Intracellular delivery of proteins into mammalian living cells by polyethylenimine-cationization

Journal of Bioscience and Bioengineering

Volumn 99, Issue 2, 2005, Pages 95-103

  Futami, Junichiro ^a,b   Kitazoe, Midori ^a   Maeda, Takashi ^a   Nukui, Emiko ^a   Sakaguchi, Masakiyo ^c   Kosaka, Jun ^c   Miyazaki, Masahiro ^c   Kosaka, Megumi ^a   Tada, Hiroko ^a   Seno, Masaharu ^a   Sasaki, Junzo ^c   Huh, Nam Hu ^c   Namba, Masayoshi ^d   Yamada, Hidenori ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NIPPON SHOKUBAI CO LTD   (Japan)

^c OKAYAMA UNIVERSITY   (Japan)

^d Niimi University   (Japan)

Author keywords

Cationization; Chemical modification; Endocytosis; Polyethylenimine (PEI); Protein transduction

Indexed keywords

CELLS; DNA; GENES; IONIZATION; POSITIVE IONS;

CYTOSOL; GREEN FLUORESCENT PROTEINS (GFP); IMMUNOGLOBULIN (IGG); POLYETHYLENIMINE (PEI);

PROTEINS;

DNA; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G; POLYETHYLENEIMINE; PROTEIN; RIBONUCLEASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CHEMICAL MODIFICATION; CONJUGATION; CYTOSOL; ENDOCYTOSIS; HUMAN; HUMAN CELL; IONIZATION; MACROMOLECULE; MAMMAL CELL; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN TRANSPORT;

EID: 20144389743     PISSN: 13891723     EISSN: None     Source Type: Journal    
DOI: 10.1263/jbb.99.95     Document Type: Article

References (44)

1. 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, 10444-10450 (1994).
2. Vives, E., Brodin, P., and Lebleu, B.: A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem., 272, 16010-16017 (1997).
3. 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, 1569-1572 (1999).
4. Wender, P. A., Mitchell, D. J., Pattabiraman, K., Pelkey, E. T., Steinman, L., and Rothbard, J. B.: The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters. Proc. Natl. Acad. Sci. USA, 97, 13003-13008 (2000).
5. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y.: Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem., 276, 5836-5840 (2001).
6. Matsushita, M., Tomizawa, K., Moriwaki, A., Li, S. T., Terada, H., and Matsui, H.: A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. J. Neurosci., 21, 6000-6007 (2001).
7. Gius, D. R., Ezhevsky, S. A., Becker-Hapak, M., Nagahara, H., Wei, M. C., and Dowdy, S. F.: Transduced p16INK4a peptides inhibit hypophosphorylation of the retinoblastoma protein and cell cycle progression prior to activation of Cdk2 complexes in late G1. Cancer Res., 59, 2577-2580 (1999).
8. Nagahara, H., Vocero-Akbani, A. M., Snyder, E. L., Ho, A., Latham, D. G., Lissy, N. A., Becker-Hapak, M., Ezhevsky, S. A., and Dowdy, S. F.: Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med., 4, 1449-1452 (1998).
9. Takenobu, T., Tomizawa, K., Matsushita, M., Li, S. T., Moriwaki, A., Lu, Y. F., and Matsui, H.: Development of p53 protein transduction therapy using membrane-permeable peptides and the application to oral cancer cells. Mol. Cancer Ther., 1, 1043-1049 (2002).
10. Vocero-Akbani, A. M., Heyden, N. V., Lissy, N. A., Ratner, L., and Dowdy, S. F.: Killing HIV-infected cells by transduction with an HIV protease-activated caspase-3 protein. Nat. Med., 5, 29-33 (1999).
11. Peitz, M., Pfannkuche, K., Rajewsky, K., and Edenhofer, F.: Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: a tool for efficient genetic engineering of mammalian genomes. Proc. Natl. Acad. Sci. USA, 99, 4489-4494 (2002).
12. Suzuki, T., Futaki, S., Niwa, M., Tanaka, S., Ueda, K., and Sugiura, Y.: Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem., 277, 2437-2443 (2002).
13. 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 mechanism of cellular uptake. J. Biol. Chem., 278, 585-590 (2003).
14. Lundberg, M., Wikstrom, S., and Johansson, M.: Cell surface adherence and endocytosis of protein transduction domains. Mol. Ther., 8, 143-150 (2003).
15. Fittipaldi, A., Ferrari, A., Zoppe, M., Arcangeli, C., Pellegrini, V., Beltram, F., and Giacca, M.: Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion protein. J. Biol. Chem., 278, 34141-34149 (2003).
16. Maeda, T., Kitazoe, M., Tada, H., de Llorens, R., Salomon, D. S., Ueda, M., Yamada, H., and Seno, M.: Growth inhibition of mammalian cells by eosinophil cationic protein. Eur. J. Biochem., 269, 307-316 (2002).
17. Kumagai, A. K., Eisenberg, J. B., and Pardridge, W. M.: Absorptive-mediated endocytosis of cationized albumin and a beta-endorphin- cationized albumin chimeric peptide by isolated brain capillaries. Model system of blood-brain barrier transport. J. Biol. Chem., 262, 15214-15219 (1987).
18. Apple, R. J., Domen, P. L., Muckerheide, A., and Michael, J. G.: Cationization of protein antigens. IV. Increased antigen uptake by antigen-presenting cells. J. Immunol., 140, 3290-3295 (1988).
19. Triguero, D., Buciak, J. B., Yang, J., and Pardridge, W. M.: Blood-brain barrier transport of cationized immunoglobulin G: enhanced delivery compared to native protein. Proc. Natl. Acad. Sci. USA, 86, 4761-4765 (1989).
20. Triguero, D., Buciak, J. L., and Pardridge, W. M.: Cationization of immunoglobulin G results in enhanced organ uptake of the protein after intravenous administration in rats and primate. J. Pharmacol. Exp. Ther., 258, 186-192 (1991).
21. Pardridge, W. M., Bickel, U., Buciak, J., Yang, J., and Diagne, A.: Enhanced endocytosis and anti-human immunodeficiency virus type 1 activity of anti-rev antibodies after cationization. J. Infect. Dis., 169, 55-61 (1994).
22. Pardridge, W. M., Kang, Y. S., Yang, J., and Buciak, J. L.: Enhanced cellular uptake and in vivo biodistribution of a monoclonal antibody following cationization. J. Pharm. Sci., 84, 943-948 (1995).
23. Pardridge, W. M., Buciak, J., Yang, J., and Wu, D.: Enhanced endocytosis in cultured human breast carcinoma cells and in vivo biodistribution in rats of a humanized monoclonal antibody after cationization of the protein. J. Pharmacol. Exp. Ther., 286, 548-554 (1998).
24. Hong, G., Bazin-Redureau, M. I., and Scherrmann, J. M.: Pharmacokinetics and organ distribution of cationized colchicine-specific IgG and Fab fragments in rat. J. Pharm. Sci., 88, 147-153 (1999).
25. Futami, J., Maeda, T., Kitazoe, M., Nukui, E., Tada, H., Seno, M., Kosaka, M., and Yamada, H.: Preparation of potent cytotoxic ribonucleases by cationization: enhanced cellular uptake and decreased interaction with ribonuclease inhibitor by chemical modification of carboxyl groups. Biochemistry, 40, 7518-7524 (2001).
26. Futami, J., Nukui, E., Maeda, T., Kosaka, M., Tada, H., Seno, M., and Yamada, H.: Optimum modification for the highest cytotoxicity of cationized ribonuclease. J. Biochem. (Tokyo), 132, 223-228 (2002).
27. Godbey, W. T., Wu, K. K., and Mikos, A. G.: Poly(ethylenimine) and its role in gene delivery. J. Control. Release, 60, 149-160 (1999).
28. Lemkine, G. F. and Demeneix, B. A.: Polyethylenimines for in vivo gene delivery. Curr. Opin. Mol. Ther., 3, 178-182 (2001).
29. Matsuura, M., Yamazaki, Y., Sugiyama, M., Kondo, M., Ori, H., Nango, M., and Oku, N.: Polycation liposome-mediated gene transfer in vivo. Biochim. Biophys. Acta, 1612, 136-143 (2003).
30. Sakaguchi, M., Miyazaki, M., Inoue, Y., Tsuji, T., Kouchi, H., Tanaka, T., Yamada, H., and Namba, M.: Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts. J. Cell Biol., 149, 1193-1206 (2000).
31. Bello, J. and Nowoswiat, E. F.: Multiple carboxymethylation of histidines in bovine ribonuclease A. Eur. J. Biochem., 22, 225-234 (1971).
32. Yamada, H., Imoto, T., Fujita, K., Okazaki, K., and Motomura, M.: Selective modification of aspartic acid-101 in lysozyme by carbodiimide reaction. Biochemistry, 20, 4836-4842 (1981).
33. Peterkofsky, B. and Prather, W.: Correlation between the rates of aerobic glycolysis and glucose transport, unrelated to neoplastic transformation, in a series of BALB 3T3-derived cell lines. Cancer Res., 42, 1809-1816 (1982).
34. Namba, M., Nishitani, K., Hyodoh, F., Fukushima, F., and Kimoto, T.: Neoplastic transformation of human diploid fibroblasts (KMST-6) by treatment with 60Co gamma rays. Int. J. Cancer, 35, 275-280 (1985).
35. Rybak, S. M. and Newton, D. L.: Natural and engineered cytotoxic ribonucleases: therapeutic potential. Exp. Cell Res., 253, 325-335 (1999).
36. Futami, J., Tsushima, Y., Murato, Y., Tada, H., Sasaki, J., Seno, M., and Yamada, H.: Tissue-specific expression of pancreatic-type RNases and RNase inhibitor in humans. DNA Cell Biol., 16, 413-419 (1997).
37. Dickson, K. A., Dahlberg, C. L., and Raines, R. T.: Compensating effects on the cytotoxicity of ribonuclease A variants. Arch. Biochem. Biophys., 415, 172-177 (2003).
38. Kneen, M., Farinas, J., Li, Y., and Verkman, A. S.: Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J., 74, 1591-1599 (1998).
39. Dröse, S. and Altendorf, K.: Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol., 200 (Pt 1), 1-8 (1997).
40. Sakaguchi, M., Miyazaki, M., Takaishi, M., Sakaguchi, Y., Makino, E., Kataoka, N., Yamada, H., Namba, M., and Huh, N. H.: S100C/A11 is a key mediator of Ca(2+)-induced growth inhibition of human epidermal keratinocytes. J. Cell Biol., 163, 825-835 (2003).
41. Gahmberg, C. G. and Tolvanen, M.: Why mammalian cell surface proteins are glycoproteins. Trends Biochem. Sci., 248, 308-311 (1996).
42. Varki, A.: Metabolic radiolabeling of glycoconjugates. Methods Enzymol., 230, 16-32 (1994).
43. Reuter, G. and Schauer, R.: Determination of sialic acids. Methods Enzymol., 230, 168-199 (1994).
44. Futami, J., Tsushima, Y., Tada, H., Seno, M., and Yamada, H.: Convenient and efficient in vitro folding of disulfide-containing globular protein from crude bacterial inclusion bodies. J. Biochem. (Tokyo), 127, 435-441 (2000).