.1007/s00018-005-5373-z 16261252
18. Gofman Y. Linser S. Rzeszutek A. Shental-Bechor D. Funari S.S. Ben Tal N. Willumeit R. 2010. Interaction of an antimicrobial peptide with membranes: experiments and simulations with NKCS. J. Phys. Chem. B, 114 (12): 4230-4237. 10.1021/jp909154y 20201501
19. Großauer J. Kosol S. Schrank E. Zangger K. 2010. The peptide hormone ghrelin binds to membrane-mimetics via its octanoyl chain and an adjacent phenylalanine. Bioorg. Med. Chem. 18 (15): 5483-5488. 10.1016/j.bmc.2010.06.062 20621491
20. Haney E.F. Lau F. Vogel H.J. 2007. Solution structures and model membrane interactions of lactoferrampin, an antimicrobial peptide derived from bovine lactoferrin. Biochim. Biophys. Acta, 1768 (10): 2355-2364. 10.1016/j.bbamem. 2007.04.018 17560539
21. Haney E.F. Nazmi K. Lau F. Bolscher J.G. Vogel H.J. 2009. Novel lactoferrampin antimicrobial peptides derived from human lactoferrin. Biochimie, 91 (1): 141-154. 10.1016/j.biochi.2008.04.013 18534196
22. Hwang T.L. Shaka A.J. 1995. Water suppression that works'excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. A, 112 (2): 275-279. 10.1006/jmra.1995.1047
23. Janes, R.W., and Wallace, B.A. (Editors). 2009. An introduction to circular dichroism and synchrotron radiation circular dichroism spectroscopy. In Modern techniques for circular dichroism and synchrotron radiation circular dichroism spectroscopy. IOS Press, Amsterdam. pp. 1-18.
24. Johnson B.A. 2004. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278: 313-352. 15318002
25. Koradi R. Billeter M. Wuthrich K. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1): 51-55, 29-32. 10.1016/0263-7855(96)00009-4 8744573
26. Laskowski R.A. Rullmann J.A.C. MacArthur M.W. Kaptein R. Thornton J.M. 1996. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8 (4): 477-486. 10.1007/BF00228148 9008363
27. Li X. Li Y. Peterkofsky A. Wang G.S. 2006. NMR studies of aurein 1.2 analogs. Biochim. Biophys. Acta, 1758 (9): 1203-1214. 10.1016/j.bbamem.2006.03. 032 16716252
28. Linge J.P. O'Donoghue S.I. Nilges M. 2001. Automated assignment of ambiguous nuclear overhauser effects with ARIA. Methods Enzymol. 339: 71-90. 10.1016/S0076-6879(01)39310-2
29. Lohner, K. (Editor). 2001. The role of membrane lipid composition in cell targeting of antimicrobial peptides. In Development of novel antimicrobial agents: emerging strategies. Horizon Scientific Press, Norfolk, England. pp. 149-165.
30. Moore S.A. Anderson B.F. Groom C.R. Haridas M. Baker E.N. 1997. Three-dimensional structure of diferric bovine lactoferrin at 2.8 Å resolution. J. Mol. Biol. 274 (2): 222-236. 10.1006/jmbi.1997.1386 9398529
31. Nguyen L.T. Haney E.F. Vogel H.J. 2011. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29 (9): 464-472. 10.1016/j.tibtech.2011.05.001 21680034
32. Nicholson J.K. Foxall P.J. Spraul M. Farrant R.D. Lindon J.C. 1995. 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Anal. Chem. 67 (5): 793-811. 10.1021/ac00101a004 7762816
33. Park S. Son W.S. Kim Y.J. Kwon A.R. Lee B.J. 2007. NMR spectroscopic assessment of the structure and dynamic properties of an amphibian antimicrobial peptide (Gaegurin 4) bound to SDS micelles. J. Biochem. Mol. Biol. 40 (2): 261-269. 10.5483/BMBRep.2007.40.2.261 17394777
34. Pellegrini A. Thomas U. Bramaz N. Klauser S. Hunziker P. von Fellenberg R. 1997. Identification and isolation of a bactericidal domain in chicken egg white lysozyme. J. Appl. Microbiol. 82 (3): 372-378. 10.1046/j.1365-2672.1997. 00372.x 12455902
35. Rey J. Deville J. Chabbert M. 2010. Structural determinants stabilizing helical distortions related to proline. J. Struct. Biol. 171 (3): 266-276. 10.1016/j.jsb.2010.05.002 20457257
36. Shai Y. Oren Z. 1996. Diastereoisomers of cytolysins, a novel class of potent antibacterial peptides. J. Biol. Chem. 271 (13): 7305-7308. 10.1074/jbc.271.13.7305 8631748
37. Strøm M.B. Svendsen J.S. Rekdal Ø. 2000. Antibacterial activity of 15-residue lactoferricin derivatives. J. Pept. Res. 56 (5): 265-274. 10.1034/j.1399-3011.2000.00770.x 11095180
38. Strøm M.B. Haug B.E. Rekdal Ø. Skar M.L. Stensen W. Svendsen J.S. 2002. Important structural features of 15-residue lactoferricin derivatives and methods for improvement of antimicrobial activity. Biochem. Cell Biol. 80 (1): 65-74. 10.1139/o01-236 11908644
39. van der Kraan M.I.A. Groenink J. Nazmi K. Veerman E.C.I. Bolscher J.G.M. Amerongen A.V.N. 2004. Lactoferrampin: a novel antimicrobial peptide in the N1-domain of bovine lactoferrin. Peptides, 25 (2): 177-183. 10.1016/j.peptides. 2003.12.006 15062998
40. van der Kraan M.I.A. Nazmi K. Teeken A. Groenink J. van't Hof W. Veerman E.C.I. et al. 2005 a. Lactoferrampin, an antimicrobial peptide of bovine lactoferrin, exerts its candidacidal activity by a cluster of positively charged residues at the C-terminus in combination with a helix-facilitating N-terminal part. Biol. Chem. 386 (2): 137-142. 10.1515/BC.2005.017 15843157
41. van der Kraan M.I.A. van der Made C. Nami K. van't Hof W. Groenink J. Veerman E.C.I. et al. 2005 b. Effect of amino acid substitutions on the candidacidal activity of LFampin 265-284. Peptides, 26 (11): 2093-2097. 10.1016/j.peptides.2005.03.056 15946771
42. van der Kraan M.I.A. Nazmi K. van't Hof W. Amerongen A.V.N. Veerman E.C.I. Bolscher J.G.M. 2006. Distinct bactericidal activities of bovine lactoferrin peptides LFampin 268-284 and LFampin 265-284: Asp-Leu-Ile makes a difference. Biochem. Cell Biol. 84 (3): 358-362. 10.1139/o06-042 16936807
43. Veerman E.C. Nazmi K. Van't Hof W. Bolscher J.G. Den Hertog A.L. Nieuw Amerongen A.V. 2004. Reactive oxygen species play no role in the candidacidal activity of the salivary antimicrobial peptide histatin 5. Biochem. J. 381 (2): 447-452. 10.1042/BJ20040208 15109304
44. Vogel H.J. Schibli D.J. Jing W.G. Lohmeier-Vogel E.M. Epand R.F. Epand R.M. 2002. Towards a structure-function analysis of bovine lactoferricin and related tryptophan-and arginine-containing peptides. Biochem. Cell Biol. 80 (1): 49-63. 10.1139/o01-213 11908643
45. Wishart D.S. Sykes B.D. Richards F.M. 1992. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry, 31 (6): 1647-1651. 10.1021/bi00121a010 1737021
46. Won H.S. Kim S.S. Jung S.J. Son W.S. Lee B. Lee B.J. 2004. Structure-activity relationships of antimicrobial peptides from the skin of Rana esculenta inhabiting in Korea. Mol. Cells, 17 (3): 469-476. 15232222
47. Wong H. Bowie J.H. Carver J.A. 1997. The solution structure and activity of caerin 1.1, an antimicrobial peptide from the Australian green tree frog, Litoria splendida. Eur. J. Biochem. 247 (2): 545-557. 10.1111/j.1432-1033.1997. 00545.x 9266696
48. Wuthrich, K. 1986. NMR of proteins and nucleic acids. John Wiley & Sons Inc., New York.
49. Xiao Y.J. Dai H. Bommineni Y.R. Soulages J.L. Gong Y.X. Prakash O. Zhang G.L. 2006. Structure-activity relationships of fowlicidin-1, a cathelicidin antimicrobial peptide in chicken. FEBS J. 273 (12): 2581-2593. 10.1111/j.1742-4658.2006.05261.x 16817888
50. Yang S.T. Yub Shin S.Y. Kim Y.C. Kim Y. Hahm K.S. Kim J.I. 2002. Conformation-dependent antibiotic activity of tritrpticin, a cathelicidin-derived antimicrobial peptide. Biochem. Biophys. Res. Commun. 296 (5): 1044-1050. 10.1016/S0006-291X(02)02048-X 12207877