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Abstract:

In this study, we demonstrate that the subcellular localization of the mineralocorticoid receptor (MR) is regulated by tetratricopeptide domain (TPR) proteins. The high-molecular-weight immunophilin (IMM) FKBP52 links the MR-hsp90 complex to dynein/dynactin motors favoring the cytoplasmic transport of MR to the nucleus. Replacement of this hsp90-binding IMM by FKBP51 or the TPR peptide favored the cytoplasmic localization of MR. The complete movement machinery, including dynein and tubulin, could be recovered from paclitaxel/GTP-stabilized cytosol and was fully reassembled on stripped MR immune pellets. The whole MR-hsp90-based heterocomplex was transiently recovered in the soluble fraction of the nucleus after 10 min of incubation with aldosterone. Moreover, cross-linked MR-hsp90 heterocomplexes accumulated in the nucleus in a hormone-dependent manner, demonstrating that the heterocomplex can pass undissociated through the nuclear pore. On the other hand, a peptide that comprises the DNA-binding domain of MR impaired the nuclear export of MR, suggesting the involvement of this domain in the process. This study represents the first report describing the entire molecular system that commands MR nucleocytoplasmic trafficking and proposes that the MR-hsp90-TPR protein heterocomplex is dissociated in the nucleus rather than in the cytoplasm. Copyright © 2010, American Society for Microbiology. All Rights Reserved.

Registro:

Documento: Artículo
Título:The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events
Autor:Galigniana, M.D.; Erlejman, A.G.; Monte, M.; Gomez-Sanchez, C.; Piwien-Pilipuk, G.
Filiación:IBYME/CONICET, Vuelta de Obligado 2490, Buenos Aires C1428ADN, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Division of Endocrinology, G. V. (Sonny) Montgomery VA Medical Center, University of Mississippi Medical Center, Jackson, MS, United States
Palabras clave:aldosterone; dynein adenosine triphosphatase; fk 506 binding protein; heat shock protein 90; immunophilin; mineralocorticoid receptor; molecular motor; protein fkbp52; tubulin; unclassified drug; animal cell; article; controlled study; human; human cell; mouse; nonhuman; priority journal; protein cross linking; protein domain; protein localization; protein protein interaction; tetratricopeptide repeat; Active Transport, Cell Nucleus; Animals; Cell Line; Cell Nucleus; CHO Cells; Cricetinae; Cricetulus; Dyneins; HSP90 Heat-Shock Proteins; Humans; Immunophilins; Mice; Microtubules; Molecular Motor Proteins; Multiprotein Complexes; NIH 3T3 Cells; Nuclear Pore; Nuclear Pore Complex Proteins; Protein Binding; Protein Stability; Protein Structure, Tertiary; Rats; Receptors, Mineralocorticoid; Recombinant Proteins; Tacrolimus Binding Proteins
Año:2010
Volumen:30
Número:5
Página de inicio:1285
Página de fin:1298
DOI: http://dx.doi.org/10.1128/MCB.01190-09
Título revista:Molecular and Cellular Biology
Título revista abreviado:Mol. Cell. Biol.
ISSN:02707306
CODEN:MCEBD
CAS:aldosterone, 52-39-1, 6251-69-0; Dyneins, 3.6.4.2; HSP90 Heat-Shock Proteins; Immunophilins, 5.2.1.8; Molecular Motor Proteins; Multiprotein Complexes; Nuclear Pore Complex Proteins; Receptors, Mineralocorticoid; Recombinant Proteins; Tacrolimus Binding Proteins, 5.2.1.-; tacrolimus binding protein 4, 5.2.1.-
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_02707306_v30_n5_p1285_Galigniana.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02707306_v30_n5_p1285_Galigniana

Referencias:

  • Adam, S.A., Marr, R.S., Gerace, L., Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors (1990) J. Cell Biol, 111, pp. 807-816
  • Akner, G., Mossberg, K., Sundqvist, K.G., Gustafsson, J.A., Wikstrom, A.C., Evidence for reversible, non-microtubule and non-micro-filament-dependent nuclear translocation of hsp90 after heat shock in human fibroblasts (1992) Eur. J. Cell Biol, 58, pp. 356-364
  • Black, B.E., Holaska, J.M., Rastinejad, F., Paschal, B.M., DNA binding domains in diverse nuclear receptors function as nuclear export signals (2001) Curr. Biol, 11, pp. 1749-1758
  • Buchholz, I., Enss, K., Schafer, C., Schlune, A., Shahin, V., Oberleithner, H., Transient permeability leak of nuclear envelope induced by aldosterone (2004) J. Membr. Biol, 199, pp. 135-141
  • Cheung, P.Y., Zhang, Y., Long, J., Lin, S., Zhang, M., Jiang, Y., Wu, Z., p150(Glued), dynein, and microtubules are specifically required for activation of MKK3/6 and p38 MAPKs (2004) J. Biol. Chem, 279, pp. 45308-45311
  • Cox, M.B., Riggs, D.L., Hessling, M., Schumacher, F., Buchner, J., Smith, D.F., FK506-binding protein 52 phosphorylation: A potential mechanism for regulating steroid hormone receptor activity (2007) Mol. Endocrinol, 21, pp. 2956-2967
  • Czar, M.J., Galigniana, M.D., Silverstein, A.M., Pratt, W.B., Geldanamycin, a heat shock protein 90-binding benzoquinone ansamycin, inhibits steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus (1997) Biochemistry, 36, pp. 7776-7785
  • Davies, T.H., Ning, Y.M., Sanchez, E.R., A new first step in activation of steroid receptors: Hormone-induced switching of FKBP51 and FKBP52 immunophilins (2002) J. Biol. Chem, 277, pp. 4597-4600
  • Dhani, S.U., Mohammad-Panah, R., Ahmed, N., Ackerley, C., Ramjeesingh, M., Bear, C.E., Evidence for a functional interaction between the ClC-2 chloride channel and the retrograde motor dynein complex (2003) J. Biol. Chem, 278, pp. 16262-16270
  • Dixit, R., Levy, J.R., Tokito, M., Ligon, L.A., Holzbaur, E.L., Regulation of dynactin through the differential expression of p150Glued isoforms (2008) J. Biol. Chem, 283, pp. 33611-33619
  • Echeverria, P.C., Mazaira, G., Erlejman, A., Gomez-Sanchez, C., Piwien Pilipuk, G., Galigniana, M.D., Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta (2009) Mol. Cell. Biol, 29, pp. 4788-4797
  • Frey, S., Gorlich, D., A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes (2007) Cell, 130, pp. 512-523
  • Galigniana, M.D., Native rat kidney mineralocorticoid receptor is a phosphoprotein whose transformation to a DNA-binding form is induced by phosphatases (1998) Biochem. J, 333, pp. 555-563
  • Galigniana, M.D., Harrell, J.M., Housley, P.R., Patterson, C., Fisher, S.K., Pratt, W.B., Retrograde transport of the glucocorticoid receptor in neurites requires dynamic assembly of complexes with the protein chaperone hsp90 and is linked to the CHIP component of the machinery for proteasomal degradation (2004) Brain Res. Mol. Brain Res, 123, pp. 27-36
  • Galigniana, M.D., Harrell, J.M., Murphy, P.J., Chinkers, M., Radanyi, C., Renoir, J.M., Zhang, M., Pratt, W.B., Binding of hsp90-associated immunophilins to cytoplasmic dynein: Direct binding and in vivo evidence that the peptidylprolyl isomerase domain is a dynein interaction domain (2002) Biochemistry, 41, pp. 13602-13610
  • Galigniana, M.D., Harrell, J.M., O'Hagen, H.M., Ljungman, M., Pratt, W.B., Hsp90-binding immunophilins link p53 to dynein during p53 transport to the nucleus (2004) J. Biol. Chem, 279, pp. 22483-22489
  • Galigniana, M.D., Housley, P.R., DeFranco, D.B., Pratt, W.B., Inhibition of glucocorticoid receptor nucleocytoplasmic shuttling by okadaic acid requires intact cytoskeleton (1999) J. Biol. Chem, 274, pp. 16222-16227
  • Galigniana, M.D., Radanyi, C., Renoir, J.M., Housley, P.R., Pratt, W.B., Evidence that the peptidylprolyl isomerase domain of the hsp90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus (2001) J. Biol. Chem, 276, pp. 14884-14889
  • Galigniana, M.D., Scruggs, J.L., Herrington, J., Welsh, M.J., Carter-Su, C., Housley, P.R., Pratt, W.B., Heat shock protein 90-dependent (geldanamycin-inhibited) movement of the glucocorticoid receptor through the cytoplasm to the nucleus requires intact cytoskeleton (1998) Mol. Endocrinol, 12, pp. 1903-1913
  • Galigniana, M.D., Vicent, G.P., Piwien-Pilipuk, G., Burton, G., Lantos, C.P., Mechanism of action of the potent sodium-retaining steroid 11,19-oxidoprogesterone (2000) Mol. Pharmacol, 58, pp. 58-70
  • Gallo, L.I., Ghini, A.A., Pilipuk, G.P., Galigniana, M.D., Differential recruitment of tetratricopeptide repeat domain immunophilins to the mineralocorticoid receptor influences both heat-shock protein 90-dependent retrotransport and hormone-dependent transcriptional activity (2007) Biochemistry, 46, pp. 14044-14057
  • Giannakakou, P., Sackett, D.L., Ward, Y., Webster, K.R., Blagosklonny, M.V., Fojo, T., p53 is associated with cellular microtubules and is transported to the nucleus by dynein (2000) Nat. Cell Biol, 2, pp. 709-717
  • Gorlich, D., Kutay, U., Transport between the cell nucleus and the cytoplasm (1999) Annu. Rev. Cell Dev. Biol, 15, pp. 607-660
  • Gross, K.L., Westberry, J.M., Hubler, T.R., Sadosky, P.W., Singh, R.J., Taylor, R.L., Scammell, J.G., Androgen resistance in squirrel monkeys (Saimiri spp.) (2008) Comp. Med, 58, pp. 381-388
  • Guiochon-Mantel, A., Lescop, P., Christin-Maitre, S., Loosfelt, H., Perrot-Applanat, M., Milgrom, E., Nucleocytoplasmic shuttling of the progesterone receptor (1991) EMBO J, 10, pp. 3851-3859
  • Harrell, J.M., Kurek, I., Breiman, A., Radanyi, C., Renoir, J.M., Pratt, W.B., Galigniana, M.D., All of the protein interactions that link steroid receptor.hsp90.immunophilin heterocomplexes to cytoplasmic dynein are common to plant and animal cells (2002) Biochemistry, 41, pp. 5581-5587
  • Harrell, J.M., Murphy, P.J., Morishima, Y., Chen, H., Mansfield, J.F., Galigniana, M.D., Pratt, W.B., Evidence for glucocorticoid receptor transport on microtubules by dynein (2004) J. Biol. Chem, 279, pp. 54647-54654
  • Kampmann, M., Blobel, G., Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex (2009) Nat. Struct. Mol. Biol, 16, pp. 782-788
  • Lim, R.Y., Huang, N.P., Koser, J., Deng, J., Lau, K.H., Schwarz-Herion, K., Fahrenkrog, B., Aebi, U., Flexible phenylalanine-glycine nucleoporins as entropic barriers to nucleocytoplasmic transport (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 9512-9517
  • Lombes, M., Binart, N., Delahaye, F., Baulieu, E.E., Rafestin-Oblin, M.E., Differential intracellular localization of human mineralocorticosteroid receptor on binding of agonists and antagonists (1994) Biochem. J, 302, pp. 191-197
  • Lyman, S.K., Guan, T., Bednenko, J., Wodrich, H., Gerace, L., Influence of cargo size on Ran and energy requirements for nuclear protein import (2002) J. Cell Biol, 159, pp. 55-67
  • Madan, A.P., DeFranco, D.B., Bidirectional transport of glucocorticoid receptors across the nuclear envelope (1993) Proc. Natl. Acad. Sci. USA, 90, pp. 3588-3592
  • McKeen, H.D., McAlpine, K., Valentine, A., Quinn, D.J., McClelland, K., Byrne, C., O'Rourke, M., Robson, T., A novel FK506-like binding protein interacts with the glucocorticoid receptor and regulates steroid receptor signaling (2008) Endocrinology, 149, pp. 5724-5734
  • Melkonian, K.A., Maier, K.C., Godfrey, J.E., Rodgers, M., Schroer, T.A., Mechanism of dynamitin-mediated disruption of dynactin (2007) J. Biol. Chem, 282, pp. 19355-19364
  • Nishi, M., Ogawa, H., Ito, T., Matsuda, K.I., Kawata, M., Dynamic changes in subcellular localization of mineralocorticoid receptor in living cells: In comparison with glucocorticoid receptor using dual-color labeling with green fluorescent protein spectral variants (2001) Mol. Endocrinol, 15, pp. 1077-1092
  • Nishi, M., Takenaka, N., Morita, N., Ito, T., Ozawa, H., Kawata, M., Real-time imaging of glucocorticoid receptor dynamics in living neurons and glial cells in comparison with non-neural cells (1999) Eur. J. Neurosci, 11, pp. 1927-1936
  • Pante, N., Kann, M., Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm (2002) Mol. Biol. Cell, 13, pp. 425-434
  • Perrot-Applanat, M., Lescop, P., Milgrom, E., The cytoskeleton and the cellular traffic of the progesterone receptor (1992) J. Cell Biol, 119, pp. 337-348
  • Piwien-Pilipuk, G., Galigniana, M.D., Tautomycin inhibits phosphatase-dependent transformation of the rat kidney mineralocorticoid receptor (1998) Mol. Cell. Endocrinol, 144, pp. 119-130
  • Piwien-Pilipuk, G., Kanelakis, K.C., Galigniana, M.D., Correlation between pregnanesteroid conformation, receptor affinity, and anti-natriuretic effect (2002) Eur. J. Pharmacol, 454, pp. 131-143
  • Piwien-Pilipuk, G., Kanelakis, K.C., Ghini, A.A., Lantos, C.P., Litwack, G., Burton, G., Galigniana, M.D., Modification of an essential amino group in the mineralocorticoid receptor evidences a differential conformational change of the receptor protein upon binding of antagonists, natural agonists and the synthetic agonist 11,19-oxidoprogesterone (2002) Biochim. Biophys. Acta, 1589, pp. 31-48
  • Piwien Pilipuk, G., Vinson, G.P., Sanchez, C.G., Galigniana, M.D., Evidence for NL1-independent nuclear translocation of the mineralocorticoid receptor (2007) Biochemistry, 46, pp. 1389-1397
  • Pouton, C.W., Nuclear import of polypeptides, polynucleotides and supramolecular complexes (1998) Adv. Drug Deliv. Rev, 34, pp. 51-64
  • Pratt, W.B., Galigniana, M.D., Harrell, J.M., DeFranco, D.B., Role of hsp90 and the hsp90-binding immunophilins in signalling protein movement (2004) Cell Signal, 16, pp. 857-872
  • Pratt, W.B., Galigniana, M.D., Morishima, Y., Murphy, P.J., Role of molecular chaperones in steroid receptor action (2004) Essays Biochem, 40, pp. 41-58
  • Pratt, W.B., Toft, D.O., Steroid receptor interactions with heat shock protein and immunophilin chaperones (1997) Endocr. Rev, 18, pp. 306-360
  • Rabe, B., Vlachou, A., Pante, N., Helenius, A., Kann, M., Nuclear import of hepatitis B virus capsids and release of the viral genome (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 9849-9854
  • Ratajczak, T., Ward, B.K., Minchin, R.F., Immunophilin chaperones in steroid receptor signalling (2003) Curr. Top. Med. Chem, 3, pp. 1348-1357
  • Riggs, D.L., Cox, M.B., Tardif, H.L., Hessling, M., Buchner, J., Smith, D.F., Noncatalytic role of the FKBP52 peptidyl-prolyl isomerase domain in the regulation of steroid hormone signaling (2007) Mol. Cell. Biol, 27, pp. 8658-8669
  • Riggs, D.L., Roberts, P.J., Chirillo, S.C., Cheung-Flynn, J., Prapapanich, V., Ratajczak, T., Gaber, R., Smith, D.F., The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo (2003) EMBO J, 22, pp. 1158-1167
  • Robertson, N.M., Schulman, G., Karnik, S., Alnemri, E., Litwack, G., Demonstration of nuclear translocation of the mineralocorticoid receptor (MR) using an anti-MR antibody and confocal laser scanning microscopy (1993) Mol. Endocrinol, 7, pp. 1226-1239
  • Rossi, G.P., Sechi, L.A., Giacchetti, G., Ronconi, V., Strazzullo, P., Funder, J.W., Primary aldosteronism: Cardiovascular, renal and metabolic implications (2008) Trends Endocrinol. Metab, 19, pp. 88-90
  • Russell, L.C., Whitt, S.R., Chen, M.S., Chinkers, M., Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90 (1999) J. Biol. Chem, 274, pp. 20060-20063
  • Sanchez, E.R., Hirst, M., Scherrer, L.C., Tang, H.Y., Welsh, M.J., Harmon, J.M., Simons Jr., S.S., Pratt, W.B., Hormonefree mouse glucocorticoid receptors overexpressed in Chinese hamster ovary cells are localized to the nucleus and are associated with both hsp70 and hsp90 (1990) J. Biol. Chem, 265, pp. 20123-20130
  • Savory, J.G., Hsu, B., Laquian, I.R., Giffin, W., Reich, T., Hache, R.J., Lefebvre, Y.A., Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor (1999) Mol. Cell. Biol, 19, pp. 1025-1037
  • Schafer, C., Shahin, V., Albermann, L., Hug, M.J., Reinhardt, J., Schillers, H., Schneider, S.W., Oberleithner, H., Aldosterone signaling pathway across the nuclear envelope (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 7154-7159
  • Seksek, O., Biwersi, J., Verkman, A.S., Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus (1997) J. Cell Biol, 138, pp. 131-142
  • Silverstein, A.M., Galigniana, M.D., Chen, M.S., Owens-Grillo, J.K., Chinkers, M., Pratt, W.B., Protein phosphatase 5 is a major component of glucocorticoid receptor.hsp90 complexes with properties of an FK506-binding immunophilin (1997) J. Biol. Chem, 272, pp. 16224-16230
  • Silverstein, A.M., Galigniana, M.D., Kanelakis, K.C., Radanyi, C., Renoir, J.M., Pratt, W.B., Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, hsp90, and cytoplasmic dynein (1999) J. Biol. Chem, 274, pp. 36980-36986
  • Smith, D.F., Toft, D.O., Minireview: The intersection of steroid receptors with molecular chaperones: observations and questions (2008) Mol. Endocrinol, 22, pp. 2229-2240
  • Smith, D.F., Whitesell, L., Nair, S.C., Chen, S., Prapapanich, V., Rimerman, R.A., Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent (1995) Mol. Cell. Biol, 15, pp. 6804-6812
  • Tsai, N.P., Tsui, Y.C., Wei, L.N., Dynein motor contributes to stress granule dynamics in primary neurons (2009) Neuroscience, 159, pp. 647-656
  • Vallee, R.B., Williams, J.C., Varma, D., Barnhart, L.E., Dynein: An ancient motor protein involved in multiple modes of transport (2004) J. Neurobiol, 58, pp. 189-200
  • Vicent, G.P., Pecci, A., Ghini, A., Piwien-Pilipuk, G., Galigniana, M.D., Differences in nuclear retention characteristics of agonist-activated glucocorticoid receptor may determine specific responses (2002) Exp. Cell Res, 276, pp. 142-154
  • Viengchareun, S., D. Le Menuet, L. Martinerie, M. Munier, L. Pascual-Le Tallec, and M. Lombes. 2007. The mineralocorticoid receptor: insights into its molecular and (patho)physiological biology. Nucl. Recept. Signal. 5:e012; Wochnik, G.M., Ruegg, J., Abel, G.A., Schmidt, U., Holsboer, F., Rein, T., FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells (2005) J. Biol. Chem, 280, pp. 4609-4616
  • Wolf, I.M., Periyasamy, S., Hinds Jr., T., Yong, W., Shou, W., Sanchez, E.R., Targeted ablation reveals a novel role of FKBP52 in genespecific regulation of glucocorticoid receptor transcriptional activity (2009) J. Steroid Biochem. Mol. Biol, 113, pp. 36-45
  • Yang, J., Liu, J., DeFranco, D.B., Subnuclear trafficking of glucocorticoid receptors in vitro: Chromatin recycling and nuclear export (1997) J. Cell Biol, 137, pp. 523-538

Citas:

---------- APA ----------
Galigniana, M.D., Erlejman, A.G., Monte, M., Gomez-Sanchez, C. & Piwien-Pilipuk, G. (2010) . The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events. Molecular and Cellular Biology, 30(5), 1285-1298.
http://dx.doi.org/10.1128/MCB.01190-09
---------- CHICAGO ----------
Galigniana, M.D., Erlejman, A.G., Monte, M., Gomez-Sanchez, C., Piwien-Pilipuk, G. "The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events" . Molecular and Cellular Biology 30, no. 5 (2010) : 1285-1298.
http://dx.doi.org/10.1128/MCB.01190-09
---------- MLA ----------
Galigniana, M.D., Erlejman, A.G., Monte, M., Gomez-Sanchez, C., Piwien-Pilipuk, G. "The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events" . Molecular and Cellular Biology, vol. 30, no. 5, 2010, pp. 1285-1298.
http://dx.doi.org/10.1128/MCB.01190-09
---------- VANCOUVER ----------
Galigniana, M.D., Erlejman, A.G., Monte, M., Gomez-Sanchez, C., Piwien-Pilipuk, G. The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events. Mol. Cell. Biol. 2010;30(5):1285-1298.
http://dx.doi.org/10.1128/MCB.01190-09