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Expert Opinion on Drug Delivery Volume 6, 2009 - Issue 10
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Therapeutic peptides for cancer therapy. Part II – cell cycle inhibitory peptides and apoptosis-inducing peptides

Drazen Raucher The University of Mississippi Medical Center, Department of Biochemistry, 2500 North State Street, Jackson, MS 39216, USA +1 00 1 601 984 1510; +1 00 1 601 984 1501; [email protected]
,
Shama Moktan The University of Mississippi Medical Center, Department of Biochemistry, 2500 North State Street, Jackson, MS 39216, USA +1 00 1 601 984 1510; +1 00 1 601 984 1501; [email protected]
,
Iqbal Massodi The University of Mississippi Medical Center, Department of Biochemistry, 2500 North State Street, Jackson, MS 39216, USA +1 00 1 601 984 1510; +1 00 1 601 984 1501; [email protected]
&
Gene L Bidwell III The University of Mississippi Medical Center, Department of Biochemistry, 2500 North State Street, Jackson, MS 39216, USA +1 00 1 601 984 1510; +1 00 1 601 984 1501; [email protected]
Pages 1049-1064 | Published online: 10 Sep 2009

Bibliography

  • Lipka E, Crison J, Amidon GL. Transmembrane transport of peptide type compounds: prospects for oral delivery. J Control Release 1996;39(2-3):121-9
  • Talmadge JE. Pharmacodynamic aspects of peptide administration biological response modifiers. Adv Drug Deliv Rev 1998;33(3):241-52
  • Derossi D, Joliot AH, Chassaing G, et al. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994;269(14):10444-50
  • 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(25):16010-7
  • Lin YZ, Yao SY, Veach RA, et al. Inhibition of nuclear translocation of transcription factor NF-kappa B by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J Biol Chem 1995;270(24):14255-8
  • Derossi D, Chassaing G, Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol 1998;8(2):84-7
  • Lundberg P, Langel U. A brief introduction to cell-penetrating peptides. J Mol Recognit 2003;16(5):227-33
  • Gupta B, Levchenko TS, Torchilin VP. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev 2005;57(4):637-51
  • Leuschner C, Hansel W. Membrane disrupting lytic peptides for cancer treatments. Curr Pharm Des 2004;10(19):2299-310
  • Fischer PM, Lane DP. Inhibitors of cyclin-dependent kinases as anti-cancer therapeutics. Curr Med Chem 2000;7(12):1213-45
  • Luo Y, Hurwitz J, Massague J. Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature 1995;375(6527):159-61
  • Chen IT, Akamatsu M, Smith ML, et al. Characterization of p21Cip1/Waf1 peptide domains required for cyclin E/Cdk2 and PCNA interaction. Oncogene 1996;12(3):595-607
  • Bonfanti M, Taverna S, Salmona M, et al. p21WAF1-derived peptides linked to an internalization peptide inhibit human cancer cell growth. Cancer Res 1997;57(8):1442-6
  • Warbrick E, Lane DP, Glover DM, et al. A small peptide inhibitor of DNA replication defines the site of interaction between the cyclin-dependent kinase inhibitor p21WAF1 and proliferating cell nuclear antigen. Curr Biol 1995;5(3):275-82
  • Pan ZQ, Reardon JT, Li L, et al. Inhibition of nucleotide excision repair by the cyclin-dependent kinase inhibitor p21. J Biol Chem 1995;270(37):22008-16
  • Ball KL, Lain S, Fahraeus R, et al. Cell-cycle arrest and inhibition of Cdk4 activity by small peptides based on the carboxy-terminal domain of p21WAF1. Curr Biol 1997;7(1):71-80
  • Cayrol C, Knibiehler M, Ducommun B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 1998;16(3):311-20
  • Mutoh M, Lung FD, Long YQ, et al. A p21(Waf1/Cip1)carboxyl-terminal peptide exhibited cyclin-dependent kinase-inhibitory activity and cytotoxicity when introduced into human cells. Cancer Res 1999;59(14):3480-8
  • Mattock H, Lane DP, Warbrick E. Inhibition of cell proliferation by the PCNA-binding region of p21 expressed as a GFP miniprotein. Exp Cell Res 2001;265(2):234-41
  • Urry DW, Luan C-H, Parker TM, et al. Temperature of polypeptide inverse temperature transition depends on mean residue hydrophobicity. J Am Chem Soc 1991;113:4346-8
  • Liu W, Dreher MR, Chow DC, et al. Tracking the in vivo fate of recombinant polypeptides by isotopic labeling. J Control Release 2006;114(2):184-92
  • Meyer DE, Kong GA, Dewhirst MW, et al. Targeting a genetically engineered elastin like polypeptide to solid tumors by local hyperthermia. Cancer Res 2001;61(4):1548-54
  • Liu W, Dreher MR, Furgeson DY, et al. Tumor accumulation, degradation and pharmacokinetics of elastin-like polypeptides in nude mice. J Control Release 2006;116(2):170-8
  • Dreher MR, Liu W, Michelich CR, et al. Thermal cycling enhances the accumulation of a temperature-sensitive biopolymer in solid tumors. Cancer Res 2007;67(9):4418-24
  • Massodi I, Bidwell GL 3rd, Raucher D. Evaluation of cell penetrating peptides fused to elastin-like polypeptide for drug delivery. J Control Release 2005;108(2-3):396-408
  • Sadler K, Eom KD, Yang JL, et al. Translocating proline-rich peptides from the antimicrobial peptide bactenecin 7. Biochemistry 2002;41(48):14150-7
  • Massodi I, Moktan S, Rawat A, et al. Inhibition of ovarian cancer cell proliferation by a cell cycle inhibitory peptide fused to a thermally responsive elastin like polypeptide carrier. Int J Cancer 2009. In press
  • Fåhraeus R, Paramio JM, Ball KL, et al. Inhibition of pRb phosphorylation and cell-cycle progression by a 20-residue peptide derived from p16CDKN2/INK4A. Curr Biol 1996;6(1):84-91
  • Fahraeus R, Lain S, Ball KL, et al. Characterization of the cyclin-dependent kinase inhibitory domain of the INK4 family as a model for a synthetic tumour suppressor molecule. Oncogene 1998;16(5):587-96
  • Fujimoto K, Hosotani R, Miyamoto Y, et al. Inhibition of pRb phosphorylation and cell cycle progression by an antennapedia-p16(INK4A) fusion peptide in pancreatic cancer cells. Cancer Lett 2000;159(2):151-8
  • Hosotani R, Miyamoto Y, Fujimoto K, et al. Trojan p16 peptide suppresses pancreatic cancer growth and prolongs survival in mice. Clin Cancer Res 2002;8(4):1271-6
  • Kondo E, Seto M, Yoshikawa K, et al. Highly efficient delivery of p16 antitumor peptide into aggressive leukemia/lymphoma cells using a novel transporter system. Mol Cancer Ther 2004;3(12):1623-30
  • Midgley CA, Desterro JM, Saville MK, et al. An N-terminal p14ARF peptide blocks Mdm2-dependent ubiquitination in vitro and can activate p53 in vivo. Oncogene 2000;19(19):2312-23
  • Kondo E, Tanaka T, Miyake T, et al. Potent synergy of dual antitumor peptides for growth suppression of human glioblastoma cell lines. Mol Cancer Ther 2008;7(6):1461-71
  • Fåhraeus R, Lane DP. The p16(INK4a) tumour suppressor protein inhibits alphavbeta3 integrin-mediated cell spreading on vitronectin by blocking PKC-dependent localization of alphavbeta3 to focal contacts. EMBO J 1999;18(8):2106-18
  • Slomiany P, Baker T, Elliott ER, et al. Changes in motility, gene expression and actin dynamics: Cdk6-induced cytoskeletal changes associated with differentiation in mouse astrocytes. J Cell Biochem 2006;99(2):635-46
  • Alhaja E, Adan J, Pagan R, et al. Anti-migratory and anti-angiogenic effect of p16: a novel localization at membrane ruffles and lamellipodia in endothelial cells. Angiogenesis 2004;7(4):323-33
  • Andrews MJ, McInnes C, Kontopidis G, et al. Design, synthesis, biological activity and structural analysis of cyclic peptide inhibitors targeting the substrate recruitment site of cyclin-dependent kinase complexes. Org Biomol Chem 2004;2(19):2735-41
  • Gondeau C, Gerbal-Chaloin S, Bello P, et al. Design of a novel class of peptide inhibitors of cyclin-dependent kinase/cyclin activation. J Biol Chem 2005;280(14):13793-800
  • Adams PD, Sellers WR, Sharma SK, et al. Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol Cell Biol 1996;16(12):6623-33
  • Chen YN, Sharma SK, Ramsey TM, et al. Selective killing of transformed cells by cyclin/cyclin-dependent kinase 2 antagonists. Proc Natl Acad Sci USA 1999;96(8):4325-9
  • Adams PD, Li X, Sellers WR, et al. Retinoblastoma protein contains a C-terminal motif that targets it for phosphorylation by cyclin-cdk complexes. Mol Cell Biol 1999;19(2):1068-80
  • Staal SP. Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc Natl Acad Sci USA 1987;84(14):5034-7
  • Bellacosa A, Testa JR, Staal SP, et al. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 1991;254(5029):274-7
  • Franke TF, Kaplan DR, Cantley LC, et al. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 1997;275(5300):665-8
  • del Peso L, Gonzalez-Garcia M, Page C, et al. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997;278(5338):687-9
  • Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997;91(2):231-41
  • Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282(5392):1318-21
  • Barkett M, Gilmore TD. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 1999;18(49):6910-24
  • Lutz RJ. Role of the BH3 (Bcl-2 homology 3) domain in the regulation of apoptosis and Bcl-2-related proteins. Biochem Soc Trans 2000;28(2):51-6
  • Laine J, Kunstle G, Obata T, et al. The protooncogene TCL1 is an Akt kinase coactivator. Mol Cell 2000;6(2):395-407
  • Hiromura M, Okada F, Obata T, et al. Inhibition of Akt kinase activity by a peptide spanning the betaA strand of the proto-oncogene TCL1. J Biol Chem 2004;279(51):53407-18
  • Luo Y, Smith RA, Guan R, et al. Pseudosubstrate peptides inhibit Akt and induce cell growth inhibition. Biochemistry 2004;43(5):1254-63
  • Sedlak TW, Oltvai ZN, Yang E, et al. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 1995;92(17):7834-8
  • Diaz JL, Oltersdorf T, Horne W, et al. A common binding site mediates heterodimerization and homodimerization of Bcl-2 family members. J Biol Chem 1997;272(17):11350-5
  • Sattler M, Liang H, Nettesheim D, et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 1997;275(5302):983-6
  • Cosulich SC, Worrall V, Hedge PJ, et al. Regulation of apoptosis by BH3 domains in a cell-free system. Curr Biol 1997;7(12):913-20
  • Holinger EP, Chittenden T, Lutz RJ. Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c-independent activation of caspases. J Biol Chem 1999;274(19):13298-304
  • Yajima H, Suzuki F. Identification of a Bcl-XL binding region within the ATPase domain of Apaf-1. Biochem Biophys Res Commun 2003;309(3):520-7
  • Conus S, Rosse T, Borner C. Failure of Bcl-2 family members to interact with Apaf-1 in normal and apoptotic cells. Cell Death Differ 2000;7(10):947-54
  • Finnegan NM, Curtin JF, Prevost G, et al. Induction of apoptosis in prostate carcinoma cells by BH3 peptides which inhibit Bak/Bcl-2 interactions. Br J Cancer 2001;85(1):115-21
  • Walsh M, Lutz RJ, Cotter TG, et al. Erythrocyte survival is promoted by plasma and suppressed by a Bak-derived BH3 peptide that interacts with membrane-associated Bcl-X(L). Blood 2002;99(9):3439-48
  • Brewis ND, Phelan A, Normand N, et al. Particle assembly incorporating a VP22-BH3 fusion protein, facilitating intracellular delivery, regulated release, and apoptosis. Mol Ther 2003;7(2):262-70
  • Kinoshita M, Hynynen K. Intracellular delivery of Bak BH3 peptide by microbubble-enhanced ultrasound. Pharm Res 2005;22(5):716-20
  • Dharap SS, Minko T. Targeted proapoptotic LHRH-BH3 peptide. Pharm Res 2003;20(6):889-96
  • Dharap SS, Qiu B, Williams GC, et al. Molecular targeting of drug delivery systems to ovarian cancer by BH3 and LHRH peptides. J Control Release 2003;91(1-2):61-73
  • Dharap SS, Chandna P, Wang Y, et al. Molecular targeting of BCL2 and BCLXL proteins by synthetic BCL2 homology 3 domain peptide enhances the efficacy of chemotherapy. J Pharmacol Exp Ther 2006;316(3):992-8
  • Li R, Boehm AL, Miranda MB, et al. Targeting antiapoptotic Bcl-2 family members with cell-permeable BH3 peptides induces apoptosis signaling and death in head and neck squamous cell carcinoma cells. Neoplasia 2007;9(10):801-11
  • Lama D, Sankararamakrishnan R. Anti-apoptotic Bcl-XL protein in complex with BH3 peptides of pro-apoptotic Bak, Bad, and Bim proteins: comparative molecular dynamics simulations. Proteins 2008;73(2):492-514
  • Narita M, Shimizu S, Ito T, et al. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 1998;95(25):14681-6
  • Polster BM, Kinnally KW, Fiskum G. BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J Biol Chem 2001;276(41):37887-94
  • Moreau C, Cartron PF, Hunt A, et al. Minimal BH3 peptides promote cell death by antagonizing anti-apoptotic proteins. J Biol Chem 2003;278(21):19426-35
  • Shangary S, Oliver CL, Tillman TS, et al. Sequence and helicity requirements for the proapoptotic activity of Bax BH3 peptides. Mol Cancer Ther 2004;3(11):1343-54
  • Kelekar A, Chang BS, Harlan JE, et al. Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol Cell Biol 1997;17(12):7040-6
  • Ottilie S, Diaz JL, Horne W, et al. Dimerization properties of human BAD. Identification of a BH-3 domain and analysis of its binding to mutant BCL-2 and BCL-XL proteins. J Biol Chem 1997;272(49):30866-72
  • Wang JL, Zhang ZJ, Choksi S, et al. Cell permeable Bcl-2 binding peptides: a chemical approach to apoptosis induction in tumor cells. Cancer Res 2000;60(6):1498-502
  • Schimmer AD, Hedley DW, Chow S, et al. The BH3 domain of BAD fused to the Antennapedia peptide induces apoptosis via its alpha helical structure and independent of Bcl-2. Cell Death Differ 2001;8(7):725-33
  • Goldsmith KC, Liu X, Dam V, et al. BH3 peptidomimetics potently activate apoptosis and demonstrate single agent efficacy in neuroblastoma. Oncogene 2006;25(33):4525-33
  • Kashiwagi H, McDunn JE, Goedegebuure PS, et al. TAT-Bim induces extensive apoptosis in cancer cells. Ann Surg Oncol 2007;14(5):1763-71
  • Walensky LD, Kung AL, Escher I, et al. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 2004;305(5689):1466-70
  • Oh KJ, Barbuto S, Pitter K, et al. A membrane-targeted BID BCL-2 homology 3 peptide is sufficient for high potency activation of BAX in vitro. J Biol Chem 2006;281(48):36999-7008
  • Walensky LD, Pitter K, Morash J, et al. A stapled BID BH3 helix directly binds and activates BAX. Mol Cell 2006;24(2):199-210
  • Chai J, Du C, Wu JW, et al. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000;406(6798):855-62
  • Wu G, Chai J, Suber TL, et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000;408(6815):1008-12
  • Fulda S, Wick W, Weller M, et al. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002;8(8):808-15
  • Arnt CR, Chiorean MV, Heldebrant MP, et al. Synthetic Smac/DIABLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ. J Biol Chem 2002;277(46):44236-43
  • Yang L, Mashima T, Sato S, et al. Predominant suppression of apoptosome by inhibitor of apoptosis protein in non-small cell lung cancer H460 cells: therapeutic effect of a novel polyarginine-conjugated Smac peptide. Cancer Res 2003;63(4):831-7
  • Heckl S, Sturzu A, Regenbogen M, et al. A novel polyarginine containing Smac peptide conjugate that mediates cell death in tumor and healthy cells. Med Chem 2008;4(4):348-54
  • Li L, Thomas RM, Suzuki H, et al. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science 2004;305(5689):1471-4
  • Mizukawa K, Kawamura A, Sasayama T, et al. Synthetic Smac peptide enhances the effect of etoposide-induced apoptosis in human glioblastoma cell lines. J Neurooncol 2006;77(3):247-55
  • Sun Y, Ottosson A, Pervaiz S, et al. Smac-mediated sensitization of human B-lymphoma cells to staurosporine- and lactacystin-triggered apoptosis is apoptosome-dependent. Leukemia 2007;21(5):1035-43
  • Fandy TE, Shankar S, Srivastava RK. Smac/DIABLO enhances the therapeutic potential of chemotherapeutic drugs and irradiation, and sensitizes TRAIL-resistant breast cancer cells. Mol Cancer 2008;7:60
  • Fotin-Mleczek M, Welte S, Mader O, et al. Cationic cell-penetrating peptides interfere with TNF signalling by induction of TNF receptor internalization. J Cell Sci 2005;118(Pt 15):3339-51
  • Kim D, Jeon C, Kim JH, et al. Cytoplasmic transduction peptide (CTP): new approach for the delivery of biomolecules into cytoplasm in vitro and in vivo. Exp Cell Res 2006;312(8):1277-88
  • Gao Z, Tian Y, Wang J, et al. A dimeric Smac/diablo peptide directly relieves caspase-3 inhibition by XIAP. Dynamic and cooperative regulation of XIAP by Smac/Diablo. J Biol Chem 2007;282(42):30718-27
  • Abhari BA, Davoodi J. A mechanistic insight into SMAC peptide interference with XIAP-Bir2 inhibition of executioner caspases. J Mol Biol 2008;381(3):645-54
  • Nikolovska-Coleska Z, Meagher JL, Jiang S, et al. Design and characterization of bivalent Smac-based peptides as antagonists of XIAP and development and validation of a fluorescence polarization assay for XIAP containing both BIR2 and BIR3 domains. Anal Biochem 2008;374(1):87-98
  • Schmaljohann D. Thermo- and pH-responsive polymers in drug delivery. Adv Drug Deliv Rev 2006;58(15):1655-70
  • Raucher D, Massodi I, Bidwell GL. Thermally targeted delivery of chemotherapeutics and anti-cancer peptides by elastin-like polypeptide. Expert Opin Drug Deliv 2008;5(3):353-69
  • Lu ZR, Shiah JG, Sakuma S, et al. Design of novel bioconjugates for targeted drug delivery. J Control Release 2002;78(1-3):165-73
  • Sudimack J, Lee RJ. Targeted drug delivery via the folate receptor. Adv Drug Deliv Rev 2000;41(2):147-62
  • Laakkonen P, Zhang L, Ruoslahti E. Peptide targeting of tumor lymph vessels. Ann NY Acad Sci 2008;1131:37-43
  • Karmali PP, Kotamraju VR, Kastantin M, et al. Targeting of albumin-embedded paclitaxel nanoparticles to tumors. Nanomedicine 2009;5(1):73-82
  • Vives E, Schmidt J, Pelegrin A. Cell-penetrating and cell-targeting peptides in drug delivery. Biochim Biophys Acta 2008;1786(2):126-38
  • Heitz F, Morris MC, Divita G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 2009;157(2):195-206
  • Schwarze SR, Ho A, Vocero-Akbani A, et al. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999;285(5433):1569-72

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