Permeabilization of mitochondria and red blood cells by polycationic peptides BTM-P1 and retro-BTM-P1

Peptides

Volumn 32, Issue 10, 2011, Pages 2010-2020

  Lemeshko, Victor V ^a  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

Cell shrinkage; Cell suicide; Membrane permeabilization; Mitochondria; Polycationic peptides; Red blood cells

Indexed keywords

BTM P1 PEPTIDE; PHOSPHATIDYLSERINE; POLYCATION; POLYPEPTIDE ANTIBIOTIC AGENT; PYRIDINE NUCLEOTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISPERSION; ERYTHROCYTE; IONIC STRENGTH; LIVER MITOCHONDRION; MALE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION SWELLING; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; RAT; SENSITIVITY ANALYSIS;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; ERYTHROCYTES; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA, LIVER; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PERMEABILITY; PROTEIN STRUCTURE, SECONDARY; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80054053679     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2011.08.023     Document Type: Article

References (75)

1. R.C. Anderson, and P.L. Yu Factors affecting the antimicrobial activity of ovine-derived cathelicidins against E. coli 0157:H7 Int J Antimicrob Agents 25 2005 205 210 (Pubitemid 40292749)
2. A. Apetrei, L. Mereuta, and T. Luchian The RH 421 styryl dye induced, pore model-dependent modulation of antimicrobial peptides activity in reconstituted planar membranes Biochim Biophys Acta 1790 2009 809 816
3. M. Arias, S. Orduz, and V.V. Lemeshko Potential-dependent permeabilization of plasma membrane by the peptide BTM-P1 derived from the Cry11Bb1 protoxin Biochim Biophys Acta 1788 2009 532 537
4. M. Arias, J.C. Quijano, V. Haridas, J.U. Gutterman, and V.V. Lemeshko Red blood cell permeabilization by hypotonic treatments, saponin, and anticancer avicins Biochim Biophys Acta 1798 2010 1189 1196
5. M.A. Baker, W.L. Maloy, M. Zasloff, and L.S. Jacob Anticancer efficacy of Magainin2 and analogue peptides Cancer Res 53 1993 3052 3057 (Pubitemid 23210311)
6. E.S. Bakker, and W.E. Mangerich Interconversion of components of the bacterial proton motive force by electrogenic potassium transport J Bacteriol 147 1978 820 826 (Pubitemid 12226305)
7. V. Buzón, and J. Cladera Effect of cholesterol on the interaction of the HIV GP41 fusion peptide with model membranes. Importance of the membrane dipole potential Biochemistry 45 2006 15768 15775 (Pubitemid 46032497)
8. H.M. Chen, W. Wang, D. Smith, and S.C. Chan Effects of the anti-bacterial peptide cecropin B and its analogs, cecropins B-1 and B-2, on liposomes, bacteria, and cancer cells Biochim Biophys Acta 1336 1997 171 179 (Pubitemid 27364170)
9. L.B. Chen Mitochondrial membrane potential in living cells Ann Rev Cell Biol 4 1988 155 181 (Pubitemid 19139255)
10. Y. Chen, A.I. Vasil, L. Rehaume, C.T. Mant, J.L. Burns, and M.L. Vasil Comparison of biophysical and biologic properties of alpha-helical enantiomeric antimicrobial peptides Chem Biol Drug Des 67 2006 162 173 (Pubitemid 43881376)
11. C. Chicharro, C. Granata, R. Lozano, D. Andreu, and L. Rivas N-terminal fatty acid substitution increases the leishmanicidal activity of CA(1-7)M(2-9), a cecropin-melittin hybrid peptide Antimicrob Agents Chemother 45 2001 2441 2449 (Pubitemid 32801893)
12. M. Chorev, and M. Goodman Recent developments in retro peptides and proteins - an ongoing topochemical exploration Trends Biotechnol 13 1995 438 445
13. R.A. Cruciani, J.L. Barker, M. Zasloff, H.C. Chen, and O. Colamonici Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation Proc Natl Acad Sci USA 88 1991 3792 3796 (Pubitemid 21916710)
14. S. Davis, M.J. Weiss, J.R. Wong, T.J. Lampidis, and L.B. Chen Mitochondrial and plasma membrane potentials cause unusual accumulation and retention of rhodamine 123 by human breast adenocarcinoma-derived MCF-7 cells J Biol Chem 260 1985 13844 13850 (Pubitemid 16233244)
15. G. Del Rio, S. Castro-Obregon, R. Rao, H.M. Ellerby, and D.E. Bredesen APAP, a sequence-pattern recognition approach identifies substance P as a potential apoptotic peptide FEBS Lett 494 2001 213 219 (Pubitemid 32322685)
16. A. Devin, B. Guérin, and M. Rigoulet Control of oxidative phosphorylation in rat liver mitochondria: effect of ionic media Biochim Biophys Acta 1319 1997 293 300 (Pubitemid 27156901)
17. H.M. Ellerby, W. Arap, L.M. Ellerby, R. Kain, R. Andrusiak, and G.D. Rio Anti-cancer activity of targeted pro-apoptotic peptides Nat Med 5 1999 1032 1038 (Pubitemid 29439574)
18. R.M. Epand, and R.F. Epand Lipid domains in bacterial membranes and the action of antimicrobial agents Biochim Biophys Acta 1788 2009 289 294
19. C.E. Felder, J. Prilusky, I. Silman, and J.L. Sussman A server and database for dipole moments of proteins Nucleic Acids Res 35 2007 W512 W521 (Web Server issue)
20. J.C. Freedman, and T.S. Novak Electrodiffusion, barrier, and gating analysis of DIDS-insensitive chloride conductance in human red blood cells treated with valinomycin or gramicidin J Gen Physiol 109 1997 201 216 (Pubitemid 27078407)
21. J.L. Gifford, H.N. Hunter, and H.J. Vogel Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties Cell Mol Life Sci 62 2005 2588 2598 (Pubitemid 41721232)
22. A. Giuliani, G. Pirri, and S.F. Nicoletto Antimicrobial peptides: an overview of a promising class of therapeutics Cent Eur J Biol 2 2007 1 33 (Pubitemid 46450753)
23. E. Glukhov, L.L. Burrows, and C.M. Deber Membrane interactions of designed cationic antimicrobial peptides: the two thresholds Biopolymers 89 2008 360 371
24. A. Gomes, P. Bhattacharjee, R. Mishra, A.K. Biswas, S.C. Dasgupta, and B. Giri Anticancer potential of animal venoms and toxins Indian J Exp Biol 48 2010 93 103
25. E. Gross, R.S. Bedlack Jr. , and L.M. Loew Dual-wavelength ratiometric fluorescence measurement of the membrane dipole potential Biophys J 67 1994 208 216 (Pubitemid 24197886)
26. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling Electrophoresis 18 1997 2714 2723 (Pubitemid 28059943)
27. M.E. Holtzer, E. Braswell, R.H. Angeletti, L. Mints, D. Zhu, and A. Holtzer Ultracentrifuge and circular dichroism studies of folding equilibria in a retro GCN4-like leucine zipper Biophys J 78 2000 2037 2048 (Pubitemid 30183598)
28. S.Y. Hong, T.G. Park, and K.H. Lee The effect of charge increase on the specificity and activity of a short antimicrobial peptide Peptides 22 2001 1669 1674 (Pubitemid 32918246)
29. D.W. Hoskin, and A. Ramamoorthy Studies on anticancer activities of antimicrobial peptides Biochim Biophys Acta 1778 2008 357 375
30. Y. Huang, J. Huang, and Y. Chen Alpha-helical cationic antimicrobial peptides: relationships of structure and function Protein Cell 1 2010 143 152
31. A. Ito, Y. Sasaguri, S. Kitada, Y. Kusaka, K. Kuwano, and K. Masutomi A Bacillus thuringiensis crystal protein with selective cytocidal action to human cells J Biol Chem 279 2004 21282 21286 (Pubitemid 38656534)
32. M.M. Javadpour, and M.D. Barkley Self-assembly of designed antimicrobial peptides in solution and micelles Biochemistry 36 1997 9540 9549 (Pubitemid 27346995)
33. M.M. Javadpour, M.M. Juban, W.C. Lo, S.M. Bishop, J.B. Alberty, and S.M. Cowell De novo antimicrobial peptides with low mammalian cell toxicity J Med Chem 39 1996 3107 3113 (Pubitemid 26260315)
34. B. Jayaram, K. Bhushan, S.R. Shenoy, P. Narang, S. Bose, and P. Agrawal Bhageerath: an energy based web enabled computer software suite for limiting the search space of tertiary structures of small globular proteins Nucleic Acids Res 34 2006 6195 6204 (Pubitemid 44942740)
35. H. Jenssen, P. Hamill, and R.E. Hancock Peptide antimicrobial agents Clin Microbiol Rev 19 2006 491 511 (Pubitemid 44137212)
36. P. Juvvadi, S. Vunnam, B. Yoo, and R.B. Merrifield Structure-activity studies of normal and retro pig cecropin-melittin hybrids J Pept Res 53 1999 244 251 (Pubitemid 29189914)
37. A. Kessel, D. Shental-Bechor, T. Haliloglu, and N. Ben-Tal Interactions of hydrophobic peptides with lipid bilayers: Monte Carlo simulations with M2delta Biophys J 85 2003 3431 3444 (Pubitemid 37490261)
38. P.A. Knauf, G.F. Fuhrmann, S. Rothstein, and A. Rothstein The relationship between anion exchange and net anion flow across the human red blood cell membrane J Gen Physiol 69 1977 363 386 (Pubitemid 8059913)
39. F. Lang, K.S. Lang, P.A. Lang, S.M. Huber, and T. Wieder Osmotic shock-induced suicidal death of erythrocytes Acta Physiol (Oxf) 187 2006 191 198 (Pubitemid 43828776)
40. B. Law, L. Quinti, Y. Choi, R. Weissleder, and C.H. Tung A mitochondrial targeted fusion peptide exhibits remarkable cytotoxicity Mol Cancer Ther 5 2006 1944 1949 (Pubitemid 44336565)
41. V.V. Lemeshko Failure of exogenous NADH and cytochrome c to support energy-dependent swelling of mitochondria Arch Biochem Biophys 388 2001 60 66 (Pubitemid 32911563)
42. V.V. Lemeshko Cytochrome c sorption-desorption effects on the external NADH oxidation by mitochondria: experimental and computational study J Biol Chem 277 2002 17751 17757 (Pubitemid 34967581)
43. V.V. Lemeshko Potential-dependent membrane permeabilization and mitochondrial aggregation caused by anticancer polyarginine-KLA peptides Arch Biochem Biophys 493 2010 213 220
44. V.V. Lemeshko Membrane permeabilizing activity of new polycationic peptides derived from Cry type protoxins FASEB J 25 2011 759.4
45. V.V. Lemeshko, M. Arias, and S. Orduz Mitochondria permeabilization by a novel polycation peptide BTM-P1 J Biol Chem 280 2005 15579 15586 (Pubitemid 40616674)
46. Lemeshko VV, Guzman F, Patarroyo ME, Segura C, Orduz S. Synthetic peptide having an ionophoric and antimicrobial activity. US Patent No. 7,041,647 (2005).
47. V.V. Lemeshko, V. Haridas, J.C. Quijano Perez, and J.U. Gutterman Avicins, natural anticancer saponins, permeabilize mitochondrial membranes Arch Biochem Biophys 454 2006 114 122 (Pubitemid 44547869)
48. V.V. Lemeshko, and W. Kugler Synergistic inhibition of mitochondrial respiration by anticancer agent erucylphosphohomocholine and cyclosporin A J Biol Chem 282 2007 37303 37307
49. J.C. Mai, Z. Mi, S.H. Kim, B. Ng, and P.D. Robbins A proapoptotic peptide for the treatment of solid tumors Cancer Res 61 2001 7709 7712 (Pubitemid 33049352)
50. K. Matsuzaki, K. Sugishita, N. Fujii, and K. Miyajima Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2 Biochemistry 34 1995 3423 3429
51. L.J. McGuffin, K. Bryson, and D.T. Jones The PSIPRED protein structure prediction server Bioinformatics 16 2000 404 405 (Pubitemid 30417087)
52. A.N. McKeown, J.L. Naro, L.J. Huskins, and P.F. Almeida A thermodynamic approach to the mechanism of cell-penetrating peptides in model membranes Biochemistry 50 2011 654 662
53. R.B. Merrifield, P. Juvvadi, D. Andreu, J. Ubach, A. Boman, and H.G. Boman Retro and retroenantio analogs of cecropin-melittin hybrids Proc Natl Acad Sci USA 92 1995 3449 3453
54. M. Nakagaki, and S. Yokoyama Effect of choline derivatives on the critical micelle concentrations of anionic and cationic surfactants Bull Chem Soc Jpn 58 1985 753 754
55. M. Nishikawa, and K. Ogawa Antimicrobial activity of a chelatable poly(arginyl-histidine) produced by the ergot fungus Verticillium kibiense Antimicrob Agents Chemother 48 2004 229 235 (Pubitemid 38040202)
56. O.S. Ostroumova, V.V. Malev, M.G. Ilin, and L.V. Schagina Surfactin activity depends on the membrane dipole potential Langmuir 26 2010 15092 15097
57. R. Palffy, R. Gardlik, M. Behuliak, L. Kadasi, J. Turna, and P. Celec On the physiology and pathophysiology of antimicrobial peptides Mol Med 15 2009 51 59
58. N. Papo, and Y. Shai Host defense peptides as new weapons in cancer treatment Cell Mol Life Sci 62 2005 784 790 (Pubitemid 40655628)
59. S.C. Park, M.H. Kim, M.A. Hossain, S.Y. Shin, Y. Kim, and L. Stella Amphipathic alpha-helical peptide, HP (2-20), and its analogues derived from Helicobacter pylori: pore formation mechanism in various lipid compositions Biochim Biophys Acta 1778 2008 229 241
60. J.C. Parker, and V. Castranova Volume-responsive sodium and proton movements in dog red blood cells J Gen Physiol 84 1984 379 401 (Pubitemid 14035440)
61. A. Pellegrini, and R. von Fellenberg Design of synthetic bactericidal peptides derived from the bactericidal domain P(18-39) of aprotinin Biochim Biophys Acta 1433 1999 122 131 (Pubitemid 29369048)
62. S. Ran, A. Downes, and P.E. Thorpe Increased exposure of anionic phospholipids on the surface of tumor blood vessels Cancer Res 62 2002 6132 6140 (Pubitemid 35244462)
63. J.N. Sachs, H. Nanda, H.I. Petrache, and T.B. Woolf Changes in phosphatidylcholine headgroup tilt and water order induced by monovalent salts: molecular dynamics simulations Biophys J 86 2004 3772 3782 (Pubitemid 38780254)
64. C. Segura, F. Guzmán, L.M. Salazar, M.E. Patarroyo, S. Orduz, and V. Lemeshko BTM-P1 polycationic peptide biological activity and 3D-dimensional structure Biochem Biophys Res Commun 353 2007 908 914 (Pubitemid 46080383)
65. D. Shental-Bechor, T. Haliloglu, and N. Ben-Tal Interactions of cationic-hydrophobic peptides with lipid bilayers: a Monte Carlo simulation method Biophys J 93 2007 1858 1871 (Pubitemid 47437571)
66. O.E. Sorensen, N. Borregaard, and A.M. Cole Antimicrobial peptides in innate immune responses Contrib Microbiol 15 2008 61 77
67. H. Strahl, and L.W. Hamoen Membrane potential is important for bacterial cell division Proc Natl Acad Sci USA 107 2010 12281 12286
68. T. Utsugi, A.J. Schroit, J. Connor, C.D. Bucana, and I.J. Fidler Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes Cancer Res 15 1991 3062 3066
69. A. Vaz Gomes, A. de Waal, J.A. Berden, and H.V. Westerhoff Electric potentiation, cooperativity, and synergism of magainin peptides in protein-free liposomes Biochemistry 32 1993 5365 5372 (Pubitemid 23167977)
70. L. Voglino, T.J. McIntosh, and S.A. Simon Modulation of the binding of signal peptides to lipid bilayers by dipoles near the hydrocarbon-water interface Biochemistry 37 1998 12241 12252 (Pubitemid 28411310)
71. H. Woehlecke, A. Pohl, N. Alder-Baerens, H. Lage, and A. Herrmann Enhanced exposure of phosphatidylserine in human gastric carcinoma cells over expressing the half-size ABC trans-porter BCRP (ABCG2) Biochem J 376 2003 489 495 (Pubitemid 38010534)
72. J.M. Wu, P.S. Jan, H.C. Yu, H.Y. Haung, H.J. Fang, and Y.I. Chang Structure and function of a custom anticancer peptide, CB1a Peptides 30 2009 839 848
73. M.R. Yeaman, and N.Y. Yount Mechanisms of antimicrobial peptide action and resistance Pharmacol Rev 55 2003 27 55 (Pubitemid 36268398)
74. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (Pubitemid 34100944)
75. R.F. Zwaal, P. Comfurius, and E.M. Bevers Surface exposure of phosphatidylserine in pathological cells Cell Mol Life Sci 62 2005 971 988 (Pubitemid 40655614)