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Nucleocytoplasmic Communication

Nucleocytoplasmic Distribution of the Ovalbumin Serpin PI-9 Requires a Nonconventional Nuclear Import Pathway and the Export Factor Crm1

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Pages 5396-5407 | Received 17 May 2001, Accepted 18 May 2001, Published online: 28 Mar 2023

REFERENCES

  • Adam, S. A.. 1999. Transport pathways of macromolecules between the nucleus and the cytoplasm. Curr. Opin. Cell Biol. 11:402–406.
  • Andersson, S., D. L. Davis, H. Dahlback, H. Jornvall, and D. W. Russell. 1989. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J. Biol. Chem. 264:8222–8229.
  • Annand, R. R., J. R. Dahlen, C. A. Sprecher, P. de Dreu, D. C. Foster, J. A. Mankovich, R. V. Talanian, W. Kisiel, and D. A. Giegel. 1999. Caspase-1(interleukin-1b-converting enzyme) is inhibited by the human serpin analogue proteinase inhibitor 9. Biochem. J. 342:655–665.
  • Antalis, T. M., M. La Linn, K. Donnan, L. Mateo, J. Gardner, J. L. Dickinson, K. Buttigieg, and A. Suhrbier. 1998. The serine proteinase inhibitor (serpin) plasminogen activation inhibitor type 2 protects against viral cytopathic effects by constitutive interferon alpha/beta priming. J. Exp. Med. 187:1799–1811.
  • Belin, D.. 1993. Biology and facultative secretion of plasminogen activator inhibitor-2. Thromb. Haemostasis 70:144–147.
  • Biggs, J. R., J. Yang, U. Gullberg, C. Muchardt, M. Yaniv, and A. S. Kraft. 2001. The human brm protein is cleaved during apoptosis: the role of cathepsin-G. Proc. Natl. Acad. Sci. USA 98:3814–3819.
  • Bird, C. H., V. R. Sutton, J. Sun, C. E. Hirst, A. Novak, J. A. Trapani, and P. I. Bird. 1998. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol. Cell. Biol. 18:6387–6398.
  • Bird, P. I.. 1998. Serpins and regulation of cell death. Results Probl. Cell Differ. 24:63–89.
  • Bird, P. I.. 1999. Regulation of pro-apoptotic leukocyte granule serine proteinases by intracellular serpins. Immunol. Cell. Biol. 77:47–57.
  • Boche, I., and E. Fanning. 1997. Nucleocytoplasmic recycling of the nuclear localization signal receptor alpha subunit in vivo is dependent on a nuclear export signal, energy and RCC1. J. Cell Biol. 139:313–325.
  • Briggs, L. J., D. Stein, J. Goltz, V. C. Corrigan, A. Efthymiadis, S. Hubner, and D. A. Jans. 1998. The cAMP-dependent protein kinase site (Ser312) enhances dorsal nuclear import through facilitating nuclear localization sequence/importin interaction. J. Biol. Chem. 273:22745–22752.
  • Brunk, U. T., H. Dalen, K. Roberg, and H. B. Hellquist. 1997. Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts. Free Radic. Biol. Med. 23:616–626.
  • Buzza, M. S., C. E. Hirst, C. H. Bird, P. Hosking, J. McKendrick, and P. I. Bird. The granzyme B inhibitor, PI-9, is present in endothelial and mesothelial cells, suggesting it protects bystander cells during immune responses. Cell Immunol., in press.
  • Chu, M., C. H. Bird, M. S. Teasdale, and P. I. Bird. 1998. Turnover of thrombomodulin at the cell surface occurs at a similar rate to receptors that are not actively internalized. Thromb. Haemostasis 80:119–127.
  • Chuang, T. L., and R. R. Schleef. 1999. Identification of a nuclear targeting domain in the insertion between helices C and D in protease inhibitor-10. J. Biol. Chem. 274:11194–11198.
  • Coughlin, P., J. Sun, L. Cerruti, H. H. Salem, and P. Bird. 1993. Cloning and molecular characterization of a human intracellular proteinase inhibitor. Proc. Natl. Acad. Sci. USA 90:9417–9421.
  • Dickinson, J. L., E. J. Bates, A. Ferrante, and T. M. Antalis. 1995. Plasminogen activator inhibitor 2 inhibits tumor necrosis factor alpha-induced apoptosis. Evidence for an alternate biological function. J. Biol. Chem. 270:27894–27904.
  • Efthymiadis, A., L. J. Briggs, and D. A. Jans. 1998. The HIV-1 Tat nuclear localization sequence confers novel nuclear import properties. J. Biol. Chem. 273:1623–1628.
  • Efthymiadis, A., H. Shao, S. Hubner, and D. A. Jans. 1997. Kinetic characterization of the human retinoblastoma protein bipartite nuclear localization sequence (NLS) in vivo and in vitro. A comparison with the SV40 large T-antigen NLS. J. Biol. Chem. 272:22134–22139.
  • Fischer, U., J. Huber, W. C. Boelens, I. W. Mattaj, and R. Luhrmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82:475–483.
  • Golstein, P.. 1974. Sensitivity of cytotoxic T cells to T-cell mediated cytotoxicity. Nature 252:81–83.
  • Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell. Dev. Biol. 15:607–660.
  • Grigoryev, S. A., J. Bednar, and C. L. Woodcock. 1999. MENT, a heterochromatin protein that mediates higher order chromatin folding, is a new serpin family member. J. Biol. Chem. 274:5626–5636.
  • Harlow, E., and D. Lane. 1988. Antibodies. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y
  • Hausmann, G., L. A. O'Reilly, R. van Driel, J. G. Beaumont, A. Strasser, J. A. Adams, and D. C. S. Haung. 2000. Pro-apoptotic apoptosis protease-activating factor 1 (Apaf-1) has a cytoplasmic localization distinct from Bcl-2 or Bcl-xL. J. Cell Biol. 149:623–633.
  • Henderson, B. R., and A. Eleftheriou. 2000. A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp. Cell Res. 256:213–224.
  • Hood, J. K., and P. A. Silver. 1999. In or out? Regulating nuclear transport. Curr. Opin. Cell Biol. 11:241–247.
  • Hubner, S., C. Y. Xiao, and D. A. Jans. 1997. The protein kinase CK2 site (Ser111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J. Biol. Chem. 272:17191–17195.
  • Huntington, J. A., R. A. Read, and R. W. Carrell. 2000. Structure of a serpin-protease complex shows inhibition by deformation. Nature 407:923–926.
  • Jans, D. A., L. J. Briggs, P. Jans, C. J. Froelich, G. Parasivam, S. Kumar, V. R. Sutton, and J. A. Trapani. 1998. Nuclear targeting of the serine proteinase granzyme A (fragmentin-1). J. Cell Sci. 111:2645–2654.
  • Jans, D. A., M. J. Ackermann, J. R. Bischoff, D. H. Beach, and R. Peters. 1991. p34cdc2-mediated phosphorylation at T124 inhibits nuclear import of SV-40 T antigen proteins. J. Cell Biol. 115:1203–1212.
  • Jans, D. A., and P. Jans. 1994. Negative charge at the casein kinase II site flanking the nuclear localization signal of the SV40 large T-antigen is mechanistically important for enhanced nuclear transport. Oncogene 9:2961–2968.
  • Jans, D. A., P. Jans, L. J. Briggs, V. Sutton, and J. A. Trapani. 1996. Nuclear transport of granzyme B (fragmentin 2). J. Biol. Chem. 271:30781–30789.
  • Jenkins, Y., M. McEntee, K. Weis, and W. C. Greene. 1998. Characterization of HIV-1 Vpr nuclear import: analysis of signals and pathways. J. Cell Biol. 143:875–885.
  • Kranz, D. M., and H. N. Eisen. 1987. Resistance of cytotoxic lymphocytes to lysis by a clone of cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 84:3375–3379.
  • Madison, E. L., and P. Bird. 1992. A vector, pSHT, for the expression and secretion of protein domains in mammalian cells. Gene 121:179–180.
  • Miyata, T., M. Nangaku, D. Suzuki, R. Inagi, K. Uragami, H. Sakai, K. Okubo, and K. Kurokawa. 1998. A mesangium-predominant gene, megsin, is a new serpin upregulated in IgA nephropathy. J. Clin. Investig. 120:828–836.
  • Murphy, R., and S. R. Wente. 1996. An RNA-export mediator with an essential nuclear export signal. Nature 383:357–360.
  • Nagata, S.. 1997. Apoptosis by death factor. Cell 88:355–365.
  • Nagler-Anderson, C., C. R. Verret, A. A. Firmenich, M. Berne, and H. N. Eisen. 1988. Resistance of primary CD8+ cytotoxic T lymphocytes to lysis by cytotoxic granules from cloned T cell lines. J. Immunol. 141:3299–3305.
  • Nigg, E. A.. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386:779–787.
  • Ochs, R., M. Lischwe, P. O'Leary, and H. Busch. 1983. Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp. Cell Res. 46:139–149.
  • Ooms, L., J. Nicholl, P. Bird, and G. R. Sutherland. 1995. Localization of the human monocyte/neutrophil elastase inhibitor gene to chromosome 6p25. Chromosome Res. 3:447
  • Pemberton, L. F., J. S. Rosenblum, and G. Blobel. 1999. Nuclear import of the TATa-binding protein: mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting. J. Cell Biol. 145:1407–1417.
  • Perkins, A., A. W. Cochrane, S. M. Ruben, and C. A. Rosen. 1989. Structural and functional characterization of the human immunodeficiency virus rev protein. J. Acquir. Immune Defic. Syndr. 2:256–263.
  • Potempa, J., E. Korzus, and J. Travis. 1994. The serpin superfamily of proteinase inhibitors: structure, function and regulation. J. Biol. Chem. 269:15957–15960.
  • Remold-O'Donnell, E.. 1993. The ovalbumin family of serpin proteins. FEBS Lett. 315:105–108.
  • Rihs, H. P., and R. Peters. 1989. Nuclear transport kinetics depend on phosphorylation-site-containing sequences flanking the karyophilic signal of the simian virus 40 T-antigen. EMBO J. 8:1479–1484.
  • Schick, C., Y. Kamachi, A. J. Bartuski, S. Cataltepe, N. M. Schechter, P. A. Pemberton, and G. A. Silverman. 1997. Squamous cell carcinoma antigen 2 is a novel serpin that inhibits the chymotrypsin-like proteinases cathepsin G and mast cell chymase. J. Biol. Chem. 272:1849–1855.
  • Schick, C., P. A. Pemberton, G.-P. Shi, Y. Kamachi, S. Cataltepe, A. J. Bartuski, E. R. Gornstein, D. Bromme, H. A. Chapman, and G. A. Silverman. 1998. Cross-class inhibition of the cysteine proteinases cathepsins K, L, and S by the serpin squamous cell carcinoma antigen 1: a kinetic analysis. Biochemistry 37:5258–5266.
  • Schikendanz, J., K. H. Scheidtmann, and G. Walter. 1986. Kinetics of nuclear transport and oligomerization of simian virus 40 large T antigen. Virology 148:47–57.
  • Scott, F. L., P. B. Coughlin, C. Bird, L. Cerruti, J. A. Hayman, and P. Bird. 1996. Proteinase inhibitor 6 cannot be secreted, which suggests it is a new type of cellular serpin. J. Biol. Chem. 271:1605–1612.
  • Scott, F. L., C. E. Hirst, J. Sun, S. P. Bottomley, C. H. Bird, and P. I. Bird. 1999. The intracellular serpin proteinase inhibitor 6 (PI-6) is expressed in monocytes and granulocytes and is a potent inhibitor of the azurophilic granule proteinase, cathepsin G. Blood 93:2089–2097.
  • Shi, L., S. Mai, S. Israels, K. A. Browne, J. A. Trapani, and A. H. Greenberg. 1997. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization. J. Exp. Med. 185:855–866.
  • Smyth, M. J., and J. A. Trapani. 1995. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol. Today 16:202–206.
  • Stein, P. E., and R. W. Carrell. 1995. What do dysfunctional serpins tell us about molecular mobility and disease. Struct. Biol. 2:96–113.
  • Stochaj, U., and K. L. Rother. 1999. Nucleocytoplasmic trafficking of proteins: with or without Ran?. Bioessays 21:579–589.
  • Sugimori, T., J. Cooley, J. R. Hoidal, and E. Remold-O'Donnell. 1995. Inhibitory properties of recombinant monocyte/neutrophil elastase inhibitor. Am. J. Respir. Cell Mol. Biol. 13:314–322.
  • Sun, J., C. H. Bird, V. Sutton, L. McDonald, P. B. Coughlin, T. A. De Jong, J. A. Trapani, and P. I. Bird. 1996. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 271:27802–27809.
  • Teasdale, M. S., C. H. Bird, and P. Bird. 1994. Internalization of the anticoagulant thrombomodulin is constitutive and does not require a signal in the cytoplasmic domain. Immunol. Cell Biol. 72:480–488.
  • Trapani, J. A.. 1998. Dual mechanisms of apoptosis induction by cytotoxic lymphocytes. Int. Rev. Cytol. 182:111–192.
  • Trapani, J. A., and P. I. Bird. 2000. Granzymes: mediation of pro-apoptotic and nonapoptotic functions of cytolytic lymphocytes and regulation by endogenous and circulating inhibitors. Cytotoxic cells: basic mechanisms and medical applications.. M. V. Sitkovsky, and P. A. Henkart. 179–196. Lippincott, Williams & Wilkins, Philadelphia, Pa
  • Trapani, J. A., K. A. Browne, M. J. Smyth, and D. A. Jans. 1996. Localization of granzyme B in the nucleus. J. Biol. Chem. 271:4127–4133.
  • Trapani, J. A., M. J. Smyth, V. A. Apostolidis, M. Dawson, and K. Browne. 1994. Granule serine proteinases are normal nuclear constituents of natural killer cells. J. Biol. Chem. 269:18359–18365.
  • Tsay, Y.-G., N. Y. Lin, P. G. Voss, R. J. Patterson, and J. L. Wang. 1999. Export of galactin-3 from nuclei of digitonin-permeabilized mouse 3T3 fibroblasts. Exp. Cell Res. 252:250–261.
  • Vancurova, I., W. Lou, T. M. Paine, and P. L. Paine. 1993. Nucleoplasmin uptake by facilitated transport and intranuclear binding. Eur. J. Cell Biol. 62:22–33.
  • Vyakarnam, A., A. J. Lenneman, K. M. Lakkides, R. J. Patterson, and J. L. Wang. 1998. A comparative nuclear localization study of galectin-1 with other splicing components. Exp. Cell Res. 242:419–428.
  • Whisstock, J., R. Skinner, and A. M. Lesk. 1998. An atlas of serpin conformations. Trends Biochem. Sci. 23:63–67.
  • Whisstock, J. C., J. A. Irving, S. P. Bottomley, R. N. Pike, and A. M. Lesk. 1999. Serpins in the Caenorhabditis elegans genome. Proteins 36:31–41.
  • Yodoi, J., K. Teshigawara, T. Nikaido, K. Fukui, T. Noma, T. Honjo, M. Takigawa, M. Sasaki, N. Minato, M. Tsudo, et al.. 1985. TCGF (IL 2)-receptor inducing factor(s). I. Regulation of IL 2 receptor on a natural killer-like cell line (YT cells). J. Immunol. 134:1623–1630.
  • Zhou, Q., and G. S. Salvesen. 1997. Activation of pro-caspase-7 by serine proteases includes a non-canonical specificity. Biochem. J. 324:361–364.
  • Zhou, Q., S. Snipas, K. Orth, M. Muzio, V. Dixit, and G. Salvesen. 1997. Target protease specificity of the viral serpin CrmA. J. Biol. Chem. 272:7797–7800.
  • Zou, Z., A. Anisowicz, M. J. C. Hendrix, A. Thor, M. Neveu, S. Sheng, K. Rafidi, E. Seftor, and R. Sager. 1994. Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 263:526–529.

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