Membrane-active host defense peptides - Challenges and perspectives for the development of novel anticancer drugs

Chemistry and Physics of Lipids

Volumn 164, Issue 8, 2011, Pages 766-781

  Riedl, Sabrina ^a   Zweytick, Dagmar ^a   Lohner, Karl ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

Anticancer peptides; Cancer cell membrane; Cancer selective toxicity; Membrane permeabilization; Phosphatidylserine exposure; Targeted cancer therapy

Indexed keywords

ALLOFERON 1; ALLOFERON 2; ALPHA DEFENSIN; ANTINEOPLASTIC AGENT; AUREIN DERIVATIVE; BUFORIN 2; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CECROPIN; DOLASTATIN 10; DOLASTATIN 15; EPINICIDIN 1; GAEGURIN 5; GAEGURIN 6; GOMESIN; HEPARAN SULFATE; LACTOFERRICIN B; MAGAININ DERIVATIVE; MELITTIN; PEXIGANAN; PHALLOIDIN; PHOSPHATIDYLSERINE; POLYBIA MPI; PROTEGRIN 1; PROTEIN BMAP 27; PROTEIN BMAP 28; PROTEIN NK 2; PROTEIN PEP27; SIALIC ACID; TACHYPLESIN 1; TEMPORIN A; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BETA SHEET; CANCER CELL; CANCER RESISTANCE; CELL MEMBRANE FLUIDITY; CELL SURFACE; DRUG MECHANISM; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; MELANOMA; MEMBRANE DAMAGE; MICROVILLUS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; TUMOR GROWTH;

ANTIMICROBIAL CATIONIC PEPTIDES; ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; DRUG RESISTANCE, NEOPLASM; HUMANS; IMMUNITY, INNATE;

EID: 80053440806     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2011.09.004     Document Type: Article

References (209)

1. M.L. Albert, B. Sauter, and N. Bhardwaj Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs Nature 392 1998 86 89 (Pubitemid 28150594)
2. P.F. Almeida, and A. Pokorny Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics Biochemistry 48 2009 8083 8093
3. M. An, D. Wijesinghe, O.A. Andreev, Y.K. Reshetnyak, and D.M. Engelman pH-(low)-insertion-peptide (pHLIP) translocation of membrane impermeable phalloidin toxin inhibits cancer cell proliferation Proc. Natl. Acad. Sci. U.S.A. 107 2010 20246 20250
4. O.A. Andreev, A.D. Dupuy, M. Segala, S. Sandugu, D.A. Serra, C.O. Chichester, D.M. Engelman, and Y.K. Reshetnyak Mechanism and uses of a membrane peptide that targets tumors and other acidic tissues in vivo Proc. Natl. Acad. Sci. U.S.A. 104 2007 7893 7898 (Pubitemid 47185847)
5. S. Aviel-Ronen, S.K. Lau, M. Pintilie, D. Lau, N. Liu, M.S. Tsao, and S. Jothy Glypican-3 is overexpressed in lung squamous cell carcinoma, but not in adenocarcinoma Mod. Pathol. 21 2008 817 825 (Pubitemid 351896655)
6. S. Bafna, S. Kaur, and S.K. Batra Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells Oncogene 29 2010 2893 2904
7. 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)
8. B. Bechinger, and K. Lohner Detergent-like actions of linear amphipathic cationic antimicrobial peptides Biochim. Biophys. Acta 1758 2006 1529 1539 (Pubitemid 44436087)
9. B. Bechinger Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape Curr. Opin. Colloid Interface Sci. 14 2009 349 355
10. E.M. Bevers, P. Comfurius, D.W. Dekkers, M. Harmsma, and R.F. Zwaal Regulatory mechanisms of transmembrane phospholipid distributions and pathophysiological implications of transbilayer lipid scrambling Lupus 7 suppl. 2 1998 S126 S131
11. E.M. Bevers, P. Comfurius, and R.F. Zwaal Regulatory mechanisms in maintenance and modulation of transmembrane lipid asymmetry: pathophysiological implications Lupus 5 1996 480 487 (Pubitemid 26354072)
12. S.K. Bhutia, and T.K. Maiti Targeting tumors with peptides from natural sources Trends Biotechnol. 26 2008 210 217
13. S.E. Blondelle, and K. Lohner Optimization and high-throughput screening of antimicrobial peptides Curr. Pharm. Des. 16 2010 3204 3211
14. R. Campanella Membrane lipids modifications in human gliomas of different degree of malignancy J. Neurosurg. Sci. 36 1992 11 25
15. G. Capranico, K.W. Kohn, and Y. Pommier Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin Nucleic Acids Res. 18 1990 6611 6619
16. K.L. Carraway, S.A. Price-Schiavi, X. Zhu, and M. Komatsu Membrane mucins and breast cancer Cancer Control 6 1999 613 614 (Pubitemid 30003287)
17. J. Cassidy, and J.L. Misset Oxaliplatin-related side effects: characteristics and management Semin. Oncol. 29 2002 11 20 (Pubitemid 35191037)
18. A. Cazet, S. Julien, M. Bobowski, M.A. Krzewinski-Recchi, A. Harduin-Lepers, S. Groux-Degroote, and P. Delannoy Consequences of the expression of sialylated antigens in breast cancer Carbohydr. Res. 345 2010 1377 1383
19. CBTRUS, 2008. Statistical Report: Primary Brain Tumors in the United States, 2000-2004. Central Brain Tumor Registry of the United States, 2008.
20. J.B. Chaires Thermodynamics of the daunomycin-DNA interaction: ionic strength dependence of the enthalpy and entropy Biopolymers 24 1985 403 419 (Pubitemid 15149583)
21. S.C. Chan, L. Hui, and H.M. Chen Enhancement of the cytolytic effect of anti-bacterial cecropin by the microvilli of cancer cells Anticancer Res. 18 1998 4467 4474 (Pubitemid 29043678)
22. Y.R. Chan, and R.L. Gallo PR-39, a syndecan-inducing antimicrobial peptide, binds and affects p130Cas J. Biol. Chem. 273 1998 28978 28985 (Pubitemid 28507592)
23. Y.R. Chan, M. Zanetti, R. Gennaro, and R.L. Gallo Anti-microbial activity and cell binding are controled by sequence determinants in the anti-microbial peptide PR-39 J. Invest. Dermatol. 116 2001 230 235 (Pubitemid 32173726)
24. P.B. Chapman, L.H. Einhorn, M.L. Meyers, S. Saxman, A.N. Destro, K.S. Panageas, C.B. Begg, S.S. Agarwala, L.M. Schuchter, M.S. Ernstoff, A.N. Houghton, and J.M. Kirkwood Phase III multicenter randomized trial of the dartmouth regimen versus dacarbazine in patients with metastatic melanoma J. Clin. Oncol. 17 1999 2745 2751 (Pubitemid 29415231)
25. J. Chaudhary, and M. Munshi Scanning electron microscopic analysis of breast aspirates Cytopathology 6 1995 162 167
26. 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)
27. Y. Chen, X. Xu, S. Hong, J. Chen, N. Liu, C.B. Underhill, K. Creswell, and L. Zhang RGD-tachyplesin inhibits tumor growth Cancer Res. 61 2001 2434 2438 (Pubitemid 32685820)
28. S. Chernysh, S.I. Kim, G. Bekker, V.A. Pleskach, N.A. Filatova, V.B. Anikin, V.G. Platonov, and P. Bulet Antiviral and antitumor peptides from insects Proc. Natl. Acad. Sci. U.S.A. 99 2002 12628 12632
29. 2+ entry and subsequent apoptosis induced by melittin in human MG63 osteosarcoma cells Life Sci. 80 2007 364 369
30. M. Cichorek, K. Kozlowska, J.M. Witkowski, and M. Zarzeczna Flow cytometric estimation of the plasma membrane diversity of transplantable melanomas, using annexin V Folia Histochem. Cytobiol. 38 2000 41 43 (Pubitemid 30063971)
31. J. Connor, C. Bucana, I.J. Fidler, and A.J. Schroit Differentiation- dependent expression of phosphatidylserine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipid by prothrombinase complex formation Proc. Natl. Acad. Sci. U.S.A. 86 1989 3184 3188 (Pubitemid 19129581)
32. 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. U.S.A. 88 1991 3792 3796 (Pubitemid 21916710)
33. A. Davis, J. Jang, K.M. Middleton, Y. Wang, I. Weisz, Y. Ling, and G. Bekesi Novel suicide ligands of tubulin arrest cancer cells in S-phase Neoplasia 1 1999 498 507
34. S.R. Dennison, M. Whittaker, F. Harris, and D.A. Phoenix Anticancer alpha-helical peptides and structure/function relationships underpinning their interactions with tumour cell membranes Curr. Protein Pept. Sci. 7 2006 487 499 (Pubitemid 44883926)
35. S. Dennison, F. Harris, T. Bhatt, J. Singh, and D. Phoenix A theoretical analysis of secondary structural characteristics of anticancer peptides Mol. Cell. Biochem. 333 2010 129 135
36. I. Dobrzynska, J. Kotynska, and Z. Figaszewski Changes in electrical charge of phosphatidylcholine and phosphatidylserine liposomal membranes caused by adsorption of monovalent ions Chem Analityczna 52 2007 931 944
37. W. Domagala, and L.G. Koss Surface configuration of human tumor cells obtained by fine needle aspiration biopsy Scan. Electron. Micros. 3 1980 101 108
38. J. Doyle, C.S. Brinkworth, K.L. Wegener, J.A. Carver, L.E. Llewellyn, I.N. Olver, J.H. Bowie, P.A. Wabnitz, and M.J. Tyler nNOS inhibition, antimicrobial and anticancer activity of the amphibian skin peptide, citropin 1.1 and synthetic modifications. The solution structure of a modified citropin 1.1 Eur. J. Biochem. 270 2003 1141 1153 (Pubitemid 36384447)
39. S. Drechsler, and J. Andrä Online monitoring of metabolism and morphology of peptide-treated neuroblastoma cancer cells and keratinocytes J. Bioenerg. Biomembr. 43 2011 275 285
40. K. Dredge, B. Marriott, S. Todryk, and A. Dalgleish Adjuvants and the promotion of Th1-type cytokines in tumour immunotherapy Cancer Immunol. Immunother. 51 2002 521 531 (Pubitemid 35232001)
41. D.M. Easton, A. Nijnik, M.L. Mayer, and R.E.W. Hancock Potential of immunomodulatory host defense peptides as novel anti-infectives Trends Biotechnol. 27 2009 582 590
42. S. Ebbinghaus, E. Hersh, C.C. Cunningham, S. O'Day, D. McDermott, J. Stephenson, D.A. Richards, J. Eckardt, O.L. Haider, and L.A. Hammon Phase II study of synthadotin (SYN-D; ILX651) administered daily for 5 consecutive days once every 3 weeks (qdx5q3w) in patients (Pts) with inoperable locally advanced or metastatic melanoma J. Clin. Oncol. 22 suppl. 2004 7530
43. L.T. Eliassen, B.E. Haug, G. Berge, and O. Rekdal Enhanced antitumour activity of 15-residue bovine lactoferricin derivatives containing bulky aromatic amino acids and lipophilic N-terminal modifications J Pept. Sci. 9 2003 510 517 (Pubitemid 37009928)
44. L.T. Eliassen, G. Berge, A. Leknessund, M. Wikman, I. Lindin, C. Lokke, F. Ponthan, J.I. Johnsen, B. Sveinbjornsson, P. Kogner, T. Flaegstad, and O. Rekdal The antimicrobial peptide, lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo Int. J. Cancer 119 2006 493 500 (Pubitemid 43955700)
45. L.T. Eliassen, G. Berge, B. Sveinbjornsson, J.S. Svendsen, L.H. Vorland, and O. Rekdal Evidence for a direct antitumor mechanism of action of bovine lactoferricin Anticancer Res. 22 2002 2703 2710 (Pubitemid 36069301)
46. R.M. Epand, R.F. Epand, C.J. Arnusch, B. Papahadjopoulos-Sternberg, G. Wang, and Y. Shai Lipid clustering by three homologous arginine-rich antimicrobial peptides is insensitive to amino acid arrangement and induced secondary structure Biochim. Biophys. Acta 1798 2010 1272 1280
47. 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
48. R.M. Epand, and R.F. Epand Bacterial membrane lipids in the action of antimicrobial agents J. Pept. Sci. 17 2011 298 305
49. E. Espinosa, P. Zamora, J. Feliu, and M. González Barón Classification of anticancer drugs - a new system based on therapeutic targets Cancer Treat. Rev. 29 2003 515 523 (Pubitemid 37428323)
50. B. Fadnes, O. Rekdal, and L. Uhlin-Hansen The anticancer activity of lytic peptides is inhibited by heparan sulfate on the surface of the tumor cells BMC Cancer 9 2009 183
51. B. Fadnes, L. Uhlin-Hansen, I. Lindin, and O. Rekdal Small lytic peptides escape the inhibitory effect of heparan sulfate on the surface of cancer cells BMC Cancer 11 2011 116
52. V.A. Fadok, D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Bratton, and P.M. Henson Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages J. Immunol. 148 1992 2207 2216
53. S.J. Furlong, J.S. Mader, and D.W. Hoskin Bovine lactoferricin induces caspase-independent apoptosis in human B-lymphoma cells and extends the survival of immune-deficient mice bearing B-lymphoma xenografts Exp. Mol. Pathol. 88 2010 371 375
54. 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)
55. J.P. Gillet, and M.M. Gottesman Mechanisms of multidrug resistance in cancer Methods Mol. Biol. 596 2010 47 76
56. M.M. Gottesman Mechanisms of cancer drug resistance Annu. Rev. Med. 53 2002 615 627 (Pubitemid 34177898)
57. S.M. Gregory, A. Cavenaugh, V. Journigan, A. Pokorny, and P.F.F. Almeida A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide Cecropin A Biophys. J. 94 2008 1667 1680
58. J.R. Griffiths Are cancer cells acidic? Br. J. Cancer 64 1991 425 427
59. E. Habermann, and T.J. Jentsch Sequenzanalyse des Melttins aus den tryptischen und peptischen Spaltsstücken des Bienengiftes, Hoppe Seylers Z. Physiol. Chem. 348 1967 37 50
60. R.E.W. Hancock, and H.G. Sahl Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 24 2006 1551 1557 (Pubitemid 44967479)
61. H. Helmbach, E. Rossmann, M.A. Kern, and D. Schadendorf Drug-resistance in human melanoma Int. J. Cancer 93 2001 617 622 (Pubitemid 32695107)
62. A. Hickel, S. Danner-Pongratz, H. Amenitsch, G. Degovics, M. Rappolt, K. Lohner, and G. Pabst Influence of antimicrobial peptides on the formation of nonlamellar lipid mesophases Biochim. Biophys. Acta 1778 2008 2325 2333
63. L. Holle, W. Song, E. Holle, Y. Wei, T. Wagner, and X. Yu A matrix metalloproteinase 2 cleavable melittin/avidin conjugate specifically targets tumor cells in vitro and in vivo Int. J. Oncol. 22 2003 93 98
64. D.W. Hoskin, and A. Ramamoorthy Studies on anticancer activities of antimicrobial peptides Biochim. Biophys. Acta 1778 2008 357 375
65. K. Hristova, M.E. Selsted, and S.H. White Critical role of lipid composition in membrane permeabilization by rabbit neutrophil defensins J. Biol. Chem. 272 1997 24224 24233 (Pubitemid 27418623)
66. H.W. Huang Molecular mechanism of antimicrobial peptides: the origin of cooperativity Biochim. Biophys. Acta 1758 2006 1292 1302 (Pubitemid 44436067)
67. J.F. Hunt, P. Rath, K.J. Rothschild, and D.M. Engelman Spontaneous, pH-dependent membrane insertion of a transbilayer alpha-helix Biochemistry 36 1997 15177 15192 (Pubitemid 27527982)
68. J.N Israelachvili, S. Marcelja, and R.G. Horn Physical principles of membrane organization Q. Rev. Biophys. 13 1980 121 200
69. T. Iwasaki, J. Ishibashi, H. Tanaka, M. Sato, A. Asaoka, D. Taylor, and M. Yamakawa Selective cancer cell cytotoxicity of enantiomeric 9-mer peptides derived from beetle defensins depends on negatively charged phosphatidylserine on the cell surface Peptides 30 2009 660 668
70. K.L. Jackson, J.A. Henderson, and A.J. Phillips The halichondrins and E7389 Chem. Rev. 109 2009 3044 3079
71. G.C. Jayson, M. Lyon, C. Paraskeva, J.E. Turnbull, J.A. Deakin, and J.T. Gallagher Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro J. Biol. Chem. 273 1998 51 57 (Pubitemid 28042175)
72. P. Joanne, P. Nicolas, and C. El Amri Antimicrobial peptides and viral fusion peptides: how different they are? Protein Pept. Lett. 16 2009 743 750
73. B. Kalyanaraman, J. Joseph, S. Kalivendi, S. Wang, E. Konorev, and S. Kotamraju Doxorubicin-induced apoptosis: implications in cardiotoxicity Mol. Cell. Biochem. 234-235 2002 119 124 (Pubitemid 34777848)
74. T. Katsu, S. Nakao, and S. Iwanaga Mode of action of an antimicrobial peptide, tachyplesin I, on biomembranes Biol. Pharm. Bull. 16 1993 178 181 (Pubitemid 23129195)
75. S. Kim, S.S. Kim, Y.J. Bang, S.J. Kim, and B.J. Lee In vitro activities of native and designed peptide antibiotics against drug sensitive and resistant tumor cell lines Peptides 24 2003 945 953 (Pubitemid 37130165)
76. C. Kirszberg, L.G. Lima, d.O. Da Silva, W. Pickering, E. Gray, T.W. Barrowcliffe, V.M. Rumjanek, and R.Q. Monteiro Simultaneous tissue factor expression and phosphatidylserine exposure account for the highly procoagulant pattern of melanoma cell lines Melanoma Res. 19 2009 301 308
77. L. Kjellen, and U. Lindahl Proteoglycans: structures and interactions Annu. Rev. Biochem. 60 1991 443 475
78. J. Kleeff, T. Ishiwata, A. Kumbasar, H. Friess, M.W. Büchler, A.D. Lander, and M. Korc The cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer J. Clin. Invest. 102 1998 1662 1673 (Pubitemid 28516251)
79. P. Koszalka, E. Kamysz, M. Wejda, W. Kamysz, and J. Bigda Antitumor activity of antimicrobial peptides against U937 histiocytic cell line Acta Biochimica Polonica 58 2011 111 117
80. D.W. Kufe Mucins in cancer: function, prognosis and therapy Nat. Rev. Cancer 9 2009 874 885
81. J. Lehmann, M. Retz, S.S. Sidhu, H. Suttmann, M. Sell, F. Paulsen, J. Harder, G. Unteregger, and M. Stockle Antitumor activity of the antimicrobial peptide magainin II against bladder cancer cell lines Eur. Urol. 50 2006 141 147 (Pubitemid 43850110)
82. D. Lee, K. Hahm, Y. Park, H. Kim, W. Lee, S. Lim, Y. Seo, and C. Choi Functional and structural characteristics of anticancer peptide Pep27 analogues Cancer Cell Int. 5 2005 21 34
83. 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
84. C. Leuschner, and W. Hansel Membrane disrupting lytic peptides for cancer treatments Curr. Pharm. Des. 10 2004 2299 2310 (Pubitemid 38855038)
85. Q. Li, G. Ouyang, X. Peng, and S. Hong Effects of tachyplesin on the regulation of cell cycle in human hepatocarcinoma SMMC-7721 cells World J. Gastroenterol. 9 2003 454 458 (Pubitemid 36372106)
86. Y.C. Li, M.J. Park, S.K. Ye, C.W. Kim, and Y.N. Kim Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents Am. J. Pathol. 168 2006 1107 1118
87. B.F. Liebersbach, and R.D. Sanderson Expression of syndecan-1 inhibits cell invasion into type I collagen J. Biol. Chem. 269 1994 20013 20019 (Pubitemid 24250921)
88. W.J. Lin, Y.L. Chien, C.Y. Pan, T.L. Lin, J.Y. Chen, S.J. Chiu, and C.F. Hui Epinecidin-1, an antimicrobial peptide from fish (Epinephelus coioides) which has an antitumor effect like lytic peptides in human fibrosarcoma cells Peptides 30 2009 283 290
89. A. Litynska, M. Przybylo, E. Pochec, D. Hoja-Lukowicz, D. Ciolczyk, P. Laidler, and D. Gil Comparison of the lectin-binding pattern in different human melanoma cell lines Melanoma Res. 11 2001 205 212 (Pubitemid 32578806)
90. K. Lohner The role of membrane lipid composition in cell targeting of antimicrobial peptides K. Lohner, Development of Novel Antimicrobial Agents: Emerging Strategies 2001 Horizon Scientific Press Wymondham, Norfolk, U.K. 149 165
91. K. Lohner New strategies for novel antibiotics: peptides targeting bacterial cell membranes Gen. Physiol. Biophys. 28 2009 105 116
92. K. Lohner, and S.E. Blondelle Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics Comb. Chem. High Throughput Screen. 8 2005 241 256 (Pubitemid 40488604)
93. K. Lohner, A. Latal, R.I. Lehrer, and T. Ganz Differential scanning microcalorimetry indicates that human defensin, HNP-2, interacts specifically with biomembrane mimetic systems Biochemistry 36 1997 1525 1531 (Pubitemid 27074977)
94. K. Lohner, and E.J. Prenner Differential scanning calorimetry and X-ray diffraction studies of the specificity of the interaction of antimicrobial peptides with membrane-mimetic systems Biochim. Biophys. Acta 1462 1999 141 156
95. S.J. Ludtke, K. He, W.T. Heller, T.A. Harroun, L. Yang, and H.W. Huang Membrane pores induced by magainin Biochemistry 35 1996 13723 13728 (Pubitemid 26363914)
96. J.S. Mader, and D.W. Hoskin Cationic antimicrobial peptides as novel cytotoxic agents for cancer treatment Expert Opin. Investig. Drugs 15 2006 933 946 (Pubitemid 44177845)
97. J.S. Mader, J. Salsman, D.M. Conrad, and D.W. Hoskin Bovine lactoferricin selectively induces apoptosis in human leukemia and carcinoma cell lines Mol. Cancer Ther. 4 2005 612 624 (Pubitemid 40601843)
98. J.S Mader, N. Mookherjee, R.E.W. Hancock, and R.C. Bleackley The human host defense peptide LL-37 induces apoptosis in a calpain- and apoptosis-inducing factor-dependent manner involving bax activity Mol. Cancer Res. 7 2009 689 702
99. A. Makovitzki, A. Fink, and Y. Shai Suppression of human solid tumor growth in mice by intratumor and systemic inoculation of histidine-rich and pH-dependent host defense-like lytic peptides Cancer Res. 69 2009 3458 3463
100. Y. Manavbasi, Y. Gofman, N. Ben Tal, R. Willumeit, D. Zweytick, and K. Lohner Structural aspects of the interaction of Nk-2 derived peptides with cancer cells Biophys. J. 98 2010 277a
101. N. Mandard, P. Bulet, A. Caille, S. Daffre, and F. Vovelle The solution structure of gomesin, an antimicrobial cysteine-rich peptide from the spider Eur. J. Biochem. 269 2002 1190 1198 (Pubitemid 34175378)
102. D. Marsh Lateral pressure in membranes Biochim. Biophys. Acta 1286 1996 183 223 (Pubitemid 26426521)
103. S.J. Martin, C.P. Reutelingsperger, A.J. McGahon, J.A. Rader, R.C. van Schie, D.M. LaFace, and D.R. Green Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl J. Exp. Med. 182 1995 1545 1556
104. K. Matsuda, H. Maruyama, F. Guo, J. Kleeff, J. Itakura, Y. Matsumoto, A.D. Lander, and M. Korc Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells Cancer Res. 61 2001 5562 5569 (Pubitemid 32694943)
105. K. Matsuzaki, O. Murase, N. Fujii, and K. Miyajima An antimicrobal peptide, Magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation Biochemistry 35 1996 11361 11368 (Pubitemid 26299310)
106. K. Matsuzaki, S. Yoneyama, and K. Miyajima Pore formation and transition of melittin Biophys. J. 73 1997 831 838
107. G.L. May, L.C. Wright, M. Dyne, W.B. Mackinnon, R.M. Fox, and C.E. Mountford Plasma membrane lipid composition of vinblastine sensitive and resistant human leukaemic lymphoblasts Int. J. Cancer 42 1988 728 733 (Pubitemid 19008916)
108. A. Mazzoni, and F. Trave Cytoplasmic membrane cholesterol and doxorubicin cytotoxicity in drug-sensitive and multidrug-resistant human ovarian cancer cells Oncol. Res. 5 1993 75 82 (Pubitemid 23222565)
109. M.R. Middleton, S.M. Lee, A. Arance, M. Wood, N. Thatcher, and G.P. Margison O6-methylguanine formation, repair protein depletion and clinical outcome with a 4 h schedule of temozolomide in the treatment of advanced melanoma: results of a phase II study Int. J. Cancer 88 2000 469 473
110. T.W. Miller, J.S. Isenberg, and D.D. Roberts Molecular regulation of tumor angiogenesis and perfusion via redox signaling Chem. Rev. 109 2009 3099 3124
111. T. Miyashita, and J.C. Reed Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line Blood 81 1993 151 157 (Pubitemid 23013689)
112. K. Miyazaki, M. Kobayashi, T. Natsume, M. Gondo, T. Mikami, K. Sakakibara, and S. Tsukagoshi Synthesis and antitumor activity of novel dolastatin 10 Chem. Pharm. Bull. 43 1995 1706 1718
113. D.O. Moon, S.Y. Park, Y.H. Choi, N.D. Kim, C. Lee, and G.Y. Kim Melittin induces Bcl-2 and caspase-3-dependent apoptosis through downregulation of Akt phosphorylation in human leukemic U937 cells Toxicon 51 2008 112 120
114. G. Morgan, R. Ward, and M. Barton The contribution of cytotoxic chemotherapy to 5-year survival in adult malignancies Clin. Oncol. 16 2004 549 560 (Pubitemid 39517664)
115. J.M. Nabholtz, and D. Slamon New adjuvant strategies for breast cancer: meeting the challenge of integrating chemotherapy and trastuzumab (Herceptin) Semin. Oncol. 28 2001 1 12
116. T. Nakamura, H. Furunaka, T. Miyata, F. Tokunaga, T. Muta, S. Iwanaga, M. Niwa, T. Takao, and Y. Shimonishi Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure J. Biol. Chem. 263 1988 16709 16713 (Pubitemid 18268849)
117. T. Nakatsura, T. Kageshita, S. Ito, K. Wakamatsu, M. Monji, Y. Ikuta, S. Senju, T. Ono, and Y. Nishimura Identification of glypican-3 as a novel tumor marker for melanoma Clin. Cancer Res. 10 2004 6612 6621 (Pubitemid 39346558)
118. I. Nakazawa, and M. Iwaizumi A role of the cancer cell membrane fluidity in the cancer metastases: an ESR study, Tohoku J. Exp. Med. 157 1989 193 198 (Pubitemid 19170530)
119. K. Newell, A. Franchi, J. Pouysségur, and I. Tannock Studies with glycolysis-deficient cells suggest that production of lactic acid is not the only cause of tumor acidity Proc. Natl. Acad. Sci. U.S.A. 90 1993 1127 1131 (Pubitemid 23053964)
120. D.J. Newman, and G.M. Cragg Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 70 2007 461 477 (Pubitemid 46595760)
121. L.T. Nguyen, D.J. Schibli, and H.J. Vogel Structural studies and model membrane interactions of two peptides derived from bovine lactoferricin J. Pept. Sci. 11 2005 379 389 (Pubitemid 40959938)
122. T. Ohtake, Y. Fujimoto, K. Ikuta, H. Saito, M. Ohhira, M. Ono, and Y. Kohgo Proline-rich antimicrobial peptide, PR-39 gene transduction altered invasive activity and actin structure in human hepatocellular carcinoma cells Br. J. Cancer 81 1999 393 403 (Pubitemid 29458791)
123. J. Onishi, M.K. Roy, L.R. Juneja, Y. Watanabe, and Y. Tamai A lactoferrin-derived peptide with cationic residues concentrated in a region of its helical structure induces necrotic cell death in a leukemic cell line (HL-60) J. Pept. Sci. 14 2008 1032 1038
124. H. Ostolaza, B. Bartolomé, I.O. de Zárate, F. de la Cruz, and F.M. Goni Release of lipid vesicle contents by the bacterial protein toxin [alpha]-haemolysin Biochim. Biophys. Acta 1147 1993 81 88 (Pubitemid 23104891)
125. N. Papo, A. Braunstein, Z. Eshhar, and Y. Shai Suppression of human prostate tumor growth in mice by a cytolytic d-, l-amino acid peptide: membrane lysis, increased necrosis, and inhibition of prostate-specific antigen secretion Cancer Res. 64 2004 5779 5786 (Pubitemid 39095578)
126. 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 (Pubitemid 36959242)
127. N. Papo, and Y. Shai Host defense peptides as new weapons in cancer treatment Cell. Mol. Life Sci. 62 2005 784 790 (Pubitemid 40655628)
128. N. Papo, D. Seger, A. Makovitzki, V. Kalchenko, Z. Eshhar, H. Degani, and Y. Shai Inhibition of tumor growth and elimination of multiple metastases in human prostate and breast xenografts by systemic inoculation of a host defense-like lytic peptide Cancer Res. 66 2006 5371 5378 (Pubitemid 43844963)
129. N.G. Park, S. Lee, O. Oishi, H. Aoyagi, S. Iwanaga, S. Yamashita, and M. Ohno Conformation of tachyplesin I from Tachypleus tridentatus when interacting with lipid matrixes Biochemistry 31 1992 12241 12247 (Pubitemid 23011373)
130. I. Pastan, and R.J. Kreitman Immunotoxins for targeted cancer therapy Adv. Drug Deliv. Rev. 31 1998 53 88 (Pubitemid 28191876)
131. K.A. Peck-Miller, R.P. Darveau, and H.P. Fell Identification of serum components that inhibit the tumoricidal activity of amphiphilic alpha helical peptides Cancer Chemother. Pharmacol. 32 1993 109 115 (Pubitemid 23131929)
132. R. Perez-Tomas Multidrug resistance: retrospect and prospects in anti-cancer drug treatment Curr. Med. Chem. 13 2006 1859 1876
133. G.R. Pettit, Y. Kamano, C.L. Herald, A.A. Tuinman, F.E. Boettner, H. Kizu, J.M. Schmidt, L. Baczynskyj, K.B. Tomer, and R.J. Bontems The isolation and structure of a remarkable marine animal antineoplastic constituent: dolastatin 10 J. Am. Chem. Soc. 109 1987 6883 6885 (Pubitemid 18036607)
134. A. Pokorny, and P.F.F. Almeida Kinetics of dye efflux and lipid flip-flop induced by δ-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic, α-helical peptides Biochemistry 43 2004 8846 8857 (Pubitemid 38880055)
135. A. Pokorny, E.M. Kilelee, D. Wu, and P.F.F. Almeida The activity of the amphipathic peptide δ-lysin correlates with phospholipid acyl chain structure and bilayer elastic properties Biophys. J. 95 2008 4748 4755
136. D.L. Rabenstein Heparin and heparan sulfate: structure and function Nat. Prod. Rep. 19 2002 312 331 (Pubitemid 34656777)
137. 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)
138. L.V. Rao, J.F. Tait, and A.D. Hoang Binding of annexin V to a human ovarian carcinoma cell line (OC-2008). Contrasting effects on cell surface factor VIIa/tissue factor activity and prothrombinase activity Thromb. Res. 67 1992 517 531
139. R. Rathinakumar, and W.C. Wimley Biomolecular engineering by combinatorial design and high-throughput screening: small, soluble peptides that permeabilize membranes J. Am. Chem. Soc. 130 2008 9849 9858
140. R. Rathinakumar, and W.C. Wimley High-throughput discovery of broad-spectrum peptide antibiotics FASEB J. 24 2010 3232 3238
141. Y.K. Reshetnyak, O.A. Andreev, U. Lehnert, and D.M. Engelman Translocation of molecules into cells by pH-dependent insertion of a transmembrane helix Proc. Natl. Acad. Sci. U.S.A. 103 2006 6460 6465
142. Y.K. Reshetnyak, M. Segala, O.A. Andreev, and D.M. Engelman A monomeric membrane peptide that lives in three worlds: in solution, attached to, and inserted across lipid bilayers Biophys. J. 93 2007 2363 2372 (Pubitemid 47511136)
143. S. Riedl, B. Rinner, M. Asslaber, H. Schaider, S. Walzer, A. Novak, K. Lohner, and D. Zweytick In search of a novel target - phosphatidylserine exposed by non-apoptotic tumor cells and metastases of malignancies with poor treatment efficacy Biochim. Biophys. Acta 1808 2011 2638 2645
144. S. Riedl, B. Rinner, S. Tumer, H. Schaider, K. Lohner, and D. Zweytick Targeting the cancer cell membrane specifically with human lactoferricin derivatives Ann. Oncol. 22 suppl. 3 2011 iii31 iii34
145. A. Risso, M. Zanetti, and R. Gennaro Cytotoxicity and apoptosis mediated by two peptides of innate immunity Cell. Immunol. 189 1998 107 115 (Pubitemid 28507251)
146. C.M. Rodrigues, S. Sola, R.E. Castro, P.A. Laires, D. Brites, and J.J. Moura Perturbation of membrane dynamics in nerve cells as an early event during bilirubin-induced apoptosis J. Lipid Res. 43 2002 885 894 (Pubitemid 34602610)
147. E.G. Rodrigues, A.S. Dobroff, C.F. Cavarsan, T. Paschoalin, L. Nimrichter, R.A. Mortara, E.L. Santos, M.A. Fazio, A. Miranda, S. Daffre, and L.R. Travassos Effective topical treatment of subcutaneous murine B16F10-Nex2 melanoma by the antimicrobial peptide gomesin Neoplasia 10 2008 61 68 (Pubitemid 351170713)
148. T. Rozek, K.L. Wegener, J.H. Bowie, I.N. Olver, J.A. Carver, J.C. Wallace, and M.J. Tyler The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis the solution structure of aurein 1.2 Eur. J. Biochem. 267 2000 5330 5341
149. F. Safaiyan, U. Lindahl, and M. Salmivirta Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells Eur. J. Biochem. 252 1998 576 582 (Pubitemid 28156884)
150. R.D. Sanderson Heparan sulfate proteoglycans in invasion and metastasis Semin. Cell Dev. Biol. 12 2001 89 98
151. D. Schadendorf, M. Worm, B. Algermissen, C.M. Kohlmus, and B.M. Czarnetzki Chemosensitivity testing of human malignant melanoma. A retrospective analysis of clinical response and in vitro drug sensitivity Cancer 73 1994 103 108 (Pubitemid 24012729)
152. H. Schröder-Borm, R. Bakalova, and J. Andrä The NK-lysin derived peptide NK-2 preferentially kills cancer cells with increased surface levels of negatively charged phosphatidylserine FEBS Lett. 579 2005 6128 6134 (Pubitemid 41546259)
153. F. Schroeder, and J.M. Gardiner Membrane lipids and enzymes of cultured high- and low-metastatic B16 melanoma variants Cancer Res. 44 1984 3262 3269 (Pubitemid 14098566)
154. F. Schweizer Cationic amphiphilic peptides with cancer-selective toxicity Eur. J. Pharmacol. 625 2009 190 194
155. M. Seigneuret, and P.F. Devaux ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes Proc. Natl. Acad. Sci. U.S.A. 81 1984 3751 3755 (Pubitemid 14087796)
156. E. Sevcsik, G. Pabst, W. Richter, S. Danner, H. Amenitsch, and K. Lohner Interaction of LL-37 with model membrane systems of different complexity: influence of the lipid matrix Biophys. J. 94 2008 4688 4699
157. M. Shadidi, and M. Sioud Selective targeting of cancer cells using synthetic peptides Drug Resist. Updat. 6 2003 363 371 (Pubitemid 38173587)
158. Y. Shai Mode of action of membrane active antimicrobial peptides Biopolymers 66 2002 236 248 (Pubitemid 36098316)
159. S.V. Sharma Melittin resistance: a counterselection for ras transformation Oncogene 7 1992 193 201
160. G.V. Sherbet Membrane fluidity and cancer metastasis Exp. Cell Biol. 57 1989 198 205 (Pubitemid 19261731)
161. G.V. Sherbet, and S. Jackson Temperature-dependent surface charge modulation, membrane fluidity, and metastatic ability of L51178Y lymphoma Anticancer Res. 6 1986 129 134
162. D.S Shewach, and R.D. Kuchta Introduction to cancer chemotherapeutics Chem. Rev. 109 2009 2859 2861
163. S. Shi, Y. Wang, Y. Liang, and Q. Li Effects of tachyplesin and n-sodium butyrate on proliferation and gene expression of human gastric adenocarcinoma cell line BGC-823 World J. Gastroenterol. 12 2006 1694 1698
164. S. Shore Review of the nitrogen mustards Hahnemann Mon. 82 1947 461 470
165. P.I. Silva, S. Daffre, and P. Bulet Isolation and characterization of gomesin, an 18-residue cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to horseshoe crab antimicrobial peptides of the Tachyplesin family J. Biol. Chem. 275 2000 33464 33470
166. T.L. Simmons, E. Andrianasolo, K. McPhail, P. Flatt, and W.H. Gerwick Marine natural products as anticancer drugs Mol. Cancer Ther. 4 2005 333 342 (Pubitemid 40340212)
167. L.L. Smith, K. Brown, P. Carthew, C.K. Lim, E.A. Martin, J. Styles, and I.N. White Chemoprevention of breast cancer by tamoxifen: risks and opportunities Crit. Rev. Toxicol. 30 2000 571 594
168. P.W. Soballe, W.L. Maloy, M.L. Myrga, L.S. Jacob, and M. Herlyn Experimental local therapy of human melanoma with lytic magainin peptides Int. J. Cancer 60 1995 280 284
169. M.S. Soengas, P. Capodieci, D. Polsky, J. Mora, M. Esteller, X. Opitz-Araya, R. McCombie, J.G. Herman, W.L. Gerald, Y.A. Lazebnik, C. Cordon-Cardo, and S.W. Lowe Inactivation of the apoptosis effector Apaf-1 in malignant melanoma Nature 409 2001 207 211 (Pubitemid 32144287)
170. M. Sok, M. Sentjurc, M. Schara, J. Stare, and T. Rott Cell membrane fluidity and prognosis of lung cancer Ann. Thorac. Surg. 73 2002 1567 1571 (Pubitemid 34596594)
171. E. Staudegger, E.J. Prenner, M. Kriechbaum, G. Degovics, R.N.A.H. Lewis, R.N. McElhaney, and K. Lohner X-ray studies on the interaction of the antimicrobial peptide gramicidin S with microbial lipid extracts: evidence for cubic phase formation Biochim. Biophys. Acta 1468 2000 213 230
172. K. Sugahara, T. Mikami, T. Uyama, S. Mizuguchi, K. Nomura, and H. Kitagawa Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate Curr. Opin. Struct. Biol. 13 2003 612 620 (Pubitemid 37244117)
173. H. Suttmann, M. Retz, F. Paulsen, J. Harder, U. Zwergel, J. Kamradt, B. Wullich, G. Unteregger, M. Stockle, and J. Lehmann Antimicrobial peptides of the Cecropin-family show potent antitumor activity against bladder cancer cells BMC Urol. 8 2008 5
174. B. Szachowicz-Petelska, I. Dobrzynska, Z. Figaszewski, and S. Sulkowski Changes in physico-chemical properties of human large intestine tumour cells membrane Mol. Cell. Biochem. 238 2002 41 47 (Pubitemid 35023527)
175. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat. Rev. Drug Discov. 5 2006 219 234 (Pubitemid 43336035)
176. K. Tanaka, Y. Fujimoto, M. Suzuki, Y. Suzuki, T. Ohtake, H. Saito, and Y. Kohgo PI3-kinase p85α is a target molecule of proline-rich antimicrobial peptide to suppress proliferation of ras-transformed cells Jpn. J. Cancer Res. 92 2001 959 967 (Pubitemid 32970437)
177. D. Thévenin, M. An, and D.M. Engelman pHLIP-mediated translocation of membrane-impermeable molecules into cells Chem. Biol. 16 2009 754 762
178. E. Tkachenko, J.M. Rhodes, and M. Simons Syndecans: new kids on the signaling block Circ. Res. 96 2005 488 500 (Pubitemid 40463457)
179. P.J. Tofilon, and K. Camphausen Molecular targets for tumor radiosensitization Chem. Rev. 109 2009 2974 2988
180. M.T. Tosteson, and D.C. Tosteson The sting. Melittin forms channels in lipid bilayers Biophys. J. 36 1981 109 116 (Pubitemid 12216808)
181. 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. 51 1991 3062 3066
182. W.J. van Blitterswijk Alteration in lipid fluidity in the plasma membrane of tumor cells M. Shinitzky, Physiology of Membrane Fluidity 1984 CRC Press Boca Raton, FL, USA 53 84
183. W.C. Van de, C. Lahorte, H. Vermeersch, D. Loose, K. Mervillie, N.D. Steinmetz, J.L. Vanderheyden, C.A. Cuvelier, G. Slegers, and R.A. Dierck Quantitative tumor apoptosis imaging using technetium-99m-HYNIC annexin V single photon emission computed tomography J. Clin. Oncol. 21 2003 3483 3487 (Pubitemid 46594081)
184. H.J. Vogel, D.J. Schibli, W. Jing, E.M. Lohmeier-Vogel, R.F. Epand, and R.M. Epand Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides Biochem. Cell. Biol. 80 2002 49 63 (Pubitemid 34194228)
185. F.L. Wang, S.X. Cui, L.P. Sun, X.J. Qu, Y.Y. Xie, L. Zhou, Y.L. Mu, W. Tang, and Y.S. Wang High expression of alpha 2,3-linked sialic acid residues is associated with the metastatic potential of human gastric cancer Cancer Detect. Prev. 32 2009 437 443
186. G. Wang, X. Li, and Z. Wang APD2: the updated antimicrobial peptide database and its application in peptide design Nucleic Acids Res. 37 2009 D933 D937
187. K.R. Wang, B.Z. Zhang, W. Zhang, J.X. Yan, J. Li, and R. Wang Antitumor effects, cell selectivity and structure-activity relationship of a novel antimicrobial peptide polybia-MPI Peptides 29 2008 963 968
188. K.R. Wang, J.X. Yan, B.Z. Zhang, J.J. Song, P.f. Jia, and R. Wang Novel mode of action of polybia-MPI, a novel antimicrobial peptide, in multi-drug resistant leukemic cells Cancer Lett. 278 2009 65 72
189. Z. Wang, and G. Wang APD: the antimicrobial peptide database Nucleic Acids Res. 32 2004 D590 D592
190. M. Wieczorek, H. Jenssen, J. Kindrachuk, W.R.P. Scott, M. Elliott, K. Hilpert, J.T.J. Cheng, R.E.W. Hancock, and S.K. Straus Structural studies of a peptide with immune modulating and direct antimicrobial activity Chem. Biol. 17 2010 970 980
191. R. Willumeit, M. Kumpugdee, S.S. Funari, K. Lohner, B. Pozo-Navas, K. Brandenburg, S. Linser, and J. Andrä Structural rearrangement of model membranes by the peptide antibiotic NK-2 Biochim. Biophys. Acta 1669 2005 125 134 (Pubitemid 40704730)
192. W. Wimley, and K. Hristova Antimicrobial peptides: successes, challenges and unanswered questions J. Membr. Biol. 239 2011 27 34
193. W.C. Wimley Describing the mechanism of antimicrobial peptide action with the interfacial activity model ACS Chem. Biol. 5 2010 905 917
194. W.C. Wimley, T.P. Creamer, and S.H. White Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides Biochemistry 35 1996 5109 5124
195. D. Winder, W.H. Günzburg, V. Erfle, and B. Salmons Expression of antimicrobial peptides has an antitumour effect in human cells Biochem. Biophys. Res. Commun. 242 1998 608 612 (Pubitemid 28412575)
196. H. Woehlecke, A. Pohl, N. Alder-Baerens, H. Lage, and A. Herrmann Enhanced exposure of phosphatidylserine in human gastric carcinoma cells overexpressing the half-size ABC transporter BCRP (ABCG2) Biochem. J. 376 2003 489 495 (Pubitemid 38010534)
197. N. Xu, Y.S. Wang, W.B. Pan, B. Xiao, Y.J. Wen, X.C. Chen, L.J. Chen, H.X. Deng, J. You, B. Kan, A.F. Fu, D. Li, X. Zhao, and Y.Q. Wei Human alpha-defensin-1 inhibits growth of human lung adenocarcinoma xenograft in nude mice Mol. Cancer Ther. 7 2008 1588 1597
198. N. Yang, T. Lejon, and O. Rekdal Antitumour activity and specificity as a function of substitutions in the lipophilic sector of helical lactoferrin-derived peptide J. Pept. Sci. 9 2003 300 311 (Pubitemid 36665526)
199. N. Yang, M.B. Strom, S.M. Mekonnen, J.S. Svendsen, and O. Rekdal The effects of shortening lactoferrin derived peptides against tumour cells, bacteria and normal human cells J. Pept. Sci. 10 2004 37 46 (Pubitemid 38100727)
200. Y.-C. Yoo, S. Watanabe, R. Watanabe, K. Hata, K. Shimazaki, and I. Azuma Bovine lactoferrin and lactoferricin, a peptide derived from bovine lactoferrin, inhibit tumor metastasis in mice Jpn. J. Cancer Res. 88 1997 184 190 (Pubitemid 27129646)
201. M. Zasloff Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor Proc. Natl. Acad. Sci. U.S.A. 84 1987 5449 5453 (Pubitemid 17129018)
202. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (Pubitemid 34100944)
203. W. Zhang, J. Li, L.W. Liu, K.R. Wang, J.J. Song, J.X. Yan, Z.Y. Li, B.Z. Zhang, and R. Wang A novel analog of antimicrobial peptide Polybia-MPI, with thioamide bond substitution, exhibits increased therapeutic efficacy against cancer and diminished toxicity in mice Peptides 31 2010 1832 1838
204. M. Zoonens, Y.K. Reshetnyak, and D.M. Engelman Bilayer interactions of pHLIP, a peptide that can deliver drugs and target tumors Biophys. J. 95 2008 225 235
205. R.F. Zwaal, and A.J. Schroit Pathophysiologic implications of membrane phospholipid asymmetry in blood cells Blood 89 1997 1121 1132 (Pubitemid 27079974)
206. D. Zweytick, G. Pabst, P.M. Abuja, A. Jilek, S.E. Blondelle, J. Andrä, R. Jerala, D. Monreal, G. Martinez de Tejada, and K. Lohner Influence of N-acylation of a peptide derived from human lactoferricin on membrane selectivity Biochim. Biophys. Acta 1758 2006 1426 1435 (Pubitemid 44436072)
207. D. Zweytick, S. Riedl, B. Rinner, M. Asslaber, H. Schaider, S. Walzer, A. Novak, and K. Lohner In search of new targets - the membrane lipid phosphatidylserine - the underestimated Achilles' heel of cancer cells Ann. Oncol. 22 suppl. 3 2011 iii42 iii43
208. D. Zweytick, S. Tumer, S.E. Blondelle, and K. Lohner Membrane curvature stress and antibacterial activity of lactoferricin derivatives Biochem. Biophys. Res. Commun. 369 2008 395 400
209. D. Zweytick, G. Deutsch, J. Andrä, S.E. Blondelle, E. Vollmer, R. Jerala, and K. Lohner Studies on lactoferricin derived E. coli membrane active peptides reveal differences in the mechanism of N-acylated versus non-acylated peptides J. Biol. Chem. 24 2011 21266 21276