The Non-Peptidic Part Determines the Internalization Mechanism and Intracellular Trafficking of Peptide Amphiphiles

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Missirlis, Dimitris ^a,b,c   Teesalu, Tambet ^d,e   Black, Matthew ^a   Tirrell, Matthew ^a,f  

^a University of California at Berkeley   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^d Faculty of Medicine   (Estonia)

^e BURNHAM INSTITUTE   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOPHILE; CLATHRIN; MACROGOL; PALMITIC ACID; PEPTIDE AMPHIPHILE; STEARIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; IN VITRO STUDY; INTERNALIZATION; INTRACELLULAR TRANSPORT; LIPID RAFT; PROTEIN MODIFICATION; PROTEIN TRANSPORT;

CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; EXOCYTOSIS; HUMANS; MALE; MEMBRANE MICRODOMAINS; NANOSTRUCTURES; PEPTIDES; POLYETHYLENE GLYCOLS; PROSTATIC NEOPLASMS; PROTEIN TRANSPORT;

EID: 84872506496     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054611     Document Type: Article

References (33)

1. Ruoslahti E, Bhatia SN, Sailor MJ, (2010) Targeting of drugs and nanoparticles to tumors. The Journal of Cell Biology 188: 759-768 doi:10.1083/jcb.200910104.
2. Teesalu T, Sugahara KN, Ruoslahti E, (2012) Mapping of vascular ZIP codes by phage display. Meth Enzymol 503: 35-56 doi:10.1016/B978-0-12-396962-0.00002-1.
3. Foerg C, Merkle HP, (2007) On the biomedical promise of cell penetrating peptides: Limits versus prospects. J Pharm Sci 97: 144-162 doi:10.1002/jps.21117.
4. Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E, (2009) C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proceedings of the National Academy of Sciences 106: 16157-16162 doi:10.1073/pnas.0908201106.
5. Roth L, Agemy L, Kotamraju VR, Braun G, Teesalu T, et al. (2011) Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene. doi:10.1038/onc.2011.537.
6. Cui H, Webber MJ, Stupp SI, (2010) Self-assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials. Biopolymers 94: 1-18 doi:10.1002/bip.21328.
7. Lin BF, Marullo RS, Robb MJ, Krogstad DV, Antoni P, et al. (2011) De Novo Design of Bioactive Protein-Resembling Nanospheres via Dendrimer-Templated Peptide Amphiphile Assembly. Nano Lett 11: 3946-3950 doi:10.1021/nl202220q.
8. Braun GB, Pallaoro A, Wu G, Missirlis D, Zasadzinski JA, et al. (2009) Laser-Activated Gene Silencing viaGold Nanoshell-siRNA Conjugates. ACS Nano 3: 2007-2015 doi:10.1021/nn900469q.
9. Trent A, Marullo R, Lin B, Black M, Tirrell M, (2011) Structural properties of soluble peptide amphiphile micelles. Soft Matter 7: 9572 doi:10.1039/c1sm05862b.
10. Kastantin M, Ananthanarayanan B, Karmali P, Ruoslahti E, Tirrell M, (2009) Effect of the Lipid Chain Melting Transition on the Stability of DSPE-PEG(2000) Micelles. Langmuir 25: 7279-7286 doi:10.1021/la900310k.
11. Peters D, Kastantin M, Kotamraju VR, Karmali PP, Gujraty K, et al. (2009) Targeting atherosclerosis by using modular, multifunctional micelles. Proceedings of the National Academy of Sciences 106: 9815-9819 doi:10.1073/pnas.0903369106.
12. Karmali PP, Kotamraju VR, Kastantin M, Black M, Missirlis D, et al. (2009) Targeting of albumin-embedded paclitaxel nanoparticles to tumors. Nanomedicine 5: 73-82 doi:10.1016/j.nano.2008.07.007.
13. Sugahara KN, Teesalu T, Karmali PP, Kotamraju VR, Agemy L, et al. (2009) Tissue-Penetrating Delivery of Compounds and Nanoparticles into Tumors. Cancer Cell 16: 510-520 doi:10.1016/j.ccr.2009.10.013.
14. Kastantin M, Missirlis D, Black M, Ananthanarayanan B, Peters D, et al. (2010) Thermodynamic and Kinetic Stability of DSPE-PEG(2000) Micelles in the Presence of Bovine Serum Albumin. J Phys Chem B 114: 12632-12640 doi:10.1021/jp1001786.
15. Missirlis D, Krogstad DV, Tirrell M, (2010) Internalization of p53 14-29Peptide Amphiphiles and Subsequent Endosomal Disruption Results in SJSA-1 Cell Death. Mol Pharmaceutics 7: 2173-2184 doi:10.1021/mp100193h.
16. Missirlis D, Khant H, Tirrell M, (2009) Mechanisms of Peptide Amphiphile Internalization by SJSA-1 Cells in Vitro†. Biochemistry 48: 3304-3314 doi:10.1021/bi802356k.
17. Berndt P, Fields GB, Tirrell M, (1995) Synthetic lipidation of peptides and amino acids: monolayer structure and properties. JACS 117: 9515-9522.
18. Chinnapen DJF, Chinnapen H, Saslowsky D, Lencer WI, (2007) Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiology Letters 266: 129-137 doi:10.1111/j.1574-6968.2006.00545.x.
19. Torgersen ML, Skretting G, van Deurs B, Sandvig K, (2001) Internalization of cholera toxin by different endocytic mechanisms. Journal of Cell Science 114: 3737-3747.
20. Hansen CG, Nichols BJ, (2009) Molecular mechanisms of clathrin-independent endocytosis. Journal of Cell Science 122: 1713-1721 doi:10.1242/jcs.033951.
21. Sabharanjak S, Sharma P, Parton RG, Mayor S, (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Developmental Cell 2: 411-423.
22. Ramprasad OG, Srinivas G, Rao KS, Joshi P, Thiery JP, et al. (2007) Changes in cholesterol levels in the plasma membrane modulate cell signaling and regulate cell adhesion and migration on fibronectin. Cell Motil Cytoskeleton 64: 199-216 doi:10.1002/cm.20176.
23. West MA, Bretscher MS, Watts C, (1989) Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 109: 2731-2739.
24. Zerial M, McBride H, (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117 doi:10.1038/35052055.
25. Stenmark H, (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525 doi:10.1038/nrm2728.
26. Schmidt N, Mishra A, Lai GH, Wong GCL, (2010) Arginine-rich cell-penetrating peptides. FEBS Letters 584: 1806-1813 doi:10.1016/j.febslet.2009.11.046.
27. Silvius JR, Zuckermann MJ, (1993) Interbilayer transfer of phospholipid-anchored macromolecules via monomer diffusion. Biochemistry 32: 3153-3161 doi:10.1021/bi00063a030.
28. Shahinian S, Silvius JR, (1995) Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34: 3813-3822 doi:10.1021/bi00011a039.
29. Zacharias DA, Violin JD, Newton AC, Tsien RY, (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916 doi:10.1126/science.1068539.
30. Chatterjee S, Mayor S, (2001) The GPI-anchor and protein sorting. Cell Mol Life Sci 58: 1969-1987.
31. Bhagatji P, Leventis R, Comeau J, Refaei M, Silvius JR, (2009) Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins. The Journal of Cell Biology 186: 615-628 doi:10.1083/jcb.200903102.
32. Mukherjee S, Soe TT, Maxfield FR, (1999) Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol 144: 1271-1284.
33. Wang T-Y, Leventis R, Silvius JR, (2005) Artificially lipid-anchored proteins can elicit clustering-induced intracellular signaling events in Jurkat T-lymphocytes independent of lipid raft association. J Biol Chem 280: 22839-22846 doi:10.1074/jbc.M502920200.