Current strategies for the development of peptide-based anti-cancer therapeutics

Journal of Peptide Science

Volumn 11, Issue 11, 2005, Pages 713-726

  Borghouts, Corina ^a   Kunz, Christian ^a   Groner, Bernd ^a  

^a INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

Aptamers; Cancer; Cellular targeting; Intracellular drug targets; Liposomes; Peptide therapy; Protein transduction; Scaffolds

Indexed keywords

DOXORUBICIN; IMMUNOLIPOSOME; LIPOSOME; ONCOPROTEIN; PEPTIDE DERIVATIVE; PEPTIDE LIBRARY; SCAFFOLD PROTEIN; THIOREDOXIN;

ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; BREAST CANCER; CANCER THERAPY; CARDIOMYOPATHY; CELL TRANSFORMATION; CELL TRANSPORT; DRUG BINDING; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG IDENTIFICATION; DRUG RECEPTOR BINDING; DRUG RELEASE; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE FUNCTION; GENOME ANALYSIS; HUMAN; HUMAN GENOME; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; ONCOGENE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; TARGET CELL; TUMOR SUPPRESSOR GENE;

ANTINEOPLASTIC AGENTS; HUMANS; ONCOGENES; PEPTIDES;

EID: 28044454553     PISSN: 10752617     EISSN: None     Source Type: Journal    
DOI: 10.1002/psc.717     Document Type: Review

References (145)

1. Hanahan D, Weinberg PA. The hallmarks of cancer. Cell 2000; 100: 57-70.
2. Hahn WC, Weinberg RA. Rules for making human tumor cells. N. Engl. J. Med. 2002; 347: 1593-1603.
3. Feinberg AP. The epigenetics of cancer etiology. Semin. Cancer Biol. 2004; 14: 427-432.
4. Futreal PA, Coin L, Marshall M, Down T, Hubbard T, Wooster R, Rahman N, Stratton MR. A census of human cancer genes. Nat. Rev. Cancer 2004; 4: 177-183.
5. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 2002; 3: 415-428.
6. Weinstein IB. Cancer. addiction to oncogenes-the Achilles heal of cancer. Science 2002; 297: 63-64.
7. Felsher DW, Bishop JM. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol. Cell 1999; 4: 199-207.
8. Giuriato S, Rabin K, Fan AC, Shachaf CM, Felsher DW. Conditional animal models: a strategy to define when oncogenes will be effective targets to treat cancer. Semin. Cancer Biol. 2004; 14: 3-11.
9. Jain M, Arvanitis C, Chu K, Dewey W, Leonhardt E, Trinh M, Sundberg CD, Bishop JM, Felsher DW. Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 2002; 297: 102-104.
10. Gunther EJ, Moody SE, Belka GK, Hahn KT, Innocent N, Dugan KD, Cardiff RD, Chodosh LA. Impact of p53 loss on reversal and recurrence of conditional Wnt-induced tumorigenesis. Genes Dev. 2003; 17: 488-501.
11. Chin L, Tam A, Pomerantz J, Wong M, Holash J, Bardeesy N, Shen Q, O'Hagan R, Pantginis J, Zhou H, Horner JW, Cordon-Cardo C, Yancopoulos GD, DePinho RA. 2nd Essential role for oncogenic Ras in tumour maintenance. Nature 1999; 400: 468-472.
12. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, Whitsett JA, Koretsky A, Varmus HE. Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev. 2001; 15: 3249-3262.
13. Moody SE, Sarkisian CJ, Hahn KT, Gunther EJ, Pickup S, Dugan KD, Innocent N, Cardiff RD, Schnall MD, Chodosh LA. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2002; 2: 451-461.
14. Wang R, Ferrell LD, Faouzi S, Maher JJ, Bishop JM. Activation of the Met receptor by cell attachment induces and sustains hepatocellular carcinomas in transgenic mice. J. Cell Biol. 2001; 153: 1023-1034.
15. Xie W, Chow LT, Paterson AJ, Chin E, Kudlow JE. Conditional expression of the ErbB2 oncogene elicits reversible hyperplasia in stratified epithelia and up-regulation of TGFalpha expression in transgenic mice. Oncogene 1999; 18: 3593-3607.
16. Ewald D, Li M, Efrat S, Auer G, Wall RJ, Furth PA, Hennighausen L. Time-sensitive reversal of hyperplasia in transgenic mice expressing SV40 T antigen. Science 1996; 273: 1384-1386.
17. Huettner CS, Zhang P, Van Etten RA, Tenen DG. Reversibility of acute B-cell leukaemia induced by BCR-ABL1. Nat. Genet. 2000; 24: 57-60.
18. Karlsson A, Giuriato S, Tang F, Fung-Weier J, Levan G, Felsher DW. Genomically complex lymphomas undergo sustained tumor regression upon MYC inactivation unless they acquire novel chromosomal translocations. Blood 2003; 101: 2797-2803.
19. Boxer RB, Jang JW, Sintasath L, Chodosh LA. Lack of sustained regression of c-MYC-induced mammary adenocarcinomas following brief or prolonged MYC inactivation. Cancer Cell 2004; 6: 577-586.
20. Shachaf CM, Kopelman AM, Arvanitis C, Karlsson A, Beer S, Mandl S, Bachmann MH, Borowsky AD, Ruebner B, Cardiff RD, Yang Q, Bishop JM, Contag CH, Felsher DW. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004; 431: 1112-1117.
21. Baudino TA, McKay C, Pendeville-Samain H, Nilsson JA, Maclean KH, White EL, Davis AC, Ihle JN, Cleveland JL. c-Myc is essential for vasculogenesis and angiogenesis during development and tumor progression. Genes Dev. 2002; 16: 2530-2543.
22. Felsher DW. Cancer revoked: oncogenes as therapeutic targets. Nat. Rev. Cancer 2003; 3: 375-380.
23. Buerger C, Nagel-Wolfrum K, Kunz C, Wittig I, Butz K, Hoppe-Seyler F, Groner B. Sequence-specific peptide aptamers, interacting with the intracellular domain of the epidermal growth factor receptor, interfere with Stat3 activation and inhibit the growth of tumor cells. J. Biol. Chem. 2003; 278: 37610-37621.
24. Kardinal C, Konkol B, Lin H, Eulitz M, Schmidt EK, Estrov Z, Talpaz M, Arlinghaus RB, Feller SM. Chronic myelogenous leukemia blast cell proliferation is inhibited by peptides that disrupt Grb2-SoS complexes. Blood 2001; 98: 1773-1781.
25. Mai JC, Mi Z, Kim SH, Ng B, Robbins PD. A proapoptotic peptide for the treatment of solid tumors. Cancer Res. 2001; 61: 7709-7712.
26. Mendoza FJ, Espino PS, Cann KL, Bristow N, McCrea K, Los M. Anti-tumor chemotherapy utilizing peptide-based approaches-apoptotic pathways, kinases, and proteasome as targets. Arch. Immunol. Ther. Exp. (Warsz) 2005; 53: 47-60.
27. Nagel-Wolfrum K, Buerger C, Wittig I, Butz K, Hoppe-Seyler F, Groner B. The interaction of specific peptide aptamers with the DNA binding domain and the dimerization domain of the transcription factor Stat3 inhibits transactivation and induces apoptosis in tumor cells. Mol. Cancer Res. 2004; 2: 170-182.
28. Wang HL, Kurtz A. Breast cancer growth inhibition by delivery of the MDGI-derived peptide P108. Oncogene 2000; 19: 2455-2460.
29. Zhang J, Spring H, Schwab M. Neuroblastoma tumor cell-binding peptides identiffied through random peptide phage display. Cancer Lett. 2001; 171: 153-164.
30. Lev DC, Kim LS, Melnikova V, Ruiz M, Ananthaswamy HN, Price JE. Dual blockade of EGFR and ERK1/2 phosphorylation potentiates growth inhibition of breast cancer cells. Br. J. Cancer 2004; 91: 795-802.
31. McCarty MF. Targeting multiple signaling pathways as a strategy for managing prostate cancer: multifocal signal modulation therapy. Integr. Cancer Ther. 2004; 3: 349-380.
32. Tortora G, Caputo R, Damiano V, Melisi D, Bianco R, Fontanini G, Veneziani BM, De Placido S, Bianco AR, Ciardiello F. Combination of a selective cyclooxygenase-2 inhibitor with epidermal growth factor receptor tyrosine kinase inhibitor ZD 1839 and protein kinase A antisense causes cooperative antitumor and antiangiogenic effect. Clin. Cancer Res. 2003; 9: 1566-1572.
33. Polo JM, Dell'Oso T, Ranuncolo SM, Cerchietti L, Beck D, Da Silva GF, Prive GG, Licht JD, Melnick A. Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nat. Med. 2004; 10: 1329-1335.
34. Katterle Y, Brandt BH, Dowdy SF, Niggemann B, Zanker KS, Dittmar T. Antitumour effects of PLC-gamma1-(SH2)2-TAT fusion proteins on EGFR/c-erbB-2-positive breast cancer cells. Br. J. Cancer 2004; 90: 230-235.
35. Picksley SM, Vojtesek B, Sparks A, Lane DP. Immunochemical analysis of the interaction of p53 with MDM2;-fine mapping of the MDM2 binding site on p53 using synthetic peptides. Oncogene 1994; 9: 2523-2529.
36. Kanovsky M, Raffo A, Drew L, Rosal R, Do T, Friedman FK, Rubinstein P, Visser J, Robinson R, Brandt-Rauf PW, Michl J, Fine RL, Pincus MR. Peptides from the amino terminal mdm-2-binding domain of p53, designed from conformational analysis, are selectively cytotoxic to transformed cells. Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 12438-12443.
37. May MJ, D'Acquisto F, Madge LA, Glockner J, Pober JS, Ghosh S. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science 2000; 289: 1550-1554.
38. Sugioka R, Shimizu S, Funatsu T, Tamagawa H, Sawa Y, Kawakami T, Tsujimoto Y. BH4-domain peptide from Bcl-xL exerts anti-apoptotic activity in vivo. Oncogene 2003; 22: 8432-8440.
39. Colas P. Combinatorial protein reagents to manipulate protein function. Curr. Opin. Chem. Biol. 2000; 4: 54-59.
40. Ladner RC. Constrained peptides as binding entities. Trends Biotechnol. 1995; 13: 426-430.
41. Westerlund-Wikstrom B. Peptide display on bacterial flagella: principles and applications. Int. J. Med. Microbiol. 2000; 290: 223-230.
42. Bjorklund M, Heikkila P, Koivunen E. Peptide inhibition of catalytic and noncatalytic activities of matrix metalloproteinase-9 blocks tumor cell migration and invasion. J. Biol. Chem. 2004; 279: 29589-29597.
43. Fairbrother WJ, Christinger HW, Cochran AG, Fuh G, Keenan CJ, Quan C, Shriver SK, Tom JY, Wells JA, Cunningham BC. Novel peptides selected to bind vascular endothelial growth factor target the receptor-binding site. Biochemistry 1998; 37: 17754-17764.
44. Kim MY, Byeon CW, Hong KH, Han KH, Jeong S. Inhibition of the angiogenesis by the MCP-1 (monocyte chemoattractant protein-1) binding peptide. FEBS Lett. 2005; 579: 1597-1601.
45. Skelton NJ, Chen YM, Dubree N, Quan C, Jackson DY, Cochran A, Zobel K, Deshayes K, Baca M, Pisabarro MT, Lowman HB. Structure-function analysis of a phage display-derived peptide that binds to insulin-like growth factor binding protein 1. Biochemistry 2001; 40: 8487-8498.
46. Wu P, Leinonen J, Koivunen E, Lankinen H, Stenman UH. Identification of novel prostate-specific antigen-binding peptides modulating its enzyme activity. Eur. J. Biochem. 2000; 267: 6212-6220.
47. Nakamura T, Takasugi H, Aizawa T, Yoshida M, Mizuguchi M, Mori Y, Shinoda H, Hayakawa Y, Kawano K. Peptide mimics of epidermal growth factor (EGF) with antagonistic activity. J. Biotechnol. 2005; 116: 211-219.
48. Szecsi PB, Riise E, Roslund LB, Engberg J, Turesson I, Buhl L, Schafer-Nielsen C. Identification of patient-specific peptides for detection of M-proteins and myeloma cells. Br. J. Haematol. 1999; 107: 357-364.
49. Hoppe-Seyler F, Crnkovic-Mertens I, Tomai E, Butz K. Peptide aptamers: specific inhibitors of protein function. Curr. Mol. Med. 2004; 4: 529-538.
50. Vidal M, Brachmann RK, Fattaey A, Harlow E, Boeke JD. Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 10315-10320.
51. Peelle B, Lorens J, Li W, Bogenberger J, Payan DG, Anderson DC. Intracellular protein scaffold-mediated display of random peptide libraries for phenotypic screens in mammalian cells. Chem. Biol. 2001; 8: 521-534.
52. Gallagher WM, Cairney M, Schott B, Roninson IB, Brown R. Identification of p53 genetic suppressor elements which confer resistance to cisplatin. Oncogene 1997; 14: 185-193.
53. Borghouts C, Kunz C, Groner B. Peptide aptamers: recent developments for cancer therapy. Expert Opin. Biol. Ther. 2005; 5: 783-797.
54. Butz K, Denk C, Fitscher B, Crnkovic-Mertens I, Ullmann A, Schroder CH, Hoppe-Seyler F. Peptide aptamers targeting the hepatitis B virus core protein: a new class of molecules with antiviral activity. Oncogene 2001; 20: 6579-6586.
55. Butz K, Denk C, Ullmann A, Scheffner M, Hoppe-Seyler F. Induction of apoptosis in human papillomavirus positive cancer cells by peptide aptamers targeting the viral E6 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 6693-6697.
56. Fabbrizio E, Le Cam L, Polanowska J, Kaczorek M, Lamb N, Brent R, Sardet C. Inhibition of mammalian cell proliferation by genetically selected peptide aptamers that functionally antagonize E2F activity. Oncogene 1999; 18: 4357-4363.
57. Nauenburg S, Zwerschke W, Jansen-Durr P. Induction of apoptosis in cervical carcinoma cells by peptide aptamers that bind to the HPV-16 E7 oncoprotein. FASEB J. 2001; 15: 592-594.
58. Schmidt S, Diriong S, Mery J, Fabbrizio E, Debant A. Identification of the first Rho-GEF inhibitor, TRIPalpha, which targets the RhoA-specific GEF domain of Trio. FEBS Lett. 2002; 523: 35-42.
59. Perez JJ, Corcho F, Llorens O. Molecular modeling in the design of peptidomimetics and peptide surrogates. Curr. Med. Chem. 2002; 9: 2209-2229.
60. Ripka AS, Rich DH. Peptidomimetic design. Curr. Opin. Chem. Biol. 1998; 2: 441-452.
61. Hamamoto K, Kida Y, Zhang Y, Shimizu T, Kuwano K. Antimicrobial activity and stability to proteolysis of small linear cationic peptides with D-amino acid substitutions. Microbiol. Immunol. 2002; 46: 741-749.
62. Van Regenmortel MH, Muller S. D-peptides as immunogens and diagnostic reagents. Curr. Opin. Biotechnol. 1998; 9: 377-382.
63. Zhou N, Luo Z, Luo J, Fan X, Cayabyab M, Hiraoka M, Liu D, Han X, Pesavento J, Dong CZ, Wang Y, An J, Kaji H, Sodroski JG, Huang Z. Exploring the stereochemistry of CXCR4-peptide recognition and inhibiting HIV-1 entry with D-peptides derived from chemokines. J. Biol. Chem. 2002; 277: 17476-17485.
64. Chin JW, Cropp TA, Anderson JC, Mukherji M, Zhang Z, Schultz PG. An expanded eukaryotic genetic code. Science 2003; 301: 964-967.
65. Foubister V. Scientists expand the genetic code. Drug Discov. Today 2003; 8: 239-240.
66. Roisin A, Robin JP, Dereuddre-Bosquet N, Vitte AL, Dormont D, Clayette P, Jalinot P. Inhibition of HIV-1 replication by cell-penetrating peptides binding Rev. J. Biol. Chem. 2004; 279: 9208-9214.
67. Bottger V, Bottger A, Howard SF, Picksley SM, Chene P, Garcia-Echeverria C, Hochkeppel HK, Lane DP. Identification of novel mdm2 binding peptides by phage display. Oncogene 1996; 13: 2141-2147.
68. Garcia-Echeverria C, Chene P, Blommers MJ, Furet P. Discovery of potent antagonists of the interaction between human double minute 2 and tumor suppressor p53. J. Med. Chem. 2000; 43: 3205-3208.
69. Chene P. Inhibiting the p53-MDM2 interaction: an important target for cancer therapy. Nat. Rev. Cancer 2003; 3: 102-109.
70. Ladner RC, Sato AK, Gorzelany J, de Souza M. Phage display-derived peptides as therapeutic alternatives to antibodies. Drug Discov. Today 2004; 9: 525-529.
71. Geyer CR, Colman-Lerner A, Brent R. "Mutagenesis" by peptide aptamers identifies genetic network members and pathway connections. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 8567-8572.
72. Colas P, Cohen B, Jessen T, Grishina I, McCoy J, Brent R. Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 1996; 380: 548-550.
73. Blum JH, Dove SL, Hochschild A, Mekalanos JJ. Isolation of peptide aptamers that inhibit intracellular processes. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 2241-2246.
74. Li C, Plugariu CG, Bajgier J, White JR, Liefer KM, Wu SJ, Chaiken I. Coiled coil miniprotein randomization on phage leads to charge pattern mimicry of the receptor recognition determinant of interleukin 5. J. Mol. Recognit. 2002; 15: 33-43.
75. Myszka DG, Chaiken IM. Design and characterization of an intramolecular antiparallel coiled coil peptide. Biochemistry 1994; 33: 2363-2372.
76. Miceli R, Myszka D, Mao J, Sathe G, Chaiken I. The coiled coil stem loop miniprotein as a presentation scaffold. Drug Des. Discov. 1996; 13: 95-105.
77. Tang A, Wang C, Stewart R, Kopecek J. Self-assembled peptides exposing epitopes recognizable by human lymphoma cells. Bioconjug. Chem. 2000; 11: 363-371.
78. Gururaja TL, Narasimhamurthy S, Payan DG, Anderson DC. A novel artificial loop scaffold for the noncovalent constraint of peptides. Chem. Biol. 2000; 7: 515-527.
79. Lai JR, Gellman SH. Reinvestigation of the proposed folding and self-association of the Neuropeptide Head Activator. Protein Sci. 2003; 12: 560-566.
80. Abedi MR, Caponigro G, Kamb A. Green fluorescent protein as a scaffold for intracellular presentation of peptides. Nucleic Acids Res. 1998; 26: 623-630.
81. Caponigro G, Abedi MR, Hurlburt AP, Maxfield A, Judd W, Kamb A. Transdominant genetic analysis of a growth control pathway. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 7508-7513.
82. Muyldermans S. Single domain camel antibodies: current status. J. Biotechnol. 2001; 74: 277-302.
83. Arbabi Ghahroudi M, Desmyter A, Wyns L, Hamers R, Muyldermans S. Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett. 1997; 414: 521-526.
84. Ramsland PA, Kaushik A, Marchalonis JJ, Edmundson AB. Incorporation of long CDR3s into V domains: implications for the structural evolution of the antibody-combining site. Exp. Clin. Immunogenet. 2001; 18: 176-198.
85. Cortez-Retamozo V, Backmann N, Senter PD, Wernery U, De Baetselier P, Muyldermans S, Revets H. Efficient cancer therapy with a nanobody-based conjugate. Cancer Res. 2004; 64: 2853-2857.
86. Martin F, Volpari C, Steinkuhler C, Dimasi N, Brunetti M, Biasiol G, Altamura S, Cortese R, De Francesco R, Sollazzo M. Affinity selection of a camelized V(H) domain antibody inhibitor of hepatitis C virus NS3 protease. Protein Eng. 1997; 10: 607-614.
87. Christmann A, Walter K, Wentzel A, Kratzner R, Kolmar H. The cystine knot of a squash-type protease inhibitor as a structural scaffold for Escherichia coli cell surface display of conformationally constrained peptides. Protein Eng. 1999; 12: 797-806.
88. Le Nguyen D, Heitz A, Chiche L, Castro B, Boigegrain RA, Favel A, Coletti-Previero MA. Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 1990; 72: 431-435.
89. Baggio R, Burgstaller P, Hale SP, Putney AR, Lane M, Lipovsek D, Wright MC, Roberts RW, Liu R, Szostak JW, Wagner RW. Identification of epitope-like consensus motifs using mRNA display. J. Mol. Recognit. 2002; 15: 126-134.
90. Cohen BA, Colas P, Brent R. An artificial cell-cycle inhibitor isolated from a combinatorial library. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 14272-14277.
91. Tamm I, Trepel M, Cardo-Vila M, Sun Y, Welsh K, Cabezas E, Swatterthwait A, Arap W, Reed JC, Pasqualini R. Peptides targeting caspase inhibitors. J. Biol. Chem. 2003; 278: 14401-14405.
92. Sandrock T, Poritz M, Kim M, Feldhaus MJ, Roth B, Caponigro G, Kamb A. Expression levels of transdominant peptides and proteins in Saccharomyces cerevisiae. Yeast 2002; 19: 1-7.
93. Klevenz B, Butz K, Hoppe-Seyler F. Peptide aptamers: exchange of the thioredoxin-A scaffold by alternative platform proteins and its influence on target protein binding. Cell. Mol. Life Sci. 2002; 59: 1993-1998.
94. Cheng X, Boyer JL, Juliano RL. Selection of peptides that functionally replace a zinc finger in the Sp1 transcription factor by using a yeast combinatorial library. Proc. Natl. Acad. Sci. U. S. A. 1997; 94: 14120-14125.
95. Norman TC, Smith DL, Sorger PK, Drees BL, O'Rourke SM, Hughes TR, Roberts CJ, Friend SH, Fields S, Murray AW. Genetic selection of peptide inhibitors of biological pathways. Science 1999; 285: 591-595.
96. McConnell SJ, Hoess RH. Tendamistat as a scaffold for conformationally constrained phage peptide libraries. J. Mol. Biol. 1995; 250: 460-470.
97. Rottgen P, Collins J. A human pancreatic secretory trypsin inhibitor presenting a hypervariable highly constrained epitope via monovalent phagemid display. Gene 1995; 164: 243-250.
98. Perea SE, Reyes O, Puchades Y, Mendoza O, Vispo NS, Torrens I, Santos A, Silva R, Acevedo B, Lopez E, Falcon V, Alonso DF. Antitumor effect of a novel proapoptotic peptide that impairs the phosphorylation by the protein kinase 2 (casein kinase 2). Cancer Res. 2004; 64: 7127-7129.
99. Scott CP, Abel-Santos E, Jones AD, Benkovic SJ. Structural requirements for the biosynthesis of backbone cyclic peptide libraries. Chem. Biol. 2001; 8: 801-815.
100. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R. Naturally occurring antibodies devoid of light chains. Nature 1993; 363: 446-448.
101. Lauwereys M, Arbabi Ghahroudi M, Desmyter A, Kinne J, Holzer W, De Genst E, Wyns L, Muyldermans S. Potent enzyme inhibitors derived from dromedary heavy-chain antibodies. EMBO J. 1998; 17: 3512-3520.
102. Desmyter A, Transue TR, Ghahroudi MA, Thi MH, Poortmans F, Hamers R, Muyldermans S, Wyns L. Crystal structure of a camel single-domain VH antibody fragment in complex with lysozyme. Nat. Struct. Biol. 1996; 3: 803-811.
103. Padlan EA. X-ray crystallography of antibodies. Adv. Protein Chem. 1996; 49: 57-133.
104. Skerra A. Engineered protein scaffolds for molecular recognition. J. Mol. Recognit. 2000; 13: 167-187.
105. Egleton RD, Davis TP. Bioavailability and transport of peptides and peptide drugs into the brain. Peptides 1997; 18: 1431-1439.
106. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 1994; 269: 10444-10450.
107. Phelan A, Elliott G, O'Hare P. Intercellular delivery of functional p53 by the herpes virus protein VP22. Nat. Biotechnol. 1998; 16: 440-443.
108. Fawell S, Seery J, Daikh Y, Moore C, Chen LL, Pepinsky B, Barsoum J. Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. U. S. A. 1994; 91: 664-668.
109. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 2002; 8: 808-815.
110. Mi Z, Mai J, Lu X, Robbins PD. Characterization of a class of cationic peptides able to facilitate efficient protein transduction in vitro and in vivo. Mol. Ther. 2000; 2: 339-347.
111. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999; 285: 1569-1572.
112. Snyder EL, Meade BR, Dowdy SF. Anti-cancer protein transduction strategies: reconstitution of p27 tumor suppressor function. J. Controlled Release 2003; 91: 45-51.
113. Console S, Marty C, Garcia-Echeverria C, Schwendener R, Ballmer-Hofer K. Antennapedia and HIV transactivator of transcription (TAT) "protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J. Biol. Chem. 2003; 278: 35109-35114.
114. Vives E, Brodin P, Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 1997; 272: 16010-16017.
115. Suzuki T, Futaki S, Niwa M, Tanaka S, Ueda K, Sugiura Y. Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 2002; 277: 2437-2443.
116. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 2003; 278: 585-590.
117. Fittipaldi A, Ferrari A, Zoppe M, Arcangeli C, Pellegrini V, Beltram F, Giacca M. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem. 2003; 278: 34141-34149.
118. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 2004; 10: 310-315.
119. Foerg C, Ziegler U, Fernandez-Carneado J, Giralt E, Rennert R, Beck-Sickinger AG, Merkle HP. Decoding the entry of two novel cell-penetrating peptides in HeLa cells: lipid raft-mediated endocytosis and endosomal escape. Biochemistry 2005; 44: 72-81.
120. Caron NJ, Quenneville SP, Tremblay JP. Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem. Biophys. Res. Commun. 2004; 319: 12-20.
121. Vendeville A, Rayne F, Bonhoure A, Bettache N, Montcourrier P, Beaumelle B. HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses. Mol. Biol. Cell 2004; 15: 2347-2360.
122. Mastrobattista E, Koning GA, van Bloois L, Filipe AC, Jiskoot W, Storm G. Functional characterization of an endosome-disruptive peptide and its application in cytosolic delivery of immunoliposome-entrapped proteins. J. Biol. Chem. 2002; 277: 27135-27143.
123. Han X, Bushweller JH, Cafiso DS, Tamm LK. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 2001; 8: 715-720.
124. Darbinian N, Gallia GL, King J, Del Valle L, Johnson EM, Khalili K, Growth inhibition of glioblastoma cells by human Pur(alpha). J. Cell. Physiol. 2001; 189: 334-340.
125. Arteaga CL. The epidermal growth factor receptor: from mutant oncogene in nonhuman cancers to therapeutic target in human neoplasia. J. Clin. Oncol. 2001; 19: 32S-40S.
126. Ozanne B, Richards CS, Hendler F, Burns D, Gusterson B. Overexpression of the EGF receptor is a hallmark of squamous cell carcinomas. J. Pathol. 1986; 149: 9-14.
127. Buettner R, Mora LB, Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 2002; 8: 945-954.
128. Datta K, Sundberg C, Karumanchi SA, Mukhopadhyay D. The 104-123 amino acid sequence of the beta-domain of von Hippel-Lindau gene product is sufficient to inhibit renal tumor growth and invasion. Cancer Res. 2001; 61: 1768-1775.
129. Harada H, Hiraoka M, Kizaka-Kondoh S. Antitumor effect of TAT-oxygen-dependent degradation-caspase-3 fusion protein specifically stabilized and activated in hypoxic tumor cells. Cancer Res. 2002; 62: 2013-2018.
130. Snyder EL, Meade BR, Saenz CC, Dowdy SF. Treatment of terminal peritoneal carcinomatosis by a transducible p53-activating peptide. PLoS Biol. 2004; 2: E36.
131. Gabizon A, Martin F. Polyethylene glycol-coated (pegylated) liposomal doxorubicin. Rationale for use in solid tumours. Drugs 1997; 54(Suppl 4): 15-21.
132. Rose PG. Pegylated liposomal doxorubicin: optimizing the dosing schedule in ovarian cancer. Oncologist 2005; 10: 205-214.
133. Robert NJ, Vogel CL, Henderson IC, Sparano JA, Moore MR, Silverman P, Overmoyer BA, Shapiro CL, Park JW, Colbern GT, Winer EP, Gabizon AA. The role of the liposomal anthracyclines and other systemic therapies in the management of advanced breast cancer. Semin. Oncol. 2004; 31: 106-146.
134. O'Shaughnessy JA. Pegylated liposomal doxorubicin in the treatment of breast cancer. Clin. Breast Cancer 2003; 4: 318-328.
135. Abraham SA, Waterhouse DN, Mayer LD, Cullis PR, Madden TD, Bally MB. The liposomal formulation of doxorubicin. Methods Enzymol. 2005; 391: 71-97.
136. Cattel L, Ceruti M, Dosio F. From conventional to stealth liposomes: a new Frontier in cancer chemotherapy. J. Chemother. 2004; 16(Suppl 4): 94-97.
137. Chekhonin VP, Zhirkov YA, Gurina OI, Ryabukhin IA, Lebedev SV, Kashparov IA, Dmitriyeva TB. PEGylated immunoliposomes directed against brain astrocytes. Drug Deliv. 2005; 12: 1-6.
138. Fonseca C, Moreira JN, Ciudad CJ, Pedroso de Lima MC, Simoes S. Targeting of sterically stabilised pH-sensitive liposomes to human T-leukaemia cells. Eur. J. Pharm. Biopharm. 2005; 59: 359-366.
139. Moreira JN, Hansen CB, Gaspar R, Allen TM. A growth factor antagonist as a targeting agent for sterically stabilized liposomes in human small cell lung cancer. Biochim. Biophys. Acta 2001; 1514: 303-317.
140. Weidman SD, Lark RH, Coney LR, Fort DW, Frasca V, Zurawski VR, Kamen BA. Distribution of the folate, receptor GP38 in normal and malignant cell lines and tissues. Cancer Res. 1992; 52: 3396-3401.
141. Pan XQ, Zheng X, Shi G, Wang H, Ratnam M, Lee RJ. Strategy for the treatment of acute myelogenous leukemia based on folate receptor beta-targeted liposomal doxorubicin combined with receptor induction using all-trans retinoic acid. Blood 2002; 100: 594-602.
142. Lee RJ, Low PS. Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim. Biophys. Acta 1995; 1233: 134-144.
143. Lopes de Menezes DE, Pilarski LM, Allen TM. In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-cell lymphoma. Cancer Res. 1998; 58: 3320-3330.
144. Singh M. Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Des. 1999; 5: 443-451.
145. Wang S, Lee RJ, Cauchon G, Gorenstein DG, Low PS. Delivery of antisense oligodeoxyribonucleotides against the human epidermal growth factor receptor into cultured KB cells with liposomes conjugated to folate via polyethylene glycol. Proc. Natl. Acad. Sci. U. S. A. 1995; 92: 3318-3322.