Host-defense peptide mimicry for novel antitumor agents

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4299-4307

  Held Kuznetsov, Viktoria ^a   Rotem, Shahar ^a   Assaraf, Yehuda G ^a   Mor, Amram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Antimicrobial peptide; Combination therapy; Drug design; Monotherapy; Multidrug resistance; Peptide mimetic

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; DOXORUBICIN; HOST DEFENSE PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASSAY; CANCER INHIBITION; CARCINOMA CELL; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; FIBROBLAST; HYDROPHOBICITY; MALE; MOLECULAR MIMICRY; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; SINGLE DRUG DOSE;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CRICETINAE; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; HUMANS; MALE; MICE; MICE, INBRED C57BL; NEOPLASMS, EXPERIMENTAL; PROSTATIC NEOPLASMS; RATS;

MUS; QUERCUS;

EID: 72749100683     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-136358     Document Type: Article

References (62)

1. Assaraf, Y. G. (2006) The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist. Updat. 9, 227-246
2. Higgins, C. F. (2007) Multiple molecular mechanisms for multidrug resistance transporters. Nature 446, 749-757 (Pubitemid 46582024)
3. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature 415, 389-395
4. Shaw, J. E., Epand, R. F., Hsu, J. C., Mo, G. C., Epand, R. M., and Yip, C. M. (2008) Cationic peptide-induced remodelling of model membranes: direct visualization by in situ atomic force microscopy. J. Struct. Biol. 162, 121-138
5. Epand, R. F., Mowery, B. P., Lee, S. E., Stahl, S. S., Lehrer, R. I., Gellman, S. H., and Epand, R. M. (2008) Dual mechanism of bacterial lethality for a cationic sequence-random copolymer that mimics host-defense antimicrobial peptides. J. Mol. Biol. 379, 38-50
6. Takeshima, K., Chikushi, A., Lee, K. K., Yonehara, S., and Matsuzaki, K. (2003) Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J. Biol. Chem. 278, 1310-1315 (Pubitemid 36790815)
7. Chen, H. M., Wang, W., Smith, D., and Chan, S. C. (1997) 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, 171-179 (Pubitemid 27364170)
8. Chen, J., Xu, X. M., Underhill, C. B., Yang, S., Wang, L., Chen, Y., Hong, S., Creswell, K., and Zhang, L. (2005) Tachyplesin activates the classic complement pathway to kill tumor cells. Cancer Res. 65, 4614-4622 (Pubitemid 40740797)
9. Cruciani, R. A., Barker, J. L., Zasloff, M., Chen, H. C., and Colamonici, O. (1991) Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc. Natl. Acad. Sci. U. S. A. 88, 3792-3796 (Pubitemid 21916710)
10. Ghavami, S., Asoodeh, A., Klonisch, T., Halayko, A. J., Kadkhoda, K., Kroczak, T. J., Gibson, S. B., Booy, E. P., Naderi- Manesh, H., and Los, M. (2008) Brevinin-2R(1) semi-selectively kills cancer cells by a distinct mechanism, which involves the lysosomal-mitochondrial death pathway. J. Cell. Mol. Med. 12, 1005-1022 (Pubitemid 351718078)
11. Xu, N., Wang, Y. S., Pan, W. B., Xiao, B., Wen, Y. J., Chen, X. C., Chen, L. J., Deng, H. X., You, J., Kan, B., Fu, A. F., Li, D., Zhao, X., and Wei, Y. Q. (2008) Human alpha-defensin-1 inhibits growth of human lung adenocarcinoma xenograft in nude mice. Mol. Cancer Ther. 7, 1588-1597
12. 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)
13. Mader, J. S., Salsman, J., Conrad, D. M., and Hoskin, D. W. (2005) Bovine lactoferricin selectively induces apoptosis in human leukemia and carcinoma cell lines. Mol. Cancer Ther. 4, 612-624 (Pubitemid 40601843)
14. Makovitzki, A., Fink, A., and Shai, Y. (2009) 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, 3458-3463
15. Papo, N., Shahar, M., Eisenbach, L., and Shai, Y. (2003) A novel lytic peptide composed of DL-amino acids selectively kills cancer cells in culture and in mice. J. Biol. Chem. 278, 21018-21023 (Pubitemid 36806412)
16. Cruciani, R. A., Barker, J. L., Durell, S. R., Raghunathan, G., Guy, H. R., Zasloff, M., and Stanley, E. F. (1992) Magainin 2, a natural antibiotic from frog skin, forms ion channels in lipid bilayer membranes. Eur. J. Pharmacol. 226, 287-296
17. Papo, N., Braunstein, A., Eshhar, Z., and Shai, Y. (2004) 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, 5779-5786 (Pubitemid 39095578)
18. Sharma, S. V. (1992) Melittin resistance: a counterselection for ras transformation. Oncogene 7, 193-201
19. Liu, S., Yu, M., He, Y., Xiao, L., Wang, F., Song, C., Sun, S., Ling, C., and Xu, Z. (2008) Melittin prevents liver cancer cell metastasis through inhibition of the Rac1-dependent pathway. Hepatology 47, 1964-1973 (Pubitemid 351945563)
20. Soballe, P. W., Maloy, W. L., Myrga, M. L., Jacob, L. S., and Herlyn, M. (1995) Experimental local therapy of human melanoma with lytic magainin peptides. Int. J. Cancer 60, 280-284
21. Chuang, C. M., Monie, A., Wu, A., Mao, C. P., and Hung, C. F. (2009) Treatment with LL-37 peptide enhances antitumor effects induced by CpG oligodeoxynucleotides against ovarian cancer. Hum. Gene. Ther. 20, 303-313
22. Wang, C., Chen, T., Zhang, N., Yang, M., Li, B., Lu, X., Cao, X., and Ling, C. (2009) Melittin, a major component of bee venom, sensitizes human hepatocellular carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by activating CaMKII-TAK1-JNK/p38 and inhibiting IκBα kinase-NFκB. J. Biol. Chem. 284, 3804-3813
23. Hancock, R. E., and Sahl, H. G. (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557
24. Radzishevsky, I. S., Rotem, S., Bourdetsky, D., Navon-Venezia, S., Carmeli, Y., and Mor, A. (2007) Improved antimicrobial peptides based on acyl-lysine oligomers. Nat. Biotechnol. 25, 657-659 (Pubitemid 46897206)
25. Radzishevsky, I., Krugliak, M., Ginsburg, H., and Mor, A. (2007) Antiplasmodial activity of lauryl-lysine oligomers. Antimicrob. Agents Chemother. 51, 1753-1759
26. Radzishevsky, I. S., Kovachi, T., Porat, Y., Ziserman, L., Zaknoon, F., Danino, D., and Mor, A. (2008) Structure-activity relationships of antibacterial acyl-lysine oligomers. Chem. Biol. 15, 354-362
27. Rotem, S., and Mor, A. (2009) Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta 1788, 1582-1592
28. Rotem, S., Radzishevsky, I. S., Bourdetsky, D., Navon-Venezia, S., Carmeli, Y., and Mor, A. (2008) Analogous oligo-acyl-lysines with distinct antibacterial mechanisms. FASEB J. 22, 2652-2661
29. Foster, B. A., Gingrich, G. R., Kwon, E. D., Madias, C., and Greenberg, N. M. (1997) Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 57, 3325-3330 (Pubitemid 27355467)
30. Chang, C. C., Liang, Y. C., Klutz, A., Hsu, C. I., Lin, C. F., Mold, D. E., Chou, T. C., Lee, Y. C., and Huang, R. C. (2006) Reversal of multidrug resistance by two nordihydroguaiaretic acid derivatives, M4N and maltose-M3N, and their use in combination with doxorubicin or paclitaxel. Cancer Chemother. Pharmacol. 58, 640-653 (Pubitemid 44167390)
31. Tyagi, A. K., Singh, R. P., Agarwal, C., Chan, D. C., and Agarwal, R. (2002) Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin-induced growth Inhibition, G2-M arrest, and apoptosis. Clin. Cancer Res. 8, 3512-3519 (Pubitemid 35340729)
32. Ohsaki, Y., Gazdar, A. F., Chen, H. C., and Johnson, B. E. (1992) Antitumor activity of magainin analogues against human lung cancer cell lines. Cancer Res. 52, 3534-3538
33. Yang, N., Stensen, W., Svendsen, J. S., and Rekdal, O. (2002) Enhanced antitumor activity and selectivity of lactoferrin-derived peptides. J. Pept. Res. 60, 187-197 (Pubitemid 35155428)
34. Eliassen, L. T., Berge, G., Leknessund, A., Wikman, M., Lindin, I., Lokke, C., Ponthan, F., Johnsen, J. I., Sveinbjornsson, B., Kogner, P., Flaegstad, T., and Rekdal, O. (2006) The antimicrobial peptide, lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo. Int. J. Cancer 119, 493-500 (Pubitemid 43955700)
35. Krugliak, M., Feder, R., Zolotarev, V. Y., Gaidukov, L., Dagan, A., Ginsburg, H., and Mor, A. (2000) Antimalarial activities of dermaseptin S4 derivatives. Antimicrob. Agents Chemother. 44, 2442-2451
36. Kanome, T., Itoh, N., Ishikawa, F., Mori, K., Kim-Kaneyama, J. R., Nose, K., and Shibanuma, M. (2007) Characterization of Jumping translocation breakpoint (JTB) gene product isolated as a TGF-•1-inducible clone involved in regulation of mitochondrial function, cell growth and cell death. Oncogene 26, 5991-6001 (Pubitemid 47373803)
37. Epand, R. M., Rotem, S., Mor, A., Berno, B., and Epand, R. F. (2008) Bacterial membranes as a predictor of antimicrobial potency. J. Am. Chem. Soc. 130, 14346-14352
38. Borgnia, M. J., Eytan, G. D., and Assaraf, Y. G. (1996) Competition of hydrophobic peptides, cytotoxic drugs, and chemosensitizers on a common P-glycoprotein pharmacophore as revealed by its ATPase activity. J. Biol. Chem. 271, 3163-3171
39. Bram, E. E., Ifergan, I., Grimberg, M., Lemke, K., Skladanowski, A., and Assaraf, Y. G. (2007) C421 allele-specific ABCG2 gene amplification confers resistance to the antitumor triazoloacridone C-1305 in human lung cancer cells. Biochem. Pharmacol. 74, 41-53 (Pubitemid 46802491)
40. Hooijberg, J. H., Peters, G. J., Assaraf, Y. G., Kathmann, I., Priest, D. G., Bunni, M. A., Veerman, A. J., Scheffer, G. L., Kaspers, G. J., and Jansen, G. (2003) The role of multidrug resistance proteins MRP1, MRP2 and MRP3 in cellular folate homeostasis. Biochem. Pharmacol. 65, 765-771 (Pubitemid 36293693)
41. Wielinga, P. R., Reid, G., Challa, E. E., van der Heijden, I., van Deemter, L., de Haas, M., Mol, C., Kuil, A. J., Groeneveld, E., Schuetz, J. D., Brouwer, C., De Abreu, R. A., Wijnholds, J., Beijnen, J. H., and Borst, P. (2002) Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol. Pharmacol. 62, 1321-1331 (Pubitemid 35407456)
42. Chongsiriwatana, N. P., Patch, J. A., Czyzewski, A. M., Dohm, M. T., Ivankin, A., Gidalevitz, D., Zuckermann, R. N., and Barron, A. E. (2008) Peptoids that mimic the structure, function, and mechanism of helical antimicrobial peptides. Proc. Natl. Acad. Sci. U. S. A. 105, 2794-2799 (Pubitemid 351723623)
43. Gademann, K., and Seebach, D. (2001) Synthesis of cyclo-tripeptides and their biological in vitro evaluation as antiproliferatives against the growth of human cancer cell lines. Helvetica Chimica Acta 84, 2924-2937 (Pubitemid 33091791)
44. Mowery, B. P., Lee, S. E., Kissounko, D. A., Epand, R. F., Epand, R. M., Weisblum, B., Stahl, S. S., and Gellman, S. H. (2007) Mimicry of antimicrobial host-defense peptides by random copolymers. J. Am. Chem. Soc. 129, 15474-15476
45. Tew, G. N., Liu, D., Chen, B., Doerksen, R. J., Kaplan, J., Carroll, P. J., Klein, M. L., and DeGrado, W. F. (2002) De novo design of biomimetic antimicrobial polymers. Proc. Natl. Acad. Sci. U. S. A. 99, 5110-5114 (Pubitemid 34411511)
46. Utsugi, T., Schroit, A. J., Connor, J., Bucana, C. D., and Fidler, I. J. (1991) Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes. Cancer Res. 51, 3062-3066
47. Yogeeswaran, G., and Salk, P. L. (1981) Metastatic potential is positively correlated with cell surface sialylation of cultured murine tumor cell lines. Science 212, 1514-1516 (Pubitemid 11063023)
48. Bullard, K. M., Kim, H. R., Wheeler, M. A., Wilson, C. M., Neudauer, C. L., Simpson, M. A., and McCarthy, J. B. (2003) Hyaluronan synthase-3 is upregulated in metastatic colon carcinoma cells and manipulation of expression alters matrix retention and cellular growth. Int. J. Cancer 107, 739-746
49. Chan, S. C., Hui, L., and Chen, H. M. (1998) Enhancement of the cytolytic effect of anti-bacterial cecropin by the microvilli of cancer cells. Anticancer Res. 18, 4467-4474 (Pubitemid 29043678)
50. Fotin-Mleczek, M., Fischer, R., and Brock, R. (2005) Endocytosis and cationic cell-penetrating peptides-a merger of concepts and methods. Curr. Pharm. Des. 11, 3613-3628 (Pubitemid 41630988)
51. Nakase, I., Niwa, M., Takeuchi, T., Sonomura, K., Kawabata, N., Koike, Y., Takehashi, M., Tanaka, S., Ueda, K., Simpson, J. C., Jones, A. T., Sugiura, Y., and Futaki, S. (2004) Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol. Ther. 10, 1011-1022 (Pubitemid 39625245)
52. Wadia, J. S., Stan, R. V., and Dowdy, S. F. (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10, 310-315
53. Risso, A., Braidot, E., Sordano, M. C., Vianello, A., Macri, F., Skerlavaj, B., Zanetti, M., Gennaro, R., and Bernardi, P. (2002) BMAP-28, an antibiotic peptide of innate immunity, induces cell death through opening of the mitochondrial permeability transition pore. Mol. Cell. Biol. 22, 1926-1935 (Pubitemid 34175007)
54. Az-Achirica, P., Prieto, S., Ubach, J., Andreu, D., Rial, E., and Rivas, L. (1994) Permeabilization of the mitochondrial inner membrane by short cecropin-A-melittin hybrid peptides. Eur. J. Biochem. 224, 257-263 (Pubitemid 24267129)
55. Heerdt, B. G., Houston, M. A., and Augenlicht, L. H. (2005) The intrinsic mitochondrial membrane potential of colonic carcinoma cells is linked to the probability of tumor progression. Cancer Res. 65, 9861-9867
56. Heerdt, B. G., Houston, M. A., Wilson, A. J., and Augenlicht, L. H. (2003) The intrinsic mitochondrial membrane potential (Deltapsim) is associated with steady-state mitochondrial activity and the extent to which colonic epithelial cells undergo butyrate- mediated growth arrest and apoptosis. Cancer Res. 63, 6311-6319
57. Galluzzi, L., Larochette, N., Zamzami, N., and Kroemer, G. (2006) Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25, 4812-4830 (Pubitemid 44192089)
58. Luzio, J. P., Pryor, P. R., and Bright, N. A. (2007) Lysosomes: fusion and function. Nat. Rev. Mol. Cell. Biol. 8, 622-632
59. Kroemer, G., and Jaattela, M. (2005) Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5, 886-897 (Pubitemid 41746033)
60. Guicciardi, M. E., Leist, M., and Gores, G. J. (2004) Lysosomes in cell death. Oncogene 23, 2881-2890
61. Hoskin, D. W., and Ramamoorthy, A. (2008) Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 1778, 357-375
62. Lincke, C. R., van der Bliek, A. M., Schuurhuis, G. J., van der Velde-Koerts, T., Smit, J. J., and Borst, P. (1990) Multidrug resistance phenotype of human BRO melanoma cells transfected with a wild-type human mdr1 complementary DNA. Cancer Res. 50, 1779-1785