Biochemical investigation of active intracellular transport of polymeric gene-delivery vectors

Journal of Pharmaceutical Sciences

Volumn 97, Issue 4, 2008, Pages 1399-1413

  Drake, David M ^a   Pack, Daniel W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Active transport; Gene delivery; Intracellular trafficking; Microtubules; Molecular motors; Nonviral vectors; PEI

Indexed keywords

9 (2 HYDROXY 3 NONYL)ADENINE; ACTIN; ADENOSINE TRIPHOSPHATASE INHIBITOR; ADENYLYLIMIDODIPHOSPHATE; COLCHICINE; CYTOCHALASIN D; CYTOSKELETON PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; LACTONE; MOLECULAR MOTOR; PACLITAXEL; PLASMID DNA; POLYETHYLENEIMINE; POLYMER; ROSE BENGAL; VANADIC ACID;

ACTIVE TRANSPORT; ARTICLE; CANCER CELL CULTURE; CELL STRAIN HEK293; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DEPOLYMERIZATION; DRUG EFFECT; ENDOCYTOSIS; FLOW CYTOMETRY; GENE DELIVERY SYSTEM; GENE THERAPY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MICROTUBULE; NONVIRAL GENE DELIVERY SYSTEM; PROTEIN EXPRESSION; TRANSGENE; CELL LINE; DRUG ANTAGONISM; GENE VECTOR; METABOLISM; PHYSIOLOGY;

ACTINS; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; CYTOCHALASIN D; DYNEIN ATPASE; GENE THERAPY; GENETIC VECTORS; HUMANS; KINESIN; MICROTUBULES; POLYETHYLENEIMINE;

EID: 42049093679     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.21106     Document Type: Article

References (53)

1. Scollay R. 2001. Gene therapy: A brief overview of the past, present, and future. Annu NY Acad Sci 953:26-30.
2. Verma IM, Somia N. 1997. Gene therapy - Promises, problems and prospects. Nature 389:239-242.
3. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP. 1995. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: Polyethylenimine. Proc Natl Acad Sci USA 92:7297-7301.
4. Pack DW, Hoffman AS, Pun S, Stayton PS. 2005. Design and development of polymers for gene delivery. Nat Rev Drug Disc 4:581-593.
5. Samaj J, Baluska F, Voigt B, Schlicht M, Volkmann D, Menzel D. 2004. Endocytosis, actin cytoskeleton, and signaling. Plant Physiol 135: 1150-1161.
6. Nichols BJ, Lippincott-Schwartz J. 2001. Endocytosis without clathrin coats. Trends Cell Biol 11: 406-412.
7. Sigismund S,Woelk T, Puri C,Maspero E,Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA 102:2760-2765.
8. Suh J, Wirtz D, Hanes J. 2003. Efficient active transport of gene nanocarriers to the cell nucleus. Proc Natl Acad Sci USA 100:3878-3882.
9. Suh J, Wirtz D, Hanes J. 2004. Real-time intracellular transport of gene nanocarriers studied by multiple particle tracking. Biotechnol Prog 20:598-602.
10. Forrest ML, Pack DW. 2002. On the kinetics of polyplex endocytic trafficking: Implications for gene delivery vector design. Mol Ther 6:57-66.
11. Akinc A, Thomas M, Klibanov AM, Langer R. 2005. Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis. J Gene Med 7:657-663.
12. Kichler A, Leborgne C, Marz J, Danos O, Bechinger B. 2003. Histidine-rich amphipathic peptide antibiotics promote efficient delivery of DNA into mammalian cells. Proc Natl Acad Sci USA 100:1564-1568.
13. Douar AM, Poulard K, Stockholm D, Danos O. 2001. Intracellular trafficking of adeno-associated virus vectors: Routing to the late endosomal compartment and proteasome degradation. J Virol 75:1824-1833.
14. Kim J, Chen CP, Rice KG. 2005. The proteasome metabolizes peptide-mediated nonviral gene delivery systems. Gene Ther 12:1581-1590.
15. Goddette DW, Frieden C. 1986. Actin polymerization. The mechanism of action of cytochalasin D. J Biol Chem 261:15974-15980.
16. Skoufias DA, Wilson L. 1992. Mechanism of inhibition of microtubule polymerization by colchicine: Inhibitory potencies of unliganded colchicine and tubulin-colchicine complexes. Biochem 31:738-746.
17. Yvon AM, Wadsworth P, Jordan MA. 1999. Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell 10: 947-959.
18. Bouchard P, Penningroth SM, Cheung A, Gagnon C, Bardin CW. 1981. erythro-9-[3-(2-Hydroxynonyl)]adenine is an inhibitor of sperm motility that blocks dynein ATPase and protein carboxylmethylase activities. Proc Natl Acad Sci USA 78:1033-1036.
19. Kobayashi T, Martensen T, Nath J, Flavin M. 1978. Inhibition of dynein ATPase by vanadate, and its possible use as a probe for the role of dynein in cytoplasmic motility. Biochem Biophys Res Commun 81:1313-1318.
20. Hopkins SC, Vale RD, Kuntz ID. 2000. Inhibitors of kinesin activity from structure-based computer screening. Biochem 39:2805-2814.
21. Bananis E, Murray JW, Stockert RJ, Satir P, Wolkoff AW. 2000. Microtubule and motor-dependent endocytic vesicle sorting in vitro. J Cell Biol 151:179-186.
22. Hasegawa S, Hirashima N, Nakanishi M. 2001. Microtubule involvement in the intracellular dynamics for gene transfection mediated by cationic liposomes. Gene Ther 8:1669-1673.
23. Wang L, MacDonald RC. 2004. Effects of micro-tubule-depolymerizing agents on the transfection of cultured vascular smooth muscle cells: Enhanced expression with free drug and especially with drug-gene lipoplexes. Mol Ther 9:729-737.
24. Stevens MG, Olsen SC. 1993. Comparative analysis of using MTT and XTT in colorimetric assays for quantitating bovine neutrophil bactericidal activity. J Immunol Methods 157:225-231.
25. Cooper JA. 1987. Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473-1478.
26. Rogers SL, Gelfand VI. 2000. Membrane trafficking, organelle transport, and the cytoskeleton. Curr Opin Cell Biol 12:57-62.
27. Mellman I. 1996. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12:575-625.
28. Brady ST. 1991. Molecular motors in the nervous system. Neuron 7:521-533.
29. Schaeffer HJ, Schwender CF. 1974. Enzyme inhibitors. 26. Bridging hydrophobic and hydrophilic regions on adenosine deaminase with some 9-(2-hydroxy-3-alkyl)adenines. J Med Chem 17:6-8.
30. Vallee RB, Shpetner HS. 1990. Motor proteins of cytoplasmic microtubules. Annu Rev Biochem 59: 909-932.
31. Hirokawa N. 1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519-526.
32. Karcher RL, Deacon SW, Gelfand VI. 2002. Motor-cargo interactions: The key to transport specificity. Trends Cell Biol 12:21-27.
33. Murray JW, Bananis E, Wolkoff AW. 2000. Reconstitution of ATP-dependent movement of endocytic vesicles along microtubules in vitro: An oscillatory bidirectional process. Mol Biol Cell 11:419-433.
34. Bananis E, Nath S, Gordon K, Satir P, Stockert RJ, Murray JW, Wolkoff AW. 2004. Microtubule-dependent movement of late endocytic vesicles in vitro: Requirements for dynein and kinesin. Mol Biol Cell 15:3688-3697.
35. McGovern SL, Caselli E, Grigorieff N, Shoichet BK. 2002. A common mechanism underlying promiscuous inhibitors from virtual and high-throughput screening. J Med Chem 45:1712-1722.
36. Kichler A, Leborgne C, Coeytaux E, Danos O. 2001. Polyethylenimine- mediated gene delivery: A mechanistic study. J Gene Med 3:135-144.
37. Medina-Kauwe LK, Xie J, Hamm-Alvarez S. 2005. Intracellular trafficking of nonviral vectors. Gene Ther 12:1734-1751.
38. Carlier MF, Criquet P, Pantaloni D, Korn ED. 1986. Interaction of cytochalasin D with actin filaments in the presence of ADP and ATP. J Biol Chem 261:2041-2050.
39. Jeng RL, Welch MD. 2001. Cytoskeleton: Actin and endocytosis - No longer the weakest link. Curr Biol 11:R691-R694.
40. Mukherjee S, Ghosh RN, Maxfield FR. 1997. Endocytosis. Physiol Rev 77:759-803.
41. Heinzelmann M, Platz A, Flodgaard H, Polk HC Jr, Miller FN. 1999. Endocytosis of heparin-binding protein (CAP37) is essential for the enhancement of lipopolysaccharide-induced TNF-alpha production in human monocytes. J Immunol 162: 4240-4245.
42. Jackman MR, Shurety W, Ellis JA, Luzio JP. 1994. Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J Cell Sci 107:2547-2556.
43. Fujimoto LM, Roth R, Heuser JE, Schmid SL. 2000. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1:161-171.
44. Bayer N, Schober D, Prchla E, Murphy RF, Blaas D, Fuchs R. 1998. Effect of bafilomycin Al and nocodazole on endocytic transport in HeLa cells: Implications for viral uncoating and infection. J Virol 72:9645-9655.
45. Panda D, Jordan MA, Chu KC, Wilson L. 1996. Differential effects of vinblastine on polymerization and dynamics at opposite microtubule ends. J Biol Chem 271:29807-29812.
46. Kulkarni RP, Castelino K, Majumdar A, Fraser SE. 2006. Intracellular transport dynamics of endo-somes containing DNA polyplexes along the microtubule network. Biophys J 90:L42-L44.
47. Sonee M, Barron E, Yarber FA, Hamm-Alvarez SF. 1998. Taxol inhibits endosomal-lysosomal membrane trafficking at two distinct steps in CV-1 cells. Am J Physiol 275:C1630-C1639.
48. Wagner OI, Ascano J, Tokito M, Leterrier JF, Janmey PA, Holzbaur EL. 2004. The interaction of neurofilaments with the microtubule motor cytoplasmic dynein. Mol Biol Cell 15:5092-5100.
49. Bhalla KN. 2003. Microtubule-targeted anticancer agents and apoptosis. Oncogene 22:9075-9086.
50. Seargeant LE, Stinson RA. 1979. Inhibition of human alkaline phosphatases by vanadate. Biochem J 181:247-250.
51. Kashina AS, Baskin RJ, Cole DG, Wedaman KP, Saxton WM, Scholey JM. 1996. A bipolar kinesin. Nature 379:270-272.
52. Matuliene J, Essner R, Ryu J, Hamaguchi Y, Baas PW, Haraguchi T, Hiraoka Y, Kuriyama R. 1999. Function of a minus-end-directed kinesin-like motor protein in mammalian cells. J Cell Sci 112: 4041-4050.
53. Leopold PL, Pfister KK. 2006. Viral strategies for intracellular trafficking: Motors and microtubules. Traffic 7:516-523.