Cell surface binding and uptake of arginine- and lysine-rich penetratin peptides in absence and presence of proteoglycans

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 11, 2012, Pages 2669-2678

  Åmand, Helene L ^a   Rydberg, Hanna A ^a   Fornander, Louise H ^a   Lincoln, Per ^a   Nordén, Bengt ^a   Esbjörner, Elin K ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Arginine; Cell penetrating peptide; Cellular uptake; Membrane affinity; Penetratin; Proteoglycan

Indexed keywords

ARGININE; CELL PENETRATING PEPTIDE; HEPARIN; LYSINE; PROTEOGLYCAN;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL SURFACE; CELL TYPE; CLUSTER ANALYSIS; CONTROLLED STUDY; FLOW CYTOMETRY; HAMSTER; HYDROPHOBICITY; INTERMETHOD COMPARISON; INTERNALIZATION; MEMBRANE BINDING; MOLECULAR DYNAMICS; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; STATIC ELECTRICITY; SURFACE PROPERTY; WILD TYPE;

ANIMALS; ARGININE; CARRIER PROTEINS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; FLUORESCENCE; HEPARIN; LYSINE; PROTEIN BINDING; PROTEOGLYCANS;

EID: 84864062843     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.06.006     Document Type: Article

References (49)

1. Ü. Langel Handbook of Cell-penetrating Peptides 2nd ed. 2007 CRC Press, Taylor & Francis Group Boca Raton, FL
2. A.D. Frankel, and C.O. Pabo Cellular uptake of the TAT protein from human immunodeficiency virus Cell 55 1988 1189 1193 (Pubitemid 19020071)
3. M. Green, and P.M. Loewenstein Autonomous functional domains of chemically synthesized human immunodeficiency virus TAT trans-activator protein Cell 55 1988 1179 1188 (Pubitemid 19020070)
4. A. Joliot, C. Pernelle, H. Deagostini-Bazin, and A. Prochiantz Antennapedia homeobox peptide regulates neural morphogenesis Proc. Natl. Acad. Sci. U. S. A. 88 1991 1864 1868 (Pubitemid 21916327)
5. F. Madani, S. Lindberg, Ü. Langel, S. Futaki, and A. Gräslund Mechanisms of cellular uptake of cell-penetrating peptides J. Biophys. 2011 2011 414729
6. G.M. Poon, and J. Gariepy Cell-surface proteoglycans as molecular portals for cationic peptide and polymer entry into cells Biochem. Soc. Trans. 35 2007 788 793 (Pubitemid 47310369)
7. H. Räägel, P. Säälik, and M. Pooga Peptide-mediated protein delivery-which pathways are penetrable? Biochim. Biophys. Acta 1798 2010 2240 2248
8. S. Trabulo, A.L. Cardoso, M. Mano, and M.C.P. de Lima Cell-penetrating peptides - mechanisms of cellular uptake and generation of delivery systems Pharmaceuticals 3 2010 961 993
9. H.L. Åmand, K. Fant, B. Nordén, and E.K. Esbjörner Stimulated endocytosis in penetratin uptake: effect of arginine and lysine Biochem. Biophys. Res. Commun. 371 2008 621 625
10. I.A. Khalil, K. Kogure, S. Futaki, and H. Harashima High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression J. Biol. Chem. 281 2006 3544 3551 (Pubitemid 43845971)
11. J.S. Wadia, R.V. Stan, and S.F. Dowdy Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat. Med. 10 2004 310 315 (Pubitemid 38667624)
12. I.M. Kaplan, J.S. Wadia, and S.F. Dowdy Cationic TAT peptide transduction domain enters cells by macropinocytosis J. Control. Release 102 2005 247 253 (Pubitemid 40093789)
13. S. Console, C. Marty, C. Garcia-Echeverria, R. Schwendener, and K. Ballmer-Hofer 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 2003 35109 35114 (Pubitemid 37102274)
14. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501 (Pubitemid 46105438)
15. J.P. Richard, K. Melikov, H. Brooks, P. Prevot, B. Lebleu, and L.V. Chernomordik Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J. Biol. Chem. 280 2005 15300 15306 (Pubitemid 40562886)
16. M. Tyagi, M. Rusnati, M. Presta, and M. Giacca Internalization of HIV-1 TAT requires cell surface heparan sulfate proteoglycans J. Biol. Chem. 276 2001 3254 3261
17. A. Wittrup, S.H. Zhang, G.B. ten Dam, T.H. van Kuppevelt, P. Bengtson, M. Johansson, J. Welch, M. Morgelin, and M. Belting ScFv antibody-induced translocation of cell-surface heparan sulfate proteoglycan to endocytic vesicles: evidence for heparan sulfate epitope specificity and role of both syndecan and glypican J. Biol. Chem. 284 2009 32959 32967
18. E.G. Argyris, J. Kulkosky, M.E. Meyer, Y. Xu, M. Mukhtar, R.J. Pomerantz, and K.J. Williams The perlecan heparan sulfate proteoglycan mediates cellular uptake of HIV-1 Tat through a pathway responsible for biological activity Virology 330 2004 481 486 (Pubitemid 39572853)
19. T. Letoha, A. Keller-Pinter, E. Kusz, C. Kolozsi, Z. Bozso, G. Toth, C. Vizler, Z. Olah, and L. Szilak Cell-penetrating peptide exploited syndecans Biochim. Biophys. Acta 1798 2010 2258 2265
20. M. Belting, A. Wittrup, and S. Sandgren Proteoglycans as endocytosis receptors Ü. Langel, Handbook of Cell-penetrating Peptides 2007 CRC Press, Taylor & Francis Group Boca Raton, FL 219 234
21. J.M. Gump, R.K. June, and S.F. Dowdy Revised role of glycosaminoglycans in TAT protein transduction domain-mediated cellular transduction J. Biol. Chem. 285 2010 1500 1507
22. R.J. Naik, P. Chandra, A. Mann, and M. Ganguli Exogenous and cell surface glycosaminoglycans alter DNA delivery efficiency of arginine and lysine homopeptides in distinctly different ways J. Biol. Chem. 286 2011 18982 18993
23. N.W. Luedtke, P. Carmichael, and Y. Tor Cellular uptake of aminoglycosides, guanidinoglycosides, and poly-arginine J. Am. Chem. Soc. 125 2003 12374 12375 (Pubitemid 37254733)
24. P.E. Thorén, D. Persson, P. Isakson, M. Goksör, A. Önfelt, and B. Nordén Uptake of analogs of penetratin, Tat(48-60) and oligoarginine in live cells Biochem. Biophys. Res. Commun. 307 2003 100 107 (Pubitemid 36808542)
25. P.A. Wender, D.J. Mitchell, K. Pattabiraman, E.T. Pelkey, L. Steinman, and J.B. Rothbard The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters Proc. Natl. Acad. Sci. U. S. A. 97 2000 13003 13008
26. D.J. Mitchell, D.T. Kim, L. Steinman, C.G. Fathman, and J.B. Rothbard Polyarginine enters cells more efficiently than other polycationic homopolymers J. Pept. Res. 56 2000 318 325
27. J.B. Rothbard, T.C. Jessop, R.S. Lewis, B.A. Murray, and P.A. Wender Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells J. Am. Chem. Soc. 126 2004 9506 9507 (Pubitemid 39031015)
28. M. Pooga, M. Hällbrink, M. Zorko, and Ü. Langel Cell penetration by transportan FASEB J. 12 1998 67 77 (Pubitemid 28060272)
29. M.C. Morris, L. Chaloin, J. Mery, F. Heitz, and G. Divita A novel potent strategy for gene delivery using a single peptide vector as a carrier Nucleic Acids Res. 27 1999 3510 3517 (Pubitemid 29414679)
30. M.C. Morris, J. Depollier, J. Mery, F. Heitz, and G. Divita A peptide carrier for the delivery of biologically active proteins into mammalian cells Nat. Biotechnol. 19 2001 1173 1176 (Pubitemid 33115705)
31. G. Drin, S. Cottin, E. Blanc, A.R. Rees, and J. Temsamani Studies on the internalization mechanism of cationic cell-penetrating peptides J. Biol. Chem. 278 2003 31192 31201 (Pubitemid 36994635)
32. F. Burlina, S. Sagan, G. Bolbach, and G. Chassaing Quantification of the cellular uptake of cell-penetrating peptides by MALDI-TOF mass spectrometry Angew. Chem. Int. Ed Engl. 44 2005 4244 4247 (Pubitemid 40968506)
33. C.Y. Jiao, D. Delaroche, F. Burlina, I.D. Alves, G. Chassaing, and S. Sagan Translocation and endocytosis for cell-penetrating peptide internalization J. Biol. Chem. 284 2009 33957 33965
34. H.L. Åmand, C.L. Boström, P. Lincoln, B. Nordén, and E.K. Esbjörner Binding of cell-penetrating penetratin peptides to plasma membrane vesicles correlates directly with cellular uptake Biochim. Biophys. Acta, Biomembr. 1808 2011 1860 1867
35. C.E. Caesar, E.K. Esbjörner, P. Lincoln, and B. Nordén Membrane interactions of cell-penetrating peptides probed by tryptophan fluorescence and dichroism techniques: correlations of structure to cellular uptake Biochemistry 45 2006 7682 7692 (Pubitemid 43894958)
36. E.K. Esbjörner, P. Lincoln, and B. Nordén Counterion-mediated membrane penetration: cationic cell-penetrating peptides overcome Born energy barrier by ion-pairing with phospholipids Biochim. Biophys. Acta, Biomembr. 1768 2007 1550 1558 (Pubitemid 46782707)
37. D. Persson, P.E. Thorén, P. Lincoln, and B. Nordén Vesicle membrane interactions of penetratin analogues Biochemistry 43 2004 11045 11055 (Pubitemid 39433693)
38. A. Rullo, J. Qian, and M. Nitz Peptide-glycosaminoglycan cluster formation involving cell penetrating peptides Biopolymers 95 2011 722 731
39. A. Ziegler, and J. Seelig High affinity of the cell-penetrating peptide HIV-1 Tat-PTD for DNA Biochemistry 46 2007 8138 8145 (Pubitemid 47051649)
40. S.W. Provencher Contin - a general-purpose constrained regularization program for inverting noisy linear algebraic and integral-equations Comput. Phys. Commun. 27 1982 229 242
41. I.D. Alves, C. Bechara, A. Walrant, Y. Zaltsman, C.Y. Jiao, and S. Sagan Relationships between membrane binding, affinity and cell internalization efficacy of a cell-penetrating peptide: penetratin as a case study PLoS One 6 2011 e24096
42. A. Walrant, I. Correia, C.Y. Jiao, O. Lequin, E.H. Bent, N. Goasdoue, C. Lacombe, G. Chassaing, S. Sagan, and I.D. Alves Different membrane behaviour and cellular uptake of three basic arginine-rich peptides Biochim. Biophys. Acta 1808 2011 382 393
43. I. Capila, and R.J. Linhardt Heparin-protein interactions Angew. Chem. Int. Ed Engl. 41 2002 391 412
44. J.R. Fromm, R.E. Hileman, E.E. Caldwell, J.M. Weiler, and R.J. Linhardt Differences in the interaction of heparin with arginine and lysine and the importance of these basic amino acids in the binding of heparin to acidic fibroblast growth factor Arch. Biochem. Biophys. 323 1995 279 287
45. G. Salvi, P. De Los Rios, and M. Vendruscolo Effective interactions between chaotropic agents and proteins Proteins 61 2005 492 499 (Pubitemid 41547405)
46. N. Sakai, and S. Matile Anion-mediated transfer of polyarginine across liquid and bilayer membranes J. Am. Chem. Soc. 125 2003 14348 14356 (Pubitemid 37452373)
47. A. Yamaji-Hasegawa, and M. Tsujimoto Asymmetric distribution of phospholipids in biomembranes Biol. Pharm. Bull. 29 2006 1547 1553 (Pubitemid 44166349)
48. A. Varki Sialic acids in human health and disease Trends Mol. Med. 14 2008 351 360
49. T. Angata, and A. Varki Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective Chem. Rev. 102 2002 439 469 (Pubitemid 35381636)