Gly6 of kalata B1 is critical for the selective binding to phosphatidylethanolamine membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 9, 2012, Pages 2354-2361

  Hall, Kristopher ^a   Lee, Tzong Hsien ^a   Daly, Norelle L ^b   Craik, David J ^b   Aguilar, Marie Isabel ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

AFM; Antimicrobial peptide; Cyclotide; Peptide lipid interaction; Phospholipid membrane; SPR

Indexed keywords

ALANINE DERIVATIVE; DIMYRISTOYLETHANOLAMINE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; KALATA B1; LIPID; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CELL MEMBRANE; CIRCULAR DICHROISM; CYCLOTIDES; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DISULFIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; KINETICS; LIPIDS; LIPOSOMES; MEMBRANES, ARTIFICIAL; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLETHANOLAMINES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SURFACE PLASMON RESONANCE; TIME FACTORS;

EID: 84861847904     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.04.007     Document Type: Article

References (42)

1. D.J. Craik, N.L. Daly, T. Bond, C. Waine, Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif, J. Mol. Biol. 294 (1999) 1327-1336. (Pubitemid 30008803)
2. D.J. Craik, N.L. Daly, C. Waine, The cystine knot motif in toxins and implications for drug design, Toxicon 39 (2001) 43-60.
3. C. Jennings, J. West, C. Waine, D. Craik, M. Anderson, Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis, Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 10614-10619. (Pubitemid 32878669)
4. D.J. Craik, M.A. Anderson, D.G. Barry, R.J. Clark, N.L. Daly, C.V. Jennings, J. Mulvenna, Discovery and structures of the cyclotides: novel macrocyclic peptides from plants, Lett. Pept. Sci. 8 (2002) 119-128. (Pubitemid 34836483)
5. L. Gran, Oxytocic principles of Oldenlandia affinis, Lloydia 36 (1973) 174-178.
6. L. Gran, F. Sandberg, K. Sletten, Oldenlandia affinis (R&S) DC, A plant containing uteroactive peptides used in African traditional medicine, J. Ethnopharmacol. 70 (2000) 197-203. (Pubitemid 30317360)
7. K.R. Gustafson, R.C. Sowder, I.L.E. Henderson, I.C. Parsons, Y. Kashman, J.H. Cardellina, I.J.B. McMahon, R.W. Buckheit, J.L.K. Pannell, M.R. Boyd, Circulins A and B. Novel human immunodeficiency virus (HIV)-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc. 116 (1994) 9337-9338.
8. K.M. Witherup, M.J. Bogusky, P.S. Anderson, H. Ramjit, R.W. Ransom, T. Wood, M. Sardana, Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes, J. Nat. Prod. 57 (1994) 1619-1625.
9. T. Schopke, M.I. Hasan Agha, R. Kraft, A. Otto, K. Hiller, Compounds with hemolytic activity from Viola tricolor L. and Viola arvensis murray, Sci. Pharm. 61 (1993) 145-153. (Pubitemid 23244214)
10. A.M. Broussalis, U. Göransson, J.D. Coussio, G. Ferraro, V. Martino, P. Claeson, First cyclotide from Hybanthus (Violaceae), Phytochemistry 58 (2001) 47-51. (Pubitemid 32750848)
11. C.V. Jennings, K.J. Rosengren, N.L. Daly, M. Plan, J. Stevens, M.J. Scanlon, C. Waine, D.G. Norman, M.A. Anderson, D.J. Craik, Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: do Mobius strips exist in nature? Biochemistry 44 (2005) 851-860. (Pubitemid 40129645)
12. P. Lindholm, U. Goransson, S. Johansson, P. Claeson, J. Gullbo, R. Larsson, L. Bohlin, A. Backlund, Cyclotides: a novel type of cytotoxic agents, Mol. Cancer Ther. 1 (2002) 365-369.
13. H.R. Bokesch, L.K. Pannell, P.K. Cochran, R.C. Sowder 2nd, T.C. McKee, M.R. Boyd, A novel anti-HIV macrocyclic peptide from Palicourea condensata, J. Nat. Prod. 64 (2001) 249-250. (Pubitemid 32198360)
14. J.P. Tam, Y.A. Lu, J.L. Yang, K.W. Chiu, An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 8913-8918. (Pubitemid 29374682)
15. H. Kamimori, K. Hall, D.J. Craik, M.I. Aguilar, Studies on the membrane interactions of the cyclotides kalata B1 and kalata B6 on model membrane systems by surface plasmon resonance, Anal. Biochem. 337 (2005) 149-153. (Pubitemid 40092791)
16. E. Svangard, R. Burman, S. Gunasekera, H. Lovborg, J. Gullbo, U. Goransson, Mechanism of action of cytotoxic cyclotides: cycloviolacin O2 disrupts lipid membranes, J. Nat. Prod. 70 (2007) 643-647. (Pubitemid 46797871)
17. Y.H. Huang, M.L. Colgrave, N.L. Daly, A. Keleshian, B. Martinac, D.J. Craik, The biological activity of the prototypic cyclotide kalata b1 is modulated by the formation of multimeric pores, J. Biol. Chem. 284 (2009) 20699-20707.
18. A. Nourse, M. Trabi, N.L. Daly, D.J. Craik, A comparison of the self-association behavior of the plant cyclotides kalata B1 and kalata B2 via analytical ultracentrifugation, J. Biol. Chem. 279 (2004) 562-570. (Pubitemid 38044859)
19. O. Saether, D.J. Craik, I.D. Campbell, K. Sletten, J. Juul, D.G. Norman, Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1, Biochemistry 34 (1995) 4147-4158.
20. M.L. Colgrave, D.J. Craik, Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot, Biochemistry 43 (2004) 5965-5975. (Pubitemid 38669464)
21. J.F. Hernandez, J. Gagnon, L. Chiche, T.M. Nguyen, J.P. Andrieu, A. Heitz, T. Trinh Hong, T.T. Pham, D. Le Nguyen, Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure, Biochemistry 39 (2000) 5722-5730. (Pubitemid 30307960)
22. L. Sando, S.T. Henriques, F. Foley, S.M. Simonsen, N.L. Daly, K. Hall, N., K.R. Gustafson, M.I. Aguilar, D.J. Craik,A synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor, ChemBioChem. 12 (2011) 2456-2462.
23. S.M. Simonsen, L. Sando, K.J. Rosengren, C.K. Wang, M.L. Colgrave, N.L. Daly, D.J. Craik, Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity, J. Biol. Chem. 283 (2008) 9805-9813.
24. T.H. Lee, H. Mozsolits, M.I. Aguilar, Measurement of the affinity of melittin for zwitterionic and anionic membranes using immobilized lipid biosensors, J. Pept. Res. 58 (2001) 464-476. (Pubitemid 34169374)
25. H. Mozsolits, M.I. Aguilar, Surface plasmon resonance spectroscopy: an emerging tool for the study of peptide-membrane interactions, Biopolymers 66 (2002) 3-18.
26. H. Mozsolits, H.J. Wirth, J. Werkmeister, M.I. Aguilar, Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance, Biochim. Biophys. Acta 1512 (2001) 64-76. (Pubitemid 32381023)
27. I. Horcas, R. Fernandez, J.M. Gomez-Rodriguez, J. Colchero, J. Gomez-Herrero, A.M. Baro, WSXM: a software for scanning probe microscopy and a tool for nanotechnology, Rev. Sci. Instrum. 78 (2007) 013705.
28. K. Hall, M.I. Aguilar, Membrane interactions of antimicrobial beta-peptides: the role of amphipathicity versus secondary structure induction, Biopolymers 92 (2009) 554-564.
29. K. Hall, T.H. Lee, M.I. Aguilar, The role of electrostatic interactions in the membrane binding of melittin, J. Mol. Recognit. 24 (2011) 108-118.
30. K. Hall, H. Mozsolits, M. Aguilar, Surface plasmon resonance analysis of antimicrobial peptide-membrane interactions: affinity & mechanism of action, Lett. Pept. Sci. 10 (2003) 475-485. (Pubitemid 40379038)
31. A. Mechler, S. Praporski, S. Piantavigna, S.M. Heaton, K.N. Hall, M.I. Aguilar, L.L. Martin, Structure and homogeneity of pseudo-physiological phospholipid bilayers and their deposition characteristics on carboxylic acid terminated self-assembled monolayers, Biomaterials 30 (2009) 682-689.
32. M.L. Colgrave, A.C. Kotze, Y.H. Huang, J. O'Grady, S.M. Simonsen, D.J. Craik, Cyclotides: natural, circular plant peptides that possess significant activity against gastrointestinal nematode parasites of sheep, Biochemistry 47 (2008) 5581-5589. (Pubitemid 351705169)
33. N.L. Daly, S. Love, P.F. Alewood, D.J. Craik, Chemical synthesis and folding pathways of large cyclic polypeptides: studies of the cystine knot polypeptide kalata B1, Biochemistry 38 (1999) 10606-10614.
34. S.T. Henriques, Y.H. Huang, K.J. Rosengren, H.G. Franquelim, F.A. Carvalho, A. Johnson, S. Sonza, G. Tachedjian, M.A. Castanho, N.L. Daly, D.J. Craik, Decoding the membrane activity of the cyclotide kalata B1: the importance of phosphatidylethanolamine phospholipids and lipid organization on hemolytic and anti- HIV activities, J. Biol. Chem. 286 (2011) 24231-24241.
35. R. Burman, A.A. Stromstedt, M. Malmsten, U. Goransson, Cyclotide-membrane interactions: defining factors of membrane binding, depletion and disruption, Biochim. Biophys. Acta 1808 (2011) 2665-2673.
36. R.N. Lewis, D.A. Mannock, R.N. McElhaney, D.C. Turner, S.M. Gruner, Effect of fatty acyl chain length and structure on the lamellar gel to liquid-crystalline and lamellar to reversed hexagonal phase transitions of aqueous phosphatidylethanolamine dispersions, Biochemistry 28 (1989) 541-548.
37. J.M. Seddon, Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids, Biochim. Biophys. Acta 1031 (1990) 1-69.
38. A.M. Bouchet, M.A. Frias, F. Lairion, F. Martini, H. Almaleck, G. Gordillo, E.A. Disalvo, Structural and dynamical surface properties of phosphatidylethanolamine containing membranes, Biochim. Biophys. Acta 1788 (2009) 918-925.
39. S.H. Hu, J. Gehrmann, P.F. Alewood, D.J. Craik, J.L. Martin, Crystal structure at 1.1 A resolution of alpha-conotoxin PnIB: comparison with alpha-conotoxins PnIA and GI, Biochemistry 36 (1997) 11323-11330. (Pubitemid 27408614)
40. A. Nicke, M.L. Loughnan, E.L. Millard, P.F. Alewood, D.J. Adams, N.L. Daly, D.J. Craik, R.J. Lewis, Isolation, structure, and activity of GID, a novel alpha 4/7-conotoxin with an extended N-terminal sequence, J. Biol. Chem. 278 (2003) 3137-3144. (Pubitemid 36801224)
41. D.G. Barry, N.L. Daly, R.J. Clark, L. Sando, D.J. Craik, Linearization of a naturally occurring circular protein maintains structure but eliminates hemolytic activity, Biochemistry 42 (2003) 6688-6695. (Pubitemid 36666109)
42. Z.O. Shenkarev, K.D. Nadezhdin, V.A. Sobol, A.G. Sobol, L. Skjeldal, A.S. Arseniev, Conformation and mode of membrane interaction in cyclotides. Spatial structure of kalata B1 bound to a dodecylphosphocholine micelle, FEBS J. 273 (2006) 2658-2672.