Characterization of a novel cell penetrating peptide derived from human Oct4

Cell Regeneration

Volumn 3, Issue 1, 2014, Pages 3:2-

  Harreither, Eva ^a   Rydberg, Hanna A ^b   Åmand, Helene L ^b   Jadhav, Vaibhav ^a   Fliedl, Lukas ^d   Benda, Christina ^e   Esteban, Miguel A ^e   Pei, Duanqing ^e   Borth, Nicole ^a,d   Grillari Voglauer, Regina ^a,c,d   Hommerding, Oliver ^f   Edenhofer, Frank ^f,g   Nordén, Bengt ^b   Grillari, Johannes ^a,c  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c Evercyte GmbH   (Austria)

^d AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^e GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^f UNIVERSITY OF BONN   (Germany)

^g UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cell penetrating peptides; Cellular internalization; Homeodomain transcription factors; Oct4; Penetratin; Reprogramming

Indexed keywords

CELL PENETRATING PEPTIDE; FLUORESCEIN ISOTHIOCYANATE; HYBRID PROTEIN; OCT4 PTD CRE FUSION PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PENETRATIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONJUGATION; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; ENDOCYTOSIS; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID MEMBRANE; MEMBRANE BINDING; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TRANSDUCTION DOMAIN;

MAMMALIA;

EID: 84988290493     PISSN: None     EISSN: 20459769     Source Type: Journal    
DOI: 10.1186/2045-9769-3-2     Document Type: Article

References (67)

1. Ziegler A. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv Drug Deliv Rev 2008, 60:580-597. 10.1016/j.addr.2007.10.005, 18045730.
2. Lindgren M, Langel U. Classes and prediction of cell-penetrating peptides. Methods Mol Biol 2011, 683:3-19. 10.1007/978-1-60761-919-2_1, 21053118.
3. Madani F, Lindberg S, Langel U, Futaki S, Gräslund A. Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011, 2011:414729. 3103903, 21687343.
4. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988, 55:1189-1193. 10.1016/0092-8674(88)90263-2, 2849510.
5. Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 1988, 55:1179-1188. 10.1016/0092-8674(88)90262-0, 2849509.
6. Dupont E, Prochiantz A, Joliot A. Identification of a signal peptide for unconventional secretion. J Biol Chem 2007, 282:8994-9000. 10.1074/jbc.M609246200, 17242404.
7. Joliot A, Pernelle C, Deagostini-Bazin H, Prochiantz A. Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci USA 1991, 88:1864-1868. 10.1073/pnas.88.5.1864, 51126, 1672046.
8. 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.
9. Schmidt N, Mishra A, Lai GH, Wong GCL. Arginine-rich cell-penetrating peptides. FEBS Lett 2010, 584:1806-1813. 10.1016/j.febslet.2009.11.046, 19925791.
10. Jiao C-Y, Delaroche D, Burlina F, Alves ID, Chassaing G, Sagan S. Translocation and endocytosis for cell-penetrating peptide internalization. J Biol Chem 2009, 284:33957-33965. 10.1074/jbc.M109.056309, 2797166, 19833724.
11. Christiaens B, Grooten J, Reusens M, Joliot A, Goethals M, Vandekerckhove J, Prochiantz A, Rosseneu M. Membrane interaction and cellular internalization of penetratin peptides. Eur J Biochem 2004, 271:1187-1197. 10.1111/j.1432-1033.2004.04022.x, 15009197.
12. Letoha T, Gaál S, Somlai C, Venkei Z, Glavinas H, Kusz E, Duda E, Czajlik A, Peták F, Penke B. Investigation of penetratin peptides. Part 2. In vitro uptake of penetratin and two of its derivatives. J Pept Sci 2005, 11:805-811. 10.1002/psc.678, 15942927.
13. Magzoub M, Eriksson LEG, Gräslund A. Comparison of the interaction, positioning, structure induction and membrane perturbation of cell-penetrating peptides and non-translocating variants with phospholipid vesicles. Biophys Chem 2003, 103:271-288. 10.1016/S0301-4622(02)00321-6, 12727289.
14. Eiríksdóttir E, Konate K, Langel U, Divita G, Deshayes S. Secondary structure of cell-penetrating peptides controls membrane interaction and insertion. Biochim Biophys Acta 2010, 1798:1119-1128. 10.1016/j.bbamem.2010.03.005, 20214875.
15. Magzoub M, Eriksson LEG, Gräslund A. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles: effects of surface charge and peptide concentration. Biochim Biophys Acta 2002, 1563:53-63. 10.1016/S0005-2736(02)00373-5, 12007625.
16. Noguchi H, Kaneto H, Weir GC, Bonner-weir S. Protein Transduction Domain Can Transduce Pancreatic Duct and Islet Cells. Diabetes 2003, 52:1732-1737. 10.2337/diabetes.52.7.1732, 12829640.
17. Kong K-A, Gadi J, Park HW, Bok J, Kim MH. The third helix of the murine Hoxc8 homeodomain facilitates protein transduction in mammalian cells. Biochem Biophys Res Commun 2008, 377:161-164. 10.1016/j.bbrc.2008.09.100, 18835255.
18. Chatelin L, Volovitch M, Joliot AH, Perez F, Prochiantz A. Transcription factor hoxa-5 is taken up by cells in culture and conveyed to their nuclei. Mech Dev 1996, 55:111-117. 10.1016/0925-4773(95)00478-5, 8861092.
19. Han K, Jeon MJ, Kim KA, Park J, Choi SY. Efficient intracellular delivery of GFP by homeodomains of Drosophila Fushi-tarazu and Engrailed proteins. Mol Cells 2000, 10:728-732. 10.1007/s10059-000-0728-7, 11211880.
20. Balayssac S, Burlina F, Convert O, Bolbach G, Chassaing G, Lequin O. Comparison of penetratin and other homeodomain-derived cell-penetrating peptides: interaction in a membrane-mimicking environment and cellular uptake efficiency. Biochemistry 2006, 45:1408-1420. 10.1021/bi0518390, 16445283.
21. Lu J, Li G, Lan MS, Zhang S, Fan W, Wang H, Lu D. Pax4 paired domain mediates direct protein transduction into mammalian cells. Endocrinology 2007, 148:5558-5565. 10.1210/en.2007-0636, 17717051.
22. Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 1990, 344:435-439. 10.1038/344435a0, 1690859.
23. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391. 10.1016/S0092-8674(00)81769-9, 9814708.
24. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676. 10.1016/j.cell.2006.07.024, 16904174.
25. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Schöler HR, Duan L, Ding S. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, 4:381-384. 10.1016/j.stem.2009.04.005, 19398399.
26. Arnold A, Naaldijk YM, Fabian C, Wirth H, Binder H, Nikkhah G, Armstrong L, Stolzing A. Reprogramming of Human Huntington Fibroblasts Using mRNA. ISRN Cell Biol 2012, 2012:1-12.
27. Thier M, Münst B, Mielke S, Edenhofer F. Cellular reprogramming employing recombinant sox2 protein. Stem Cells Int 2012, 2012:549846. 3368608, 22693519.
28. Bosnali M, Edenhofer F. Generation of transducible versions of transcription factors Oct4 and Sox2. Biol Chem 2008, 389:851-861.
29. Kim D, Kim C-H, Moon J-I, Chung Y-G, Chang M-Y, Han B-S, Ko S, Yang E, Cha KY, Lanza R, Kim K-S. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009, 4:472-476. 10.1016/j.stem.2009.05.005, 2705327, 19481515.
30. Wieser M, Stadler G, Jennings P, Streubel B, Pfaller W, Ambros P, Riedl C, Katinger H, Grillari J, Grillari-Voglauer R. hTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am J Physiol Renal Physiol 2008, 295:F1365-F1375. 10.1152/ajprenal.90405.2008, 18715936.
31. 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. 10.1038/nm996, 14770178.
32. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63. 10.1016/0022-1759(83)90303-4, 6606682.
33. Nan YH, Park I-S, Hahm K-S, Shin SY. Antimicrobial activity, bactericidal mechanism and LPS-neutralizing activity of the cell-penetrating peptide pVEC and its analogs. J Pept Sci 2011, 17:812-817. 10.1002/psc.1408, 21956793.
34. Rydberg HA, Matson M, Amand HL, Esbjörner EK, Nordén B. Effects of Tryptophan Content and Backbone Spacing on the Uptake Efficiency of Cell-Penetrating Peptides. Biochemistry 2012, 52:5531-5539.
35. Nordén B, Rodger A, Dafforn TR. Linear Dichroism and Circular Dichroism - a Textbook on Polarized-Light Spectroscopy 2010, 304. RSC Publishing.
36. Rydberg HA, Carlsson N, Nordén B. Membrane interaction and secondary structure of de novo designed arginine-and tryptophan peptides with dual function. Biochem Biophys Res Commun 2012, 427:261-265. 10.1016/j.bbrc.2012.09.030, 22989747.
37. Ardhammar M, Lincoln P, Nordén B. Invisible liposomes: refractive index matching with sucrose enables flow dichroism assessment of peptide orientation in lipid vesicle membrane. Proc Natl Acad Sci USA 2002, 99:15313-15317. 10.1073/pnas.192583499, 137713, 12422017.
38. Peitz M, Pfannkuche K, Rajewsky K, Edenhofer F. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: a tool for efficient genetic engineering of mammalian genomes. Proc Natl Acad Sci USA 2002, 99:4489-4494. 10.1073/pnas.032068699, 123675, 11904364.
39. Thier M, Münst B, Edenhofer F. Exploring refined conditions for reprogramming cells by recombinant Oct4 protein. Int J Dev Biol 2010, 54:1713-1721. 10.1387/ijdb.103193mt, 21404191.
40. Thier M, Wörsdörfer P, Lakes YB, Gorris R, Herms S, Opitz T, Seiferling D, Quandel T, Hoffmann P, Nöthen MM, Brüstle O, Edenhofer F. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012, 10:473-479. 10.1016/j.stem.2012.03.003, 22445518.
41. Amand HL, Fant K, Nordén B, Esbjörner EK. Stimulated endocytosis in penetratin uptake: effect of arginine and lysine. Biochem Biophys Res Commun 2008, 371:621-625. 10.1016/j.bbrc.2008.04.039, 18423373.
42. Esch D, Vahokoski J, Groves MR, Pogenberg V, Cojocaru V, Vom Bruch H, Han D, Drexler HCA, Araúzo-Bravo MJ, Ng CKL, Jauch R, Wilmanns M, Schöler HR. A unique Oct4 interface is crucial for reprogramming to pluripotency. Nat Cell Biol 2013, 15:295-301. 10.1038/ncb2680, 23376973.
43. Aschauer L, Gruber LN, Pfaller W, Limonciel A, Athersuch TJ, Cavill R, Khan A, Gstraunthaler G, Grillari J, Grillari R, Hewitt P, Leonard MO, Wilmes A, Jennings P. Delineation of the key aspects in the regulation of epithelial monolayer formation. Mol Cell Biol 2013, 33:2535-2550. 10.1128/MCB.01435-12, 3700122, 23608536.
44. Esbjörner EK, Caesar CEB, Albinsson B, Lincoln P, Nordén B. Tryptophan orientation in model lipid membranes. Biochem Biophys Res Commun 2007, 361:645-650.
45. Kellendonk C, Tronche F, Monaghan AP, Angrand PO, Stewart F, Schütz G. Regulation of Cre recombinase activity by the synthetic steroid RU 486. Nucleic Acids Res 1996, 24:1404-1411. 10.1093/nar/24.8.1404, 145830, 8628671.
46. Fischer PM, Zhelev NZ, Wang S, Melville JE, Fåhraeus R, Lane DP. Structure-activity relationship of truncated and substituted analogues of the intracellular delivery vector Penetratin. J Pept Res 2000, 55:163-172. 10.1034/j.1399-3011.2000.00163.x, 10784032.
47. Nolden L, Edenhofer F, Haupt S, Koch P, Wunderlich FT, Siemen H, Brüstle O. Site-specific recombination in human embryonic stem cells induced by cell-permeant Cre recombinase. Nat Methods 2006, 3:461-467. 10.1038/nmeth884, 16721380.
48. Ferrari A, Pellegrini V, Arcangeli C, Fittipaldi A, Giacca M, Beltram F. Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol Ther 2003, 8:284-294. 10.1016/S1525-0016(03)00122-9, 12907151.
49. Edenhofer F. Protein transduction revisited: novel insights into the mechanism underlying intracellular delivery of proteins. Curr Pharm Des 2008, 14:3628-3636. 10.2174/138161208786898833, 19075739.
50. Amand HL, Rydberg HA, Fornander LH, Lincoln P, Nordén B, Esbjörner EK. Cell surface binding and uptake of arginine- and lysine-rich penetratin peptides in absence and presence of proteoglycans. Biochim Biophys Acta 2012, 1818:2669-2678. 10.1016/j.bbamem.2012.06.006, 22705501.
51. Rothbard JB, Jessop TC, Lewis RS, Murray BA, Wender PA. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J Am Chem Soc 2004, 126:9506-9507. 10.1021/ja0482536, 15291531.
52. Duchardt F, Ruttekolk IR, Verdurmen WPR, Lortat-Jacob H, Bürck J, Hufnagel H, Fischer R, van den Heuvel M, Löwik DWPM, Vuister GW, Ulrich A, de Waard M, Brock R. A cell-penetrating peptide derived from human lactoferrin with conformation-dependent uptake efficiency. J Biol Chem 2009, 284:36099-36108. 10.1074/jbc.M109.036426, 2794725, 19858187.
53. Zaro JL, Vekich JE, Tran T, Shen W-C. Nuclear localization of cell-penetrating peptides is dependent on endocytosis rather than cytosolic delivery in CHO cells. Mol Pharm 2009, 6:337-344. 10.1021/mp800239p, 3638978, 19718791.
54. Noguchi H, Matsushita M, Matsumoto S, Lu Y-F, Matsui H, Bonner-Weir S. Mechanism of PDX-1 protein transduction. Biochem Biophys Res Commun 2005, 332:68-74. 10.1016/j.bbrc.2005.04.092, 15896300.
55. di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang J-M, Taly J-F, Notredame C. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 2011, 39(Web Server issue):W13-W17. 3125728, 21558174.
56. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302:205-217. 10.1006/jmbi.2000.4042, 10964570.
57. Crooks GE, Hon G, Chandonia J-M, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14:1188-1190. 10.1101/gr.849004, 419797, 15173120.
58. Milletti F. Cell-penetrating peptides: classes, origin, and current landscape. Drug Discov Today 2012, 17:850-860. 10.1016/j.drudis.2012.03.002, 22465171.
59. Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, Prochiantz A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J Biol Chem 1996, 271:18188-18193. 10.1074/jbc.271.30.18188, 8663410.
60. Caesar CEB, Esbjörner EK, Lincoln P, Nordén B. Membrane interactions of cell-penetrating peptides probed by tryptophan fluorescence and dichroism techniques: correlations of structure to cellular uptake. Biochemistry 2006, 45:7682-7692. 10.1021/bi052095t, 16768464.
61. Thorén PE, Persson D, Isakson P, Goksör M, Önfelt A, Nordén B. Uptake of analogs of penetratin, Tat(48-60) and oligoarginine in live cells. Biochem Biophys Res Commun 2003, 307:100-107. 10.1016/S0006-291X(03)01135-5, 12849987.
62. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J. Studies on the internalization mechanism of cationic cell-penetrating peptides. J Biol Chem 2003, 278:31192-31201. 10.1074/jbc.M303938200, 12783857.
63. Verstreken P, Ohyama T, Bellen HJ. FM 1-43 labeling of synaptic vesicle pools at the Drosophila neuromuscular junction. Methods Mol Biol 2008, 440:349-369. 10.1007/978-1-59745-178-9_26, 2712823, 18369958.
64. Jones SW, Christison R, Bundell K, Voyce CJ, Brockbank SMV, Newham P, Lindsay MA. Characterisation of cell-penetrating peptide-mediated peptide delivery. Br J Pharmacol 2005, 145:1093-1102. 10.1038/sj.bjp.0706279, 1576229, 15937518.
65. Lundberg P, El-Andaloussi S, Sütlü T, Johansson H, Langel U. Delivery of short interfering RNA using endosomolytic cell-penetrating peptides. FASEB J 2007, 21:2664-2671. 10.1096/fj.06-6502com, 17463227.
66. Joliot A, Prochiantz A. Homeoproteins as natural Penetratin cargoes with signaling properties. Adv Drug Deliv Rev 2008, 60:608-613. 10.1016/j.addr.2007.09.004, 18037528.
67. Tassetto M, Maizel A, Osorio J, Joliot A. Plant and animal homeodomains use convergent mechanisms for intercellular transfer. EMBO Rep 2005, 6:885-890. 10.1038/sj.embor.7400487, 1369162, 16113652.