N-terminal peptides from unprocessed prion proteins enter cells by macropinocytosis

Biochemical and Biophysical Research Communications

Volumn 348, Issue 2, 2006, Pages 379-385

  Magzoub, Mazin ^a   Sandgren, Staffan ^b   Lundberg, Pontus ^a   Oglecka, Kamila ^a   Lilja, Johanna ^b   Wittrup, Anders ^b   Goran Eriksson L E ^a   Langel, Ülo ^a   Belting, Mattias ^b   Gräslund, Astrid ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Cell penetrating peptide; Endocytosis; Macropinocytosis; N terminus; Prion protein; Proteoglycan

Indexed keywords

DNA; GOLD; METHIONYLVALYLLYSYLSERYLLYSYLISOLEUCYLGLYCYLSERYLTRYPTOPHYLISOLEUCYLLEUCYL VALYLLEUCYLPHENYLALANYLVALYLALANYLMETHIONYLTRYPTOPHANYLSERYLASPARTYLVALYLGLYCYL LEUCYLCYSTEINYLLYSYLLYSYLARGINYLPROLYLLYSYLPROLINE; PEPTIDE; PRION PROTEIN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; DNA PROTEIN COMPLEX; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; HYDROPHOBICITY; INTERNALIZATION; MAMMAL CELL; NONHUMAN; PINOCYTOSIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; VIRUS INFECTIVITY;

ANDROSTADIENES; ANIMALS; CATTLE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOCHALASIN D; PEPTIDE FRAGMENTS; PINOCYTOSIS; PRIONS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

BOS TAURUS; MAMMALIA;

EID: 33746911543     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.07.065     Document Type: Article

References (35)

1. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. USA 95 (1998) 13363-13383
2. Caughey B., and Lansbury Jr. P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26 (2003) 267-298
3. Collins S.J., Lawson V.A., and Masters C.L. Transmissible spongiform encephalopathies. The Lancet 363 (2004) 51-61
4. Mironov Jr. A., Latawiec D., Wille H., Bouzamondo-Bernstein E., Legname G., Williamson R.A., Burton D., DeArmond S.J., Prusiner S.B., and Peters P.J. Cytosolic prion protein in neurons. J. Neurosci. 23 (2003) 7183-7193
5. Barmada S.J., and Harris D.A. Visualization of prion infection in transgenic mice expressing green fluorescent protein-tagged prion protein. J. Neurosci. 25 (2005) 5824-5832
6. Gu Y., Hinnerwisch J., Fredricks R., Kalepu S., Mishra R.S., and Singh N. Identification of cryptic nuclear localization signals in the prion protein: implications for prion disease pathogenesis. Neurobiol. Dis. 12 (2003) 133-149
7. Mangé A., Crozet C., Lehmann S., and Béranger F. Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin. J. Cell. Sci. 117 (2004) 2411-2416
8. Ma J., and Lindquist S. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc. Natl. Acad. Sci. USA 98 (2001) 14955-14960
9. Wang X., Wang F., Sy M., and Ma J. Calpain and other cytosolic proteases can contribute to the degradation of retro-translocated prion protein in the cytosol. J. Biol. Chem. 280 (2005) 317-325
10. Rane N.S., Yonkovich J.L., and Hegde R.S. Protection from cytosolic prion protein toxicity by modulation of protein translocation. EMBO J. 23 (2004) 4550-4559
11. Harris D.A. Trafficking, turnover and membrane topology of PrP. British Med. Bull. 66 (2003) 71-85
12. Stewart R.S., Drisaldi B., and Harris D.A. A transmembrane form of the prion protein contains an uncleaved signal peptide and is retained in the endoplasmic reticulum. Mol. Biol. Cell 12 (2001) 881-889
13. Stewart R.S., and Harris D.A. A transmembrane form of the prion protein is localized in the Golgi apparatus of neurons. J. Biol. Chem. 280 (2005) 15855-15864
14. Hegde R.S., Mastrianni J.A., Scott M.R., DeFea K.A., Tremblay P., Torchia M., DeArmond S.J., Prusiner S.B., and Lingappa V.R. A transmembrane form of the prion protein in neurodegenerative disease. Science 279 (1998) 827-834
15. Lundberg P., Magzoub M., Lindberg M., Hällbrink M., Jarvet J., Eriksson L.E.G., Langel U., and Gräslund A. Cell membrane translocation of the N-terminal (1-28) part of the prion protein. Biochem. Biophys. Res. Commun. 299 (2002) 85-90
16. Magzoub M., and Gräslund A. Cell-penetrating peptides: from inception to application. Q. Rev. Biophys. 37 (2004) 147-195
17. Conner S.D., and Schmid S.L. Regulated portals of entry into the cell. Nature 422 (2003) 37-44
18. Belting M. Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem. Sci. 28 (2003) 145-151
19. Sandgren S., Cheng F., and Belting M. Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans. J. Biol. Chem. 277 (2002) 38877-38883
20. Warner R.G., Hundt C., Weiss S., and Turnbull J.E. Identification of the heparan sulfate binding sites in the cellular prion protein. J. Biol. Chem. 277 (2002) 18421-18430
21. Ben-Zaken O., Tzaban S., Tal Y., Horonchik L., Esko J.D., Vlodavsky I., and Taraboulos A. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278 (2003) 40041-40049
22. Horonchik L., Tzaban S., Ben-Zaken O., Zedidia Y., Rouvinski A., Papy-Garcia D., Barritault D., Vlodavsky I., and Taraboulos A. Heparan sulfate is a cellular receptor for purified infectious prions. J. Biol. Chem. 280 (2005) 17062-17067
23. Sampath P., and Pollard T.D. Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30 (1991) 1973-1980
24. Vermeulen M., Giordano M., Trevani A.S., Sedlik C., Gamberale R., Fernández-Calotti P., Salamone G., Raiden S., Sanjurjo J., and Geffner J.R. Loss of binding and entry of liposome-DNA complexes decreases transfection efficiency in differentiated airway epithelial cells. J. Immunol. 172 (2004) 3196-3204
25. Simonsen A., Lippe R., Christoforidis S., Gaullier J.M., Brech A., Callaghan J., Toh B.H., Murphy C., Zerial M., and Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394 (1998) 494-498
26. Donne D.G., Viles J.H., Groth D., Mehlhorn I., James T.L., Cohen F.E., Prusiner S.B., Wright P.E., and Dyson H.J. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N-terminus is highly flexible. Proc. Natl. Acad. Sci. USA 94 (1997) 13452-13457
27. Zahn R., Liu A., Lührs T., Riek R., von Schroetter C., Lopez Garcia F., Billeter M., Calzolai L., Wider G., and Wüthrich K. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. USA 97 (2000) 145-150
28. Lopez Garcia F., Zahn R., Riek R., and Wüthrich K. NMR structure of the bovine prion protein. Proc. Natl. Acad. Sci. USA 97 (2000) 8334-8339
29. Magzoub M., Ogle{ogonek}cka K., Pramanik A., Eriksson L.E.G., and Gräslund A. Membrane perturbation effects of peptides derived from the N-termini of unprocessed prion proteins. Biochim. Biophys. Acta 1716 (2005) 126-136
30. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699
31. Wang X., Wang F., Arterburn L., Wollman R., and Ma J. The interaction between cytoplasmic prion protein and the hydrophobic lipid core of membrane correlates with neurotoxicity. J. Biol. Chem. 281 (2006) 13559-13565
32. Wadia J.S., Stan R.V., and Dowdy S.F. Transducible Tat-HA fusogenic peptide enhances escape of Tat-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10 (2004) 310-315
33. Nakase I., Niwa M., Takeuchi T., Sonomura K., Kawabata N., Koike Y., Takehashi M., Tanaka S., Ueda K., Simpson J.C., Jones A.T., Sugiura Y., and Futaki S. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol. Ther. 10 (2004) 1011-1022
34. Dupont E., Joliot A., and Prochiantz A. Penetratins. In: Langel U. (Ed). Cell-Penetrating Peptides: Processes and Applications (2002), CRC press, Boca Raton 23-51
35. Vivès E., and Lebleau B. The Tat-derived cell-penetrating peptide. In: Langel U. (Ed). Cell-Penetrating Peptides: Processes and Applications (2002), CRC Press, Boca Raton 3-21