Uptake and trafficking of DNA in keratinocytes: Evidence for DNA-binding proteins

Gene Therapy

Volumn 11, Issue 9, 2004, Pages 765-774

  Basner Tschakarjan, E ^a   Mirmohammadsadegh, A ^a   Baer, A ^a   Hengge, U R ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

DNA binding proteins; Ezrin; Keratinocytes; Plasmid DNA; Receptor mediated uptake; Trafficking

Indexed keywords

AMILORIDE; AMILORIDE DERIVATIVE; CELL RECEPTOR; CHLORPROMAZINE; CLATHRIN; CYCLOHEXIMIDE; DIGOXIGENIN; DNA BINDING PROTEIN; EPIDERMAL GROWTH FACTOR; EZRIN; FILIPIN; FLUORESCEIN ISOTHIOCYANATE; GREEN FLUORESCENT PROTEIN; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; MOESIN; NAKED DNA; NYSTATIN; PLASMID DNA; RNA;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CATTLE; CAVEOLA; CELL LABELING; CELL SURFACE; CELL TRANSPORT; CELLULAR DISTRIBUTION; COATED PIT; CONCENTRATION RESPONSE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA BINDING; ENDOSOME; EXPRESSION VECTOR; EXTRACTION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; KERATINOCYTE; LYSOSOME; MASS SPECTROMETRY; MATERIAL COATING; MEASUREMENT; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SOUTHWESTERN BLOTTING; THYMUS; TIME;

ANIMALS; CATTLE; CELLS, CULTURED; CYCLOHEXIMIDE; CYTOSKELETAL PROTEINS; DNA; DNA-BINDING PROTEINS; ENDOCYTOSIS; EPIDERMIS; HUMANS; KERATINOCYTES; MICROFILAMENT PROTEINS; PHOSPHOPROTEINS; PLASMIDS; PROTEIN SYNTHESIS INHIBITORS;

VECTORS;

EID: 2442645112     PISSN: 09697128     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.gt.3302221     Document Type: Article

References (70)

1. Hengge UR et al. Cytokine gene expression in epidermis with biological effects following injection of naked DNA. Nat Genet 1995; 10: 161-166.
2. Hengge UR, Walker PS, Vogel JC. Expression of naked DNA in human, pig and mouse skin. J Clin Invest 1996; 97: 2911-2916.
3. Condon C et al. DNA-based immunization by in vivo transfection of dendritic cells. Nat Med 1996; 2: 1122-1128.
4. Fan H, Lin Q, Morrissey GR, Khavari PA. Immunization via hair follicles by topical application of naked DNA to normal skin. Nat Biotechnol 1999; 17: 870-872.
5. Yu WH et al. Topical gene delivery to murine skin. J Invest Dermatol 1999; 112: 370-375.
6. Domashenko A, Gupta S, Cotsarelis G. Efficient delivery of transgenes to human hair follicle progenitor cells using topical lipoplex. Nat Biotechnol 2000; 18: 420-423.
7. Udvardi A et al. Uptake of exogenous DNA via the skin. J Mol Med 1999; 77: 744-750.
8. Wolff JA et al. Expression of naked plasmids by cultured myotubes and entry of plasmids into T tubules and caveolae of mammalian skeletal muscle. J Cell Sci 1992; 103: 1249-1259.
9. Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998; 67: 199-225.
10. Mukherjee S, Gnosh RN, Maxfield FR. Endocytosis. Physiol Rev 1997; 77: 759-790.
11. Kwiatkowska K, Sobota A. Signaling pathways in phagocytosis. BioEssays 1999; 5: 422-431.
12. Gottlieb TA, Ivanov IE, Adesnik M, Sabatini DD. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 1993; 120: 695-710.
13. Marchese C et al. Receptor-mediated endocytosis of keratinocyte growth factor. J Cell Sci 1998; 111: 3517-3527.
14. Strous GJ, Govers R. The ubiquitin-proteasome system and endocytosis. J Cell Sci 1999; 112: 1417-1423.
15. Fajac I, Briand P, Monsigny M, Midoux P. Sugar-mediated uptake of glycosylated polylysines and gene transfer into normal and cystic fibrosis airway epithelial cells. Hum Gene Ther 1999; 10: 395-406.
16. Smith RM, Wu GY. Hepatocyte-directed gene delivery by receptor-mediated endocytosis. Semin Liver Dis 1999; 19: 83-92.
17. Pishvaee B, Payne GS. Clathrin coats - threads laid bare. Cell 1998; 95: 443-446.
18. Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 1994; 127: 1217-1232.
19. Budker V et al. Hypothesis: naked plasmid DNA is taken up by cells in vivo by a receptor-mediated process. J Gene Med 2000; 2: 76-88.
20. McNeil PL, Vogel SS, Miyake K, Terasaki M. Patching plasma membrane disruptions with cytoplasmic membrane. J Cell Sci 2000; 113: 1891-1902.
21. Bennett RM, Gabor GT, Merritt MM. DNA binding to human leukocytes. Evidence for a receptor-mediated association, internalization, and degradation of DNA. J Clin Invest 1985; 76: 2182-2190.
22. Hefeneider SH et al. Identification of a cell-surface DNA receptor and its association with systemic lupus erythematodes. J Invest Dermatol 1990; 94: 79S-84S.
23. Schubbert R, Renz D, Schmitz B, Doerfler W. Foreign (M13) DNA ingested by mice reaches peripheral leukocytes, spleen, and liver via the intestinal wall mucosa and can be covalently linked to mouse DNA. Proc Natl Acad Sci USA 1997; 94: 961-966.
24. Gasparro FP et al. Cell membrane DNA: a new target for psoralen photoadduct formation. Photochem Photobiol 1990; 52: 315-321.
25. Hagstrom JE et al. Nonnuclear DNA binding proteins in striated muscle. Biochem Mol Med 1990; 58: 113-121.
26. Levy MY, Barron LG, Meyer KB, Szoka Jr FC. Characterization of plasmid DNA transfer into mouse skeletal muscle: evaluation of uptake mechanism, expression and secretion of gene products into blood. Gene Therapy 1996; 3: 201-211.
27. Hengge UR et al. How realistic is cutaneous gene therapy? Exp Dermatol 1999; 8: 419-431.
28. Hengge UR et al. The derivation and characterization of pig keratinocyte cell lines that retain the ability to differentiate. J Invest Dermatol 1996; 106: 287-293.
29. Zelphati O, Liang X, Hobart P, Felgner P. Gene chemistry: functionally and conformationally intact fluorescent plasmid DNA. Hum Gene Ther 1999; 10: 15-24.
30. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 1989; 109: 2731-2739; (Erratum in J Cell Biol 110: 859).
31. Oka JA, Christensen MD, Weigel PH. Hyperosmolarity inhibits galactosyl receptor-mediated but not fluid phase endocytosis in isolated rat hepatocytes. J Biol Chem 1989; 264: 12016-12024.
32. Mirmohammadsadegh A, Maschke J, Basner-Tschakarjan E, Hengge UR. Induction of acute phase genes in keratinocytes following exposure to oligodeoxynucleotides. J Mol Med 2002; 80: 377-383.
33. Trigatti BL, Mangroo D, Gerber GE. Photoaffinity labeling and fatty acid permeation in 3T3-L1 adipocytes. J Biol Chem 1991; 266: 22621-22625.
34. Klose J. Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutation in mammals. Humangenetik 1975; 26: 231-243.
35. Bowen B, Steinberg J, Laemmli UK, Weintraub H. The detection of DNA-binding proteins by protein blotting. Nucleic Acids Res 1980; 8: 1-20.
36. Mirmohammadsadegh A et al. Calgranulin C is overexpressed in lesional psoriasis. J Invest Dermatol 2000; 114: 1207-1208.
37. Fujimoto T, Miyawaki A, Mikoshiba K. Inositol 1,4,5,trisphosphate receptor-like protein in plasmalemmal caveolae is linked to actin filaments. J Cell Sci 1995; 108: 7-15.
38. Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 1996; 135: 1249-1260.
39. Wattiaux R et al. Endosomes, lysosomes: their implication in gene transfer. Adv Drug Deliv Rev 2000; 41: 201-208.
40. Davis L. The nuclear pore complex. Annu Rev Biochem 1995; 64: 865-896.
41. Dowty ME et al. Plasmid DNA entry into postmitotic nuclei of primary rat myotubes. Proc Natl Acad Sci USA 1995; 92: 4572-4576.
42. Hagstrom JE et al. Nuclear import of DNA in digitonin-permeabilized cells. J Cell Sci 1997; 110: 2323-2331.
43. Watts C, Marsh M. Endocytosis: what goes in and how? J Cell Sci 1992; 103: 1-8.
44. Cupers P et al. Three unrelated perturbations similarly uncouple fluid, bulk-membrane, and receptor endosomal flow in rat fetal fibroblasts. Biochem Biophys Res Commun 1996; 236: 661-664.
45. Tammi R et al. Hyaluronan enters keratinocytes by a novel endocytic route for catabolism. J Biol Chem 2001; 276: 35111-35122.
46. Batard P, Jordan M, Wurm F. Transfer of high copy number plasmid into mammalian cells by calcium phosphate transfection. Gene 2001; 270: 61-68.
47. Ciftci K, Levy RJ. Enhanced plasmid DNA transfection with lysosomotropic agents in cultured fibroblasts. Int J Pharmacol 2001; 218: 81-92.
48. Hengge UR, Dexling B, Mirmohammadsadegh A. Safety and pharmacokinetics of naked plasmid DNA in the skin: studies on dissemination and ectopic expression. J Invest Dermatol 2001; 116: 979-982.
49. Laktionov PP et al. Characterisation of membrane oligonucleotide-binding proteins and oligonucleotide uptake in keratinocytes. Nucleic Acids Res 1999; 27: 2315-2324.
50. White PJ et al. Oligonucleotide uptake in cultured keratinocytes: influence of confluence, cationic liposomes, and keratinocyte cell type. J Invest Dermatol 1999; 112: 699-705.
51. Hanss B et al. Identification and characterization of a cell membrane nucleic acid channel. Proc Natl Acad Sci USA 1998; 95: 1921-1926.
52. Sato N et al. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J Cell Sci 1992; 103: 131-143.
53. Bretscher A. Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr Opin Cell Biol 1999; 11: 109-116.
54. Gautreau A, Poullet P, Louvard D, Arpin M. Ezrin, a plasma membrane-microfilament linker, signals cell survival through the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA 1999; 96: 7300-7305.
55. Fazioli F et al. The ezrin-like family of tyrosine kinase substrates: receptor-specific pattern of tyrosine phosphorylation and relationship to malignant transformation. Oncogene 1993; 8: 1335-1345.
56. Tsukita S et al. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 1994; 126: 391-401.
57. Yonemura S et al. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J Cell Biol 1998; 140: 885-895.
58. Majander-Nordenswan P et al. Genomic structure of the human ezrin gene. Hum Genet 1998; 103: 662-665.
59. Reczek D, Berryman M, Bretscher A. Identification of EBP50: a PDZ-containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J Cell Biol 1997; 139: 169-179.
60. Reczek D, Bretscher A. The carboxyl-terminal region of EBP50 binds to a site in the amino-terminal domain of ezrin that is masked in the dormant molecule. J Biol Chem 199; 273: 18452-18458.
61. Gary R, Bretscher A. Heterotypic and homotypic associations between ezrin and moesin, two putative membrane-cytoskeletal linking proteins. Proc Natl Acad Sci USA 1993; 90: 10846-10850.
62. Matsui T et al. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 1998; 140: 647-657.
63. Krieg J, Hunter T. Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J Biol Chem 1992; 267: 19258-19265.
64. Bretscher MS, Aguado-Velasco C. EGF induces recycling membrane to form ruffles. Curr Biol 1998; 8: 721-724.
65. Bretscher A. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J Cell Biol 199; 108: 921-930.
66. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992; 70: 389-399.
67. Hirao M et al. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association; possible involvement of phosphatidylinositol turnover and rho-dependent signaling pathway. J Cell Biol 1996; 135: 37-51.
68. Mackay DJG, Esch F, Furthmayr H, Hall A. Rho- and Rac-dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J Cell Biol 1997; 138: 927-938.
69. Takahashi K et al. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 1997; 272: 23371-23375.
70. Doi Y et al. Normal development of mice and unimpaired cell adhesion/cell motility/actin-based cytoskeleton without compensatory up-regulation of ezrin or radixin in moesin gene knockout. J Biol Chem 1999; 22: 2315-2321.