The human cathelicidin peptide LL-37 and truncated variants induce segregation of lipids and proteins in the plasma membrane of Candida albicans

Biological Chemistry

Volumn 387, Issue 10-11, 2006, Pages 1495-1502

  Den Hertog, Alice L ^a,c   Van Marle, Jan ^b   Veerman, Enno C I ^a   Valentijn Benz, Marianne ^a   Nazmi, Kamran ^a   Kalay, Hakan ^c   Grün, Christian H ^c   Van't Hof, Wim ^a   Bolscher, Jan G M ^a   Amerongen, Arie V Nieuw ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antimicrobial peptides; Candida albicans; Freeze fracture; LL 37; Phase separation

Indexed keywords

CATHELICIDIN; CATHELICIDIN PEPTIDE LL 25; CATHELICIDIN PEPTIDE LL 31; CATHELICIDIN PEPTIDE LL 37; CATHELICIDIN PEPTIDE RK 31; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CONTROLLED STUDY; CYTOCHEMISTRY; ELECTRON MICROSCOPY; FLUORESCENCE ANALYSIS; FUNCTIONAL PROTEOMICS; LIPID ANALYSIS; MASS SPECTROMETRY; MEMBRANE STRUCTURE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEIN VARIANT;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; CANDIDA ALBICANS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; HUMANS; LIPID METABOLISM; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; SEQUENCE ALIGNMENT; VARIATION (GENETICS);

CANDIDA ALBICANS;

EID: 33750623420     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2006.187     Document Type: Conference Paper

References (35)

1. Bagnat, M., Chang, A., and Simons, K. (2001). Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 12, 4129-4138.
2. Connor, J., Pak, C.C., and Schroit, A.J. (1994). Exposure of phosphatidylserine in the outer leaflet of human red blood cells-relationship to cell-density, cell age, and clearance by mononuclear-cells. J. Biol. Chem. 269, 399-2404.
3. Cope, J.E. (1980). The porosity of the cell wall of Candida albicans. J. Gen. Microbiol. 119, 253-255.
4. Davidson, D.J., Currie, A.J., Reid, G.S., Bowdish, D.M., MacDonald, K.L., Ma, R.C., Hancock, R.E., and Speert, D.P. (2004). The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 172, 1146-1156.
5. De Nobel, J.G. and Barnett, J.A. (1991). Passage of molecules through yeast cell walls: a brief essay-review. Yeast 7, 313-323.
6. den Hertog, A.L., Wong Fong Sang, H.W., Kraayenhof, R., Bolscher, J.G.M., Van't Hof, W., Veerman, E.C.I., and Nieuw Amerongen, A.V. (2004). Interactions of histatin 5 and histatin 5-derived peptides with liposome membranes: surface effects, translocation and permeabilization. Biochem. J. 379, 665-672.
7. den Hertog, A.L., Van Marie, J., Van Veen, H.A., Van't Hof, W., Bolscher, J.G.M., Veerman, E.C.I., and Nieuw Amerongen, A.V. (2005). Candidacidal effects of two antimicrobial peptides: histatin 5 causes small membrane defects, but LL-37 causes massive disruption of the cell membrane. Biochem. J. 388, 689-695.
8. Elssner, A., Duncan, M., Gavrilin, M., and Wewers, M.D. (2004). A novel P2X7 receptor activator, the human cathelicidin-derived peptide LL37, induces IL-1β processing and release. J. Immunol. 172, 4987-4994.
9. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L., and Henson, P.M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
10. Fratti, R.A., Jun, Y., Merz, A.J., Margolis, N., and Wickner, W. (2004). Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J. Cell Biol. 167, 1087-1098.
11. Gates, M.A., Thorkildson, P., and Kozel, T.R. (2004). Molecular architecture of the Cryptococcus neoformans capsule. Mol. Microbiol. 52, 13-24.
12. Hancock, R.E.W. and Rozek, A. (2002). Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206, 143-149.
13. He, K., Ludtke, S.J., Huang, H.W., and Worcester, D.L. (1995). Antimicrobial peptide pores in membranes detected by neutron in-plane scattering. Biochemistry 34, 15614-15618.
14. He, K., Ludtke, S.J., Worcester, D.L., and Huang, H.W. (1996). Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys. J. 70, 2659-2666.
15. Henzler-Wildman, K.A., Lee, D.K., and Ramamoorthy, A. (2003). Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42, 6545-6558.
16. Henzler-Wildman, K.A., Martinez G.V., Brown M.F., and Ramamoorthy A. (2004). Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43, 8459-8469.
17. Lopez-Garcia, B., Lee, P.H., Yamasaki, K., and Gallo, R.L. (2005). Anti-fungal activity of cathelicidins and their potential role in Candida albicans skin infection. J. Invest. Dermatol. 125, 108-115.
18. Malinska, K., Malinsky, J., Opekarova, M., and Tanner, W. (2003). Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14, 4427-4436.
19. Martin, S.W., and Konopka, J.B. (2004). Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3, 675-684.
20. Morris, R., Cox, H., Mombelli, E., and Quinn, P.J. (2004). Rafts, little caves and large potholes: how lipid structure interacts with membrane proteins to create functionally diverse membrane environments. Subcell. Biochem. 37, 35-118.
21. 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.
22. Orr, G., Hu, D., Ozcelik, S., Opresko, L.K., Wiley, H.S., and Colson, S.D. (2005). Cholesterol dictates the freedom of EGF receptors and HER2 in the plane of the membrane. Biophys. J. 89, 1362-1373.
23. Pichler, H., and Riezman, H. (2004). Where sterols are required for endocytosis. Biochim. Biophys. Acta 1666, 51-61.
24. Pike, L.J. 2005. Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim. Biophys. Acta 1746, 260-273.
25. Ruissen, A.L.A., Groenink, J., Van't Hof, W., Walgreen-Weterings, E., Van Marie, J., Van Veen, H.A., Voorhout, W.F., Veerman, E.C.I., and Nieuw Amerongen, A.V. (2002). Histatin 5 and derivatives. Their localization and effects on the ultrastructural level. Peptides 23, 1391-1399.
26. Severs, N.J. and Robenek, H. (1983). Detection of microdomains in biomembranes - an appraisal of recent developments in freeze-fracture cytochemistry. Biochim. Biophys. Acta 737, 373-408.
27. Sørensen, O.E., Follin, P., Johnsen, A.H., Calafat, J., Tjabringa, G.S., Hiemstra, P.S., and Borregaard, N. (2001). Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97, 3951-3959.
28. Tjabringa, G.S., Aarbiou, J., Ninaber, D.K., Drijfhout, J.W., Sorensen, O.E., Borregaard, N., Rabe, K.F., and Hiemstra, P.S. (2003). The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J. Immunol. 171, 6690-6696.
29. Umebayashi, K. and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 161, 1117-1131.
30. Van der Kraan, M.I.A., Nazmi, K., Groenink J., Van't Hof, W., Veerman, E.C.I., Bolscher, J.G.M., and Nieuw Amerongen, A.V. (2005). Ultrastructural effects of antimicrobial peptides from bovine lactoferrin on the membranes of Candida albicans and Escherichia coli. Peptides 26, 1537-1542.
31. Van't Hof, W., Veerman, E.C.I., Helmerhorst, E.J., and Nieuw Amerongen, A.V. (2001). Antimicrobial peptides: properties and applicability. Biol. Chem. 382, 597-619.
32. Westerhoff, H.V., Zasloff, M., Rosner J.L., Hendler, R.W., De, W.A., Vaz, G.A., Jongsma, P.M., Riethorst, A., and Juretic, D. (1995). Functional synergism of the magainins PGLa and magainin-2 in Escherichia coli, tumor cells and liposomes. Eur. J. Biochem. 228, 257-264.
33. Yates, J.R., Eng, J.K., McCormack, A.L., and Schieltz, D. (1995). Method to correlate tandem mass-spectra of modified peptides to amino-acid-sequences in the protein database. Anal. Chem. 67, 1426-1436.
34. Zanetti, M. (2004). Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75, 39-48.
35. Zwaal, R.F.A. and Schroit, A.J. (1997). Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89, 1121-1132.