Cell penetrating peptides and cationic antibacterial peptides: Two sides of the same coin

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 14448-14457

  Rodriguez Plaza, Jonathan G ^a   Morales Nava, Rosmarbel ^b   Diener, Christian ^a   Schreiber, Gabriele ^c   Gonzalez, Zyanya D ^a   Ortiz, Maria Teresa Lara ^a   Blake, Ivan Ortega ^b   Pantoja, Omar ^c   Volkmer, Rudolf ^d,e   Klipp, Edda ^f   Herrmann, Andreas ^f   Del Rio, Gabriel ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^c INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^f HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; MOLECULAR BIOLOGY;

ANTIBACTERIAL PEPTIDES; CELL-PENETRATING PEPTIDE; COMPUTATIONAL MODEL; ELECTRICAL POTENTIAL; FUNCTIONAL REDUNDANCY; HUMAN CELLS; PHYSICOCHEMICAL PROPERTY; RECEPTOR-MEDIATED ENDOCYTOSIS;

PEPTIDES;

ANTIMICROBIAL CATIONIC PEPTIDE; CELL PENETRATING PEPTIDE; IZTLI PEPTIDE 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; CANDIDA GLABRATA; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; EMERICELLA NIDULANS; ENDOCYTOSIS; EVOLUTIONARY ALGORITHM; FUNGAL STRAIN; INTERNALIZATION; IONTOPHORESIS; LIPID BILAYER; MEMBRANE POTENTIAL; MOLECULAR WEIGHT; NONHUMAN; PEPTIDE ANALYSIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE;

ANTIMICROBIAL PEPTIDES; CELL-PENETRATING PEPTIDES; COMPUTATIONAL BIOLOGY; MEMBRANE BIOPHYSICS; RECEPTOR ENDOCYTOSIS;

ALGORITHMS; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; ENDOCYTOSIS; HEK293 CELLS; HUMANS; KINETICS; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84901439796     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.515023     Document Type: Article

References (53)

1. Ellerby, H. M., Bredesen, D. E., Fujimura, S., and John, V. (2008) Hunterkiller peptide (HKP) for targeted therapy. J. Med. Chem. 51, 5887-5892
2. Arap, W., Haedicke, W., Bernasconi, M., Kain, R., Rajotte, D., Krajewski, S., Ellerby, H. M., Bredesen, D. E., Pasqualini, R., and Ruoslahti, E. (2002) Targeting the prostate for destruction through a vascular address. Proc. Natl. Acad. Sci. U.S.A. 99, 1527-1531 (Pubitemid 34136526)
3. Kolonin, M. G., Saha, P. K., Chan, L., Pasqualini, R., and Arap, W. (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat. Med. 10, 625-632 (Pubitemid 38796854)
4. Ellerby, H. M., Arap, W., Ellerby, L. M., Kain, R., Andrusiak, R., Rio, G. D., Krajewski, S., Lombardo, C. R., Rao, R., Ruoslahti, E., Bredesen, D. E., and Pasqualini, R. (1999) Anti-cancer activity of targeted pro-apoptotic peptides. Nat. Med. 5, 1032-1038 (Pubitemid 29439574)
5. Vives, E. (2005) 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, 77-85 (Pubitemid 41737254)
6. Deshayes, S., Morris, M. C., Divita, G., and Heitz, F. (2005) Cell-penetrating peptides: tools for intracellular delivery of therapeutics. Cell. Mol. Life Sci. 62, 1839-1849 (Pubitemid 41188523)
7. Jones, A. T., and Sayers, E. J. (2012) Cell entry of cell penetrating peptides: tales of tails wagging dogs. J. Control Release 161, 582-591
8. Pooga, M., and Langel, U. (2005) Synthesis of cell-penetrating peptides for cargo delivery. Methods Mol. Biol. 298, 77-89
9. Duchardt, F., Fotin-Mleczek, M., Schwarz, H., Fischer, R., and Brock, R. (2007) A comprehensive model for the cellular uptake of cationic cellpenetrating peptides. Traffic 8, 848-866 (Pubitemid 46971632)
10. Zorko, M., and Langel, U. (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv. Drug Deliv. Rev. 57, 529-545 (Pubitemid 40255559)
11. del Rio, G., Castro-Obregon, S., Rao, R., Ellerby, H. M., and Bredesen, D. E. (2001) APAP, a sequence-pattern recognition approach identifies substance P as a potential apoptotic peptide. FEBS Lett. 494, 213-219 (Pubitemid 32322685)
12. Li, L., Shi, Y., Su, G., and Le, G. (2012) Selectivity for and destruction of Salmonella typhimurium via a membrane damage mechanism of a cellpenetrating peptide ppTG20 analogue. Int. J. Antimicrob. Agents 40, 337-343
13. Nan, Y. H., Park, I. S., Hahm, K. S., and Shin, S. Y. (2011) Antimicrobial activity, bactericidal mechanism, and LPS-neutralizing activity of the cellpenetrating peptide pVEC and its analogs. J. Pept. Sci. 17, 812-817
14. Brogden, K. A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250 (Pubitemid 40298223)
15. Rodríguez Plaza, J. G., Villalon, Rojas, A., Herrera, S., Garza-Ramos, G., Torres Larios, A., Amero, C., Zarraga Grandos, G., Gutierrez Aguilar, M., Lara Ortiz, M. T., Polanco Gonzalez, C., Uribe Carvajal, S., Coria, R., Peña Díaz, A., Bredesen, D. E., Castro-Obregon, S., and del Rio, G. (2012) Moonlighting peptides with emerging function. PloS One 7, e40125
16. Raths, S. K., Naider, F., and Becker, J. M. (1988) Peptide analogues compete with the binding of β-factor to its receptor in Saccharomyces cerevisiae. J. Biol. Chem. 263, 17333-17341
17. Jenness, D. D., Burkholder, A. C., and Hartwell, L. H. (1983) Binding of β-factor pheromone to yeast a cells: chemical and genetic evidence for an β-factor receptor. Cell 35, 521-529 (Pubitemid 14202930)
18. Bajaj, A., Celić, A., Ding, F. X., Naider, F., Becker, J. M., and Dumont, M. E. (2004) A fluorescent β-factor analogue exhibits multiple steps on binding to its G protein-coupled receptor in yeast. Biochemistry 43, 13564-13578 (Pubitemid 39391157)
19. Blumer, K. J., Reneke, J. E., and Thorner, J. (1988) The STE2 gene product is the ligand-binding component of the β-factor receptor of Saccharomyces cerevisiae. J. Biol. Chem. 263, 10836-10842
20. Jenness, D. D., and Spatrick, P. (1986) Down regulation of the β-factor pheromone receptor in S. Cerevisiae. Cell 46, 345-353 (Pubitemid 16031673)
21. Dube, P., and Konopka, J. B. (1998) Identification of a polar region in transmembrane domain 6 that regulates the function of the G proteincoupled β-factor receptor. Mol. Cell. Biol. 18, 7205-7215 (Pubitemid 28533040)
22. David, N. E., Gee, M., Andersen, B., Naider, F., Thorner, J., and Stevens, R. C. (1997) Expression and purification of the Saccharomyces cerevisiae β-factor receptor (Ste2p), a 7-transmembrane-segment G protein-coupled receptor. J. Biol. Chem. 272, 15553-15561 (Pubitemid 27255586)
23. Dosil, M., Schandel, K. A., Gupta, E., Jenness, D. D., and Konopka, J. B. (2000) The C terminus of the Saccharomyces cerevisiae β-factor receptor contributes to the formation of preactivation complexes with its cognate G protein. Mol. Cell. Biol. 20, 5321-5329 (Pubitemid 30431585)
24. Chen, Q., and Konopka, J. B. (1996) Regulation of the G-protein-coupled β-factor pheromone receptor by phosphorylation. Mol. Cell. Biol. 16, 247-257
25. Lee, B. K., Khare, S., Naider, F., and Becker, J. M. (2001) Identification of residues of the Saccharomyces cerevisiae G protein-coupled receptor contributing to β-factor pheromone binding. J. Biol. Chem. 276, 37950-37961
26. Weiner, J. L., Guttierez-Steil, C., and Blumer, K. J. (1993) Disruption of receptor-G protein coupling in yeast promotes the function of an SST2- dependent adaptation pathway. J. Biol. Chem. 268, 8070-8077 (Pubitemid 23120389)
27. Hicke, L., Zanolari, B., and Riezman, H. (1998) Cytoplasmic tail phosphorylation of the β-factor receptor is required for its ubiquitination and internalization. J. Cell Biol. 141, 349-358 (Pubitemid 28237084)
28. Soid-Raggi, G., Sánchez, O., and Aguirre, J. (2006) TmpA, a member of a novel family of putative membrane flavoproteins, regulates asexual development in Aspergillus nidulans. Mol. Microbiol. 59, 854-869
29. Paternostre, M., Ollivon, M., and Bolard, J. (1996) in Manual on Membrane Lipids (Prasat, R., ed) pp. 202-247, Springer, Berlin
30. Coronado, R., and Latorre, R. (1983) Phospholipid bilayers made from monolayers on patch-clamp pipettes. Biophys. J. 43, 231-236
31. Suarez-Isla, B. A., Wan, K., Lindstrom, J., and Montal, M. (1983) Singlechannel recordings from purified acetylcholine receptors reconstituted in bilayers formed at the tip of patch pipets. Biochemistry 22, 2319-2323 (Pubitemid 13093543)
32. Thomson, K. B., Faeder, J., Sytchev, I., and Endy, D. (2012) Yeast Pheromone Model, Stanford University, Palo Alto, CA
33. Toshima, J. Y., Toshima, J., Kaksonen, M., Martin, A. C., King, D. S., and Drubin, D. G. (2006) Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent β-factor derivatives. Proc. Natl. Acad. Sci. U.S.A. 103, 5793-5798
34. +-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 817-845 (Pubitemid 33720056)
35. Henriques, S. T., Melo, M. N., and Castanho, M. A. (2006) Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 399, 1-7 (Pubitemid 44505401)
36. Kilk, K., Mahlapuu, R., Soomets, U., and Langel, U. (2009) Analysis of in vitro toxicity of five cell-penetrating peptides by metabolic profiling. Toxicology 265, 87-95
37. Matsuzaki, K., Murase, O., Fujii, N., and Miyajima, K. (1995) Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 34, 6521-6526
38. Cohen, B. E. (2010) Amphotericin B membrane action: role for two types of ion channels in eliciting cell survival and lethal effects. J. Membr. Biol. 238, 1-20
39. Morgera, F., Vaccari, L., Antcheva, N., Scaini, D., Pacor, S., and Tossi, A. (2009) Primate cathelicidin orthologues display different structures and membrane interactions. Biochem. J. 417, 727-735
40. González-Damián, J., and Ortega-Blake, I. (2010) Effect of membrane structure on the action of polyenes II: nystatin activity along the phase diagram of ergosterol- and cholesterol-containing POPC membranes. J. Membr. Biol. 237, 41-49
41. Récamier, K. S., Hernández-Gómez, A., González-Damián, J., and Ortega-Blake, I. (2010) Effect of membrane structure on the action of polyenes: I. nystatin action in cholesterol- and ergosterol-containing membranes. J. Membr. Biol. 237, 31-40
42. Mak, D. O., and Webb, W. W. (1995) Two classes of alamethicin transmembrane channels: molecular models from single-channel properties. Biophys. J. 69, 2323-2336
43. Venegas, B., González-Damián, J., Celis, H., and Ortega-Blake, I. (2003) Amphotericin B channels in the bacterial membrane: role of sterol and temperature. Biophys. J. 85, 2323-2332 (Pubitemid 37210782)
44. Harriss, L. M., Cronin, B., Thompson, J. R., and Wallace, M. I. (2011) Imaging multiple conductance states in an alamethicin pore. J. Am. Chem. Soc. 133, 14507-14509
45. Huang, W., Zhang, Z., Han, X., Tang, J., Wang, J., Dong, S., and Wang, E. (2002) Ion channel behavior of amphotericin B in sterol-free and cholesterol- or ergosterol-containing supported phosphatidylcholine bilayer model membranes investigated by electrochemistry and spectroscopy. Biophys. J. 83, 3245-3255 (Pubitemid 36041943)
46. Oltvai, Z. N., and Barabási, A. L. (2002) Systems biology. Life's complexity pyramid. Science 298, 763-764 (Pubitemid 35231516)
47. Birchler, J. A., and Veitia, R. A. (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl. Acad. Sci. U.S.A. 109, 14746-14753
48. Kafri, R., Springer, M., and Pilpel, Y. (2009) Genetic redundancy: new tricks for old genes. Cell 136, 389-392
49. McBride, S. M., and Sonenshein, A. L. (2011) The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile. Microbiology 157, 1457-1465
50. Soscia, S. J., Kirby, J. E., Washicosky, K. J., Tucker, S. M., Ingelsson, M., Hyman, B., Burton, M. A., Goldstein, L. E., Duong, S., Tanzi, R. E., and Moir, R. D. (2010) The Alzheimer's disease-associated amyloid β-protein is an antimicrobial peptide. PloS ONE 5, e9505
51. Kagan, B. L., Jang, H., Capone, R., Teran Arce, F., Ramachandran, S., Lal, R., and Nussinov, R. (2012) Antimicrobial properties of amyloid peptides. Mol. Pharm. 9, 708-717
52. Domergue, R., Castaño, I., De Las Peñas, A., Zupancic, M., Lockatell, V., Hebel, J. R., Johnson, D., and Cormack, B. P. (2005) Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308, 866-870 (Pubitemid 40629269)
53. Kawasaki L, (2002) SakA MAP kinase is involved in stress signal transduction, sexual development, and spore viability in Aspergillus nidulans. Mol Microbiol. 45, 1153-1163 (Pubitemid 35007456)