Bioportide: An emergent concept of bioactive cell-penetrating peptides

Cellular and Molecular Life Sciences

Volumn 69, Issue 17, 2012, Pages 2951-2966

  Howl, John ^a   Matou Nasri, Sabine ^b   West, David C ^c   Farquhar, Michelle ^d   Slaninová, Jiřina ^e   Östenson, Claes Göran ^f   Zorko, Matjaz ^g   Östlund, Pernilla ^h   Kumar, Shant ⁱ   Langel, Ülo ^h   McKeating, Jane ^d   Jones, Sarah ^a  

^a UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

^b MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^f KAROLINSKA INSTITUTE   (Sweden)

^g UNIVERSITY OF LJUBLJANA   (Slovenia)

^h STOCKHOLM UNIVERSITY   (Sweden)

ⁱ UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Angiogenesis; Bioportide; Camptide; Cell penetrating peptide; Insulin secretion; Nosangiotide; Second messenger; Viral infectivity

Indexed keywords

BIOPORTIDE; CALCITONIN RECEPTOR; CAMPTIDE; CELL PENETRATING PEPTIDE; CYCLIC AMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; NITRIC OXIDE; NOSANGIOTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL MOTION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CHORIOALLANTOIS; CONTROLLED STUDY; ENDOTHELIUM CELL; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INSULIN RELEASE; INTRACELLULAR SIGNALING; MALE; NONHUMAN; PANCREAS ISLET; QUANTITATIVE STRUCTURE ACTIVITY RELATION; RAT; VIRUS INFECTIVITY;

ANIMALS; AORTA; ASTROCYTOMA; BRAIN; CATTLE; CELL MEMBRANE PERMEABILITY; CELL-PENETRATING PEPTIDES; CELLS, CULTURED; CHEMOTAXIS; CHORIOALLANTOIC MEMBRANE; CYCLIC AMP; DERMIS; DIABETES MELLITUS, TYPE 2; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENDOTHELIUM, VASCULAR; FEMALE; HEPACIVIRUS; HEPATITIS C; HUMANS; INSULIN; ISLETS OF LANGERHANS; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN TRANSPORT; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; RATS; RATS, WISTAR; URINARY BLADDER NEOPLASMS; UTERINE CONTRACTION;

EID: 84864970396     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-0979-4     Document Type: Article

References (58)

1. Langel Ü (ed) (2011) Cell-penetrating peptides (Methods in molecular biology 683) Humana Press, New York
2. D Derossi AH Joliot G Chassaing A Prochiantz 1994 The third helix of the Antennapedia homeodomain translocates through biological membranes J Biol Chem 269 10444 10450 8144628 1:CAS:528:DyaK2cXlt1Oqt7Y%3D
3. E Vives P Brodin B Lebleau 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 9188504 10.1074/jbc.272.25.16010 1:CAS:528:DyaK2sXktFGnsb4%3D
4. M Pooga M Hällbrink M Zorko Ü Langel 1998 Cell penetration by transportan FASEB J 12 67 77 9438412 1:CAS:528:DyaK1cXktlKnsA%3D%3D
5. Deshayes S, Konate K, Aldrian G, Heitz F, Divita G (2011) Interactions of amphipathic CPPs with model membranes. In: Langel Ü (ed) Cell-penetrating peptides (Methods in Molecular Biology 683). Humana Press, New York, pp 41-56
6. WPR Verdurmen R Brock 2011 Biological responses towards cationic peptides and drug carriers Trends Pharamcol Sci 32 116 124 10.1016/j.tips.2010.11.005 1:CAS:528:DC%2BC3MXhsFyhur8%3D
7. S Jones C Martel A Belzacq-Casagrande C Brenner J Howl 2008 Mitoparan and target-selective chimeric analogues: membrane translocation and intracellular redistribution induces mitochondrial apoptosis Biochim Biophys Acta 1783 849 863 18267123 10.1016/j.bbamcr.2008.01.009 1:CAS:528:DC%2BD1cXkvVOgs7c%3D
8. S Jones T Holm I Mäger Ü Langel J Howl 2010 Characterisation of bioactive cell-penetrating peptides from cytochrome c: protein mimicry and the development of a novel apoptogenic agent Chem Biol 17 735 744 20659686 10.1016/j.chembiol.2010.05.018 1:CAS:528:DC%2BC3cXptleitLs%3D
9. P Portoghese 1989 Bivalent ligands and the message-address concept in the design of selective opioid receptor antagonists Trends Pharmacol Sci 10 230 235 2549665 10.1016/0165-6147(89)90267-8 1:CAS:528:DyaL1MXkslSisLk%3D
10. J Howl S Jones 2008 Proteomimetic cell-penetrating peptides Int J Pept Res Ther 14 359 366 10.1007/s10989-008-9135-2 1:CAS:528:DC%2BD1cXhsVKjt7rE
11. WAF1/CIP1 is pro-apoptogenic Peptides 28 731 740 17287047 10.1016/j.peptides.2006.12.013 1:CAS:528:DC%2BD2sXislGqsb0%3D
12. M Hällbrink K Kilk A Elmquist P Lundberg M Lindgren Y Jiang M Pooga U Soomets Ü Langel 2005 Prediction of cell-penetrating peptides Int J Pept Res Ther 11 249 259 10.1007/s10989-005-9393-1
13. M Hansen K Kilk Ü Langel 2007 Predicting cell-penetrating peptides Adv Drug Deliver Rev 60 572 579 10.1016/j.addr.2007.09.003
14. P Östlund K Kilk M Lindgren M Hällbrink Y Jiang M Budhina K Cerne A Bavec C-G Östenson M Zorko Ü Langel 2005 Cell-penetrating mimics of agonist-activated G-protein coupled receptors Int J Pept Res Ther 11 237 247 10.1007/s10989-005-9329-9
15. EE Moore RE Kuestener SD Stroop FJ Grant SL Matthewes CL Brady PM Sexton DM Findlay 1995 Functionally different isoforms of the human calcitonin receptor result from alternative splicing of the gene transcript Mol Endocrinol 9 959 968 7476993 10.1210/me.9.8.959 1:CAS:528:DyaK2MXnsVGku70%3D
16. M Aoyagi AS Arvai JA Tainer ED Getzoff 2003 Structural basis for endothelial nitric oxide synthase binding to calmodulin EMBO J 22 766 775 12574113 10.1093/emboj/cdg078 1:CAS:528:DC%2BD3sXit1yhu78%3D
17. P Ponten EH Macintyre 1968 Long term culture of normal and neoplastic human glia Acta Pathol Microbiol Scand 74 465 486 4313504 10.1111/j.1699-0463. 1968.tb03502.x 1:STN:280:DyaE3c7is1ektg%3D%3D
18. J Brown SJ Reading S Jones CJ Fitchett J Howl A Martin C Longland F Michelangeli YE Dubrova C Brown 2000 Critical evaluation of ECV304 as a human endothelial cell model determined by genetic analysis and functional responses: a comparison with the human bladder cancer derived epithelial cell line T24/83 Lab Invest 80 37 45 10653001 10.1038/labinvest.3780006 1:CAS:528: DC%2BD3cXhtVeqsrc%3D
19. KJ Blight JA McKeating CM Rice 2002 Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication J Virol 76 13001 13014 12438626 10.1128/JVI.76.24.13001-13014.2002 1:CAS:528:DC%2BD38XptVyns7Y%3D
20. BD Lindenbach MJ Evans AJ Syder B Wolk TL Tellinghuisen CC Liu T Maruyama RO Hynes DR Burton JA McKeating CM Rice 2005 Complete replication of hepatitis C virus in cell culture Science 309 623 626 15947137 10.1126/science.1114016 1:CAS:528:DC%2BD2MXmsFChtr4%3D
21. MJ Evans T von Hahn DM Tscherne AJ Syder M Panis B Wolk T Hatziioannou JA McKeating PD Bieniasz CM Rice 2007 Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry Nature 446 801 805 17325668 10.1038/nature05654 1:CAS:528:DC%2BD2sXktVeqtrs%3D
22. C-G Östenson S Efendic 2007 Islet gene expression and function in type 2 diabetes; studies in the Goto-Kakizaki rat and humans Diabetes Obes Metab 9 180 186 17919192 10.1111/j.1463-1326.2007.00787.x
23. J Howl RM Mondszein M Wheatley 1998 Characterization of G protein-coupled receptors expressed by ECV304 human endothelial cells Endothelium 6 23 32 9832330 10.3109/10623329809053402 1:CAS:528:DyaK1cXntVKhtrY%3D
24. P Holton 1948 A modification of the method of Dale and Lindlow for standardization of posterior pituitary extract Br J Pharmacol 3 328 334 1:STN:280:DyaH1M%2FitlCjsA%3D%3D
25. R Munsick 1960 Effect of magnesium ion on the response of the rat uterus to neurohypophysial hormones and analogues Endocrinology 66 451 457 10.1210/endo-66-3-451 1:CAS:528:DyaF3cXhtFWhsr8%3D
26. Slaninová J (1987) Fundamental biological evaluation. In: Lebl M, Jost K, Brtnik F (eds) Handbook of neurohypophyseal hormone analogs, vol I. CRC Press, Boca Raton, pp 83-107
27. J Dekanski 1952 The quantitative assay of vasopressin Br J Pharmacol 7 567 572 1:STN:280:DyaG3s%2FktlKgtw%3D%3D
28. MJ Farquhar HJ Harris S Jones SU Nielsen CL Brimacombe S Molina GL Toms P Maurel J Howl SVD van Ijzendoorn P Balfe A McKeating 2008 Protein kinase A dependent step(s) in hepatitis c virus entry and infectivity J Virol 82 8797 8811 18579596 10.1128/JVI.00592-08 1:CAS:528:DC%2BD1cXhtVClt7zF
29. West DC, Thompson WD, Sells PG, Burbridge MF (2001) Angiogenesis assays using the chick chorioallantoic membrane. In: Murray JC (ed) Methods in molecular medicine-angiogenesis: reviews and protocols. Humana Press, New York, pp 107-130
30. Y Li V Gama T Yoshida JA Gomez K Ishikawa H Sasaguri HY Cohen DA Sinclair H Mizusawa S Matsuyama 2007 Bax-inhibiting peptide protects cells from polyglutamine toxicity caused by Ku70 acetylation Cell Death Differ 14 2058 2067 17885668 10.1038/sj.cdd.4402219 1:CAS:528:DC%2BD2sXhtlajs7nK
31. K Löfgren A Wahlström P Lundberg Ü Langel A Gräslund K Bedecs 2008 Antiprion properties of prion protein-derived cell-penetrating peptides FASEB J 22 2177 2184 18296502 10.1096/fj.07-099549
32. M Hirose M Takatori Y Kuroda M Abe E Murata T Isada K Ueda K Shigemi M Shibazaki F Shimizu M Hirata K Fukazawa M Sakaguchi K Kegeyama Y Tanaka 2008 Effect of synthetic cell-penetrating peptides on TrkA activity in PC12 cells J Pharamcol Sci 106 107 113 10.1254/jphs.FPZ070263 1:CAS:528:DC%2BD1cXhslGnu7Y%3D
33. J-M Choi M-H Ahn W-J Chae Y-G Jung J-C Park J-W Park T-K Park J-H Lee B-F Seo K-D Kim E-S Kim D-H Lee S-K Lee S-K Lee 2006 Intranasal delivery of the cytoplasmic domain of CTLA-4 using a novel protein transduction domain prevents allergic inflammation Nat Med 12 574 579 16604087 10.1038/nm1385 1:CAS:528:DC%2BD28Xkt1KjurY%3D
34. CT McCusker Y Wang J Shan MW Kinyanjui A Villeneuve H Michael ED Fixman 2007 Inhibition of experimental allergic airways disease by local application of a cell-penetrating dominant-negative STAT-6 peptide J Immunol 179 2556 2564 17675518 1:CAS:528:DC%2BD2sXosVyqsbk%3D
35. E Makino N Sakaguchi K Iwatsuki N-H Huh 2004 Introduction of an N-terminal peptide of S100C/A11 into human cells induces apoptotic cell death J Mol Med 82 612 620 15241500 10.1007/s00109-004-0560-1 1:CAS:528: DC%2BD2cXntlWmsLs%3D
36. BR Keleman K Hsiao SA Goueli 2002 Selective in vivo inhibition of mitogen-activated protein kinase activation using cell-permeable peptides J Biol Chem 277 8741 8748 10.1074/jbc.M108459200
37. i3α induces the dual phosphorylation of p42/p44 MAP kinases Biochim Biophys Acta 1745 207 214 15953648 10.1016/j.bbamcr.2005.05.006 1:CAS:528:DC%2BD2MXpslCgt7k%3D
38. SB Fonseca MP Pereira SO Kelley 2009 Recent advances in the use of cell-penetrating peptides for medical and biological applications Adv Drug Deliv Rev 61 953 964 19538995 10.1016/j.addr.2009.06.001 1:CAS:528: DC%2BD1MXht1Wrsb%2FN
39. S Futaki T Suzuki W Ohashi T Yagami S Tanaka K Ueda Y Sugiura 2001 Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery J Biol Chem 276 5836 5840 11084031 10.1074/jbc.M007540200 1:CAS:528:DC%2BD3MXhs1KmtL0%3D
40. P Vanhee AM van der Sloot E Verschueren L Serrano F Rousseau J Schymkowitz 2011 Computational design of peptide ligands Trends Biotechnol 29 231 239 21316780 10.1016/j.tibtech.2011.01.004 1:CAS:528:DC%2BC3MXltFegt78%3D
41. WPR Verdurmen R Brock 2011 Biological responses towards cationic peptides and drug carriers Trends Pharmacol Sci 32 116 124 21167610 10.1016/j.tips.2010. 11.005 1:CAS:528:DC%2BC3MXhsFyhur8%3D
42. J Brugnano BC Ward A Panitch 2010 Cell-penetrating peptides can exert biological activity: a review BioMol Concepts 1 109 116 10.1515/bmc.2010.016
43. K Saar M Lindgren M Hansen E Eiríksdóttir Y Jiang K Rosenthal-Aizman M Sassian Ü Langel 2005 Cell-penetrating peptides: a comparative membrane toxicity study Anal Biochem 345 55 65 16137634 10.1016/j.ab.2005.07.033 1:CAS:528:DC%2BD2MXhtVeiu7zF
44. B Ward BL Seal CM Brophy A Panitch 2009 Design of a bioactive cell-penetrating peptide: when a transduction domain does more than transducer J Pept Sci 15 668 674 19691016 10.1002/psc.1168 1:CAS:528:DC%2BD1MXhtFSnsbbL
45. JP Richard K Melikov E Vives C Ramos B Verbeure MJ Gait LV Chernomordik B Lebleu 2003 Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake J Biol Chem 278 585 590 12411431 10.1074/jbc.M209548200 1:CAS:528:DC%2BD38XpvVWnsrk%3D
46. G Ter-Avetisyan G Tünnemann D Nowak M Nitschke A Herrmann M Drab MC Cardoso 2009 Cell entry of arginine-rich peptides is independent of endocytosis J Biol Chem 284 3370 3378 19047062 10.1074/jbc.M805550200 1:CAS:528: DC%2BD1MXht1Ortr8%3D
47. H Räägel P Säälik M Hansen Ü Langel M Pooga 2009 CPP-protein constructs induce a population of non-acidic vesicles during trafficking through endo-lysosomal pathway J Control Release 139 10 117 10.1016/j.jconrel.2009.06.028
48. DC Fry LT Vasilev 2005 Targeting protein-protein interactions for cancer therapy J Mol Med 83 955 963 16283145 10.1007/s00109-005-0705-x 1:CAS:528:DC%2BD2MXht1Oks7%2FM
49. LD D'Andrea A Del Gatto C Pedone E Benedetti 2006 Peptide-based molecules in angiogenesis Chem Biol Drug Des 67 115 126 16492159 10.1111/j.1747-0285. 2006.00356.x
50. W Low A Mortlock L Petrovska T Dottorini G Dougan A Crisanti 2007 Functional cell permeable motifs within medically relevant proteins J Biotechnol 129 55 564 10.1016/j.jbiotec.2007.01.019
51. EE Moore RE Kuestener SD Stroop FJ Grant SL Matthewes CL Brady PM Sexton DM Findlay 1995 Functionally different isoforms of the human calcitonin receptor result from alternative splicing of the gene transcript Mol Endocrinol 9 959 968 7476993 10.1210/me.9.8.959 1:CAS:528:DyaK2MXnsVGku70%3D
52. DR Nussenzveig CN Thaw MC Gershengorn 1994 Inhibition of inositol phosphate second messenger formation by intracellular loop one of a human calcitonin receptor J Biol Chem 269 28123 28129 7961748 1:CAS:528: DyaK2cXmvFaqtLg%3D
53. Rivinoja A, Laakkonen P (2011) Identification of homing peptides using the in vivo phage display technology. In: Langel Ü (ed) Cell-penetrating peptides. Methods and Protocols. Humana Press, New York, pp 401-415
54. OH Aina R Liu JL Sutcliffe J Marik C-X Pan KS Lam 2007 From combinatorial chemistry to cancer-targeting peptides Mol Pharm 5 631 651 10.1021/mp700073y
55. T Jiang ES Olson QT Nguyen M Roy PA Jennings RY Tsien 2004 Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc Natl Acad Sci USA 101 17867 17872 15601762 10.1073/pnas.0408191101 1:CAS:528: DC%2BD2MXjtVSmuw%3D%3D
56. M Chorev M Goodman 1995 Recent developments in retro peptides and proteins-an ongoing topochemical exploration Trends Biotechnol 13 438 445 7546569 10.1016/S0167-7799(00)88999-4 1:CAS:528:DyaK2MXosFOls7g%3D
57. J Howl S Jones 2009 Transport molecules using reverse sequence HIV-Tat polypeptides: not just any old Tat? Expert Opin Ther Pat 19 1329 1333 19555160 10.1517/17530050902824829 1:CAS:528:DC%2BD1MXhtVWitLzE
58. T Holm H Räägel S El Andaloussi M Hein M Mäe M Pooga Ü Langel 2011 Retro-inversion of certain cell-penetrating peptides causes severe cellular toxicity Biochim Biophys Acta 1808 1544 1551 21070744 10.1016/j.bbamem.2010.10.019 1:CAS:528:DC%2BC3MXkvFalurY%3D