Intracellular delivery of proteins into mouse Müller glia cells in vitro and in vivo using Pep-1 transfection reagent

Journal of Neuroscience Methods

Volumn 177, Issue 2, 2009, Pages 403-419

  Wang, Minhua H ^a   Frishman, Laura J ^a   Otteson, Deborah C ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

Chariot; CPP; ERG; Immunohistochemistry; Intravitreal; M ller glia; Pep 1; Protein transfection; Retina; Vimentin

Indexed keywords

ANTIBODY; BETA GALACTOSIDASE; GLUTAMATE AMMONIA LIGASE; IMMUNOGLOBULIN G; PEP 1 REAGENT; PROTEIN; REAGENT; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DARK ADAPTATION; ELECTRORETINOGRAM; FEMALE; GLIA CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TIME; MALE; MOUSE; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RETINA; RETINA NERVE CELL; SURFACE PROPERTY; TISSUE PRESERVATION; VITREOUS BODY;

ANIMALS; ANTIBODIES; BETA-GALACTOSIDASE; CELLS, CULTURED; CYSTEAMINE; DRUG DELIVERY SYSTEMS; ELECTRORETINOGRAPHY; FEMALE; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEUROGLIA; NEURONS; PEPTIDES; PROTEINS; RETINA; STAINING AND LABELING; TRANSFECTION; VITREOUS BODY;

EID: 58249114220     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2008.10.039     Document Type: Article

References (59)

1. An J.J., Kim S.Y., Lee S.H., Kim D.W., Ryu H.J., Yeo S.I., et al. Transduced PEP-1-Grb7 fusion protein suppressed LPS-induced COX-2 expression. J Biochem Mol Biol 40 (2007) 189-195
2. Aoshiba K., Yokohori N., and Nagai A. Alveolar wall apoptosis causes lung destruction and emphysematous changes. Am J Respir Cell Mol Biol 28 (2003) 555-562
3. Barnett E.M., Elangovan B., Bullok K.E., and Piwnica-Worms D. Selective cell uptake of modified Tat peptide-fluorophore conjugates in rat retina in ex vivo and in vivo models. Invest Ophthalmol Vis Sci 47 (2006) 2589-2595
4. Bourges J.L., Gautier S.E., Delie F., Bejjani R.A., Jeanny J.C., Gurny R., et al. Ocular drug delivery targeting the retina and retinal pigment epithelium using polylactide nanoparticles. Invest Ophthalmol Vis Sci 44 (2003) 3562-3569
5. Bui B.V., and Fortune B. Ganglion cell contributions to the rat full-field electroretinogram. J Physiol 555 (2004) 153-173
6. Cho J.H., Hwang I.K., Yoo K.Y., Kim S.Y., Kim D.W., Kwon Y.G., et al. Effective delivery of Pep-1-cargo protein into ischemic neurons and long-term neuroprotection of Pep-1-SOD1 against ischemic injury in the gerbil hippocampus. Neurochem Int 52 (2008) 659-668
7. Choi S.H., Kim S.Y., An J.J., Lee S.H., Kim D.W., Ryu H.J., et al. Human PEP-1-ribosomal protein S3 protects against UV-induced skin cell death. FEBS Lett 580 (2006) 6755-6762
8. Dawson W.W., Trick G.L., and Litzkow C.A. Improved electrode for electroretinography. Invest Ophthalmol Vis Sci 18 (1979) 988-991
9. Derossi D., Joliot A.H., Chassaing G., and Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 269 (1994) 10444-10450
10. Deshayes S., Heitz A., Morris M.C., Charnet P., Divita G., and Heitz F. Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis. Biochemistry 43 (2004) 1449-1457
11. Elliott G., and O'Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88 (1997) 223-233
12. Fawell S., Seery J., Daikh Y., Moore C., Chen L.L., Pepinsky B., et al. Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 91 (1994) 664-668
13. Frankel A.D., and Pabo C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55 (1988) 1189-1193
14. Frishman L.J., and Steinberg R.H. Light-evoked increases in [K+]o in proximal portion of the dark-adapted cat retina. J Neurophysiol 61 (1989) 1233-1243
15. Green M., and Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55 (1988) 1179-1188
16. Heiduschka P., Fietz H., Hofmeister S., Schultheiss S., Mack A.F., Peters S., et al. Penetration of bevacizumab through the retina after intravitreal injection in the monkey. Invest Ophthalmol Vis Sci 48 (2007) 2814-2823
17. Henriques S.T., and Castanho M.A. Consequences of nonlytic membrane perturbation to the translocation of the cell penetrating peptide pep-1 in lipidic vesicles. Biochemistry 43 (2004) 9716-9724
18. Henriques S.T., and Castanho M.A. Translocation or membrane disintegration? Implication of peptide-membrane interactions in pep-1 activity. J Pept Sci 14 (2008) 482-487
19. Henriques S.T., Costa J., and Castanho M.A. Translocation of beta-galactosidase mediated by the cell-penetrating peptide pep-1 into lipid vesicles and human HeLa cells is driven by membrane electrostatic potential. Biochemistry 44 (2005) 10189-10198
20. Hood D.C., and Birch D.G. A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Vis Neurosci 5 (1990) 379-387
21. Jamison J.A., Bush R.A., Lei B., and Sieving P.A. Characterization of the rod photoresponse isolated from the dark-adapted primate ERG. Vis Neurosci 18 (2001) 445-455
22. Jat P.S., Noble M.D., Ataliotis P., Tanaka Y., Yannoutsos N., Larsen L., et al. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci USA 88 (1991) 5096-5100
23. Jiang J., Borisenko G.G., Osipov A., Martin I., Chen R., Shvedova A.A., et al. Arachidonic acid-induced carbon-centered radicals and phospholipid peroxidation in cyclo-oxygenase-2-transfected PC12 cells. J Neurochem 90 (2004) 1036-1049
24. Johnson L.N., Cashman S.M., and Kumar-Singh R. Cell-penetrating peptide for enhanced delivery of nucleic acids and drugs to ocular tissues including retina and cornea. Mol Ther 16 (2008) 107-114
25. Kim D.W., Kim S.Y., An J.J., Lee S.H., Jang S.H., Won M.H., et al. Expression, purification and transduction of PEP-1-botulinum neurotoxin type A (PEP-1-BoNT/A) into skin. J Biochem Mol Biol 39 (2006) 642-647
26. Klymkowsky M.W., Miller R.H., and Lane E.B. Morphology, behavior, and interaction of cultured epithelial cells after the antibody-induced disruption of keratin filament organization. J Cell Biol 96 (1983) 494-509
27. Kouklis P.D., Traub P., and Georgatos S.D. Involvement of the consensus sequence motif at coil 2b in the assembly and stability of vimentin filaments. J Cell Sci 102 Pt 1 (1992) 31-41
28. Lee Y.P., Kim D.W., Lee M.J., Jeong M.S., Kim S.Y., Lee S.H., et al. Human brain pyridoxal-5′-phosphate phosphatase (PLPP):protein transduction of PEP-1-PLPP into PC12 cells. BMB Rep 41 (2008) 408-413
29. Lieber J.G., and Evans R.M. Disruption of the vimentin intermediate filament system during adipose conversion of 3T3-L1 cells inhibits lipid droplet accumulation. J Cell Sci 109 Pt 13 (1996) 3047-3058
30. Lindgren M., Hallbrink M., Prochiantz A., and Langel U. Cell-penetrating peptides. Trends Pharmacol Sci 21 (2000) 99-103
31. Mano T., and Puro D.G. Phagocytosis by human retinal glial cells in culture. Invest Ophthalmol Vis Sci 31 (1990) 1047-1055
32. Maron M.B., Folkesson H.G., Stader S.M., and Walro J.M. PKA delivery to the distal lung air spaces increases alveolar liquid clearance after isoproterenol-induced alveolar epithelial PKA desensitization. Am J Physiol Lung Cell Mol Physiol 289 (2005) L349-L354
33. Mitra A.K. Ophthalmic drug delivery systems. 2nd ed. (2003), Informa Health Care
34. Morris M.C., Depollier J., Mery J., Heitz F., and Divita G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 19 (2001) 1173-1176
35. Munoz-Morris M.A., Heitz F., Divita G., and Morris M.C. The peptide carrier Pep-1 forms biologically efficient nanoparticle complexes. Biochem Biophys Res Commun 355 (2007) 877-882
36. Myrberg H., Lindgren M., and Langel U. Protein delivery by the cell-penetrating peptide YTA2. Bioconjug Chem 18 (2007) 170-174
37. Nagahara H., Vocero-Akbani A.M., Snyder E.L., Ho A., Latham D.G., Lissy N.A., et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 4 (1998) 1449-1452
38. Otteson D., Lewis R., and Zack D. Isolation of a Conditionally Immortalized Müller Cell Line. Invest Ophthalmol Vis Sci 47 (2006) [ARVO E-Abstract 132]
39. Phelan A., Elliott G., and O'Hare P. Intercellular delivery of functional p53 by the herpesvirus protein VP22. Nat Biotechnol 16 (1998) 440-443
40. Pooga M., Hallbrink M., Zorko M., and Langel U. Cell penetration by transportan. FASEB J 12 (1998) 67-77
41. Prahlad V., Yoon M., Moir R.D., Vale R.D., and Goldman R.D. Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J Cell Biol 143 (1998) 159-170
42. Prochiantz A. Getting hydrophilic compounds into cells: lessons from homeopeptides. Curr Opin Neurobiol 6 (1996) 629-634
43. Raz D., Fariss R.N., Vijayasarathy C., Campos M.M., Bush R.A., and Sieving P.A. Probing Kir channel function in vivo: potassium regulation in the RCS rat model of retinal degeneration. Ophthalmol Vis. Sci. 49 (2007) [E-Abstract 1936]
44. Remacle A.G., Rozanov D.V., Baciu P.C., Chekanov A.V., Golubkov V.S., and Strongin A.Y. The transmembrane domain is essential for the microtubular trafficking of membrane type-1 matrix metalloproteinase (MT1-MMP). J Cell Sci 118 (2005) 4975-4984
45. Richard J.P., Melikov K., Vives E., Ramos C., Verbeure B., Gait M.J., Chernomordik L.V., and Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanisms of cellular uptake. J Biol Chem 278 (2003) 585-590
46. Robson J.G., and Frishman L.J. Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12 (1995) 837-850
47. Robson J.G., Maeda H., Saszik S.M., and Frishman L.J. In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vis Res 44 (2004) 3253-3268
48. Robson J.G., Saszik S.M., Ahmed J., and Frishman L.J. Rod and cone contributions to the a-wave of the electroretinogram of the macaque. J Physiol 547 (2003) 509-530
49. Ruggeri M., Wehbe H., Jiao S., Gregori G., Jockovich M.E., Hackam A., et al. In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 48 (2007) 1808-1814
50. Saszik S.M., Robson J.G., and Frishman L.J. Contributions of spiking and non-spiking inner retinal neurons to the Scotopic ERG of the mouse. Invest Ophthalmol Vis Sci 43 (2002) [E-Abstract 1817]
51. Saszik S.M., Robson J.G., and Frishman L.J. The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol 543 (2002) 899-916
52. Schmucker C., and Schaeffel F. A paraxial schematic eye model for the growing C57BL/6 mouse. Vis Res 44 (2004) 1857-1867
53. Schorderet D.F., Manzi V., Canola K., Bonny C., Arsenijevic Y., Munier F.L., et al. D-TAT transporter as an ocular peptide delivery system. Clin Exp Ophthalmol 33 (2005) 628-635
54. Schwarze S.R., Ho A., Vocero-Akbani A., and Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285 (1999) 1569-1572
55. Selim A.A., Abdelmagid S.M., Kanaan R.A., Smock S.L., Owen T.A., Popoff S.N., et al. Anti-osteoactivin antibody inhibits osteoblast differentiation and function in vitro. Crit Rev Eukaryot Gene Expr 13 (2003) 265-275
56. Sherry D.M., Wang M.M., and Frishman L.J. Differential distribution of vesicle associated membrane protein isoforms in the mouse retina. Mol Vis 9 (2003) 673-688
57. Wang M., Otteson D.C., and Frishman L.J. Intracellular delivery of proteins into Müller glia cells in vitro and in vivo using chariot transfection reagent. Invest Ophthalmol Vis Sci 48 (2007) [E-Abstract 1687]
58. Washbourne P., and McAllister A.K. Techniques for gene transfer into neurons. Curr Opin Neurobiol 12 (2002) 566-573
59. Weisbart R.H., Baldwin R., Huh B., Zack D.J., and Nishimura R. Novel protein transfection of primary rat cortical neurons using an antibody that penetrates living cells. J Immunol 164 (2000) 6020-6026