Signal sequences for targeting of gene therapy products to subcellular compartments: The role of CRM1 in nucleocytoplasmic shuttling of the protein switch

Pharmaceutical Research

Volumn 24, Issue 11, 2007, Pages 2146-2155

  Kakar, Mudit ^a   Cadwallader, Amy B ^a   Davis, James R ^a   Lim, Carol S ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Controlled localization; CRM1; Export signal; Import signal; Ligand binding domain; Signal sequences

Indexed keywords

DEXAMETHASONE; EXPORTIN 1; GELDANAMYCIN; GENE PRODUCT; GLUCOCORTICOID; HEAT SHOCK PROTEIN 90 INHIBITOR; LEPTOMYCIN B; MIFEPRISTONE; PROGESTERONE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENE MUTATION; GENE SWITCHING; GENE TARGETING; GENETIC TRANSFECTION; LIGAND BINDING; MOUSE; NONHUMAN; NUCLEAR IMPORT; PLASMID; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; GENE THERAPY; KARYOPHERINS; MICE; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 34848873757     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-007-9333-1     Document Type: Article

References (53)

1. D. A. Jans, C. K. Chan, and S. Huebner. Signals mediating nuclear targeting and their regulation: application in drug delivery. Med. Res. Rev. 18:189-223 (1998).
2. D. Shields. Gunter Blobel-still passionate after all these years. Trends Cell Biol. 11:349-350 (2001).
3. M. R. Hodel, A. H. Corbett, and A. E. Hodel. Dissection of a nuclear localization signal. J. Biol. Chem. 276:1317-1325 (2001).
4. M. A. Zanta, P. Belguise-Valladier, and J. P. Behr. Gene delivery: a single nuclear localization signal peptide is sufficient to carry DNA to the cell nucleus. Proc. Natl. Acad. Sci. USA 96:91-96 (1999).
5. C. Kanwal, S. Mu, S. E. Kern, and C. S. Lim. Bidirectional on/off switch for controlled targeting of proteins to subcellular compartments. J. Control. Release 98:379-393 (2004).
6. T. la Cour, L. Kiemer, A. Molgaard, R. Gupta, K. Skriver, and S. Brunak. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17:527-536 (2004).
7. L. Meunier, R. Mayer, M. Monsigny, and A. C. Roche. The nuclear export signal-dependent localization of oligonucleopeptides enhances the inhibition of the protein expression from a gene transcribed in cytosol. Nucleic Acids Res. 27:2730-2736 (1999).
8. A. Subramanian, P. Ranganathan, and S. L. Diamond. Nuclear targeting peptide scaffolds for lipofection of nondividing mammalian cells. Nat. Biotechnol. 17:873-877 (1999).
9. H. Brooks, B. Lebleu, and E. Vives. Tat peptide-mediated cellular delivery: back to basics. Adv. Drug Deliv. Rev. 57:559-577 (2005).
10. A. Nori, K. D. Jensen, M. Tijerina, P. Kopeckova, and J. Kopecek. Tat-conjugated synthetic macromolecules facilitate cytoplasmic drug delivery to human ovarian carcinoma cells. Bioconjug. Chem. 14:44-50 (2003).
11. J. R. Davis, M. Kakar, and C. S. Lim. Controlling protein compartmentalization to overcome disease. Pharm. Res. 24:17-27 (2007).
12. Y. X. Guo, K. Dallmann, and J. Kwang. Identification of nucleolus localization signal of betanodavirus GGNNV protein alpha. Virology 306:225-235 (2003).
13. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. Molecular Biology of the Cell, Garland Science, Taylor and Francis Group, 2002.
14. H. K. Anandatheerthavarada, G. Biswas, M. A. Robin, and N. G. Avadhani. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol. 161:41-54 (2003).
15. Q. Zeng, H. T. Tran, H. X. Tan, and W. Hong. The cytoplasmic domain of Vamp4 and Vamp5 is responsible for their correct subcellular targeting: the N-terminal extension of Vamp4 contains a dominant autonomous targeting signal for the trans-Golgi network. J. Biol. Chem. 278:23046-23054 (2003).
16. J. S. Bonifacino, and L. M. Traub. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395-447 (2003).
17. S. Munro, and H. R. Pelham. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899-907 (1987).
18. D. A. Andres, I. M. Dickerson, and J. E. Dixon. Variants of the carboxyl-terminal KDEL sequence direct intracellular retention. J. Biol. Chem. 265:5952-5955 (1990).
19. G. L. Hager, C. S. Lim, C. Elbi, and C. T. Baumann. Trafficking of nuclear receptors in living cells. J. Steroid Biochem. Mol. Biol. 74:249-254 (2000).
20. N. Nakamura, S. Ramaswamy, F. Vazquez, S. Signoretti, M. Loda, and W. R. Sellers. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol. Cell. Biol. 20:8969-8982 (2000).
21. T. Henkel, U. Zabel, K. van Zee, J. M. Muller, E. Fanning, and P. A. Baeuerle. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kappa B subunit. Cell 68:1121-1133 (1992).
22. M. Karin, Y. Cao, F. R. Greten, and Z. W. Li. NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2:301-310 (2002).
23. E. Colombo, P. Martinelli, R. Zamponi, D. C. Shing, P. Bonetti, L. Luzi, S. Volorio, L. Bernard, G. Pruneri, M. Alcalay, and P. G. Pelicci. Delocalization and destabilization of the Arf tumor suppressor by the leukemia-associated NPM mutant. Cancer Res. 66:3044-3050 (2006).
24. A. Ala, A. P. Walker, K. Ashkan, J. S. Dooley, and M. L. Schilsky. Wilson's disease. Lancet 369:397-408 (2007).
25. P. Ferenci. Wilson's Disease. Clin. Gastroenterol. Hepatol. 3:726-733 (2005).
26. E. M. Castano, F. Prelli, T. Wisniewski, A. Golabek, R. A. Kumar, C. Soto, and B. Frangione. Fibrillogenesis in Alzheimer's disease of amyloid beta peptides and apolipoprotein E. Biochem. J. 306 ( Pt 2):599-604 (1995).
27. W. J. Strittmatter, A. M. Saunders, M. Goedert, K. H. Weisgraber, L. M. Dong, R. Jakes, D. Y. Huang, M. Pericak-Vance, D. Schmechel, and A. D. Roses. Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease. Proc. Natl. Acad. Sci. USA 91:11183-11186 (1994).
28. S. M. Claypool, J. M. McCaffery, and C. M. Koehler. Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol. 174:379-390 (2006).
29. K. Venkatachalam, T. Hofmann, and C. Montell. Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1. J. Biol. Chem. 281:17517-17527 (2006).
30. A. Motley, M. J. Lumb, P. B. Oatey, P. R. Jennings, P. A. De Zoysa, R. J. Wanders, H. F. Tabak, and C. J. Danpure. Mammalian alanine/glyoxylate aminotransferase 1 is imported into peroxisomes via the PTS1 translocation pathway. Increased degeneracy and context specificity of the mammalian PTS1 motif and implications for the peroxisome-to-mitochondrion mistargeting of AGT in primary hyperoxaluria type 1. J. Cell. Biol. 131:95-109 (1995).
31. C. T. Baumann, C. S. Lim, and G. L. Hager. Intracellular localization and trafficking of steroid receptors. Cell Biochem. Biophys. 31:119-127 (1999).
32. G. L. Hager, C. L. Smith, G. Fragoso, R. Wolford, D. Walker, J. Barsony, and H. Htun. Intranuclear trafficking and gene targeting by members of the steroid/nuclear receptor superfamily. J. Steroid Biochem. Mol. Biol. 65:125-132 (1998).
33. M. Fornerod, M. Ohno, M. Yoshida, and I. W. Mattaj. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060 (1997).
34. D. Gorlich, and U. Kutay. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:607-660 (1999).
35. M. E. Lindsay, J. M. Holaska, K. Welch, B. M. Paschal, and I. G. Macara. Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J. Cell Biol. 153:1391-1402 (2001).
36. B. E. Black, J. M. Holaska, L. Levesque, B. Ossareh-Nazari, C. Gwizdek, C. Dargemont, and B. M. Paschal. NXT1 is necessary for the terminal step of Crm1-mediated nuclear export. J. Cell Biol. 152:141-155 (2001).
37. I. W. Mattaj, and L. Englmeier. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306 (1998).
38. L. J. Schwimmer, P. Rohatgi, B. Azizi, K. L. Seley, and D. F. Doyle. Creation and discovery of ligand-receptor pairs for transcriptional control with small molecules. Proc. Natl. Acad. Sci. USA 101:14707-14712 (2004).
39. J. Yang, and D. B. DeFranco. Assessment of glucocorticoid receptor-heat shock protein 90 interactions in vivo during nucleocytoplasmic trafficking. Mol. Endocrinol. 10:3-13 (1996).
40. M. Kakar, C. Kanwal, J. R. Davis, H. Li, and C. S. Lim. Geldanamycin, an inhibitor of Hsp90, blocks cytoplasmic retention of progesterone receptors and glucocorticoid receptors via their respective ligand binding domains. AAPS J. 8:E718-E728 (2006).
41. W. B. Pratt, and D. O. Toft. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18:306-360 (1997).
42. N. Kudo, B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547 (1998).
43. L. T. Gooljarsingh, C. Fernandes, K. Yan, H. Zhang, M. Grooms, K. Johanson, R. H. Sinnamon, R. B. Kirkpatrick, J. Kerrigan, T. Lewis, M. Arnone, A. J. King, Z. Lai, R. A. Copeland, and P. J. Tummino. A biochemical rationale for the anticancer effects of Hsp90 inhibitors: slow, tight binding inhibition by geldanamycin and its analogues. Proc. Natl. Acad. Sci. USA 103:7625-7630 (2006).
44. Y. Wang, B. W. O'Malley, Jr., S. Y. Tsai, and B. W. O'Malley. A regulatory system for use in gene transfer. Proc. Natl. Acad. Sci. USA 91:8180-8184 (1994).
45. H. Htun, J. Barsony, I. Renyi, D. L. Gould, and G. L. Hager. Visualization of glucocorticoid receptor translocation and intranuclear organization in living cells with a green fluorescent protein chimera. Proc. Natl. Acad. Sci. USA 93:4845-4850 (1996).
46. P. K. Chakraborti, M. J. Garabedian, K. R. Yamamoto, and S. S. Simons, Jr. Creation of "super" glucocorticoid receptors by point mutations in the steroid binding domain. J. Biol. Chem. 266:22075-22078 (1991).
47. C. S. Lim, C. T. Baumann, H. Htun, W. Xian, M. Irie, C. L. Smith, and G. L. Hager. Differential localization and activity of the A- and B-forms of the human progesterone receptor using green fluorescent protein chimeras. Mol. Endocrinol. 13:366-375 (1999).
48. M. Kakar, J. R. Davis, S. E. Kern, and C. S. Lim. Optimizing the protein switch: altering nuclear import and export signals, and ligand binding domain. J. Control. Release (in press).
49. Y. Wan, K. K. Coxe, V. G. Thackray, P. R. Housley, and S. K. Nordeen. Separable features of the ligand-binding domain determine the differential subcellular localization and ligand-binding specificity of glucocorticoid receptor and progesterone receptor. Mol. Endocrinol. 15:17-31 (2001).
50. B. R. Henderson, and A. Eleftheriou. A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp. Cell Res. 256:213-224 (2000).
51. T. la Cour, R. Gupta, K. Rapacki, K. Skriver, F. M. Poulsen, and S. Brunak. NESbase version 1.0: a database of nuclear export signals. Nucleic Acids Res. 31:393-396 (2003).
52. C. Kanwal, H. Li, and C. S. Lim. Model system to study classical nuclear export signals. AAPS PharmSci. 4:(2002).
53. M. J. Czar, M. D. Galigniana, A. M. Silverstein, and W. B. Pratt. Geldanamycin, a heat shock protein 90-binding benzoquinone ansamycin, inhibits steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus. Biochemistry 36:7776-7785 (1997).