Nonviral gene delivery vectors use syndecan-dependent transport mechanisms in filopodia to reach the cell surface

ACS Nano

Volumn 6, Issue 8, 2012, Pages 7521-7532

  Rehman, Zia Ur ^a   Sjollema, Klaas A ^a   Kuipers, Jeroen ^a   Hoekstra, Dick ^a   Zuhorn, Inge S ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

actin retrograde flow; filopodial extensions; lipo polyplexes; polycationic nanocarriers

Indexed keywords

ACTIN POLYMERIZATION; CATIONIC LIPIDS; CELL BODIES; CELL SURFACES; DELIVERY DEVICE; EXPERIMENTAL APPROACHES; EXPERIMENTAL CONDITIONS; FILOPODIAL EXTENSIONS; INFECTIOUS PARTICLES; LIPO/POLYPLEXES; LIPOPLEXES; LOCAL CLUSTERING; MICROSCOPIC ANALYSIS; MOTOR PROTEINS; MULTIVALENT INTERACTIONS; MYOSIN II; NANOCARRIERS; NON-VIRAL GENE DELIVERY; PATHOGENIC BACTERIUM; POLYPLEXES; RETROGRADE FLOW; SURFACE INTERACTIONS; TRANSPORT MECHANISM;

CELL MEMBRANES; FUNCTIONAL POLYMERS; GENE THERAPY; GENE TRANSFER; MOLECULAR BIOLOGY; NUCLEIC ACIDS; VIRUSES;

PROTEINS;

DNA; NANOCAPSULE; SYNDECAN;

ARTICLE; CHEMISTRY; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; METHODOLOGY; PSEUDOPODIUM; ULTRASTRUCTURE;

DNA; GENETIC VECTORS; NANOCAPSULES; PSEUDOPODIA; SYNDECANS; TRANSFECTION;

EID: 84865596170     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn3028562     Document Type: Article

References (40)

1. Kamimura, K.; Suda, T.; Zhang, G.; Liu, D. Advances in gene delivery systems Pharm. Med. 2011, 25, 293-306
2. Boussif, O.; Lezoualc'h, F.; Zanta, M. A.; Mergny, M. D.; Scherman, D.; Demeneix, B.; Behr, J. P. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: Polyethylenimine Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 7297-7301
3. Simoes, S.; Slepushkin, V.; Pires, P.; Gaspar, R.; de Lima, M. P.; Duzgunes, N. Mechanisms of gene transfer mediated by lipoplexes associated with targeting ligands or pH-sensitive peptides Gene Ther. 1999, 6, 1798-1807
4. Elouahabi, A.; Ruysschaert, J. M. Formation and intracellular trafficking of lipoplexes and polyplexes Mol. Ther. 2005, 11, 336-347
5. Zuhorn, I. S.; Kalicharan, R.; Hoekstra, D. Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis J. Biol. Chem. 2002, 277, 18021-18028
6. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis Biochem. J. 2004, 377, 159-169
7. Rejman, J.; Bragonzi, A.; Conese, M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes Mol. Ther. 2005, 12, 468-474
8. ur Rehman, Z.; Hoekstra, D.; Zuhorn, I. S. Protein kinase A inhibition modulates the intracellular routing of gene delivery vehicles in HeLa cells, leading to productive transfection J. Controlled Release 2011, 156, 76-84
9. Zuhorn, I. S.; Kalicharan, D.; Robillard, G. T.; Hoekstra, D. Adhesion receptors mediate efficient non-viral gene delivery Mol. Ther. 2007, 15, 946-953
10. Kopatz, I.; Remy, J. S.; Behr, J. P. A model for non-viral gene delivery: Through syndecan adhesion molecules and powered by actin J. Gene Med. 2004, 6, 769-776
11. Ruponen, M.; Ronkko, S.; Honkakoski, P.; Pelkonen, J.; Tammi, M.; Urtti, A. Extracellular glycosaminoglycans modify cellular trafficking of lipoplexes and polyplexes J. Biol. Chem. 2001, 276, 33875-33880
12. Giroglou, T.; Florin, L.; Schafer, F.; Streeck, R. E.; Sapp, M. Human papillomavirus infection requires cell surface heparan sulfate J. Virol. 2001, 75, 1565-1570
13. Spillmann, D. Heparan sulfate: Anchor for viral intruders? Biochimie 2001, 83, 811-817
14. Barth, H.; Schafer, C.; Adah, M. I.; Zhang, F.; Linhardt, R. J.; Toyoda, H.; Kinoshita-Toyoda, A.; Toida, T.; Van Kuppevelt, T. H.; Depla, E. et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate J. Biol. Chem. 2003, 278, 41003-41012
15. Bacsa, S.; Karasneh, G.; Dosa, S.; Liu, J.; Valyi-Nagy, T.; Shukla, D. Syndecan-1 and syndecan-2 play key roles in herpes simplex virus type-1 infection J. Gen. Virol. 2011, 92, 733-743
16. Menozzi, F. D.; Reddy, V. M.; Cayet, D.; Raze, D.; Debrie, A. S.; Dehouck, M. P.; Cecchelli, R.; Locht, C. Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions Microbes Infect. 2006, 8, 1-9
17. Smith, M. F., Jr; Novotny, J.; Carl, V. S.; Comeau, L. D. Helicobacter pylori and toll-like receptor agonists induce syndecan-4 expression in an NF-kappaB-dependent manner Glycobiology 2006, 16, 221-229
18. Schelhaas, M.; Ewers, H.; Rajamaki, M. L.; Day, P. M.; Schiller, J. T.; Helenius, A. Human papillomavirus type 16 entry: Retrograde cell surface transport along actin-rich protrusions PLoS Pathog. 2008, 4, e1000148
19. Lehmann, M. J.; Sherer, N. M.; Marks, C. B.; Pypaert, M.; Mothes, W. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells J. Cell Biol. 2005, 170, 317-325
20. Paris, S.; Burlacu, A.; Durocher, Y. Opposing roles of syndecan-1 and syndecan-2 in polyethyleneimine-mediated gene delivery J. Biol. Chem. 2008, 283, 7697-7704
21. Mattila, P. K.; Lappalainen, P. Filopodia: molecular architecture and cellular functions Nat. Rev. Mol. Cell Biol. 2008, 9, 446-454
22. Sherer, N. M.; Lehmann, M. J.; Jimenez-Soto, L. F.; Horensavitz, C.; Pypaert, M.; Mothes, W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission Nat. Cell Biol. 2007, 9, 310-315
23. Oh, M. J.; Akhtar, J.; Desai, P.; Shukla, D. A role for heparan sulfate in viral surfing Biochem. Biophys. Res. Commun. 2010, 391, 176-181
24. Romero, S.; Grompone, G.; Carayol, N.; Mounier, J.; Guadagnini, S.; Prevost, M. C.; Sansonetti, P. J.; Van Nhieu, G. T. ATP-mediated Erk1/2 activation stimulates bacterial capture by filopodia, which precedes Shigella invasion of epithelial cells Cell. Host Microbe 2011, 9, 508-519
25. Mislick, K. A.; Baldeschwieler, J. D. Evidence for the role of proteoglycans in cation-mediated gene transfer Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12349-12354
26. Ernst, S.; Langer, R.; Cooney, C. L.; Sasisekharan, R. Enzymatic degradation of glycosaminoglycans Crit. Rev. Biochem. Mol. Biol. 1995, 30, 387-444
27. Vercauteren, D.; Piest, M.; van der Aa, L. J.; Al Soraj, M.; Jones, A. T.; Engbersen, J. F.; De Smedt, S. C.; Braeckmans, K. Flotillin-dependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(amido amine)/DNA polyplexes Biomaterials 2011, 32, 3072-3084
28. Lidke, D. S.; Lidke, K. A.; Rieger, B.; Jovin, T. M.; Arndt-Jovin, D. J. Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors J. Cell Biol. 2005, 170, 619-626
29. Rustom, A.; Saffrich, R.; Markovic, I.; Walther, P.; Gerdes, H. H. Nanotubular highways for intercellular organelle transport Science 2004, 303, 1007-1010
30. Onfelt, B.; Nedvetzki, S.; Yanagi, K.; Davis, D. M. Cutting edge: Membrane nanotubes connect immune cells J. Immunol. 2004, 173, 1511-1513
31. Onfelt, B.; Purbhoo, M. A.; Nedvetzki, S.; Sowinski, S.; Davis, D. M. Long-distance calls between cells connected by tunneling nanotubules Sci. STKE 2005, 2005, pe55
32. Sherer, N. M.; Mothes, W. Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis Trends Cell Biol. 2008, 18, 414-420
33. Sowinski, S.; Jolly, C.; Berninghausen, O.; Purbhoo, M. A.; Chauveau, A.; Kohler, K.; Oddos, S.; Eissmann, P.; Brodsky, F. M.; Hopkins, C. et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission Nat. Cell Biol. 2008, 10, 211-219
34. Hope, T. J. Bridging efficient viral infection Nat. Cell Biol. 2007, 9, 243-244
35. Gallo, G.; Letourneau, P. C. Regulation of growth cone actin filaments by guidance cues J. Neurobiol. 2004, 58, 92-102
36. Freissler, E.; Meyer auf der Heyde, A.; David, G.; Meyer, T. F.; Dehio, C. Syndecan-1 and syndecan-4 can mediate the invasion of OpaHSPG-expressing Neisseria gonorrhoeae into epithelial cells Cell. Microbiol. 2000, 2, 69-82
37. Lin, C. H.; Espreafico, E. M.; Mooseker, M. S.; Forscher, P. Myosin drives retrograde F-actin flow in neuronal growth cones Neuron 1996, 16, 769-782
38. Welch, M. D.; Mallavarapu, A.; Rosenblatt, J.; Mitchison, T. J. Actin dynamics in vivo Curr. Opin. Cell Biol. 1997, 9, 54-61
39. Straight, A. F.; Cheung, A.; Limouze, J.; Chen, I.; Westwood, N. J.; Sellers, J. R.; Mitchison, T. J. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor Science 2003, 299, 1743-1747
40. Mao, Y. S.; Yamaga, M.; Zhu, X.; Wei, Y.; Sun, H. Q.; Wang, J.; Yun, M.; Wang, Y.; Di Paolo, G.; Bennett, M. et al. Essential and unique roles of PIP5K-γ and -α in Fcγ receptor-mediated phagocytosis J. Cell Biol. 2009, 184, 281-296