Sometimes it takes two to tango: Contributions of dimerization to functions of human α-defensin HNP1 peptide

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 8944-8953

  Pazgier, Marzena ^a,b   Wei, Gang ^a,c   Ericksen, Bryan ^a   Jung, Grace ^d   Wu, Zhibin ^a   De Leeuw, Erik ^a   Yuan, Weirong ^a   Szmacinski, Henryk ^a   Lu, Wei Yue ^c   Lubkowski, Jacek ^b   Lehrer, Robert I ^d   Lu, Wuyuan ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c FUDAN UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFENSINS; HOST DEFENSE; HUMAN MYELOID; LETHAL FACTOR; MINIMAL EFFECTS; N-METHYLATION; N-TERMINALS; S. AUREUS; SELF-ASSOCIATIONS; STAPHYLOCOCCUS AUREUS; STRUCTURAL EFFECT; TETRAMERIZATION; WILD TYPES; X-RAY CRYSTALLOGRAPHIC ANALYSIS;

ALKYLATION; ASSOCIATION REACTIONS; BACTERIA; DIMERS; DISEASES; ESCHERICHIA COLI; MONOMERS; X RAY CRYSTALLOGRAPHY;

DIMERIZATION;

ALPHA DEFENSIN; GLYCOPROTEIN GP 120; ISOLEUCINE; LEUCINE; PROTEIN HNP1; UNCLASSIFIED DRUG;

ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; DIMERIZATION; DISULFIDE BOND; ESCHERICHIA COLI; GENE MUTATION; HUMAN; IC 50; INNATE IMMUNITY; LETHAL GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; PROTEIN TETRAMERIZATION; STAPHYLOCOCCUS AUREUS; SURFACE PLASMON RESONANCE; WILD TYPE; X RAY CRYSTALLOGRAPHY;

ALPHA-DEFENSINS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; IMMUNITY, INNATE; MOLECULAR CONFORMATION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS 1; STAPHYLOCOCCUS AUREUS;

EID: 84858591438     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.332205     Document Type: Article

References (53)

1. Bevins, C. L. (2006) Paneth cell defensins: key effector molecules of innate immunity. Biochem. Soc. Trans. 34, 263-266
2. Ganz, T. (2003) Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-720
3. Lehrer, R. I. (2004) Primate defensins. Nat. Rev. Microbiol. 2, 727-738
4. Selsted, M. E., and Ouellette, A. J. (2005) Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6, 551-557 (Pubitemid 41710724)
5. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature 415, 389-395
6. Lehrer, R. I., and Lu, W. (2012) α-Defensins in human innate immunity. Immunol. Rev. 245, 84-112
7. Ganz, T., Selsted, M. E., Szklarek, D., Harwig, S. S., Daher, K., Bainton, D. F., and Lehrer, R. I. (1985) Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Invest. 76, 1427-1435 (Pubitemid 16193690)
8. Selsted, M. E., Harwig, S. S., Ganz, T., Schilling, J. W., and Lehrer, R. I. (1985) Primary structures of three human neutrophil defensins. J. Clin. Invest. 76, 1436-1439 (Pubitemid 16193691)
9. Gabay, J. E., Scott, R. W., Campanelli, D., Griffith, J., Wilde, C., Marra, M. N., Seeger, M., and Nathan, C. F. (1989) Antibiotic proteins of human polymorphonuclear leukocytes. Proc. Natl. Acad. Sci. U.S.A. 86, 5610-5614 (Pubitemid 19185594)
10. Wilde, C. G., Griffith, J. E., Marra, M. N., Snable, J. L., and Scott, R. W. (1989) Purification and characterization of human neutrophil peptide 4, a novel member of the defensin family. J. Biol. Chem. 264, 11200-11203 (Pubitemid 19168851)
11. Jones, D. E., and Bevins, C. L. (1992) Paneth cells of the human small intestine express an antimicrobial peptide gene. J. Biol. Chem. 267, 23216-23225
12. Jones, D. E., and Bevins, C. L. (1993) Defensin-6 mRNA in human Paneth cells. Implications for antimicrobial peptides in host defense of the human bowel. FEBS Lett. 315, 187-192 (Pubitemid 23015882)
13. Kagan, B. L., Selsted, M. E., Ganz, T., and Lehrer, R. I. (1990) Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc. Natl. Acad. Sci. U.S.A. 87, 210-214
14. Lehrer, R. I., Barton, A., Daher, K. A., Harwig, S. S., Ganz, T., and Selsted, M. E. (1989) Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity. J. Clin. Invest. 84, 553-561 (Pubitemid 19196987)
15. Klotman, M. E., and Chang, T. L. (2006) Defensins in innate antiviral immunity. Nat. Rev. Immunol. 6, 447-456
16. Kim, C., Gajendran, N., Mittrücker, H. W., Weiwad, M., Song, Y. H., Hurwitz, R., Wilmanns, M., Fischer, G., and Kaufmann, S. H. (2005) Human α-defensins neutralize anthrax lethal toxin and protect against its fatal consequences. Proc. Natl. Acad. Sci. U.S.A. 102, 4830-4835 (Pubitemid 40471539)
17. Lehrer, R. I., Jung, G., Ruchala, P., Wang, W., Micewicz, E. D., Waring, A. J., Gillespie, E. J., Bradley, K. A., Ratner, A. J., Rest, R. F., and Lu, W. (2009) Human alpha-defensins inhibit hemolysis mediated by cholesterol-dependent cytolysins. Infect. Immun. 77, 4028-4040
18. Wei, G., de Leeuw, E., Pazgier, M., Yuan, W., Zou, G., Wang, J., Ericksen, B., Lu, W. Y., Lehrer, R. I., and Lu, W. (2009) Through the looking glass, mechanistic insights from enantiomeric human defensins. J. Biol. Chem. 284, 29180-29192
19. Lehrer, R. I., Jung, G., Ruchala, P., Andre, S., Gabius, H. J., and Lu, W. (2009) Multivalent binding of carbohydrates by the human α-defensin, HD5. J. Immunol. 183, 480-490
20. Yang, D., Liu, Z. H., Tewary, P., Chen, Q., de la Rosa, G., and Oppenheim, J. J. (2007) Curr. Pharm. Des. 13, 3131-3139
21. Hill, C. P., Yee, J., Selsted, M. E., and Eisenberg, D. (1991) Crystal structure of defensin HNP-3, an amphiphilic dimer. Mechanisms of membrane permeabilization. Science 251, 1481-1485 (Pubitemid 121000438)
22. Szyk, A., Wu, Z., Tucker, K., Yang, D., Lu, W., and Lubkowski, J. (2006) Crystal structures of human α-defensins HNP4, HD5, and HD6. Protein Sci. 15, 2749-2760 (Pubitemid 44833756)
23. Wei, G., Pazgier, M., de Leeuw, E., Rajabi, M., Li, J., Zou, G., Jung, G., Yuan, W., Lu, W. Y., Lehrer, R. I., and Lu, W. (2010) Trp-26 imparts functional versatility to human α-defensin HNP1. J. Biol. Chem. 285, 16275-16285
24. Zhang, Y., Lu, W., and Hong, M. (2010) The membrane-bound structure and topology of a human α-defensin indicate a dimer pore mechanism for membrane disruption. Biochemistry 49, 9770-9782
25. Schnölzer, M., Alewood, P., Jones, A., Alewood, D., and Kent, S. B. (1992) In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, high yield assembly of difficult sequences. Int. J. Pept. Protein Res. 40, 180-193
26. Wu, Z., Powell, R., and Lu, W. (2003) Productive folding of human neutrophil alpha-defensins in vitro without the pro-peptide. J. Am. Chem. Soc. 125, 2402-2403 (Pubitemid 36512221)
27. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
28. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
29. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (Pubitemid 41087570)
30. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
31. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
32. Carson, M. (1991) RIBBONS 2.0. J. Appl. Crystallogr. 24, 958-961
33. Ericksen, B., Wu, Z., Lu, W., and Lehrer, R. I. (2005) Antibacterial activity and specificity of the six human α-defensins. Antimicrob. Agents Chemother. 49, 269-275 (Pubitemid 40065802)
34. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd Ed., pp. 353-380, Springer Science, New York
35. Ganz, T., Selsted, M. E., and Lehrer, R. I. (1986) Antimicrobial activity of phagocyte granule proteins. Semin. Respir Infect. 1, 107-117
36. Lu, W., Qasim, M. A., Laskowski, M., Jr., and Kent, S. B. (1997) Probing intermolecular main chain hydrogen bonding in serine proteinase-protein inhibitor complexes. Chemical synthesis of backbone-engineered turkey ovomucoid third domain. Biochemistry 36, 673-679 (Pubitemid 27110947)
37. Rajarathnam, K., Sykes, B. D., Kay, C. M., Dewald, B., Geiser, T., Baggiolini, M., and Clark-Lewis, I. (1994) Neutrophil activation by monomeric interleukin-8. Science 264, 90-92 (Pubitemid 24144491)
38. Wang, W., Owen, S. M., Rudolph, D. L., Cole, A. M., Hong, T., Waring, A. J., Lal, R. B., and Lehrer, R. I. (2004) Activity of α- and β-defensins against primary isolates of HIV-1. J. Immunol. 173, 515-520 (Pubitemid 38797379)
39. Monod, J., Changeux, J. P., and Jacob, F. (1963) Allosteric proteins and cellular control systems. J. Mol. Biol. 6, 306-329
40. Kuriyan, J., and Eisenberg, D. (2007) The origin of protein interactions and allostery in colocalization. Nature 450, 983-990 (Pubitemid 350273628)
41. Pabo, C. O., and Sauer, R. T. (1992) Transcription factors. Structural families and principles of DNA recognition. Annu. Rev. Biochem. 61, 1053-1095
42. Allen, S. J., Crown, S. E., and Handel, T. M. (2007) Chemokine. Receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25, 787-820 (Pubitemid 46697924)
43. Brogden, K. A. (2005) Antimicrobial peptides. Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250
44. de Leeuw, E., Burks, S. R., Li, X., Kao, J. P., and Lu, W. (2007) Structure-dependent functional properties of human defensin 5. FEBS Lett. 581, 515-520 (Pubitemid 46149601)
45. de Leeuw, E., Li, C., Zeng, P., Li, C., Diepeveen-de Buin, M., Lu, W. Y., Breukink, E., and Lu, W. (2010) Functional interaction of human neutrophil peptide-1 with the cell wall precursor lipid II. FEBS Lett. 584, 1543-1548
46. Breukink, E., Wiedemann, I., van Kraaij, C., Kuipers, O. P., Sahl, H., and de Kruijff, B. (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364 (Pubitemid 30016902)
47. Hasper, H. E., Kramer, N. E., Smith, J. L., Hillman, J. D., Zachariah, C., Kuipers, O. P., de Kruijff, B., and Breukink, E. (2006) An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313, 1636-1637 (Pubitemid 44414037)
48. Schneider, T., Kruse, T., Wimmer, R., Wiedemann, I., Sass, V., Pag, U., Jansen, A., Nielsen, A. K., Mygind, P. H., Raventós, D. S., Neve, S., Ravn, B., Bonvin, A. M., De Maria, L., Andersen, A. S., Gammelgaard, L. K., Sahl, H. G., and Kristensen, H. H. (2010) Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II. Science 328, 1168-1172
49. Schmitt, P., Wilmes, M., Pugnière, M., Aumelas, A., Bachère, E., Sahl, H. G., Schneider, T., and Destoumieux-Garzón, D. (2010) Insight into invertebrate defensin mechanism of action. Oyster defensins inhibit peptidoglycan biosynthesis by binding to lipid II. J. Biol. Chem. 285, 29208-29216
50. Sass, V., Schneider, T., Wilmes, M., Körner, C., Tossi, A., Novikova, N., Shamova, O., and Sahl, H. G. (2010) Human β-defensin 3 inhibits cell wall biosynthesis in Staphylococci. Infect. Immun. 78, 2793-2800
51. Deleted in proof
52. Hornef, M. W., Pütsep, K., Karlsson, J., Refai, E., and Andersson, M. (2004) Increased diversity of intestinal antimicrobial peptides by covalent dimer formation. Nat. Immunol. 5, 836-843 (Pubitemid 39172977)
53. Taylor, K., McCullough, B., Clarke, D. J., Langley, R. J., Pechenick, T., Hill, A., Campopiano, D. J., Barran, P. E., Dorin, J. R., and Govan, J. R. (2007) Covalent dimer species of beta-defensin Defr1 display potent antimicrobial activity against multidrug-resistant bacterial pathogens. Antimicrob. Agents Chemother. 51, 1719-1724 (Pubitemid 46744150)