Neuropilin-1 and heparan sulfate proteoglycans cooperate in cellular uptake of nanoparticles functionalized by cationic cell-penetrating peptides

Science Advances

Volumn 1, Issue 10, 2015, Pages

  Pang, Hong Bo ^a   Braun, Gary B ^a,b   Ruoslahti, Erkki ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; CELL MEMBRANES; CYTOLOGY; ENZYME ACTIVITY; GLYCOPROTEINS; MAMMALS; MOLECULAR BIOLOGY; PEPTIDES; SULFUR COMPOUNDS;

CELL PENETRATING PEPTIDES (CPPS); CELL SURFACE RECEPTORS; CELL-PENETRATING PEPTIDE; ENDOSOMAL COMPARTMENTS; HEPARAN SULFATE PROTEOGLYCANS; INTRACELLULAR DELIVERY; PROTEOLYTIC PROCESSING; SYNCHRONIZATION METHOD;

CELLS;

EID: 85038614780     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500821     Document Type: Article

References (32)

1. N. Bertrand, J. Wu, X. Xu, N. Kamaly, O. C Farokhzad, Cancer nanotechnology: The impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 66, 2-25 (2014).
2. G. Ruan, A. Agrawal, A. I. Marcus, S. Nie, Imaging and tracking of tat peptide-conjugated quantum dots in living cells: New insights into nanoparticle uptake, intracellular transport, and vesicle shedding. J. Am. Chem. Soc. 129, 14759-14766 (2007).
3. F. Madani, S. Lindberg, Ü. Langel, S. Futaki, A. Gräslund, Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 414729 (2011).
4. I. M. Kaplan, J. S. Wadia, S. F. Dowdy, Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control. Release 102, 247-253 (2005).
5. M. Tyagi, M. Rusnati, M. Presta, M. Giacca, Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276, 3254-3261 (2001).
6. S. Console, C. Marty, C. García-Echeverría, R. Schwendener, K. Ballmer-Hofer, Antennapedia and HIV transactivator of transcription (TAT) "protein transduction domains" promote endo-cytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J. Biol. Chem. 278, 35109-35114 (2003).
7. J. M. Gump, S. F. Dowdy, TAT transduction: The molecular mechanism and therapeutic prospects. Trends Mol. Med. 13, 443-448 (2007).
8. T. Kadonosono, A. Yamano, T. Goto, T. Tsubaki, M. Niibori, T. Kuchimaru, S. Kizaka-Kondoh, Cell penetrating peptides improve tumor delivery of cargos through neuropilin-1-dependent extravasation. J. Control. Release 201, 14-21 (2015).
9. L. M. Ellis, The role of neuropilins in cancer. Mol. Cancer Ther. 5, 1099-1107 (2006).
10. A. Salikhova, L Wang, A. A. Lanahan, M. Liu, M. Simons, W. P.J. Leenders, D. Mukhopadhyay, A. Horowitz, Vascular endothelial growth factor and semaphorin induce neuropilin-1 endo-cytosis via separate pathways. Circ. Res. 103, e71-e79 (2008).
11. C. W. Vander Kooi, M. A. Jusino, B. Perman, D. B. Neau, H. D. Bellamy, D.J. Leahy, Structural basis for ligand and heparin binding to neuropilin B domains. Proc. Natl. Acad. Sci. U.S.A. 104, 6152-6157 (2007).
12. M. Teran, M. A. Nugent, Synergistic binding of vascular endothelial growth factor-A and its receptors to heparin selectively modulates complex affinity. J. Biol. Chem. 290, 16451-16462 (2015).
13. Y. Shintani, S. Takashima, Y. Asano, H. Kato, Y. Liao, S. Yamazaki, O. Tsukamoto, O. Seguchi, H. Yamamoto, T. Fukushima, K. Sugahara, M. Kitakaze, M. Hori, Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. EMBO J. 25, 3045-3055 (2006).
14. T. Teesalu, K. N. Sugahara, V. R. Kotamraju, E. Ruoslahti, C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl. Acad. Sci. USA. 106, 16157-16162 (2009).
15. D. Zanuy, R. Kotla, R. Nussinov, T. Teesalu, K. N. Sugahara, C. Alemán, N. Haspel, Sequence dependence of C-end rule peptides in binding and activation of neuropilin-1 receptor. J. Struct. Biol. 182, 78-86 (2013).
16. K. N. Sugahara, G. B. Braun, T. H. de Mendoza, V. R. Kotamraju, R. P. French, A. M. Lowy, T. Teesalu, E. Ruoslahti, Tumor-penetrating iRGD peptide inhibits metastasis. Mol. Cancer Ther. 14, 120-128 (2015).
17. H.-B. Pang, G. B. Braun, T. Friman, P. Aza-Blanc, M. E. Ruidiaz, K. N. Sugahara, T. Teesalu, E. Ruoslahti, An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability. Nat. Commun. 5, 4904 (2014).
18. E. Vivès, P. Brodin, B. Lebleu, 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 (1997).
19. F. Heitz, M. C. Morris, G. Divita, Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics. Br. J. Pharmacol. 157, 195-206 (2009).
20. K. N. Sugahara, T. Teesalu, P. Prakash Karmali, V. Ramana Kotamraju, L. Agemy, O. M. Girard, D. Hanahan, R. F. Mattrey, E. Ruoslahti, Tissue-penetrating delivery of compounds and na-noparticles into tumors. Cancer Cell 16, 510-520 (2009).
21. T. Teesalu, K. N. Sugahara, E. Ruoslahti, Tumor-penetrating peptides. Front. Oncol. 3, 216 (2013).
22. G. B. Braun, T. Friman, H.-B. Pang, A. Pallaoro, T. H. de Mendoza, A.-M. A. Willmore, V. Ramana Kotamraju, A. P. Mann, Z.-G. She, K. N. Sugahara, N. O. Reich, T. Teesalu, E. Ruoslahti, Etchable plasmonic nanoparticle probes to image and quantify cellular internalization. Nat. Mater. 13, 904-911 (2014).
23. M. Lundberg, S. Wikström, M. Johansson, Cell surface adherence and endocytosis of protein transduction domains. Mol. Ther. 8, 143-150 (2003).
24. Z. He, M. Tessier-Lavigne, Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90, 739-751 (1997).
25. M. W. Parker, A. D. Linkugel, C. W. Vander Kooi, Effect of C-terminal sequence on competitive semaphorin binding to neuropilin-1. J. Mol. Biol. 425, 4405-4414 (2013).
26. L. M. Acevedo, S. Barillas, S. M. Weis, J. R. Göthert, D. A. Cheresh, Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111, 2674-2680 (2008).
27. K. N. Sugahara, T. Teesalu, P. P. Karmali, V. R. Kotamraju, L. Agemy, D. R. Greenwald, E. Ruoslahti, Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328, 1031-1035 (2010).
28. V. P. Chauhan, T. Stylianopoulos, Y. Boucher, R. K. Jain, Delivery of molecular and nanoscale medicine to tumors: Transport barriers and strategies. Annu. Rev. Chem. Biomol. Eng. 2, 281-298 (2011).
29. M. Arese, C Ferrandi, L Primo, G. Camussi, F. Bussolino, HIV-1 Tat protein stimulates in vivo vascular permeability and lymphomononuclear cell recruitment. J. Immunol. 166, 1380-1388 (2001).
30. H. Hirose, T. Takeuchi, H. Osakada, S. Pujals, S. Katayama, I. Nakase, S. Kobayashi, T. Haraguchi, S. Futaki, Transient focal membrane deformation induced by arginine-rich peptides leads to their direct penetration into cells. Mol. Ther. 20, 984-993 (2012).
31. D. M. Ward, C. M. Perou, M. Lloyd, J. Kaplan, "Synchronized" endocytosis and intracellular sorting in alveolar macrophages: The early sorting endosome is a transient organelle. J. Cell Biol. 129, 1229-1240 (1995).
32. J. Kim, J. E. Lee, S. Heynen-Genel, E. Suyama, K. Ono, K. Lee, T. Ideker, P. Aza-Blanc, J. G. Gleeson, Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464, 1048-1051 (2010).