Molecular characterization of the interaction of crotamine-derived nucleolar targeting peptides with lipid membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 11, 2012, Pages 2707-2717

  Rodrigues, Margarida ^a   Santos, Andrea ^a   De La Torre, Beatriz G ^b   Rádis Baptista, Gandhi ^b,c   Andreu, David ^b   Santos, Nuno C ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Cell penetrating peptide; Crotamine; Fluorescence spectroscopy; Membrane partition; Membrane translocation; Nucleolar targeting peptide

Indexed keywords

1 PALMITOYL 2 OLEOYL SN GLYCERO 3 PHOSPHO(19 SN GLYCEROL); 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; ACRYLAMIDE; CELL PENETRATING PEPTIDE; CROTAMINE; GLYCEROL; NUCLEOLAR TARGETING PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; LIPID BILAYER; LIPID MEMBRANE; LIPID VESICLE; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR MODEL; NUCLEOLAR LOCALIZATION SIGNAL; PARTITION COEFFICIENT; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; CELL NUCLEOLUS; CIRCULAR DICHROISM; CROTALID VENOMS; FLUORESCENCE; MEMBRANE LIPIDS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING;

EID: 84864029951     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.06.014     Document Type: Article

References (70)

1. A.D. Frankel, and C.O. Pabo Cellular uptake of the tat protein from human immunodeficiency virus Cell 55 1988 1189 1193 (Pubitemid 19020071)
2. E. Vives Present and future of cell-penetrating peptide mediated delivery systems: "is the Trojan horse too wild to go only to Troy?" J. Control. Release 109 2005 77 85 (Pubitemid 41737254)
3. P. Jarver, I. Mager, and U. Langel In vivo biodistribution and efficacy of peptide mediated delivery Trends Pharmacol. Sci. 31 2010 528 535
4. S.T. Henriques, M.N. Melo, and M.A.R.B. Castanho Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 399 2006 1 7 (Pubitemid 44505401)
5. K.M. Stewart, K.L. Horton, and S.O. Kelley Cell-penetrating peptides as delivery vehicles for biology and medicine Org. Biomol. Chem. 6 2008 2242 2255 (Pubitemid 351863664)
6. R.M. Martin, G. Tunnemann, H. Leonhardt, and M.C. Cardoso Nucleolar marker for living cells Histochem. Cell Biol. 127 2007 243 251
7. S.T. Henriques, and M.A.R.B. Castanho Environmental factors that enhance the action of the cell penetrating peptide pep-1. A spectroscopic study using lipidic vesicles Biochim. Biophys. Acta 1669 2005 75 86 (Pubitemid 40704724)
8. R.M. Johnson, S.D. Harrison, and D. Maclean Therapeutic applications of cell-penetrating peptides Methods Mol. Biol. 683 2010 535 551
9. B.R. Meade, and S.F. Dowdy Exogenous siRNA delivery using peptide transduction domains/cell penetrating peptides Adv. Drug Deliv. Rev. 59 2007 134 140 (Pubitemid 46770904)
10. J.R. Luque-Ortega, B.G. De la Torre, V. Hornillos, J.M. Bart, C. Rueda, M. Navarro, F. Amat-Guerri, A.U. Acuñ a, D. David Andreu, and L. Rivas Defeating Leishmania resistance to Miltefosine (hexadecylphosphocholine) by peptide-mediated drug smuggling: a proof of mechanism for trypanosomatid chemotherapy J. Control. Release May 18 2012 [Electronic publication ahead of print]
11. A. Joliot, C. Pernelle, H. Deagostini-Bazin, and A. Prochiantz Antennapedia homeobox peptide regulates neural morphogenesis Proc. Natl. Acad. Sci. U. S. A. 88 1991 1864 1868 (Pubitemid 21916327)
12. G. Elliott, and P. O'Hare Intercellular trafficking and protein delivery by a herpesvirus structural protein Cell 88 1997 223 233 (Pubitemid 28015871)
13. A. Kerkis, I. Kerkis, G. Radis-Baptista, E.B. Oliveira, A.M. Vianna-Morgante, L.V. Pereira, and T. Yamane Crotamine is a novel cell-penetrating protein from the venom of rattlesnake Crotalus durissus terrificus FASEB J. 18 2004 1407 1409 (Pubitemid 39561596)
14. V. Fadel, P. Bettendorff, T. Herrmann, W.F. de Azevedo Jr., E.B. Oliveira, T. Yamane, and K. Wuthrich Automated NMR structure determination and disulfide bond identification of the myotoxin crotamine from Crotalus durissus terrificus Toxicon 46 2005 759 767 (Pubitemid 41531602)
15. D.M. Hoover, O. Chertov, and J. Lubkowski The structure of human beta-defensin-1: new insights into structural properties of beta-defensins J. Biol. Chem. 276 2001 39021 39026
16. A.M. Torres, G.M. de Plater, M. Doverskog, L.C. Birinyi-Strachan, G.M. Nicholson, C.H. Gallagher, and P.W. Kuchel Defensin-like peptide-2 from platypus venom: member of a class of peptides with a distinct structural fold Biochem. J. 348 2000 649 656 (Pubitemid 30410256)
17. D. Housset, C. Habersetzer-Rochat, J.P. Astier, and J.C. Fontecilla-Camps Crystal structure of toxin II from the scorpion Androctonus australis Hector refined at 1.3 Α resolution J. Mol. Biol. 238 1994 88 103
18. A.M. Siqueira, N.F. Martins, M.E. De Lima, C.R. Diniz, A. Cartier, D. Brown, and B. Maigret A proposed 3D structure for crotamine based on homology building, molecular simulations and circular dichroism J. Mol. Graph. Model. 20 2002 389 398 (Pubitemid 34127982)
19. G. Rádis-Baptista, B.G. de la Torre, and D. Andreu A novel cell-penetrating peptide sequence derived by structural minimization of a snake toxin exhibits preferential nucleolar localization J. Med. Chem. 51 2008 7041 7044
20. M. Rodrigues, B.G. de la Torre, G. Rádis-Baptista, N.C. Santos, and D. Andreu Efficient cellular delivery of β-galactosidase mediated by NrTPs, a new family of cell-penetrating peptides Bioconjugate Chem. 22 2011 2339 2344
21. M. Vila-Perello, A. Sanchez-Vallet, F. Garcia-Olmedo, A. Molina, and D. Andreu Synthetic and structural studies on Pyrularia pubera thionin: a single-residue mutation enhances activity against Gram-negative bacteria FEBS Lett. 536 2003 215 219 (Pubitemid 36206434)
22. S. Fery-Forgues, and L. Dominique Are fluorescence quantum yields so tricky to measure? A demonstration using familiar stationery products J. Chem. Educ. 76 1999 1260 1264 (Pubitemid 129539744)
23. L.D. Mayer, M.J. Hope, and P.R. Cullis Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858 1986 161 168
24. R.F. de Almeida, J. Borst, A. Fedorov, M. Prieto, and A.J. Visser Complexity of lipid domains and rafts in giant unilamellar vesicles revealed by combining imaging and microscopic and macroscopic time-resolved fluorescence Biophys. J. 93 2007 539 553 (Pubitemid 47057819)
25. B.M. Castro, L.C. Silva, A. Fedorov, R.F. de Almeida, and M. Prieto Cholesterol-rich fluid membranes solubilize ceramide domains: implications for the structure and dynamics of mammalian intracellular and plasma membranes J. Biol. Chem. 284 2009 22978 22987
26. N. Rodriguez, F. Pincet, and S. Cribier Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy Colloids Surf. B Biointerfaces 42 2005 125 130
27. A.S. Ladokhin, S. Jayasinghe, and S.H. White How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285 2000 235 245
28. N.C. Santos, M. Prieto, and M.A.R.B. Castanho Quantifying molecular partition into model systems of biomembranes: an emphasis on optical spectroscopic methods Biochim. Biophys. Acta 1612 2003 123 135 (Pubitemid 36629567)
29. P.M. Matos, H.G. Franquelim, M.A.R.B. Castanho, and N.C. Santos Quantitative assessment of peptide-lipid interactions. Ubiquitous fluorescence methodologies Biochim. Biophys. Acta 1798 2010 1999 2012
30. M.M. Ribeiro, M.N. Melo, I.D. Serrano, N.C. Santos, and M.A. Castanho Drug-lipid interaction evaluation: why a 19th century solution? Trends Pharmacol. Sci. 31 2010 449 454
31. A. Coutinho, and M. Prieto Ribonuclease T1 and alcohol dehydrogenase fluorescence quenching by acrylamide J. Chem. Educ. 70 1993 1 4
32. J.R. Lakowicz Principles of Fluorescence Spectroscopy 2006 Springer Singapore
33. S.S. Lehrer Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion Biochemistry 10 1971 3254 3263
34. D.E. Chalpin, and A.M. Kleinfeld Interaction of fluorescence quenchers with the n-(9-anthroyloxy) fatty acid membrane probes Biochim. Biophys. Acta 731 1983 465 474
35. I.M. Frank, and S.I. Vavilov Über die wirkungssphäre der aus-löschuns-vargänge in den flureszierenden flussig-keiten Z. Phys. 69 1931 100 110
36. D.W. Marquardt An algorithm for least-squares estimation of nonlinear parameters J. Soc. Ind. Appl. Math. 11 1963 431 441
37. N.C. Santos, M. Prieto, and M.A.R.B. Castanho Interaction of the major epitope region of HIV protein gp41 with membrane model systems. A fluorescence spectroscopy study Biochemistry 37 1998 8674 8682 (Pubitemid 28299605)
38. J.R. Wardlaw, W.H. Sawyer, and K.P. Ghiggino Vertical fluctuations of phospholipid acyl chains in bilayers FEBS Lett. 223 1987 20 24
39. S.W. Provencher A constrained regularization method for inverting data represented by linear algebraic or integral equations Comput. Phys. Commun. 27 1982 213 227
40. S.W. Provencher CONTIN: a general-purpose constrained regularization program for inverting data represented by linear algebraic and integral-equations Comput. Phys. Commun. 27 1982 229 242
41. 21 promotes lipopolysaccharide aggregation and exerts its antimicrobial effects by (hemi)fusion of PG-containing membranes PLoS One 4 2009 e8385
42. J.N. Weinstein, R.D. Klausner, T. Innerarity, E. Ralston, and R. Blumenthal Phase transition release, a new approach to the interaction of proteins with lipid vesicles. Application to lipoproteins Biochim. Biophys. Acta 647 1981 270 284
43. R.W. Woody Circular dichroism Methods Enzymol. 246 1995 34 71
44. M.A. Andrade, P. Chacon, J.J. Merelo, and F. Moran Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network Protein Eng. 6 1993 383 390 (Pubitemid 23197398)
45. J.B.A. Ross, W.R. Laws, K.W. Rousslang, and H.R. Wyssbrod Tyrosine fluorescence and phosphorescence from proteins and polypeptides J.R. Lakowicz, Topics in Fluorescence Spectroscopy - Biochemical Applications vol. 3 1992 Plenum Press New York 1 63
46. R.F. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416 (Pubitemid 37210789)
47. J.L. Thewalt, and M. Bloom Phosphatidylcholine: cholesterol phase diagrams Biophys. J. 63 1992 1176 1181
48. C. Reyes Mateo, A. Ulises Acuna, and J.C. Brochon Liquid-crystalline phases of cholesterol/lipid bilayers as revealed by the fluorescence of trans-parinaric acid Biophys. J. 68 1995 978 987
49. D. Marsh Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams Biochim. Biophys. Acta 1798 2010 688 699
50. D. Marsh Handbook of Lipid Bilayers 1990 CRC Press Boca Raton, FL
51. R.B. Gennis Biomembranes: Molecular Structure and Function 1989 Springer-Verlag New York
52. K. Matsuzaki, K. Sugishita, M. Harada, N. Fujii, and K. Miyajima Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of Gram-negative bacteria Biochim. Biophys. Acta 1327 1997 119 130 (Pubitemid 27283405)
53. G. Fujii, D. Eisenberg, and M.E. Selsted Defensins promote fusion and lysis of negatively charged membranes Prot. Sci. 2 1993 1301 1312 (Pubitemid 23225654)
54. S. Goncalves, A. Teixeira, J. Abade, L.N. de Medeiros, E. Kurtenbach, and N.C. Santos Evaluation of the membrane lipid selectivity of the pea defensin Psd1 Biochim. Biophys. Acta 1818 2011 1420 1426
55. Y. Chen, and M.D. Barkley Toward understanding tryptophan fluorescence in proteins Biochemistry 37 1998 9976 9982 (Pubitemid 28366351)
56. F. Moro, F.M. Goñi, and M.A. Urbaneja Fluorescence quenching at interfaces and the permeation of acrylamide and iodide across phospholipid bilayers FEBS Lett. 330 1993 129 132 (Pubitemid 23265115)
57. H.G. Franquelim, A.S. Veiga, G. Weissmüller, N.C. Santos, and M.A. Castanho Unravelling the molecular basis of the selectivity of the HIV-1 fusion inhibitor sifuvirtide towards phosphatidylcholine-rich rigid membranes Biochim. Biophys. Acta 1798 2010 1234 1243
58. A. Chattopadhyay, and E. London Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids Biochemistry 26 1987 39 45
59. M. Castanho, M. Prieto, and A.U. Acuna The transverse location of the fluorescent probe trans-parinaric acid in lipid bilayers Biochim. Biophys. Acta 1279 1996 164 168 (Pubitemid 26083006)
60. M.X. Fernandes, J. Garcia de la Torre, and M.A. Castanho Joint determination by Brownian dynamics and fluorescence quenching of the in-depth location profile of biomolecules in membranes Anal. Biochem. 307 2002 1 12
61. M.R. Eftink, and C.A. Ghiron Fluorescence quenching of indole and model micelle systems J. Phys. Chem. 80 1976 488 493
62. N.C. Santos, A.C. Silva, M.A.R.B. Castanho, J. Martins-Silva, and C. Saldanha Evaluation of lipopolysaccharide aggregation by light scattering spectroscopy Chembiochem 4 2003 96 100 (Pubitemid 36114216)
63. S. Mukherjee, and A. Chattopadhyay Motionally restricted tryptophan environments at the peptide-lipid interface of gramicidin channels Biochemistry 33 1994 5089 5097 (Pubitemid 24150974)
64. A. Prochiantz Messenger proteins: homeoproteins, TAT and others Curr. Opin. Cell Biol. 12 2000 400 406 (Pubitemid 30453588)
65. A. Pokorny, and P.F. Almeida Kinetics of dye efflux and lipid flip-flop induced by delta-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic, alpha-helical peptides Biochemistry 43 2004 8846 8857 (Pubitemid 38880055)
66. B. Geueke, K. Namoto, I. Agarkova, J.C. Perriard, H.P. Kohler, and D. Seebach Bacterial cell penetration by beta3-oligohomoarginines: indications for passive transfer through the lipid bilayer Chembiochem 6 2005 982 985 (Pubitemid 40825335)
67. S. Trabulo, A.L. Cardoso, M. Mano, and M.C.P. Lima Cell-penetrating peptides-mechanisms of cellular uptake and generation of delivery systems Pharmaceuticals 3 2010 961 993
68. R. Fischer, M. Fotin-Mleczek, H. Hufnagel, and R. Brock Break on through to the other side-biophysics and cell biology shed light on cell-penetrating peptides Chembiochem 6 2005 2126 2142
69. P.E. Thoren, D. Persson, E.K. Esbjorner, M. Goksor, P. Lincoln, and B. Norden Membrane binding and translocation of cell-penetrating peptides Biochemistry 43 2004 3471 3489 (Pubitemid 38391703)
70. G. Radis-Baptista, B.G. de la Torre, and D. Andreu Insights into the uptake mechanism of NrTP, a cell-penetrating peptide preferentially targeting the nucleolus of tumour cells Chem. Biol. Drug Des. 79 2012 907 915