Polyplexes traffic through caveolae to the Golgi and endoplasmic reticulum en route to the nucleus

Molecular Pharmaceutics

Volumn 9, Issue 5, 2012, Pages 1280-1290

  Reilly, Meghan J ^a   Larsen, John D ^a   Sullivan, Millicent O ^a,b  

^a University of Delaware   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

endocytosis; endoplasmic reticulum; Golgi; histone peptides; intracellular trafficking; nonviral gene delivery; PEI; polyplexes

Indexed keywords

PLASMID DNA; POLYETHYLENEIMINE;

ARTICLE; CAVEOLA; CELL MIGRATION; CELL NUCLEUS; CELL TRANSPORT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GENE TARGETING; GOLGI COMPLEX; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL TRANSPORT; CAVEOLAE; CELL NUCLEUS; CHO CELLS; CRICETINAE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GENE TRANSFER TECHNIQUES; GOLGI APPARATUS; HISTONES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; PLASMIDS; POLYETHYLENEIMINE;

EID: 84860713305     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp200583d     Document Type: Article

References (68)

1. McLendon, P. M.; Fichter, K. M.; Reineke, T. M. Poly(glycoamidoamine) Vehicles Promote pDNA Uptake through Multiple Routes and Efficient Gene Expression via Caveolae-Mediated Endocytosis Mol. Pharmaceutics 2010, 7, 738-750
2. Khalil, I. A.; Kogure, K.; Akita, H.; Harashima, H. Uptake Pathways and Subsequent Intracellular Trafficking in Nonviral Gene Delivery Pharmacol. Rev. 2006, 58, 32-45
3. Medina-Kauwe, L.; Xie, J.; Hamm-Alvarez, S. Intracellular Trafficking of Nonviral Vectors Gene Ther. 2005, 12, 1734-1751
4. Midoux, P.; Breuzard, G.; Gomez, J. P.; Pichon, C. Polymer-Based Gene Delivery: A Current Review on the Uptake and Intracellular Trafficking of Polyplexes Curr. Gene Ther. 2008, 8, 335-352
5. Friend, D. S.; Papahadjopoulos, D.; Debs, R. J. Endocytosis and Intracellular Processing Accompanying Transfection Mediated by Cationic Liposomes Biochim. Biophys. Acta 1996, 1278, 41-50
6. Labat-Moleur, F.; Steffan, A. M.; Brisson, C.; Perron, H.; Feugeas, O.; Furstenberger, P.; Oberling, F.; Brambilla, E.; Behr, J. P. An Electron Microscopy Study into the Mechanism of Gene Transfer with Lipopolyamines Gene Ther. 1996, 3, 1010-1017
7. 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
8. Gabrielson, N. P.; Pack, D. W. Efficient Polyethylenimine-Mediated Gene Delivery Proceeds Via a Caveolar Pathway in HeLa Cells J. Controlled Release 2009, 136, 54-61
9. von Gersdorff, K.; Sanders, N. N.; Vandenbroucke, R.; De Smedt, S. C.; Wagner, E.; Ogris, M. The Internalization Route Resulting in Successful Gene Expression Depends on Polyethylenimine Both Cell Line and Polyplex Type Mol. Ther. 2006, 14, 745-753
10. 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
11. van der Aa, M. A.; Huth, U. S.; Hafele, S. Y.; Schubert, R.; Oosting, R. S.; Mastrobattista, E.; Hennink, W. E.; Peschka-Suss, R.; Koning, G. A.; Crommelin, D. J. Cellular Uptake of Cationic Polymer-DNA Complexes via Caveolae Plays a Pivotal Role in Gene Transfection in COS-7 Cells Pharm. Res. 2007, 24, 1590-1598
12. Palacios, A.; Moreno, A.; Oliveira, B. L.; Rivera, T.; Prieto, J.; Garcia, P.; Fernandez-Fernandez, M. R.; Bernado, P.; Palmero, I.; Blanco, F. J. The Dimeric Structure and the Bivalent Recognition of H3K4me3 by the Tumor Suppressor ING4 Suggests a Mechanism for Enhanced Targeting of the HBO1 Complex to Chromatin J. Mol. Biol. 2010, 396, 1117-1127
13. Hung, T.; Binda, O.; Champagne, K. S.; Kuo, A. J.; Johnson, K.; Chang, H. Y.; Simon, M. D.; Kutateladze, T. G.; Gozani, O. ING4Mediates Crosstalk between Histone H3 K4 Trimethylation and H3 Acetylation to Attenuate Cellular Transformation Mol. Cell 2009, 33, 248-256
14. Saksouk, N.; Avvakumov, N.; Champagne, K. S.; Hung, T.; Doyon, Y.; Cayrou, C.; Paquet, E.; Ullah, M.; Landry, A.; Cote, V.; Yang, X.; Gozani, O.; Kutateladze, T. G.; Cote, J. HBO1 HAT Complexes Target Chromatin throughout Gene Coding Regions via Multiple PHD Finger Interactions with Histone H3 Tail Mol. Cell 2009, 33, 257-265
15. Li, H. T.; Ilin, S.; Wang, W. K.; Duncan, E. M.; Wysocka, J.; Allis, C. D.; Patel, D. J. Molecular Basis for Site-Specific Read-Out of Histone H3K4me3 by the BPTF PHD Finger of NURF Nature 2006, 442, 91-95
16. Wysocka, J.; Swigut, T.; Xiao, H.; Milne, T. A.; Kwon, S. Y.; Landry, J.; Kauer, M.; Tackett, A. J.; Chait, B. T.; Badenhorst, P.; Wu, C.; Allis, C. D. A PHD Finger of NURF Couples Histone H3 Lysine 4 Trimethylation with Chromatin Remodelling Nature 2006, 442, 86-90
17. Boussif, O.; Lezoualch, 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
18. Pollard, H.; Remy, J. S.; Loussouarn, G.; Demolombe, S.; Behr, J. P.; Escande, D. Polyethylenimine but not Cationic Lipids Promotes Transgene Delivery to the Nucleus in Mammalian Cells J. Biol. Chem. 1998, 273, 7507-7511
19. Reilly, M. J.; Larsen, J. D.; Sullivan, M. O. Histone H3 Tail Peptides and Poly(ethylenimine) Have Synergistic Effects for Gene Delivery. Mol. Pharmaceutics, doi 10.1021/mp200372s.
20. Mineo, C.; Anderson, R. G. W. A Vacuolar-Type Proton ATPase Mediates Acidification of Plasmalemmal Vesicles During Potocytosis Exp. Cell Res. 1996, 224, 237-242
21. Palokangas, H.; Ying, M.; Vaananen, K.; Saraste, J. Retrograde Transport from the Pre-Golgi Intermediate Compartment and the Golgi Complex is Affected by the Vacuolar H+-ATPase Inhibitor Bafilomycin A1 Mol. Biol. Cell 1998, 9, 3561-3578
22. Hansen, C. G.; Nichols, B. J. Molecular Mechanisms of Clathrin-Independent Endocytosis J. Cell Sci. 2009, 122, 1713-1721
23. Parhamifar, L.; Larsen, A. K.; Hunter, A. C.; Andresen, T. L.; Moghimi, S. M. Polycation Cytotoxicity A Delicate Matter for Nucleic Acid Therapy-Focus on Polyethylenimine Soft Matter 2010, 6, 4001-4009
24. Pelkmans, L.; Puntener, D.; Helenius, A. Local Actin Polymerization and Dynamin Recruitment in SV40-Induced Internalization of Caveolae Science 2002, 296, 535-539
25. Pelkmans, L.; Kartenbeck, J.; Helenius, A. Caveolar Endocytosis of Simian Virus 40 Reveals a New Two-step Vesicular-Transport Pathway to the ER Nat. Cell Biol. 2001, 3, 473-483
26. Nichols, B. J. A Distinct Class of Endosome Mediates Clathrin-independent Endocytosis to the Golgi Complex Nat. Cell Biol. 2002, 4, 374-378
27. Nichols, B. J.; Lippincott-Schwartz, J. Endocytosis without Clathrin Coats Trends Cell Biol. 2001, 11, 406-412
28. Nim, S.; Le, P. U.; Dennis, J.; Nabi, I. R. Endocytosis of Cholera Toxin to the Golgi Apparatus is Negatively Regulated by Caveolin-1 Mol. Biol. Cell 2002, 13, 230A-230A
29. Le, P.; Nabi, I. Distinct Caveolae-Mediated Endocytic Pathways Target the Golgi Apparatus and the Endoplasmic Reticulum J. Cell Sci. 2003, 116, 1059-1071
30. Le, P. U.; Guay, G.; Altschuler, Y.; Nabi, I. R. Caveolin-1 is a Negative Regulator of Caveolae-Mediated Endocytosis to the Endoplasmic Reticulum J. Biol. Chem. 2002, 277, 3371-3379
31. Maxfield, F. R.; McGraw, T. E. Endocytic Recycling Nat. Rev. Mol. Cell Biol. 2004, 5, 121-132
32. Luzio, J. P.; Mullock, B. M.; Pryor, P. R.; Lindsay, M. R.; James, D. E.; Piper, R. C. Relationship between Endosomes and Lysosomes Biochem. Soc. Trans. 2001, 29, 476-480
33. Wang, L. H.; Rothberg, K. G.; Anderson, R. G. W. Mis-Assembly of Clathrin Lattices on Endosomes Reveals a Regulatory Switch for Coated Pit Formation J. Cell Biol. 1993, 123, 1107-1117
34. Ming, X.; Alam, M. R.; Fisher, M.; Yan, Y.; Chen, X.; Juliano, R. L. Intracellular Delivery of an Antisense Oligonucleotide via Endocytosis of a G Protein-Coupled Receptor Nucleic Acids Res. 2010, 38, 6567-6576
35. Lombardi, D.; Soldati, T.; Riederer, M. A.; Goda, Y.; Zerial, M.; Pfeffer, S. R. Rab9 Functions in Transport between Late Endosomes and the Trans Golgi Network EMBO J. 1993, 12, 677-682
36. Millili, P. G.; Yin, D. H.; Fan, H.; Naik, U. P.; Sullivan, M. O. Formulation of a Peptide Nucleic Acid Based Nucleic Acid Delivery Construct Bioconjugate Chem. 2010, 21, 445-455
37. Javanmoghadam-Kamrani, S.; Keyomarsi, K. Synchronization of the Cell Cycle Using Lovastatin Cell Cycle 2008, 7, 2434-2440
38. Wu, J. R.; Gilbert, D. M. Lovastatin Arrests CHO Cells between the Origin Decision Point and the Restriction Point FEBS Lett. 2000, 484, 108-112
39. Ivanov, A. I. Pharmacological Inhibition of Endocytic Pathways: Is It Specific Enough to Be Useful? Methods Mol. Biol. 2008, 440, 15-33
40. Huth, U. S.; Schubert, R.; Peschka-Suss, R. Investigating the Uptake and Intracellular Fate of pH-Sensitive Liposomes by Flow Cytometry and Spectral Bio-Imaging J. Controlled Release 2006, 110, 490-504
41. Ferreira, D.; Cortez, M.; Atayde, V. D.; Yoshida, N. Actin Cytoskeleton-Dependent and -Independent Host Cell Invasion by Trypanosoma Cruzi Is Mediated by Distinct Parasite Surface Molecules Infect. Immun. 2006, 74, 5522-5528
42. Macia, E.; Ehrlich, M.; Massol, R.; Boucrot, E.; Brunner, C.; Kirchhausen, T. Dynasore, a Cell-Permeable Inhibitor of Dynamin Dev. Cell 2006, 10, 839-850
43. Akiyama, T.; Ishida, J.; Nakagawa, S.; Ogawara, H.; Watanabe, S.; Itoh, N.; Shibuya, M.; Fukami, Y.; Genistein, A Specific Inhibitor of Tyrosine-Specific Protein Kinases J. Biol. Chem. 1987, 262, 5592-5595
44. Manders, E. M. M.; Verbeek, F. J.; Aten, J. A. Measurement of Co-Localization of Objects in Dual-Colour Confocal Images J. Microsc. 1993, 169, 375-382
45. Henley, J.; Krueger, E.; Oswald, B.; McNiven, M. Dynamin-Mediated Internalization of Caveolae J. Cell Biol. 1998, 141, 85-99
46. Lamaze, C.; Fujimoto, L. M.; Yin, H. L.; Schmid, S. L. The Actin Cytoskeleton Is Required for Receptor-Mediated Endocytosis in Mammalian Cells J. Biol. Chem. 1997, 272, 20332-20335
47. Durrbach, A.; Louvard, D.; Coudrier, E. Actin Filaments Facilitate Two Steps of Endocytosis J. Cell Sci. 1996, 109, 457-465
48. Goncalves, C.; Mennesson, E.; Fuchs, R.; Gorvel, J.; Midoux, P.; Pichon, C. Macropinocytosis of Polyplexes and Recycling of Plasmid Via the Clathrin-Dependent Pathway Impair the Transfection Efficiency of Human Hepatocarcinoma Cells Mol. Ther. 2004, 10, 373-385
49. Nabi, I. R.; Le, P. U. Caveolae/Raft-Dependent Endocytosis J. Cell Biol. 2003, 161, 673-677
50. Swanson, J. A.; Watts, C. Macropinocytosis Trends Cell Biol. 1995, 5, 424-428
51. Orlandi, P. A.; Fishman, P. H. Filipin-Dependent Inhibition of Cholera Toxin: Evidence for Toxin Internalization and Activation through Caveolae-like Domains J. Cell Biol. 1998, 141, 905-915
52. Zinchuk, V.; Zinchuk, O.; Okada, T. Quantitative Colocalization Analysis of Multicolor Confocal Immunofluorescence Microscopy Images: Pushing Pixels to Explore Biological Phenomena Acta Histochem. Cytochem. 2007, 40, 101-111
53. Hufnagel, H.; Hakim, P.; Lima, A.; Hollfelder, F. Fluid Phase Endocytosis Contributes to Transfection of DNA by PEI-25 Mol. Ther. 2009, 17, 1411-1417
54. Larsen, J. D.; Reilly, M. J.; Sullivan, M. O. Using the Epigenetic Code To Promote the Unpackaging and Transcriptional Activation of DNA Polyplexes for Gene Delivery. Mol. Pharmaceutics 2012, in press.
55. Thomsen, P.; Roepstorff, K.; Stahlhut, M.; van Deurs, B. Caveolae are Highly Immobile Plasma Membrane Microdomains, Which are Not Involved in Constitutive Endocytic Trafficking Mol. Biol. Cell 2002, 13, 238-250
56. Wacker, I.; Kaether, C.; Kromer, A.; Migala, A.; Almers, W.; Gerdes, H. H. Microtubule-Dependent Transport of Secretory Vesicles Visualized in Real Time with a GFP-Tagged Secretory Protein J. Cell Sci. 1997, 110, 1453-1463
57. Amstutz, B.; Gastaldelli, M.; Kalin, S.; Imelli, N.; Boucke, K.; Wandeler, E.; Mercer, J.; Hemmi, S.; Greber, U. F. Subversion of CtBP1-Controlled Macropinocytosis by Human Adenovirus Serotype 3 EMBO J. 2008, 27, 956-969
58. Damke, H.; Baba, T.; van der Bliek, A. M.; Schmid, S. L. Clathrin-Independent Pinocytosis Is Induced in Cells Overexpressing a Temperature-Sensitive Mutant of Dynamin J. Cell Biol. 1995, 131, 69-80
59. Damke, H.; Baba, T.; Warnock, D. E.; Schmid, S. L. Induction of Mutant Dynamin Specifically Blocks Endocytic Coated Vesicle Formation J. Cell Biol. 1994, 127, 915-934
60. Akinc, A.; Thomas, M.; Klibanov, A. M.; Langer, R. Exploring Polyethylenimine-Mediated DNA Transfection and the Proton Sponge Hypothesis J. Gene Med. 2005, 7, 657-663
61. Pelkmans, L.; Burli, T.; Zerial, M.; Helenius, A. Caveolin-Stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic Cell 2004, 118, 767-780
62. Morinaga, N.; Yahiro, K.; Matsuura, G.; Watanabe, M.; Nomura, F.; Moss, J.; Noda, M. Two Distinct Cytotoxic Activities of Subtilase Cytotoxin Produced by Shiga-Toxigenic Escherichia coli Infect. Immun. 2007, 75, 488-496
63. Chong, D. C.; Paton, J. C.; Thorpe, C. M.; Paton, A. W. Clathrin-Dependent Trafficking of Subtilase Cytotoxin, A Novel AB5 Toxin That Targets the Endoplasmic Reticulum Chaperone BiP Cell. Microbiol. 2008, 10, 795-806
64. Hariton-Gazal, E.; Rosenbluh, J.; Graessmann, A.; Gilon, C.; Loyter, A. Direct Translocation of Histone Molecules across Cell Membranes J. Cell Sci. 2003, 116, 4577-4586
65. Kaouass, M.; Beaulieu, R.; Balicki, D. Histonefection: Novel and Potent Non-Viral Gene Delivery J. Controlled Release 2006, 113, 245-254
66. Murphy, R. F.; Jorgensen, E. D.; Cantor, C. R. Kinetics of Histone Endocytosis in Chinese-Hamster Ovary Cells-A Flow Cytofluorometric Analysis J. Biol. Chem. 1982, 257, 1695-1701
67. Xu, Z.; Gong, Q.; Xia, B.; Groves, B.; Zimmermann, M.; Mugler, C.; Mu, D.; Matsumoto, B.; Seaman, M.; Ma, D. A Role of Histone H3 Lysine 4 Methyltransferase Components in Endosomal Trafficking J. Cell Biol. 2009, 186, 343-353
68. Wu, C. C.; MacCoss, M. J.; Mardones, G.; Finnigan, C.; Mogelsvang, S.; Yates, J. R., 3rd; Howell, K. E. Organellar Proteomics Reveals Golgi Arginine Dimethylation Mol. Biol. Cell 2004, 15, 2907-2919