Small-angle X-ray scattering studies of peptide-lipid interactions using the mouse paneth cell α-defensin cryptdin-4

Methods in Enzymology

Volumn 492, Issue , 2011, Pages 127-149

  Mishra, Abhijit ^a   Tai, Kenneth P ^b   Schmidt, Nathan W ^a,c   Ouellette, André J ^b   Wong, Gerard C L ^a,c  

^a Engineering IV   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; BIOMIMETIC MATERIAL; CELL PENETRATING PEPTIDE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN CRP 4; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; CRYSTALLOGRAPHY; HUMAN; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN PURIFICATION; REVIEW; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

EID: 79952000688     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381268-1.00016-1     Document Type: Chapter

References (76)

1. Aley, S. B., Zimmerman, M., Hetsko, M., Selsted, M. E., and Gillin, F. D. (1994). Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infect. Immun. 62, 5397-5403.
2. Als-Nielsen, J., and McMorrow, D. (2001). Elements of Modern X-ray Physics. John Wiley & Sons, Inc., New York.
3. Borenstein, L. A., Ganz, T., Sell, S., Lehrer, R. I., and Miller, J. N. (1991). Contribution of rabbit leukocyte defensins to the host response in experimental syphilis. Infect. Immun. 59, 1368-1377.
4. Brogden, K. (2005). Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250.
5. Chaikin, P., and Lubensky, T. (1995). Principles of Condensed Matter Physics. Cambridge University Press, Cambridge.
6. Cullity, B. (1956). Elements of X-Ray Diffraction. Addison-Wesley, Reading.
7. Cummings, J. E., Satchell, D. P., Shirafuji, Y., Ouellette, A. J., and Vanderlick, T. K. (2003). Electrostatically controlled interactions of mouse Paneth cell alpha-defensins with phospholipid membranes. Aust. J. Chem. 56, 1031-1034.
8. Cummings, J. E., and Vanderlick, T. K. (2007). Kinetics of cryptdin-4 translocation coupled with peptide-induced vesicle leakage. Biochemistry 46, 11882-11891.
9. Diamond, G., Zasloff, M., Eck, H., Brasseur, M., Maloy, W. L., and Bevins, C. L. (1991). Tracheal antimicrobial peptide, a cysteine-rich peptide from mammalian tracheal mucosa: Peptide isolation and cloning of a cDNA. Proc. Natl. Acad. Sci. USA 88, 3952-3956.
10. El-Sayed, A., Futaki, S., and Harashima, H. (2009). Delivery of macromolecules using arginine-rich cell-penetrating peptides: Ways to overcome endosomal entrapment. AAPS J. 11, 13-22.
11. Elliott, G., and O'Hare, P. (1997). Intracellular trafficking and protein delivery by a herpes virus structural protein. Cell 88, 223-233. (Pubitemid 28015871)
12. Figueredo, S., Mastroianni, J. R., Tai, K. P., and Ouellette, A. J. (2010). Expression and purification of recombinant alpha-defensins and alpha-defensin precursors in Escherichia coli. Methods Mol. Biol. 618, 47-60.
13. Frankel, A. D., and Pabo, C. O. (1988). Cellular uptake of the tat protein from human lmmunodeficiency virus. Cell 55, 1189-1193.
14. Ganz, T. (2003). Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-720.
15. 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.
16. Green, M., and Loewenstein, P. M. (1988). Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55, 1179-1188.
17. Guinier, A. (1994). X-Ray Diffraction in Crystals, Imperfect Crystals, and Amorphous Bodies. Dover, New York.
18. Hancock, R. E. W., and Sahl, H.-G. (2006). Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557.
19. Hickel, A., Danner-Pongratz, S., Amenitsch, H., Degovics, G., Rappolt, M., Lohner, K., and Pabst, G. (2008). Influence of antimicrobial peptides on the formation of nonlamellar lipid mesophases. Biochim. Biophys. Acta 1778, 2325-2333.
20. Hristova, K., Selsted, M. E., and White, S. H. (1996). Interactions of monomeric rabbit neutrophil defensins with bilayers: Comparison with dimeric human defensin HNP-2. Biochemistry 35, 11888-11894.
21. Huang, H. W. (2000). Action of antimicrobial peptides: Two-state model. Biochemistry 39, 8347-8352.
22. Joliot, A., Pernelle, C., Deagostini-Bazin, H., and Prochiantz, A. (1991). Antennapedia homeobox peptide regulates neural morphogenesis. Proc. Natl. Acad. Sci. USA 88, 1864-1868.
23. Keller, S., Gruner, S., and Gawrisch, K. (1996). Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim. Biophys. Acta 1278, 241-246.
24. Ladd, M., and Palmer, R. (1994). Structure Determination by X-Ray Crystallography. Plenum Press, New York.
25. Lehrer, R. I. (2004). Primate defensins. Nat. Rev. Microbiol. 2, 727-738.
26. Lehrer, R. I. (2007). Multispecific myeloid defensins. Curr. Opin. Hematol. 14, 16-21.
27. Lehrer, R. I., Barton, A., and Ganz, T. (1988). Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple-wavelength spectrophotometry. J. Immunol. Methods 108, 153-158.
28. Lehrer, R. I., Selsted, M. E., Szklarek, D., and Fleischmann, J. (1983). Antibacterial activity of microbicidal cationic proteins 1 and 2, natural peptide antibiotics of rabbit lung macrophages. Infect. Immun. 42, 10-14.
29. Li, Y., Beck, R., Huang, T., Choi, M. C., and Divinagracia, M. (2008). Scatterless hybrid metal-single-crystal slit for small-angle X-ray scattering and high-resolution X-ray diffraction. J. Appl. Crystallogr. 41, 1134-1139.
30. Liang, H., Harries, D., and Wong, G. (2005). Polymorphism of DNA-anionic liposome complexes reveals hierarchy of ion-mediated interactions. Proc. Natl. Acad. Sci. USA 102, 11173-11178.
31. Maemoto, A., Qu, X., Rosengren, K. J., Tanabe, H., Henschen-Edman, A., Craik, D. J., and Ouellette, A. J. (2004). Functional analysis of the {α}-defensin disulfide array in mouse cryptdin-4. J. Biol. Chem. 279, 44188-44196.
32. Matsuzaki, K. (1999). Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462, 1-10.
33. Matsuzaki, K., Sugishita, K.-I., Ishibe, N., Ueha, M., Nakata, S., Miyajima, K., and Epand, R. M. (1998). Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37, 11856-11863.
34. Mishra, A., Gordon, V., Yang, L., Coridan, R., and Wong, G. (2008). HIV TAT forms pores in membranes by inducing saddle-splay curvature: Potential role of bidentate hydrogen bonding. Angew. Chem. Intl. Ed. 47, 2986-2989.
35. Mitchell, D. J., Kim, D. T., Steinman, L., Fathman, C. G., and Rothbard, J. B. (2000). Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res. 56, 318-325.
36. Ouellette, A. J. (2006). Paneth cell alpha-defensin synthesis and function. Curr. Top. Microbiol. Immunol. 306, 1-25.
37. Ouellette, A. J., and Bevins, C. L. (2001). Paneth cell defensins and innate immunity of the small bowel. Inflamm. Bowel Dis. 7, 43-50.
38. Prenner, E. J., Lewis, R. N. A. H., Neuman, K. C., Gruner, S. M., Kondejewski, L. H., Hodges, R. S., and McElhaney, R. N. (1997). Nonlamellar phases induced by the interaction of gramicidin S with lipid bilayers. A possible relationship to membrane-disrupting activity. Biochemistry 36, 7906-7916.
39. Purdy Drew, K. R., Sanders, L. K., Culumber, Z. W., Zribi, O., and Wong, G. C. L. (2008). Cationic amphiphiles increase activity of aminoglycoside antibiotic tobramycin in the presence of airway polyelectrolytes. J. Am. Chem. Soc. 131, 486-493.
40. Purdy, K. R., Bartles, J., and Wong, G. (2007). Structural polymorphism of the actin-espin system: A prototypical system of filaments and linkers in stereocilia. Phys. Rev. Lett. 98, 058105.
41. Rädler, J., Koltover, I., Salditt, T., and Safinya, C. (1997). Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275, 810-814. (Pubitemid 27074877)
42. Rajabi, M., de Leeuw, E., Pazgier, M., Li, J., Lubkowski, J., and Lu, W. (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.
43. Rosengren, K. J., Daly, N. L., Fornander, L. M., Jonsson, L. M., Shirafuji, Y., Qu, X., Vogel, H. J., Ouellette, A. J., and Craik, D. J. (2006). Structural and functional characterization of the conserved salt bridge in mammalian paneth cell alpha-defensins: Solution structures of mouse Cryptdin-4 and (E15D)-Cryptdin-4. J. Biol. Chem. 281, 28068-28078.
44. Rothbard, J. B., Jessop, T. C., and Wender, P. A. (2005). Adaptive translocation: The role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells. Adv. Drug Deliv. Rev. 57, 495-504.
45. Sanders, L., Guáqueta, C., Angelini, T., Lee, J., Slimmer, S., Luijten, E., and Wong, G. (2005). Structure and stability of self-assembled actin-lysozyme complexes in salty water. Phys. Rev. Lett. 95, 108302.
46. Sanders, L., Xian, W., Guáqueta, C., Strohman, M., Vrasich, C., Luijten, E., and Wong, G. (2007). Control of electrostatic interactions between F-actin and genetically modified lysozyme in aqueous media. Proc. Natl. Acad. Sci. USA 104, 15994-15999.
47. Satchell, D. P., Sheynis, T., Kolusheva, S., Cummings, J. E., Vanderlick, T. K., Jelinek, R., Selsted, M. E., and Ouellette, A. J. (2003a). Quantitative interactions between cryptdin-4 amino terminal variants and membranes. Peptides 24, 1793-1803.
48. Satchell, D. P., Sheynis, T., Shirafuji, Y., Kolusheva, S., Ouellette, A. J., and Jelinek, R. (2003b). 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.
49. Schmidt, N., Mishra, A., Lai, G., Davis, M., Sanders, L., Tran, D., Garcia, A., Tai, K., McCray, P., Ouellette, A., Selsted, M., and Wong, G. (2010a). Submitted.
50. Schmidt, N. W., Mishra, A., Lai, G. H., and Wong, G. C. L. (2010a). Arginine-rich cell-penetrating peptides. FEBS Lett. 584, 1806-1813.
51. Schonwetter, B. S., Stolzenberg, E. D., and Zasloff, M. A. (1995). Epithelial antibiotics induced at sites of inflammation. Science 267, 1645-1648.
52. Schutte, B. C., Mitros, J. P., Bartlettt, J. A., Walters, J. D., Jia, H. P., Welsh, M. J., Casavant, T. L., and McCray, P. B. (2002). Discovery of five conserved beta-defensin gene clusters using a computational search strategy. Proc. Natl. Acad. Sci. USA 99, 2129-2133.
53. Seddon, J., and Templer, R. (1995). Polymorphism of lipid-water systems. In "Structure and Dynamics of Membranes: From Cell to Veiscles," (R. Lipowsky and E. Sackmann, eds.), Vol. 1. Elsevier, Amsterdam.
54. Selsted, M. E., Brown, D. M., Delange, R. J., and Lehrer, R. I. (1983). Primary structures of MCP-1 and MCP-2, natural peptide antibiotics of rabbit lung macrophages. J. Biol. Chem. 258, 14485-14489.
55. Selsted, M. E., and Harwig, S. S. (1989). Determination of the disulfide array in the human defensin HNP-2. A covalently cyclized peptide. J. Biol. Chem. 264, 4003-4007.
56. Selsted, M. E., and Ouellette, A. J. (2005). Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6, 551-557.
57. Selsted, M. E., Tang, Y. Q., Morris, W. L., McGuire, P. A., Novotny, M. J., Smith, W., Henschen, A. H., and Cullor, J. S. (1993). Purification, primary structures, and antibacterial activities of beta-defensins, a new family of antimicrobial peptides from bovine neutrophils. J. Biol. Chem. 268, 6641-6648.
58. Shai, Y. (1999). Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55-70.
59. Shirafuji, Y., Tanabe, H., Satchell, D. P., Henschen-Edman, A., Wilson, C. L., and Ouellette, A. J. (2003). Structural determinants of procryptdin recognition and cleavage by matrix metalloproteinase-7. J. Biol. Chem. 278, 7910-7919.
60. Som, A., Yang, L., Wong, G. C. L., and Tew, G. N. (2009). Divalent metal ion triggered activity of a synthetic antimicrobial in cardiolipin membranes. J. Am. Chem. Soc. 131, 15102-15103.
61. Staudegger, E., Prenner, E. J., Kriechbaum, M., Degovics, G., Lewis, R. N. A. H., McElhaney, R. N., and Lohner, K. (2000). X-ray studies on the interaction of the antimicrobial peptide gramicidin S with microbial lipid extracts: Evidence for cubic phase formation. Biochim. Biophys. Acta 1468, 213-230.
62. Warren, B. E. (1990). X-Ray Diffraction. Dover Publications, New York.
63. Wender, P. A., Galliher, W. C., Goun, E. A., Jones, L. R., and Pillow, T. H. (2008). The design of guanidinium-rich transporters and their internalization mechanisms. Adv. Drug Deliv. Rev. 60, 452-472.
64. White, S. H., Wimley, W. C., and Selsted, M. E. (1995). Structure, function, and membrane integration of defensins. Curr. Opin. Struct. Biol. 5, 521-527.
65. Winter, R., and Jeworrek, C. (2009). Effect of pressure on membranes. Soft Matter 5, 3157.
66. Wong, G. (2006). Electrostatics of rigid polyelectrolytes. Curr. Opin. Colloid Interface Sci. 11, 310-315.
67. Wong, G., Tang, J., Lin, A., Li, Y., Janmey, P., and Safinya, C. (2000). Hierarchical selfassembly of F-Actin and cationic lipid complexes: Stacked three-layer tubule networks. Science 288, 2035-2039. (Pubitemid 30397682)
68. Woolfson, M. (1997). An Introduction to X-Ray Crystallography. Cambridge University Press, Cambridge.
69. Wu, Z., Li, X., de Leeuw, E., Ericksen, B., and Lu, W. (2005). Why is the Arg5-Glu13 salt bridge conserved in mammalian alpha-defensins? J. Biol. Chem. 280, 43039-43047.
70. Yang, L., Gordon, V. D., Mishra, A., Som, A., Purdy, K. R., Davis, M. A., Tew, G. N., and Wong, G. C. L. (2007). Synthetic antimicrobial oligomers induce a composition-dependent topological transition in membranes. J. Am. Chem. Soc. 129, 12141-12147.
71. Yang, L., Gordon, V. D., Trinkle, D. R., Schmidt, N. W., Davis, M. A., DeVries, C., Som, A., Cronan, J. E., Tew, G. N., and Wong, G. C. L. (2008). Mechanism of a prototypical synthetic membrane-active antimicrobial: Efficient hole-punching via interaction with negative intrinsic curvature lipids. Proc. Natl. Acad. Sci. USA 105, 20595-20600.
72. Yang, L., Liang, H., Angelini, T. E., Butler, J., Coridan, R., Tang, J. X., and Wong, G. C. L. (2004). Self-assembled virus-membrane complexes. Nat. Mater. 3, 615-619.
73. Zanetti, M. (2004). Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75, 39-48.
74. Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389-395.
75. Zhu, S. (2008). Discovery of six families of fungal defensin-like peptides provides insights into origin and evolution of the CSalphabeta defensins. Mol. Immunol. 45, 828-838.
76. Zweytick, D., Tumer, S., Blondelle, S. E., and Lohner, K. (2008). Membrane curvature stress and antibacterial activity of lactoferricin derivatives. Biochem. Biophys. Res. Commun. 369, 395-400.