Electropositive charge in α-defensin bactericidal activity: Functional effects of Lys-for-Arg substitutions vary with the peptide primary structure

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 5035-5043

  Llenado, R Alan ^a   Weeks, Colby S ^a,b   Cocco, Melanie J ^a   Ouellette, André J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; ALPHA DEFENSIN 4; CELL PROTEIN; CRYPTDIN 4; ELASTASE; MATRILYSIN; SODIUM CHLORIDE; TRYPSIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERICIDAL ACTIVITY; CELL PERMEABILIZATION; CELL SURVIVAL; CONTROLLED STUDY; ESCHERICHIA COLI; MUTAGENESIS; NEUTROPHIL; NONHUMAN; PANETH CELL; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SENSITIVITY ANALYSIS; STRUCTURE ANALYSIS; SUBSTITUTION REACTION;

ALPHA-DEFENSINS; AMINO ACID SEQUENCE; ANIMALS; ANTI-BACTERIAL AGENTS; ARGININE; CELL MEMBRANE PERMEABILITY; ESCHERICHIA COLI; LYSINE; MACACA MULATTA; MICE; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION;

EID: 70350461418     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00695-09     Document Type: Article

References (45)

1. Aley, S. B., M. Zimmerman, M. Hetsko, M. E. Selsted, and F. D. Gillin. 1994. Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infect. Immun. 62:5397-5403.
2. Reference deleted.
3. Baud, F., and S. Karlin. 1999. Measures of residue density in protein structures. Proc. Natl. Acad. Sci. USA 96:12494-12499.
4. Borenstein, L. A., M. E. Selsted, R. I. Lehrer, and J. N. Miller. 1991. Antimicrobial activity of rabbit leukocyte defensins against Treponema pallidum subsp. pallidum. Infect. Immun. 59:1359-1367.
5. Cummings, J. E., D. P. Satchell, Y. Shirafuji, A. J. Ouellette, and T. K. Vanderlick. 2003. Electrostatically controlled interactions of mouse Paneth cell alpha-defensins with phospholipid membranes. Austr. J. Chem. 56:1031-1034.
6. Cummings, J. E., and T. K. Vanderlick. 2007. Kinetics of cryptdin-4 translocation coupled with peptide-induced vesicle leakage. Biochemistry 46:11882-11891.
7. Ernst, R. K., T. Guina, and S. I. Miller. 2001. Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect. 3:1327-1334.
8. Figueredo, S. M., C. S. Weeks, S. K. Young, and A. J. Ouellette. 2009. Anionic amino acids near the pro-alpha-defensin N terminus mediate inhibition of bactericidal activity in mouse pro-cryptdin-4. J. Biol. Chem. 284: 6826-6831.
9. Ganz, T., M. E. Selsted, D. Szklarek, S. S. Harwig, K. Daher, D. F. Bainton, and R. I. Lehrer. 1985. Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Investig. 76:1427-1435.
10. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
11. Hadjicharalambous, C., T. Sheynis, R. Jelinek, M. T. Shanahan, A. J. Ouellette, and E. Gizeli. 2008. Mechanisms of alpha-defensin bactericidal action: comparative membrane disruption by cryptdin-4 and its disulfide-null analogue. Biochemistry 47:12626-12634.
12. Hristova, K., M. E. Selsted, and S. H. White. 1996. Interactions of monomeric rabbit neutrophil defensins with bilayers: comparison with dimeric human defensin HNP-2. Biochemistry 35:11888-11894. (Pubitemid 26303708)
13. Jing, W., H. N. Hunter, H. Tanabe, A. J. Ouellette, and H. J. Vogel. 2004. Solution structure of cryptdin-4, a mouse Paneth cell alpha-defensin. Biochemistry 43:15759-15766. (Pubitemid 39665075)
14. Kamdar, K., A. Maemoto, X. Qu, S. K. Young, and A. J. Ouellette. 2008. In vitro activation of the rhesus macaque myeloid alpha-defensin precursor proRMAD-4 by neutrophil serine proteinases. J. Biol. Chem. 283:32361-32368.
15. Karlin, S., Z. Y. Zhu, and F. Baud. 1999. Atom density in protein structures. Proc. Natl. Acad. Sci. USA 96:12500-12505.
16. Lehrer, R. I. 2007. Multispecific myeloid defensins. Curr. Opin. Hematol. 14:16-21.
17. Lehrer, R. I., A. Barton, K. A. Daher, S. S. Harwig, T. Ganz, and M. E. Selsted. 1989. Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity. J. Clin. Investig. 84:553-561.
18. Lehrer, R. I., A. Barton, and T. Ganz. 1988. Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple-wavelength spectrophotometry. J. Immunol. Methods 108: 153-158.
19. Lehrer, R. I., T. Ganz, and M. E. Selsted. 1988. Oxygen-independent bactericidal systems. Mechanisms and disorders. Hematol. Oncol. Clin. N. Am. 2:159-169.
20. Maemoto, A., X. Qu, K. J. Rosengren, H. Tanabe, A. Henschen-Edman, D. J. Craik, and A. J. Ouellette. 2004. Functional analysis of the α-defensin disulfide array in mouse cryptdin-4. J. Biol. Chem. 279:44188-44196.
21. Mitchell, J. B., J. M. Thornton, J. Singh, and S. L. Price. 1992. Towards an understanding of the arginine-aspartate interaction. J. Mol. Biol. 226:251-262.
22. Ouellette, A. J. 2006. Paneth cell alpha-defensin synthesis and function. Curr. Top. Microbiol. Immunol. 306:1-25.
23. Ouellette, A. J., and C. L. Bevins. 2001. Paneth cell defensins and innate immunity of the small bowel. Inflamm. Bowel Dis. 7:43-50.
24. Patil, A., A. L. Hughes, and G. Zhang. 2004. Rapid evolution and diversifi- cation of mammalian α-defensins as revealed by comparative analysis of rodent and primate genes. Physiol. Genomics 20:1-11. (Pubitemid 40388499)
25. Rajabi, M., E. de Leeuw, M. Pazgier, J. Li, J. Lubkowski, and W. Lu. 2008. The conserved salt bridge in human alpha-defensin 5 is required for its precursor processing and proteolytic stability. J. Biol. Chem. 283:21509-21518.
26. Rosengren, K. J., N. L. Daly, L. M. Fornander, L. M. Jonsson, Y. Shirafuji, X. Qu, H. J. Vogel, A. J. Ouellette, and D. J. Craik. 2006. Structural and functional characterization of the conserved salt bridge in mammalian Paneth cell alpha-defensins: solution structures of mouse cryptidin-4 and (E15D)-cryptidin-4. J. Biol. Chem. 281:28068-28078.
27. Salzman, N. H., M. M. Chou, H. de Jong, L. Liu, E. M. Porter, and Y. Paterson. 2003. Enteric salmonella infection inhibits Paneth cell antimicrobial peptide expression. Infect. Immun. 71:1109-1115.
28. Satchell, D. P., T. Sheynis, S. Kolusheva, J. E. Cummings, T. K. Vanderlick, R. Jelinek, M. E. Selsted, and A. J. Ouellette. 2003. Quantitative interactions between cryptdin-4 amino terminal variants and membranes. Peptides 24: 1793-1803.
29. Satchell, D. P., T. Sheynis, Y. Shirafuji, S. Kolusheva, A. J. Ouellette, and R. Jelinek. 2003. Interactions of mouse Paneth cell alpha-defensins and alpha-defensin precursors with membranes: prosegment inhibition of peptide association with biomimetic membranes. J. Biol. Chem. 278: 13838-13846.
30. Selsted, M. E. 2007. A pocket guide to explorations of the defensin field. Curr. Pharm. Des. 13:3061-3064.
31. Selsted, M. E. 1993. Investigational approaches for studying the structures and biological functions of myeloid antimicrobial peptides. Genet. Eng. (N.Y.) 15:131-147.
32. Selsted, M. E., and S. S. Harwig. 1989. Determination of the disulfide array in the human defensin HNP-2. A covalently cyclized peptide. J. Biol. Chem. 264:4003-4007.
33. Selsted, M. E., and A. J. Ouellette. 2005. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6:551-557.
34. Shirafuji, Y., H. Tanabe, D. P. Satchell, A. Henschen-Edman, C. L. Wilson, and A. J. Ouellette. 2003. Structural determinants of procryptdin recognition and cleavage by matrix metalloproteinase-7. J. Biol. Chem. 278:7910-7919.
35. Tanabe, H., A. J. Ouellette, M. J. Cocco, and W. E. Robinson, Jr. 2004. Differential effects on human immunodeficiency virus type 1 replication by α-defensins with comparable bactericidal activities. J. Virol. 78:11622-11631.
36. Tanabe, H., X. Qu, C. S. Weeks, J. E. Cummings, S. Kolusheva, K. B. Walsh, R. Jelinek, T. K. Vanderlick, M. E. Selsted, and A. J. Ouellette. 2004. Structure-activity determinants in Paneth cell alpha-defensins: loss-of-function in mouse cryptdin-4 by charge-reversal at arginine residue positions. J. Biol. Chem. 279:11976-11983.
37. Tanabe, H., J. Yuan, M. M. Zaragoza, S. Dandekar, A. Henschen-Edman, M. E. Selsted, and A. J. Ouellette. 2004. Paneth cell alpha-defensins from rhesus macaque small intestine. Infect. Immun. 72:1470-1478.
38. Taudien, S., P. Galgoczy, K. Huse, K. Reichwald, M. Schilhabel, K. Szafranski, A. Shimizu, S. Asakawa, A. Frankish, I. F. Loncarevic, N. Shimizu, R. Siddiqui, and M. Platzer. 2004. Polymorphic segmental duplications at 8p23.1 challenge the determination of individual defensin gene repertoires and the assembly of a contiguous human reference sequence. BMC Genomics 5:92. (Pubitemid 41371900)
39. Tran, D., P. Tran, K. Roberts, G. Osapay, J. Schaal, A. Ouellette, and M. E. Selsted. 2008. Microbicidal properties and cytocidal selectivity of rhesus macaque theta defensins. Antimicrob. Agents Chemother. 52:944-953.
40. Weeks, C. S., H. Tanabe, J. E. Cummings, S. P. Crampton, T. Sheynis, R. Jelinek, T. K. Vanderlick, M. J. Cocco, and A. J. Ouellette. 2006. Matrix metalloproteinase-7 activation of mouse Paneth cell pro-alpha-defensins: Ser43 ↓ Ile44 proteolysis enables membrane-disruptive activity. J. Biol. Chem. 281:28932-28942.
41. White, S. H., W. C. Wimley, and M. E. Selsted. 1995. Structure, function, and membrane integration of defensins. Curr. Opin. Struct. Biol. 5:521-527.
42. Wilson, C. L., A. J. Ouellette, D. P. Satchell, T. Ayabe, Y. S. Lopez-Boado, J. L. Stratman, S. J. Hultgren, L. M. Matrisian, and W. C. Parks. 1999. Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286:113-117.
43. Reference deleted.
44. Zhu, S. 2008. Discovery of six families of fungal defensin-like peptides provides insights into origin and evolution of the CSαβ defensins. Mol. Immunol. 45:828-838.
45. Zou, G., E. de Leeuw, C. Li, M. Pazgier, P. Zeng, W. Y. Lu, J. Lubkowski, and W. Lu. 2007. Toward understanding the cationicity of defensins. Arg and Lys versus their noncoded analogs. J. Biol. Chem. 282:19653-19665.