An unusual cell penetrating peptide identified using a plasmid display-based functional selection platform

ACS Chemical Biology

Volumn 6, Issue 5, 2011, Pages 484-491

  Gao, Shan ^a,b   Simon, Melissa J ^a   Hue, Christopher D ^a   Morrison, Barclay ^a   Banta, Scott ^a  

^a Columbia University ^*  (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; CELL PENETRATING PEPTIDE; DNA; GREEN FLUORESCENT PROTEIN; LIPOFECTAMINE; PEPTIDE LIBRARY; PLASMID VECTOR; PROTEIN BAK; SG3 PEPTIDE; TAT PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ASTROCYTE; CELL DEATH; CELL STRAIN; CONFERENCE PAPER; CONTROLLED STUDY; DISPLAY SYSTEM; DNA SEQUENCE; GENETIC ENGINEERING; MOLECULAR LIBRARY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PLASMID DISPLAY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN TRANSPORT; RAT;

ANIMALS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CELL-PENETRATING PEPTIDES; GREEN FLUORESCENT PROTEINS; HEPARIN; LIPIDS; PC12 CELLS; PEPTIDE LIBRARY; PLASMIDS; RATS;

EID: 79957454873     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb100423u     Document Type: Conference Paper

References (51)

1. Dietz, G. P. and Bahr, M. (2004) Delivery of bioactive molecules into the cell: the Trojan horse approach Mol. Cell. Neurosci. 27, 85-131 (Pubitemid 39370094)
2. Torchilin, V. P. (2008) Tat peptide-mediated intracellular delivery of pharmaceutical nanocarriers Adv. Drug Delivery Rev. 60, 548-558 (Pubitemid 351215572)
3. Joliot, A. and Prochiantz, A. (2004) Transduction peptides: from technology to physiology Nat. Cell Biol. 6, 189-196 (Pubitemid 38344356)
4. Zorko, M. and Langel, U. (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery Adv. Drug Delivery Rev. 57, 529-545 (Pubitemid 40255559)
5. Deshayes, S., Morris, M. C., Divita, G., and Heitz, F. (2005) Cell-penetrating peptides: tools for intracellular delivery of therapeutics Cell. Mol. Life Sci. 62, 1839-1849 (Pubitemid 41188523)
6. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) In Vivo protein transduction: delivery of a biologically active protein into the mouse Science 285, 1569-1572 (Pubitemid 29420581)
7. Vives, E. (2005) Present and future of cell-penetrating peptide mediated delivery systems: "Is the Trojan horse too wild to go only to Troy? J. Controlled Release 109, 77-85 (Pubitemid 41737254)
8. Trehin, R. and Merkle, H. P. (2004) Chances and pitfalls of cell penetrating peptides for cellular drug delivery Eur. J. Pharm. Biopharm. 58, 209-223 (Pubitemid 39037230)
9. Chauhan, A., Tikoo, A., Kapur, A. K., and Singh, M. (2007) The taming of the cell penetrating domain of the HIV Tat: Myths and realities J. Controlled Release 117, 148-162 (Pubitemid 46172502)
10. Duchardt, F., Fotin-Mleczek, M., Schwarz, H., Fischer, R., and Brock, R. (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides Traffic 8, 848-866 (Pubitemid 46971632)
11. Poon, G. M. and Gariepy, J. (2007) Cell-surface proteoglycans as molecular portals for cationic peptide and polymer entry into cells Biochem. Soc. Trans. 35, 788-793 (Pubitemid 47310369)
12. Tyagi, M., Rusnati, M., Presta, M., and Giacca, M. (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans J. Biol. Chem. 276, 3254-3261
13. Vives, E. (2003) Cellular uptake [correction of utake] of the Tat peptide: an endocytosis mechanism following ionic interactions J. Mol. Recognit. 16, 265-271 (Pubitemid 37231695)
14. Bugatti, A., Urbinati, C., Ravelli, C., De Clercq, E., Liekens, S., and Rusnati, M. (2007) Heparin-mimicking sulfonic acid polymers as multitarget inhibitors of human immunodeficiency virus type 1 Tat and gp120 proteins Antimicrob. Agents Chemother. 51, 2337-2345 (Pubitemid 47047308)
15. Kumarasuriyar, A., Dombrowski, C., Rider, D. A., Nurcombe, V., and Cool, S. M. (2007) A novel use of TAT-EGFP to validate techniques to alter osteosarcoma cell surface glycosaminoglycan expression J. Mol. Histol. 38, 435-447 (Pubitemid 350056779)
16. Nakase, I., Tadokoro, A., Kawabata, N., Takeuchi, T., Katoh, H., Hiramoto, K., Negishi, M., Nomizu, M., Sugiura, Y., and Futaki, S. (2007) Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46, 492-501 (Pubitemid 46105438)
17. 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 (Pubitemid 38667624)
18. Simon, M. J., Gao, S., Kang, W. H., Banta, S., and Morrison, B., 3rd (2009) TAT-mediated intracellular protein delivery to primary brain cells is dependent on glycosaminoglycan expression Biotechnol. Bioeng. 104, 10-19
19. Warda, M., Toida, T., Zhang, F., Sun, P., Munoz, E., Xie, J., and Linhardt, R. J. (2006) Isolation and characterization of heparan sulfate from various murine tissues Glycoconjugate J. 23, 555-563 (Pubitemid 44477397)
20. David, G. (1993) Integral membrane heparan sulfate proteoglycans FASEB J. 7, 1023-1030 (Pubitemid 23243444)
21. Ruoslahti, E. (2002) Drug targeting to specific vascular sites Drug Discovery Today 7, 1138-1143 (Pubitemid 35346421)
22. Ruoslahti, E. and Rajotte, D. (2000) An address system in the vasculature of normal tissues and tumors Annu. Rev. Immunol. 18, 813-827 (Pubitemid 30365398)
23. Kolonin, M. G., Sun, J., Do, K. A., Vidal, C. I., Ji, Y., Baggerly, K. A., Pasqualini, R., and Arap, W. (2006) Synchronous selection of homing peptides for multiple tissues by In Vivo phage display FASEB J. 20, 979-981
24. Pasqualini, R. and Ruoslahti, E. (1996) Organ targeting In Vivo using phage display peptide libraries Nature 380, 364-366 (Pubitemid 26097120)
25. Sheng, J., Oyler, G., Zhou, B., Janda, K., and Shoemaker, C. B. (2009) Identification and characterization of a novel cell-penetrating peptide Biochem. Biophys. Res. Commun. 382, 236-240
26. Kamada, H., Okamoto, T., Kawamura, M., Shibata, H., Abe, Y., Ohkawa, A., Nomura, T., Sato, M., Mukai, Y., Sugita, T., Imai, S., Nagano, K., Tsutsumi, Y., Nakagawa, S., Mayumi, T., and Tsunoda, S. (2007) Creation of novel cell-penetrating peptides for intracellular drug delivery using systematic phage display technology originated from Tat transduction domain Biol. Pharm. Bull. 30, 218-223
27. Shadidi, M. and Sioud, M. (2003) Identification of novel carrier peptides for the specific delivery of therapeutics into cancer cells FASEB J. 17, 256-258
28. Lin, H. and Cornish, V. W. (2002) Screening and selection methods for large-scale analysis of protein function Angew. Chem., Int. Ed. 41, 4402-4425 (Pubitemid 35462383)
29. Doi, N. and Yanagawa, H. (2001) Genotype-phenotype linkage for directed evolution and screening of combinatorial protein libraries Comb. Chem. High Throughput Screening 4, 497-509 (Pubitemid 32808065)
30. Speight, R. E., Hart, D. J., Sutherland, J. D., and Blackburn, J. M. (2001) A new plasmid display technology for the in vitro selection of functional phenotype-genotype linked proteins Chem. Biol. 8, 951-965 (Pubitemid 32918925)
31. Choi, Y. S., Pack, S. P., and Yoo, Y. J. (2005) Development of a plasmid display system using GAL4 DNA binding domain for the in vitro screening of functional proteins Biotechnol. Lett. 27, 1707-1711 (Pubitemid 41507180)
32. Cull, M. G., Miller, J. F., and Schatz, P. J. (1992) Screening for receptor ligands using large libraries of peptides linked to the C-terminus of the Lac repressor Proc. Natl. Acad. Sci. U.S.A. 89, 1865-1869
33. Gao, S., Simon, M. J., Morrison, B., 3rd, and Banta, S. (2010) A plasmid display platform for the selection of peptides exhibiting a functional cell-penetrating phenotype Biotechnol. Prog. 26, 1796-1800
34. Endoh, T. and Ohtsuki, T. (2009) Cellular siRNA delivery using cell-penetrating peptides modified for endosomal escape Adv. Drug Delivery Rev. 61, 704-709
35. Magzoub, M., Pramanik, A., and Graslund, A. (2005) Modeling the endosomal escape of cell-penetrating peptides: Transmembrane pH gradient driven translocation across phospholipid bilayers Biochemistry 44, 14890-14897 (Pubitemid 41612268)
36. Gao, K. and Huang, L. (2009) Nonviral methods for siRNA delivery Mol. Pharmaceutics 6, 651-658
37. Kilk, K., El-Andaloussi, S., Jarver, P., Meikas, A., Valkna, A., Bartfai, T., Kogerman, P., Metsis, M., and Langel, U. (2005) Evaluation of transportan 10 in PEI mediated plasmid delivery assay J. Controlled Release 103, 511-523 (Pubitemid 40342545)
38. Gao, S., Simon, M. J., Morrison, B., 3rd, and Banta, S. (2009) Bifunctional chimeric fusion proteins engineered for DNA delivery: optimization of the protein to DNA ratio Biochim. Biophys. Acta 1790, 198-207
39. Yezid, H., Konate, K., Debaisieux, S., Bonhoure, A., and Beaumelle, B. (2009) Mechanism for HIV-1 Tat insertion into the endosome membrane J. Biol. Chem. 284, 22736-22746
40. Herce, H. D. and Garcia, A. E. (2007) Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes Proc. Natl. Acad. Sci. U.S.A. 104, 20805-20810
41. Thoren, P. E., Persson, D., Esbjorner, E. K., Goksor, M., Lincoln, P., and Norden, B. (2004) Membrane binding and translocation of cell-penetrating peptides Biochemistry 43, 3471-3489 (Pubitemid 38391703)
42. Holinger, E. P., Chittenden, T., and Lutz, R. J. (1999) Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c-independent activation of caspases J. Biol. Chem. 274, 13298-13304
43. Liu, Y., Li, Y., Wang, H., Yu, J., Lin, H., Xu, D., Wang, Y., Liang, A., Liang, X., Zhang, X., Fu, M., Qian, H., and Lin, C. (2009) BH3-based fusion artificial peptide induces apoptosis and targets human colon cancer Mol. Ther. 17, 1509-1516
44. Li, N., Lin, P., Cai, C., Pan, Z., Weisleder, N., and Ma, J. (2009) The amino-terminal peptide of Bax perturbs intracellular Ca2+ homeostasis to enhance apoptosis in prostate cancer cells Am. J. Physiol. Cell Physiol. 296, C267-272
45. Kumar, P., Wu, H., McBride, J. L., Jung, K. E., Kim, M. H., Davidson, B. L., Lee, S. K., Shankar, P., and Manjunath, N. (2007) Transvascular delivery of small interfering RNA to the central nervous system Nature 448, 39-43 (Pubitemid 47037001)
46. El-Andaloussi, S., Johansson, H. J., Holm, T., and Langel, U. (2007) A novel cell-penetrating peptide, M918, for efficient delivery of proteins and peptide nucleic acids Mol. Ther. 15, 1820-1826 (Pubitemid 47434189)
47. Eguchi, A., Meade, B. R., Chang, Y. C., Fredrickson, C. T., Willert, K., Puri, N., and Dowdy, S. F. (2009) Efficient siRNA delivery into primary cells by a peptide transduction domain-dsRNA binding domain fusion protein Nat. Biotechnol. 27, 567-571
48. Crombez, L., Aldrian-Herrada, G., Konate, K., Nguyen, Q. N., McMaster, G. K., Brasseur, R., Heitz, F., and Divita, G. (2009) A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells Mol. Ther. 17, 95-103
49. Eiriksdottir, E., Konate, K., Langel, U., Divita, G., and Deshayes, S. (2010) Secondary structure of cell-penetrating peptides controls membrane interaction and insertion Biochim. Biophys. Acta 1798, 1119-1128
50. Combet, C., Blanchet, C., Geourjon, C., and Deleage, G. (2000) NPS@: network protein sequence analysis Trends Biochem. Sci. 25, 147-150 (Pubitemid 30122428)
51. Hart, D. J., Speight, R. E., Cooper, M. A., Sutherland, J. D., and Blackburn, J. M. (1999) The salt dependence of DNA recognition by NF-kappaB p50: a detailed kinetic analysis of the effects on affinityand specificity Nucleic Acids Res. 27, 1063-1069 (Pubitemid 29209510)