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Abstract:

In the absence of hormone, corticosteroid receptors such as GR (glucocorticoid receptor) and MR (mineralocorticoid receptor) are primarily located in the cytoplasm. Upon steroid-binding, they rapidly accumulate in the nucleus. Regardless of their primary location, these receptors and many other nuclear factors undergo a constant and dynamic nucleocytoplasmic shuttling. All members of the steroid receptor family are known to form large oligomeric structures with the heat-shock proteins of 90-kDa (hsp90) and 70-kDa (hsp70), the small acidic protein p23, and a tetratricopeptide repeat (TPR)-domain protein such as FK506-binding proteins (FKBPs), cyclophilins (CyPs) or the serine/threonine protein phosphatase 5 (PP5). It has always been stated that the dissociation of the chaperone heterocomplex (a process normally referred to as receptor "transformation") is the first step that permits the nuclear import of steroid receptors. However the experimental evidence is consistent with a model where the chaperone machinery is required for the retrotransport of the receptor through the cytoplasm and also facilitates the passage through the nuclear pore. Recent evidence indicates that the hsp90-based chaperone system also interacts with structures of the nuclear pore such as importin β and the integral nuclear pore glycoprotein Nup62 facilitating the passage of the untransformed receptor through the nuclear pore. © 2010 Landes Bioscience.

Registro:

Documento: Artículo
Título:Role of molecular chaperones and TPR-domain proteins in the cytoplasmic transport of steroid receptors and their passage through the nuclear pore
Autor:Galigniana, M.D.; Echeverría, P.C.; Erlejman, A.G.; Piwien-Pilipuk, G.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Biología y Medicina Experimental-CONICET, Buenos Aires, Argentina
Départment de Biologie Cellulaire, Université de Genève, Geneva, Switzerland
Palabras clave:Dynein; Heat-shock proteins; Immunophilins; Importins; Nucleoporins; Shuttling; chaperone; cyclophilin; dynactin; fk 506 binding protein; glucocorticoid receptor; glycoprotein; heat shock protein 70; heat shock protein 90; immunoglobulin enhancer binding protein; karyopherin beta; mineralocorticoid receptor; nucleoporin; protein nup62; protein p23; serine threonine protein phosphatase 5; tetratricopeptide repeat protein; unclassified drug; article; cell compartmentalization; cell nucleus membrane; ligand binding; nuclear pore complex; nucleocytoplasmic transport; protein transport; signal transduction
Año:2010
Volumen:1
Número:4
Página de inicio:299
Página de fin:308
DOI: http://dx.doi.org/10.4161/nucl.1.4.11743
Título revista:Nucleus
Título revista abreviado:Nucl.
ISSN:19491034
CAS:cyclophilin, 126043-36-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19491034_v1_n4_p299_Galigniana

Referencias:

  • Aridor, M., Hannan, L.A., Traffic jams II: An update of diseases of intracellular transport (2002) Traffic, 3, pp. 781-790
  • Cobbold, C., Monaco, A.P., Sivaprasadarao, A., Ponnambalam, S., Aberrant trafficking of transmembrane proteins in human disease (2003) Trends Cell Biol, 13, pp. 639-647
  • Fabbro, M., Henderson, B.R., Regulation of tumor suppressors by nuclear-cytoplasmic shuttling (2003) Exp Cell Res, 282, pp. 59-69
  • Perry, R.B., Fainzilber, M., Nuclear transport factors in neuronal function (2009) Semin Cell Dev Biol, 20, pp. 600-606
  • Defranco, D.B., Navigating steroid hormone receptors through the nuclear compartment (2002) Mol Endocrinol, 16, pp. 1449-1455
  • 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
  • Xu, L., Massague, J., Nucleocytoplasmic shuttling of signal transducers (2004) Nat Rev Mol Cell Biol, 5, pp. 209-219
  • 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
  • Ambron, R.T., Schmied, R., Huang, C.C., Smedman, M., A signal sequence mediates the retrograde transport of proteins from the axon periphery to the cell body and then into the nucleus (1992) J Neurosci, 12, pp. 2813-2818
  • Medalia, O., Weber, I., Frangakis, A.S., Nicastro, D., Gerisch, G., Baumeister, W., Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography (2002) Science, 298, pp. 1209-1213
  • 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
  • Jiang, J., Cyr, D., Babbitt, R.W., Sessa, W.C., Patterson, C., Chaperone-dependent regulation of endothelial nitric-oxide synthase intracellular trafficking by the co-chaperone/ubiquitin ligase CHIP (2003) J Biol Chem, 278, pp. 49332-49341
  • Piwien Pilipuk, G., Galigniana, M.D., Subcellular Movement of Signalling Molecules. How and Why? (2006) Focus on Cellular Signalling, pp. 73-107. , in Leeds DT, (ed): Focus on Cellular Signalling. New York: Nova Publishers
  • 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
  • Grad, I., Picard, D., The glucocorticoid responses are shaped by molecular chaperones (2007) Mol Cell Endocrinol, 275, pp. 2-12
  • 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
  • Jackson, S.E., Queitsch, C., Toft, D., Hsp90: From structure to phenotype (2004) Nat Struct Mol Biol, 11, pp. 1152-1155
  • Wandinger, S.K., Richter, K., Buchner, J., The Hsp90 chaperone machinery (2008) J Biol Chem, 283, pp. 18473-18477
  • 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
  • McKeen, H.D., McAlpine, K., Valentine, A., Quinn, D.J., McClelland, K., Byrne, C., A novel FK506-like binding protein interacts with the glucocorticoid receptor and regulates steroid receptor signaling (2008) Endocrinology, 149, pp. 5724-5734
  • 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
  • Smith, D.F., Schowalter, D.B., Kost, S.L., Toft, D.O., Reconstitution of progesterone receptor with heat shock proteins (1990) Mol Endocrinol, 4, pp. 1704-1711
  • Hutchison, K.A., Brott, B.K., de Leon, J.H., Perdew, G.H., Jove, R., Pratt, W.B., Reconstitution of the multiprotein complex of pp60src, hsp90 and p50 in a cell-free system (1992) J Biol Chem, 267, pp. 2902-2908
  • Stancato, L.F., Chow, Y.H., Hutchison, K.A., Perdew, G.H., Jove, R., Pratt, W.B., Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system (1993) J Biol Chem, 268, pp. 21711-21716
  • Dittmar, K.D., Banach, M., Galigniana, M.D., Pratt, W.B., The role of DnaJ-like proteins in glucocorticoid receptor.hsp90 heterocomplex assembly by the reconstituted hsp90.p60.hsp70 foldosome complex (1998) J Biol Chem, 273, pp. 7358-7366
  • Pratt, W.B., Silverstein, A.M., Galigniana, M.D., A model for the cytoplasmic trafficking of signalling proteins involving the hsp90-binding immunophilins and p50cdc37 (1999) Cell Signal, 11, pp. 839-851
  • Morishima, Y., Kanelakis, K.C., Murphy, P.J., Lowe, E.R., Jenkins, G.J., Osawa, Y., The hsp90 cochaperone p23 is the limiting component of the multiprotein hsp90/hsp70-based chaperone system in vivo where it acts to stabilize the client protein: Hsp90 complex (2003) J Biol Chem, 278, pp. 48754-48763
  • Picard, D., Intracellular dynamics of the Hsp90 cochaperone p23 is dictated by Hsp90 (2006) Exp Cell Res, 312, pp. 198-204
  • Picard, D., Suslova, E., Briand, P.A., 2-color photobleaching experiments reveal distinct intracellular dynamics of two components of the Hsp90 complex (2006) Exp Cell Res, 312, pp. 3949-3958
  • Thomas, M., Harrell, J.M., Morishima, Y., Peng, H.M., Pratt, W.B., Lieberman, A.P., Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction (2006) Hum Mol Genet, 15, pp. 1876-1883
  • Toft, D.O., Recent Advances in the Study of hsp90 Structure and Mechanism of Action (1998) Trends Endocrinol Metab, 9, pp. 238-243
  • Hartl, F.U., Molecular chaperones in cellular protein folding (1996) Nature, 381, pp. 571-579
  • Kanelakis, K.C., Shewach, D.S., Pratt, W.B., Nucleotide binding states of hsp70 and hsp90 during sequential steps in the process of glucocorticoid receptor. hsp90 heterocomplex assembly (2002) J Biol Chem, 277, pp. 33698-33703
  • Smith, D.F., Sullivan, W.P., Marion, T.N., Zaitsu, K., Madden, B., McCormick, D.J., Toft, D.O., Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70 (1993) Mol Cell Biol, 13, pp. 869-876
  • Kanelakis, K.C., Morishima, Y., Dittmar, K.D., Galigniana, M.D., Takayama, S., Reed, J.C., Differential effects of the hsp70-binding protein BAG-1 on glucocorticoid receptor folding by the hsp90-based chaperone machinery (1999) J Biol Chem, 274, pp. 34134-34140
  • Young, J.C., Obermann, W.M., Hartl, F.U., Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90 (1998) J Biol Chem, 273, pp. 18007-18010
  • 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
  • Gallo, L.I., Ghini, A.A., Pilipuk, G.P., Galigniana, M.D., Differential recruitment of tetratricorpeptide 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
  • Galigniana, M.D., Harrell, J.M., Murphy, P.J., Chinkers, M., Radanyi, C., Renoir, J.M., Binding of hsp90associated 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
  • 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
  • Davies, T.H., Ning, Y.M., Sanchez, E.R., Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506 (2005) Biochemistry, 44, pp. 2030-2038
  • Witchel, S.F., Defranco, D.B., Mechanisms of disease: Regulation of glucocorticoid and receptor levels- impact on the metabolic syndrome (2006) Nat Clin Pract Endocrinol Metab, 2, pp. 621-631
  • Galigniana, M.D., Piwien Pilipuk, G., Activation of the ligand-mineralocorticoid receptor functional unit by ancient, classical and novel ligands. Structureactivity relationship (2004) Vitam Horm, 69, pp. 31-68
  • 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
  • Galigniana, M.D., Functional regulation of corticosteroid receptors by phosphorylation and redox potential (2000) Current Topics In Steroid Research, 3, pp. 1-22
  • Galigniana, M.D., Piwien Pilipuk, G., Kanelakis, K.C., Burton, G., Lantos, C.P., Molecular mechanism of activation and nuclear translocation of the mineralocorticoid receptor upon binding of pregnanesteroids (2004) Mol Cell Endocrinol, 217, pp. 167-179
  • 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., Erlejman, A.G., Monte, M., Gomezsanchez, 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 (2010) Mol Cell Biol, 30, pp. 1285-1298
  • Kardon, J.R., Vale, R.D., Regulators of the cytoplasmic dynein motor (2009) Nat Rev Mol Cell Biol, 10, pp. 854-865
  • Harrell, J.M., Murphy, P.J., Morishima, Y., Chen, H., Mansfield, J.F., Galigniana, M.D., Evidence for glucocorticoid receptor transport on microtubules by dynein (2004) J Biol Chem, 279, pp. 54647-54654
  • Elad, N., Maimon, T., Frenkiel-Krispin, D., Lim, R.Y., Medalia, O., Structural analysis of the nuclear pore complex by integrated approaches (2009) Curr Opin Struct Biol, 19, pp. 226-232
  • Lusk, C.P., Blobel, G., King, M.C., Highway to the inner nuclear membrane: Rules for the road (2007) Nat Rev Mol Cell Biol, 8, pp. 414-420
  • Terry, L.J., Shows, E.B., Wente, S.R., Crossing the nuclear envelope: Hierarchical regulation of nucleocytoplasmic transport (2007) Science, 318, pp. 1412-1416
  • Stewart, M., Molecular mechanism of the nuclear protein import cycle (2007) Nat Rev Mol Cell Biol, 8, pp. 195-208
  • Fagotto, F., Gluck, U., Gumbiner, B.M., Nuclear localization signal-independent and importin/karyopherinindependent nuclear import of beta-catenin (1998) Curr Biol, 8, pp. 181-190
  • Picard, D., Yamamoto, K.R., Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor (1987) EMBO J, 6, pp. 3333-3340
  • Walther, R.F., Atlas, E., Carrigan, A., Rouleau, Y., Edgecombe, A., Visentin, L., A serine/threoninerich motif is one of three nuclear localization signals that determine unidirectional transport of the mineralocorticoid receptor to the nucleus (2005) J Biol Chem, 280, pp. 17549-17561
  • 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
  • Passinen, S., Valkila, J., Manninen, T., Syvala, H., Ylikomi, T., The C-terminal half of Hsp90 is responsible for its cytoplasmic localization (2001) Eur J Biochem, 268, pp. 5337-5342
  • Kang, K.I., Devin, J., Cadepond, F., Jibard, N., Guiochon-Mantel, A., Baulieu, E.E., In vivo functional protein-protein interaction: Nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus (1994) Proc Natl Acad Sci USA, 91, pp. 340-344
  • 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
  • Sanchez, E.R., Hirst, M., Scherrer, L.C., Tang, H.Y., Welsh, M.J., Harmon, J.M., Hormone-free 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., Discrimination between NL1and NL2-mediated nuclear localization of the glucocorticoid receptor (1999) Mol Cell Biol, 19, pp. 1025-1037
  • Li, H., Fidler, M.L., Lim, C.S., Effect of initial subcellular localization of progesterone receptor on import kinetics and transcriptional activity (2005) Mol Pharm, 2, pp. 509-518
  • Freedman, N.D., Yamamoto, K.R., Importin 7 and importin alpha/importin beta are nuclear import receptors for the glucocorticoid receptor (2004) Mol Biol Cell, 15, pp. 2276-2286
  • Tanaka, M., Nishi, M., Morimoto, M., Sugimoto, T., Kawata, M., Yellow fluorescent protein-tagged and cyan fluorescent protein-tagged imaging analysis of glucocorticoid receptor and importins in single living cells (2003) Endocrinology, 144, pp. 4070-4079
  • Hodel, A.E., Harreman, M.T., Pulliam, K.F., Harben, M.E., Holmes, J.S., Hodel, M.R., Nuclear localization signal receptor affinity correlates with in vivo localization in Saccharomyces cerevisiae (2006) J Biol Chem, 281, pp. 23545-23556
  • Gilchrist, D., Mykytka, B., Rexach, M., Accelerating the rate of disassembly of karyopherin.cargo complexes (2002) J Biol Chem, 277, pp. 18161-18172
  • Jakel, S., Mingot, J.M., Schwarzmaier, P., Hartmann, E., Gorlich, D., Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains (2002) EMBO J, 21, pp. 377-386
  • Georget, V., Terouanne, B., Nicolas, J.C., Sultan, C., Mechanism of antiandrogen action: Key role of hsp90 in conformational change and transcriptional activity of the androgen receptor (2002) Biochemistry, 41, pp. 11824-11831
  • Denning, D.P., Patel, S.S., Uversky, V., Fink, A.L., Rexach, M., Disorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded (2003) Proc Natl Acad Sci USA, 100, pp. 2450-2455
  • Patel, S.S., Belmont, B.J., Sante, J.M., Rexach, M.F., Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex (2007) Cell, 129, pp. 83-96
  • Murphy, P.J., Morishima, Y., Chen, H., Galigniana, M.D., Mansfield, J.F., Simons Jr., S.S., Visualization and mechanism of assembly of a glucocorticoid receptor. Hsp70 complex that is primed for subsequent Hsp90dependent opening of the steroid binding cleft (2003) J Biol Chem, 278, pp. 34764-34773
  • Pemberton, L.F., Rosenblum, J.S., Blobel, G., Nuclear import of the TATA-binding protein mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting (1999) J Cell Biol, 145, pp. 1407-1417
  • Kose, S., Furuta, M., Koike, M., Yoneda, Y., Imamoto, N., The 70-kD heat shock cognate protein (hsc70) facilitates the nuclear export of the import receptors (2005) J Cell Biol, 171, pp. 19-25
  • Guerrero-Santoro, J., Yang, L., Stallcup, M.R., Defranco, D.B., Distinct, L.I.M., Domains of Hic-5/ARA55 are required for nuclear matrix targeting and glucocorticoid receptor binding and coactivation (2004) J Cell Biochem, 92, pp. 810-819
  • Tago, K., Tsukahara, F., Naruse, M., Yoshioka, T., Takano, K., Regulation of nuclear retention of glucocorticoid receptor by nuclear Hsp90 (2004) Mol Cell Endocrinol, 213, pp. 131-138

Citas:

---------- APA ----------
Galigniana, M.D., Echeverría, P.C., Erlejman, A.G. & Piwien-Pilipuk, G. (2010) . Role of molecular chaperones and TPR-domain proteins in the cytoplasmic transport of steroid receptors and their passage through the nuclear pore. Nucleus, 1(4), 299-308.
http://dx.doi.org/10.4161/nucl.1.4.11743
---------- CHICAGO ----------
Galigniana, M.D., Echeverría, P.C., Erlejman, A.G., Piwien-Pilipuk, G. "Role of molecular chaperones and TPR-domain proteins in the cytoplasmic transport of steroid receptors and their passage through the nuclear pore" . Nucleus 1, no. 4 (2010) : 299-308.
http://dx.doi.org/10.4161/nucl.1.4.11743
---------- MLA ----------
Galigniana, M.D., Echeverría, P.C., Erlejman, A.G., Piwien-Pilipuk, G. "Role of molecular chaperones and TPR-domain proteins in the cytoplasmic transport of steroid receptors and their passage through the nuclear pore" . Nucleus, vol. 1, no. 4, 2010, pp. 299-308.
http://dx.doi.org/10.4161/nucl.1.4.11743
---------- VANCOUVER ----------
Galigniana, M.D., Echeverría, P.C., Erlejman, A.G., Piwien-Pilipuk, G. Role of molecular chaperones and TPR-domain proteins in the cytoplasmic transport of steroid receptors and their passage through the nuclear pore. Nucl. 2010;1(4):299-308.
http://dx.doi.org/10.4161/nucl.1.4.11743