Characterisation of cell-penetrating peptide-mediated peptide delivery

British Journal of Pharmacology

Volumn 145, Issue 8, 2005, Pages 1093-1102

  Jones, Simon W ^a   Christison, Richard ^a   Bundell, Ken ^a   Voyce, Catherine J ^a   Brockbank, Sarah M V ^a   Newham, Peter ^a   Lindsay, Mark A ^b  

^a ASTRAZENECA   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Antennapedia; Polyarginine; Protein transduction domain; TAT; Transportan

Indexed keywords

ANTENNAPEDIA PROTEIN; CHOLERA TOXIN; CLATHRIN; POLYARGININE; PROTEIN KINASE INHIBITOR; TRANSACTIVATOR PROTEIN; TRANSFERRIN; TRANSPORTAN; UNCLASSIFIED DRUG;

ARTICLE; CELL TYPE; CELLULAR DISTRIBUTION; CONJUGATE; CYTOTOXICITY; DRUG ACTIVITY; DRUG DELIVERY SYSTEM; DRUG MECHANISM; DRUG UPTAKE; ENDOCYTOSIS; FLUORESCENCE ACTIVATED CELL SORTING; HELA CELL; HUMAN; HUMAN CELL; LIPID RAFT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CELL COUNT; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL SURVIVAL; CHO CELLS; CRICETINAE; DRUG CARRIERS; ENDOCYTOSIS; GALANIN; GENE PRODUCTS, TAT; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDES; RECOMBINANT FUSION PROTEINS; WASP VENOMS;

EID: 27644561216     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706279     Document Type: Article

References (49)

1. AARTS, M., LIU, Y., LIU, L., BESSHOH, S., ARUNDINE, M., GURD, J.W., WANG, Y.T., SALTER, M.W. & TYMIANSKI, M. (2002). Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science, 298, 846-850.
2. ASOH, S., OHSAWA, I., MORI, T., KATSURA, K., HIRAIDE, T., KATAYAMA, Y., KIMURA, M., OZAKI, D., YAMAGATA, K. & OHTA, S. (2002). Protection against ischemic brain injury by protein therapeutics. Proc. Natl. Acad. Sci. U.S.A., 99, 17107-17112.
3. BORSELLO, T., CLARKE, P.G., HIRT, L., VERCELLI, A., REPICI, M., SCHORDERET, D.F., BOGOUSSLAVSKY, J. & BONNY, C. (2003). A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med., 9, 1180-1186.
4. BUCCI, M., GRATTON, J.P., RUDIC, R.D., ACEVEDO, L., ROVIEZZO, F., CIRINO, G. & SESSA, W.C. (2000). In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat. Med., 6, 1362-1367.
5. CAO, G., PEI, W., GE, H., LIANG, Q., LUO, Y., SHARP, F.R., LU, A., RAN, R., GRAHAM, S.H. & CHEN, J. (2002). In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci., 22, 5423-5431.
6. CONSOLE, S., MARTY, C., GARCIA-ECHEVERRIA, C., SCHWENDENER, R. & BALLMER-HOFER, K. (2003). 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., 278, 35109-35114.
7. DAVID, G. (1993). Integral membrane heparan sulfate proteoglycans. FASEB J., 7, 1023-1030.
8. DEROSSI, D., CALVET, S., TREMBLEAU, A., BRUNISSEN, A., CHASSAING, G. & PROCHIANTZ, A. (1996). Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem., 271, 18188-18193.
9. DIETZ, G.P., KILIC, E. & BAHR, M. (2002). Inhibition of neuronal apoptosis in vitro and in vivo using TAT-mediated protein transduction. Mol. Cell. Neurosci., 21, 29-37.
10. FERRARI, A., PELLEGRINI, V., ARCANGELI, C., FITTIPALDI, A., GIACCA, M. & BELTRAM, F. (2003). Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol. Ther., 8, 284-294.
11. FITTIPALDI, A., FERRARI, A., ZOPPE, M., ARCANGELI, C., PELLEGRINI, V., BELTRAM, F. & GIACCA, M. (2003). Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem., 278, 34141-34149.
12. FRANKEL, A.D. & PABO, C.O. (1988). Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 55, 1189-1193.
13. FUJIMOTO, K., HOSOTANI, R., MIYAMOTO, Y., DOI, R., KOSHIBA, T., OTAKA, A., FUJII, N., BEAUCHAMP, R.D. & IMAMURA, M. (2000). Inhibition of pRb phosphorylation and cell cycle progression by an antennapedia-p16(INK4A) fusion peptide in pancreatic cancer cells. Cancer Lett., 159, 151-158.
14. GLASS, D.B., LUNDQUIST, L.J., KATZ, B.M. & WALSH, D.A. (1989). Protein kinase inhibitor-(6-22)-amide peptide analogs with standard and nonstandard amino acid substitutions for phenylalanine 10. Inhibition of cAMP-dependent protein kinase. J. Biol. Chem., 264, 14579-14584.
15. GRASSEL, S., COHEN, I.R., MURDOCH, A.D., EICHSTETTER, I. & IOZZO, R.V. (1995). The proteoglycan perlecan is expressed in the erythroleukemia cell line K562 and is upregulated by sodium butyrate and phorbol ester. Mol. Cell. Biochem., 145, 61-68.
16. GRATTON, J.P., LIN, M.I., YU, J., WEISS, E.D., JIANG, Z.L., FAIRCHILD, T.A., IWAKIRI, Y., GROSZMANN, R., CLAFFEY, K.P., CHENG, Y.C. & SESSA, W.C. (2003). Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell, 4, 31-39.
17. GREEN, I., CHRISTISON, R., VOYCE, C.J., BUNDELL, K.R. & LINDSAY, M.A. (2003). Protein transduction domains: are they delivering? Trends Pharmacol. Sci., 24, 213-215.
18. GREEN, M. & LOEWENSTEIN, P.M. (1988). Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell, 55, 1179-1188.
19. HOSOTANI, R., MIYAMOTO, Y., FUJIMOTO, K., DOI, R., OTAKA, A., FUJII, N. & IMAMURA, M. (2002). Trojan p16 peptide suppresses pancreatic cancer growth and prolongs survival in mice. Clin. Cancer Res., 8, 1271-1276.
20. JACOBSON, G.M., DOURRON, H.M., LIU, J., CARRETERO, O.A., REDDY, D.J., ANDRZEJEWSKI, T. & PAGANO, P.J. (2003). Novel NAD(P)H oxidase inhibitor suppresses angioplasty-induced superoxide and neointimal hyperplasia of rat carotid artery. Circ. Res., 92, 637-643.
21. JIMI, E., AOKI, K., SAITO, H., D'ACQUISTO, F., MAY, M.J., NAKAMURA, I., SUDO, T., KOJIMA, T., OKAMOTO, F., FUKUSHIMA, H., OKABE, K., OHYA, K. & GHOSH, S. (2004). Selective inhibition of NF-kappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat. Med., 10, 617-624.
22. JIN, L.H., BAHN, J.H., EUM, W.S., KWON, H.Y., JANG, S.H., HAN, K.H., KANG, T.C., WON, M.H., KANG, J.H., CHO, S.W., PARK, J. & CHOI, S.Y. (2001). Transduction of human catalase mediated by an HIV-1 TAT protein basic domain and arginine-rich peptides into mammalian cells. Free Radic. Biol. Med., 31, 1509-1519.
23. KILIC, E., DIETZ, G.P., HERMANN, D.M. & BAHR, M. (2002). Intravenous TAT-Bcl-Xl is protective after middle cerebral artery occlusion in mice. Ann. Neurol., 52, 617-622.
24. KILIC, U., KILIC, E., DIETZ, G.P. & BAHR, M. (2003). Intravenous TAT-GDNF is protective after focal cerebral ischemia in mice. Stroke, 34, 1304-1310.
25. KWON, H.Y., EUM, W.S., JANG, H.W., KANG, J.H., RYU, J., RYONG, L.B., JIN, L.H., PARK, J. & CHOI, S.Y. (2000). Transduction of Cu, Zn-superoxide dismutase mediated by an HIV-1 Tat protein basic domain into mammalian cells. FEBS Lett., 485, 163-167.
26. LINDGREN, M., HALLBRINK, M., PROCHIANTZ, A. & LANGEL, U. (2000). Cell-penetrating peptides. Trends Pharmacol. Sci., 21, 99-103.
27. LINDSAY, M.A. (2002). Peptide-mediated cell delivery: application in protein target validation. Curr. Opin. Pharmacol., 2, 587-594.
28. MATSUI, H., TOMIZAWA, K. & MATSUSHITA, M. (2003). Protein transduction by poly-arginine. Nippon Yakurigaku Zasshi, 121, 435-439.
29. MAY, M.J., D'ACQUISTO, F., MADGE, L.A., GLOCKNER, J., POBER, J.S. & GHOSH, S. (2000). Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science, 289, 1550-1554.
30. MYOU, S., LEFF, A.R., MYO, S., BOETTICHER, E., TONG, J.K., MELITON, A.Y., LIU, J., MUNOZ, N.M. & ZHU, X.D. (2003a). Blockade of inflammation and airway hyperresponsiveness in immune-sensitized mice by dominant-negative phosphoinositide 3-kinase-TAT. J. Exp. Med., 198, 1573-1582.
31. MYOU, S., ZHU, X.D., MYO, S., BOETTICHER, E., MELITON, A.Y., LIU, J., MUNOZ, N.M. & LEFF, A.R. (2003b). Blockade of airway inflammation and hyperresponsiveness by HIV-TAT-dominant negative Ras. J. Immunol., 171, 4379-4384.
32. NICHOLS, B.J., KENWORTHY, A.K., POLISHCHUK, R.S., LODGE, R., ROBERTS, T.H., HIRSCHBERG, K., PHAIR, R.D. & LIPPINCOTT-SCHWARTZ, J. (2001). Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell. Biol., 153, 529-541.
33. POOGA, M., KUT, C., KIHLMARK, M., HALLBRINK, M., FERNAEUS, S., RAID, R., LAND, T., HALLBERG, E., BARTFAI, T. & LANGEL, U. (2001). Cellular translocation of proteins by transportan. FASEB J., 15, 1451-1453.
34. REHMAN, K.K., BERTERA, S., BOTTINO, R., BALAMURUGAN, A.N., MAI, J.C., MI, Z., TRUCCO, M. & ROBBINS, P.D. (2003). Protection of islets by in situ peptide-mediated transduction of the Ikappa B kinase inhibitor Nemo-binding domain peptide. J. Biol. Chem., 278, 9862-9868.
35. REY, F.E., CIFUENTES, M.E., KIARASH, A., QUINN, M.T. & PAGANO, P.J. (2001). Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ. Res., 89, 408-414.
36. RICHARD, J.P., MELIKOV, K., VIVES, E., RAMOS, C., VERBEURE, B., GAIT, M.J., CHERNOMORDIK, L.V. & LEBLEU, B. (2003). Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem., 278, 585-590.
37. RUSNATI, M., TULIPANO, G., SPILLMANN, D., TANGHETTI, E., ORESTE, P., ZOPPETTI, G., GIACCA, M. & PRESTA, M. (1999). Multiple interactions of HIV-I Tat protein with size-defined heparin oligosaccharides. J. Biol. Chem., 274, 28198-28205.
38. RUSNATI, M., TULIPANO, G., URBINATI, C., TANGHETTI, E., GIULIANI, R., GIACCA, M., CIOMEI, M., CORALLINI, A. & PRESTA, M. (1998). The basic domain in HIV-1 Tat protein as a target for polysulfonated heparin-mimicking extracellular Tat antagonists. J. Biol. Chem., 273, 16027-16037.
39. RUSNATI, M., URBINATI, C., CAPUTO, A., POSSATI, L., LORTAT-JACOB, H., GIACCA, M., RIBATTI, D. & PRESTA, M. (2001). Pentosan polysulfate as an inhibitor of extracellular HIV-1 Tat. J. Biol. Chem., 276, 22420-22425.
40. SCHMID, S.L. (1997). Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem., 66, 511-548.
41. SILHOL, M., TYAGI, M., GIACCA, M., LEBLEU, B. & VIVES, E. (2002). Different mechanisms for cellular internalization of the HIV-1 Tat-derived cell penetrating peptide and recombinant proteins fused to Tat. Eur. J. Biochem., 269, 494-501.
42. SNYDER, E.L., MEADE, B.R., SAENZ, C.C. & DOWDY, S.F. (2004). Treatment of terminal peritoneal carcinomatosis by a transducible p53-activating peptide. PLoS Biol., 2, E36.
43. SUZUKI, T., FUTAKI, S., NIWA, M., TANAKA, S., UEDA, K. & SUGIURA, Y. (2002). Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem., 277, 2437-2443.
44. THOREN, P.E., PERSSON, D., ISAKSON, P., GOKSOR, M., ONFELT, A. & NORDEN, B. (2003). Uptake of analogs of penetratin, Tat(48-60) and oligoarginine in live cells. Biochem. Biophys. Res. Commun., 307, 100-107.
45. TYAGI, M., RUSNATI, M., PRESTA, M. & GIACCA, M. (2001). Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem., 276, 3254-3261.
46. VENDEVILLE, A., RAYNE, F., BONHOURE, A., BETTACHE, N., MONTCOURRIER, P. & BEAUMELLE, B. (2004). HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses. Mol. Biol. Cell., 15, 2347-2360.
47. VIVES, E., BRODIN, P. & LEBLEU, B. (1997). A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem., 272, 16010-16017.
48. WADIA, J.S. & DOWDY, S.F. (2002). Protein transduction technology. Curr. Opin. Biotechnol., 13, 52-56.
49. WADIA, J.S., STAN, R.V. & DOWDY, S.F. (2004). Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med., 10, 310-315.