Native oligomerization determines the mode of action and biological activities of human cathelicidin LL-37

Biochemical Journal

Volumn 457, Issue 2, 2014, Pages 263-275

  Xhindoli, Daniela ^a   Pacor, Sabrina ^a   Guida, Filomena ^a   Antcheva, Nikolinka ^a   Tossi, Alessandro ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Cathelicidin; Covalent dimer; Cross linking; LL 37; Oligomerization; RL 37

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; CIRCULAR DICHROISM; CROSS LINKING; CYTOTOXICITY; DIMERIZATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEMOLYSIS; HUMAN; HUMAN CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; ULTRAVIOLET IRRADIATION;

EID: 84890942880     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131048     Document Type: Article

References (42)

1. Vandamme, D., Landuyt, B., Luyten, W. and Schoofs, L. (2012) A comprehensive summary of LL-37, the factotum human cathelicidin peptide. Cell. Immunol. 280, 22-35
2. Nizet, V., Ohtake, T., Lauth, X., Trowbridge, J., Rudisill, J., Dorschner, R. A., Pestonjamasp, V., Piraino, J., Huttner, K. and Gallo, R. L. (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414, 454-457
3. Sochacki, K. A., Barns, K. J., Bucki, R. and Weisshaar, J. C. (2011) Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. Proc. Natl. Acad. Sci. U.S.A. 108, E77-E81
4. Barns, K. J. and Weisshaar, J. C. (2013) Real-time attack of LL-37 on single Bacillus subtilis cells. Biochim. Biophys. Acta 1828, 1511-1520
5. Brown, K. L., Poon, G. F., Birkenhead, D., Pena, O. M., Falsafi, R., Dahlgren, C., Karlsson, A., Bylund, J., Hancock, R. E. and Johnson, P. (2011) Host defense peptide LL-37 selectively reduces proinflammatory macrophage responses. J. Immunol. 186, 5497-5505
6. Ruan, Y., Shen, T., Wang, Y., Hou, M., Li, J. and Sun, T. (2013) Antimicrobial peptide LL-37 attenuates LTA induced inflammatory effect in macrophages. Int. Immunopharmacol. 15, 575-580
7. Agerberth, B., Charo, J., Werr, J., Olsson, B., Idali, F., Lindbom, L., Kiessling, R., Jornvall, H., Wigzell, H. and Gudmundsson, G. H. (2000) The human antimicrobial and chemotactic peptides LL-37 and -defensins are expressed by specific lymphocyte and monocyte populations. Blood 96, 3086-3093
8. Koczulla, R., von Degenfeld, G., Kupatt, C., Krotz, F., Zahler, S., Gloe, T., Issbrucker, K., Unterberger, P., Zaiou, M., Lebherz, C. et al. (2003) An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J. Clin. Invest. 111, 1665-1672
9. Heilborn, J. D., Nilsson, M. F., Kratz, G., Weber, G., Sorensen, O., Borregaard, N. and Stahle-Backdahl, M. (2003) The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Invest. Dermatol. 120, 379-389
10. Johansson, J., Gudmundsson, G. H., Rottenberg, M. E., Berndt, K. D. and Agerberth, B. (1998) Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem. 273, 3718-3724
11. Wang, G. (2008) Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles. J. Biol. Chem. 283, 32637-32643
12. Porcelli, F., Verardi, R., Shi, L., Henzler-Wildman, K. A., Ramamoorthy, A. and Veglia, G. (2008) NMR structure of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles. Biochemistry 47, 5565-5572
13. Epand, R. F., Wang, G., Berno, B. and Epand, R. M. (2009) Lipid segregation explains selective toxicity of a series of fragments derived from the human cathelicidin LL-37. Antimicrob. Agents Chemother. 53, 3705-3714
14. Hong, J., Oren, Z. and Shai, Y. (1999) Structure and organization of hemolytic and nonhemolytic diastereomers of antimicrobial peptides in membranes. Biochemistry 38, 16963-16973
15. Zelezetsky, I., Pontillo, A., Puzzi, L., Antcheva, N., Segat, L., Pacor, S., Crovella, S. and Tossi, A. (2006) Evolution of the primate cathelicidin. Correlation between structural variations and antimicrobial activity. J. Biol. Chem. 281, 19861-19871
16. Morgera, F., Vaccari, L., Antcheva, N., Scaini, D., Pacor, S. and Tossi, A. (2009) Primate cathelicidin orthologues display different structures and membrane interactions. Biochem. J. 417, 727-735
17. Tomasinsig, L., Morgera, F., Antcheva, N., Pacor, S., Skerlavaj, B., Zanetti, M. and Tossi, A. (2009) Structure dependence of biological activities for primate cathelicidins. J. Pept. Sci. 15, 576-582
18. Zhao, C., Nguyen, T., Boo, L. M., Hong, T., Espiritu, C., Orlov, D., Wang, W., Waring, A. and Lehrer, R. I. (2001) RL-37, an -helical antimicrobial peptide of the rhesus monkey. Antimicrob. Agents Chemother. 45, 2695-2702
19. Tomasinsig, L., Pizzirani, C., Skerlavaj, B., Pellegatti, P., Gulinelli, S., Tossi, A., Di Virgilio, F. and Zanetti, M. (2008) The human cathelicidin LL-37 modulates the activities of the P2X7 receptor in a structure-dependent manner. J. Biol. Chem. 283, 30471-30481
20. Murakami, M., Lopez-Garcia, B., Braff, M., Dorschner, R. A. and Gallo, R. L. (2004) Postsecretory processing generates multiple cathelicidins for enhanced topical antimicrobial defense. J. Immunol. 172, 3070-3077
21. Braff, M. H., Hawkins, M. A., Di Nardo, A., Lopez-Garcia, B., Howell, M. D., Wong, C., Lin, K., Streib, J. E., Dorschner, R., Leung, D. Y. and Gallo, R. L. (2005) Structure-function relationships among human cathelicidin peptides: Dissociation of antimicrobial properties from host immunostimulatory activities. J. Immunol. 174, 4271-4278
22. Wang, G., Elliott, M., Cogen, A. L., Ezell, E. L., Gallo, R. L. and Hancock, R. E. (2012) Structure, dynamics, and antimicrobial and immune modulatory activities of human LL-23 and its single-residue variants mutated on the basis of homologous primate cathelicidins. Biochemistry 51, 653-664
23. Sigurdardottir, T., Andersson, P., Davoudi, M., Malmsten, M., Schmidtchen, A. and Bodelsson, M. (2006) In silico identification and biological evaluation of antimicrobial peptides based on human cathelicidin LL-37. Antimicrob. Agents Chemother. 50, 2983-2989
24. Wang, G., Epand, R. F., Mishra, B., Lushnikova, T., Thomas, V. C., Bayles, K. W. and Epand, R. M. (2012) Decoding the functional roles of cationic side chains of the major antimicrobial region of human cathelicidin LL-37. Antimicrob. Agents Chemother. 56, 845-856
25. Farrell, I. S., Toroney, R., Hazen, J. L., Mehl, R. A. and Chin, J. W. (2005) Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat. Methods 2, 377-384
26. Tam, J. P. and Shen, Z. Y. (1992) Efficient approach to synthesis of two-chain asymmetric cysteine analogs of receptor-binding region of transforming growth factor-. Int. J. Pept. Protein Res. 39, 464-471
27. Waddell, W. J. (1956) A simple ultraviolet spectrophotometric method for the determination of protein. J. Lab. Clin. Med. 48, 311-314
28. Kuipers, B. J. and Gruppen, H. (2007) Prediction of molar extinction coefficients of proteins and peptides using UV absorption of the constituent amino acids at 214 nm to enable quantitative reverse phase high-performance liquid chromatography-mass spectrometry analysis. J. Agric. Food Chem. 55, 5445-5451
29. Chen, Y. H., Yang, J. T. and Chau, K. H. (1974) Determination of the helix and form of proteins in aqueous solution by circular dichroism. Biochemistry 13, 3350-3359
30. Jones, R. N., Wilson, H. W., Novick, Jr, W. J., Barry, A. L. and Thornsberry, C. (1982) In vitro evaluation of CENTA, a new -lactamase- susceptible chromogenic cephalosporin reagent. J. Clin. Microbiol. 15, 954-958
31. Ilic, N., Novkovic, M., Guida, F., Xhindoli, D., Benincasa, M., Tossi, A. and Juretic, D. (2013) Selective antimicrobial activity and mode of action of adepantins, glycine-rich peptide antibiotics based on anuran antimicrobial peptide sequences. Biochim. Biophys. Acta 1828, 1004-1012
32. Schagger, H. (2006) Tricine-SDS-PAGE. Nat. Protoc. 1, 16-22
33. Grigoryan, G. and Keating, A. E. (2008) Structural specificity in coiled-coil interactions. Curr. Opin. Struct. Biol. 18, 477-483
34. Oren, Z., Lerman, J. C., Gudmundsson, G. H., Agerberth, B. and Shai, Y. (1999) Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: Relevance to the molecular basis for its non-cell-selective activity. Biochem. J. 341, 501-513
35. Sood, R., Domanov, Y., Pietiainen, M., Kontinen, V. P. and Kinnunen, P. K. (2008) Binding of LL-37 to model biomembranes: Insight into target vs host cell recognition. Biochim. Biophys. Acta 1778, 983-996
36. Li, Y., Li, X., Li, H., Lockridge, O. and Wang, G. (2007) A novel method for purifying recombinant human host defense cathelicidin LL-37 by utilizing its inherent property of aggregation. Protein Expression Purif. 54, 157-165
37. Wagschal, K., Tripet, B. and Hodges, R. S. (1999) De novo design of a model peptide sequence to examine the effects of single amino acid substitutions in the hydrophobic core on both stability and oligomerization state of coiled-coils. J. Mol. Biol. 285, 785-803
38. Yethon, J. A., Heinrichs, D. E., Monteiro, M. A., Perry, M. B. and Whitfield, C. (1998) Involvement of waaY, waaQ, and waaP in the modification of Escherichia coli lipopolysaccharide and their role in the formation of a stable outer membrane. J. Biol. Chem. 273, 26310-26316
39. Weidenmaier, C., Peschel, A., Xiong, Y. Q., Kristian, S. A., Dietz, K., Yeaman, M. R. and Bayer, A. S. (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J. Infect. Dis. 191, 1771-1777
40. Peschel, A., Otto, M., Jack, R. W., Kalbacher, H., Jung, G. and Gotz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274, 8405-8410
41. Salvestrini, V., Zini, R., Rossi, L., Gulinelli, S., Manfredini, R., Bianchi, E., Piacibello, W., Caione, L., Migliardi, G., Ricciardi, M. R. et al. (2012) Purinergic signaling inhibits human acute myeloblastic leukemia cell proliferation, migration, and engraftment in immunodeficient mice. Blood 119, 217-226
42. Dorman, G. and Prestwich, G. D. (1994) Benzophenone photophores in biochemistry. Biochemistry 33, 5661-5673