The membrane-lytic peptides K8L9 and melittin enter cancer cells via receptor endocytosis following subcytotoxic exposure

Chemistry and Biology

Volumn 21, Issue 11, 2014, Pages 1522-1532

  Kohno, Masayuki ^a   Horibe, Tomohisa ^a   Ohara, Koji ^a   Ito, Shinji ^a   Kawakami, Koji ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; HEAT SHOCK COGNATE PROTEIN 70; LOW DENSITY LIPOPROTEIN RECEPTOR; MELITTIN; NEUROPILIN 1; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN K8L9; SMALL INTERFERING RNA; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LRP1 PROTEIN, HUMAN; PEPTIDE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL MEMBRANE; CYTOPLASM; CYTOSOL; CYTOTOXICITY; ENDOCYTOSIS; IMMUNOPRECIPITATION; LYSOSOME; MASS SPECTROMETRY; MOLECULAR INTERACTION; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; RNA INTERFERENCE; TUMOR CELL LINE;

AMINO ACID SEQUENCE; CATHEPSIN B; CELL LINE, TUMOR; CELL SURVIVAL; ENDOCYTOSIS; HSC70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; LYSOSOMES; MELITTEN; MOLECULAR SEQUENCE DATA; NEUROPILIN-1; PEPTIDES; RECEPTORS, TRANSFERRIN; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84911474070     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2014.09.008     Document Type: Article

References (61)

1. E. Agostinelli, and N. Seiler Lysosomotropic compounds and spermine enzymatic oxidation products in cancer therapy (review) Int. J. Oncol. 31 2007 473 484
2. T. Aki, A. Nara, and K. Uemura Cytoplasmic vacuolization during exposure to drugs and other substances Cell Biol. Toxicol. 28 2012 125 131
3. S. Basu, R.J. Binder, T. Ramalingam, and P.K. Srivastava CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin Immunity 14 2001 303 313
4. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250
5. L. Cruz-Chamorro, M.A. Puertollano, E. Puertollano, G.A. de Cienfuegos, and M.A. de Pablo In vitro biological activities of magainin alone or in combination with nisin Peptides 27 2006 1201 1209
6. A. De Maio Extracellular heat shock proteins, cellular export vesicles, and the Stress Observation System: a form of communication during injury, infection, and cell damage. It is never known how far a controversial finding will go! Dedicated to Ferruccio Ritossa Cell Stress Chaperones 16 2011 235 249
7. R. Deane, Z. Wu, A. Sagare, J. Davis, S. Du Yan, K. Hamm, F. Xu, M. Parisi, B. LaRue, and H.W. Hu LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms Neuron 43 2004 333 344
8. C.G. Evans, S. Wisén, and J.E. Gestwicki Heat shock proteins 70 and 90 inhibit early stages of amyloid beta-(1-42) aggregation in vitro J. Biol. Chem. 281 2006 33182 33191
9. A.L. Evdonin, I.V. Guzhova, B.A. Margulis, and N.D. Medvedeva Extracellular heat shock protein 70 mediates heat stress-induced epidermal growth factor receptor transactivation in A431 carcinoma cells FEBS Lett. 580 2006 6674 6678
10. K. Ezzat, H. Helmfors, O. Tudoran, C. Juks, S. Lindberg, K. Padari, S. El-Andaloussi, M. Pooga, and U. Langel Scavenger receptor-mediated uptake of cell-penetrating peptide nanocomplexes with oligonucleotides FASEB J. 26 2012 1172 1180
11. M. Fotin-Mleczek, S. Welte, O. Mader, F. Duchardt, R. Fischer, H. Hufnagel, P. Scheurich, and R. Brock Cationic cell-penetrating peptides interfere with TNF signalling by induction of TNF receptor internalization J. Cell Sci. 118 2005 3339 3351
12. R.S. Funk, and J.P. Krise Cationic amphiphilic drugs cause a marked expansion of apparent lysosomal volume: implications for an intracellular distribution-based drug interaction Mol. Pharm. 9 2012 1384 1395
13. S. Futaki, S. Goto, and Y. Sugiura Membrane permeability commonly shared among arginine-rich peptides J. Mol. Recognit. 16 2003 260 264
14. Y. Honjo, T. Horibe, A. Torisawa, H. Ito, A. Nakanishi, H. Mori, T. Komiya, R. Takahashi, and K. Kawakami Protein disulfide isomerase P5-immunopositive inclusions in patients with Alzheimer's disease J. Alzheimers Dis. 38 2014 601 609
15. D.W. Hoskin, and A. Ramamoorthy Studies on anticancer activities of antimicrobial peptides Biochim. Biophys. Acta 1778 2008 357 375
16. T. Ivanovic, M.A. Agosto, K. Chandran, and M.L. Nibert A role for molecular chaperone Hsc70 in reovirus outer capsid disassembly J. Biol. Chem. 282 2007 12210 12219
17. M. Kawamoto, T. Horibe, M. Kohno, and K. Kawakami HER2-targeted hybrid peptide that blocks HER2 tyrosine kinase disintegrates cancer cell membrane and inhibits tumor growth in vivo Mol. Cancer Ther. 12 2013 384 393
18. M. Kohno, T. Horibe, M. Haramoto, Y. Yano, K. Ohara, O. Nakajima, K. Matsuzaki, and K. Kawakami A novel hybrid peptide targeting EGFR-expressing cancers Eur. J. Cancer 47 2011 773 783
19. E. Kondo, K. Saito, Y. Tashiro, K. Kamide, S. Uno, T. Furuya, M. Mashita, K. Nakajima, T. Tsumuraya, and N. Kobayashi Tumour lineage-homing cell-penetrating peptides as anticancer molecular delivery systems Nat. Commun. 3 2012 951
20. S. Lambert, H. Ameels, R. Gniadecki, M. Hérin, and Y. Poumay Internalization of EGF receptor following lipid rafts disruption in keratinocytes is delayed and dependent on p38 MAPK activation J. Cell. Physiol. 217 2008 834 845
21. N.B. Last, D.E. Schlamadinger, and A.D. Miranker A common landscape for membrane-active peptides Protein Sci. 22 2013 870 882
22. S.Y. Lee, H.S. Park, S.J. Lee, and M.U. Choi Melittin exerts multiple effects on the release of free fatty acids from L1210 cells: lack of selective activation of phospholipase A2 by melittin Arch. Biochem. Biophys. 389 2001 57 67
23. H.S. Lee, C.B. Park, J.M. Kim, S.A. Jang, I.Y. Park, M.S. Kim, J.H. Cho, and S.C. Kim Mechanism of anticancer activity of buforin IIb, a histone H2A-derived peptide Cancer Lett. 271 2008 47 55
24. S.A. Lee, B.R. Kim, B.K. Kim, D.W. Kim, W.J. Shon, N.R. Lee, K.S. Inn, and B.J. Kim Heat shock protein-mediated cell penetration and cytosolic delivery of macromolecules by a telomerase-derived peptide vaccine Biomaterials 34 2013 7495 7505
25. X.S. Li, M.S. Reddy, D. Baev, and M. Edgerton Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5 J. Biol. Chem. 278 2003 28553 28561
26. T. Liu, C.K. Daniels, and S. Cao Comprehensive review on the HSC70 functions, interactions with related molecules and involvement in clinical diseases and therapeutic potential Pharmacol. Ther. 136 2012 354 374
27. S.S. Mambula, and S.K. Calderwood Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes J. Immunol. 177 2006 7849 7857
28. S.S. Mambula, M.A. Stevenson, K. Ogawa, and S.K. Calderwood Mechanisms for Hsp70 secretion: crossing membranes without a leader Methods 43 2007 168 175
29. J. Mercer, S. Knébel, F.I. Schmidt, J. Crouse, C. Burkard, and A. Helenius Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry Proc. Natl. Acad. Sci. USA 107 2010 9346 9351
30. A.B. Mochon, and H. Liu The antimicrobial peptide histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm PLoS Pathog. 4 2008 e1000190
31. R.G. Nagele, M.R. D'Andrea, W.J. Anderson, and H.Y. Wang Intracellular accumulation of β-amyloid(1-42) in neurons is facilitated by the α 7 nicotinic acetylcholine receptor in Alzheimer's disease Neuroscience 110 2002 199 211
32. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501
33. T.V. Novoselova, B.A. Margulis, S.S. Novoselov, A.M. Sapozhnikov, J. van der Spuy, M.E. Cheetham, and I.V. Guzhova Treatment with extracellular HSP70/HSC70 protein can reduce polyglutamine toxicity and aggregation J. Neurochem. 94 2005 597 606
34. J. Nylandsted, M. Gyrd-Hansen, A. Danielewicz, N. Fehrenbacher, U. Lademann, M. Høyer-Hansen, E. Weber, G. Multhoff, M. Rohde, and M. Jäättelä Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization J. Exp. Med. 200 2004 425 435
35. K. Ohara, M. Kohno, T. Hamada, and K. Kawakami Entry of a cationic lytic-type peptide into the cytoplasm via endocytosis-dependent and -independent pathways in human glioma U251 cells Peptides 50 2013 28 35
36. N. Papo, and Y. Shai New lytic peptides based on the D,L-amphipathic helix motif preferentially kill tumor cells compared to normal cells Biochemistry 42 2003 9346 9354
37. H.J. Park, D.J. Son, C.W. Lee, M.S. Choi, U.S. Lee, H.S. Song, J.M. Lee, and J.T. Hong Melittin inhibits inflammatory target gene expression and mediator generation via interaction with IkappaB kinase Biochem. Pharmacol. 73 2007 237 247
38. S. Pemberton, K. Madiona, L. Pieri, M. Kabani, L. Bousset, and R. Melki Hsc70 protein interaction with soluble and fibrillar alpha-synuclein J. Biol. Chem. 286 2011 34690 34699
39. J. Pérez-Vargas, P. Romero, S. López, and C.F. Arias The peptide-binding and ATPase domains of recombinant hsc70 are required to interact with rotavirus and reduce its infectivity J. Virol. 80 2006 3322 3331
40. C. Plank, W. Zauner, and E. Wagner Application of membrane-active peptides for drug and gene delivery across cellular membranes Adv. Drug Deliv. Rev. 34 1998 21 35
41. N. Prenzel, O.M. Fischer, S. Streit, S. Hart, and A. Ullrich The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification Endocr. Relat. Cancer 8 2001 11 31
42. H. Räägel, P. Säälik, and M. Pooga Peptide-mediated protein delivery-which pathways are penetrable? Biochim. Biophys. Acta 1798 2010 2240 2248
43. M. Renner, P.N. Lacor, P.T. Velasco, J. Xu, A. Contractor, W.L. Klein, and A. Triller Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5 Neuron 66 2010 739 754
44. T. Rossignol, B. Kelly, C. Dobson, and C. d'Enfert Endocytosis-mediated vacuolar accumulation of the human ApoE apolipoprotein-derived ApoEdpL-W antimicrobial peptide contributes to its antifungal activity in Candida albicans Antimicrob. Agents Chemother. 55 2011 4670 4681
45. E. Schmitt, M. Gehrmann, M. Brunet, G. Multhoff, and C. Garrido Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy J. Leukoc. Biol. 81 2007 15 27
46. Y. Shai, and Z. Oren From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides Peptides 22 2001 1629 1641
47. E.M. Snyder, Y. Nong, C.G. Almeida, S. Paul, T. Moran, E.Y. Choi, A.C. Nairn, M.W. Salter, P.J. Lombroso, G.K. Gouras, and P. Greengard Regulation of NMDA receptor trafficking by amyloid-beta Nat. Neurosci. 8 2005 1051 1058
48. F. Stricher, C. Macri, M. Ruff, and S. Muller HSPA8/HSC70 chaperone protein: structure, function, and chemical targeting Autophagy 9 2013 1937 1954
49. J.N. Sun, W. Li, W.S. Jang, N. Nayyar, M.D. Sutton, and M. Edgerton Uptake of the antifungal cationic peptide Histatin 5 by Candida albicans Ssa2p requires binding to non-conventional sites within the ATPase domain Mol. Microbiol. 70 2008 1246 1260
50. K. Takuma, F. Fang, W. Zhang, S. Yan, E. Fukuzaki, H. Du, A. Sosunov, G. McKhann, Y. Funatsu, and N. Nakamichi RAGE-mediated signaling contributes to intraneuronal transport of amyloid-beta and neuronal dysfunction Proc. Natl. Acad. Sci. USA 106 2009 20021 20026
51. G. Tanaka, I. Nakase, Y. Fukuda, R. Masuda, S. Oishi, K. Shimura, Y. Kawaguchi, T. Takatani-Nakase, U. Langel, and A. Gräslund CXCR4 stimulates macropinocytosis: implications for cellular uptake of arginine-rich cell-penetrating peptides and HIV Chem. Biol. 19 2012 1437 1446
52. T. Teesalu, K.N. Sugahara, V.R. Kotamraju, and E. Ruoslahti C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration Proc. Natl. Acad. Sci. USA 106 2009 16157 16162
53. J.R. Thériault, H. Adachi, and S.K. Calderwood Role of scavenger receptors in the binding and internalization of heat shock protein 70 J. Immunol. 177 2006 8604 8611
54. A.K. Varkouhi, M. Scholte, G. Storm, and H.J. Haisma Endosomal escape pathways for delivery of biologicals J. Control. Release 151 2011 220 228
55. W.P. Verdurmen, P.H. Bovee-Geurts, P. Wadhwani, A.S. Ulrich, M. Hällbrink, T.H. van Kuppevelt, and R. Brock Preferential uptake of L- versus D-amino acid cell-penetrating peptides in a cell type-dependent manner Chem. Biol. 18 2011 1000 1010
56. Y.P. Wang, F. Liu, H.W. He, Y.X. Han, Z.G. Peng, B.W. Li, X.F. You, D.Q. Song, Z.R. Li, and L.Y. Yu Heat stress cognate 70 host protein as a potential drug target against drug resistance in hepatitis B virus Antimicrob. Agents Chemother. 54 2010 2070 2077
57. N. Yamamoto, E. Matsubara, S. Maeda, H. Minagawa, A. Takashima, W. Maruyama, M. Michikawa, and K. Yanagisawa A ganglioside-induced toxic soluble Abeta assembly. Its enhanced formation from Abeta bearing the Arctic mutation J. Biol. Chem. 282 2007 2646 2655
58. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
59. W. Zhang, J. Song, R. Liang, X. Zheng, J. Chen, G. Li, B. Zhang, K. Wang, X. Yan, and R. Wang Stearylated antimicrobial peptide [D]-K6L9 with cell penetrating property for efficient gene transfer Peptides 46 2013 33 39
60. W. Zhang, J. Song, R. Liang, X. Zheng, J. Chen, G. Li, B. Zhang, X. Yan, and R. Wang Stearylated antimicrobial peptide melittin and its retro isomer for efficient gene transfection Bioconjug. Chem. 24 2013 1805 1812
61. J. Zhou, W. Liu, R.C. Pong, G. Hao, X. Sun, and J.T. Hsieh Analysis of oligo-arginine cell-permeable peptides uptake by prostate cells Amino Acids 42 2012 1253 1260