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Abstract:

The mineralocorticoid receptor (MR) forms oligomers with the heat-shock protein 90 (Hsp90) -based heterocomplex, which contains tetratricopeptide repeat (TPR) domain immunophilins (IMMs). Here we investigated the unknown biological role of IMMs in the MR•Hsp90 complex. Upon hormone binding, FKBP52 was greatly recruited to MR•Hsp90 complexes along with dynein motors, whereas FKBP51 was dissociated. Importantly, the Hsp90 inhibitor geldanamycin impaired the retrograde transport of MR, suggesting that the Hsp90•IMM•dynein molecular machinery is required for MR movement. To elucidate the mechanism of action of MR, the synthetic ligand 11,19-oxidoprogesterone was used as a tool. This steroid showed equivalent agonistic potency to natural agonists and was able to potentiate their mineralocorticoid action. Importantly, aldosterone binding recruited greater amounts of FKBP52 and dynein than 11,19- oxidoprogesterone binding to MR. Interestingly, 11,19-oxidoprogesterone binding also favored the selective recruitment of the IMM-like Ser/Thr phosphatase PP5. Each hormone/MR complex yielded different proteolytic peptide patterns, suggesting that MR acquires different conformations upon steroid binding. Also, hormone/MR complexes showed different nuclear translocation rates and subnuclear redistribution. All these observations may be related to the selective swapping of associated factors. We conclude that (a) the Hsp90•FKBP52•dyenin complex may be responsible for the retrotransport of MR; (b) a differential recruitment of TPR proteins such as FKBP51, FKBP52, and PP5 takes place during the early steps of hormone-dependent activation of the receptor; (c) importantly, this swapping of TPR proteins depends on the nature of the ligand; and (d) inasmuch as FKBP51 also showed an inhibitory effect on MR-dependent transcription, it should be dissociated from the MR•Hsp90 complex to positively regulate the mineralocorticoid effect. © 2007 American Chemical Society.

Registro:

Documento: Artículo
Título:Differential recruitment of tetratricorpeptide repeat domain immunophilins to the mineralocorticoid receptor influences both heat-shock protein 90-dependent retrotransport and hormone-dependent transcriptional activity
Autor:Gallo, L.I.; Ghini, A.A.; Pilipuk, G.P.; Galigniana, M.D.
Filiación:Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires (IIBBA-CONICET), Buenos Aires, Argentina
Unidad de Microanalisis Y Metodos Fisicos Aplicados a Quimica Organica (UMYMFOR-CONICET), Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Fundación Instituto Leloir, Av. Patricias Argentines 435, Buenos Aires C1405BWE, Argentina
Palabras clave:Hormone binding; Immunophilins; Mineralocorticoid effect; Mineralocorticoid receptors; Conformations; Enzyme inhibition; Hormones; Ligands; Transcription; Peptides; 11,19 oxidoprogesterone; 6,19 oxidoprogesterone; agents interacting with transmitter, hormone or drug receptors; aldosterone; fkbp 51; fkbp 52; geldanamycin; heat shock protein 90; immunophilin; mineralocorticoid receptor; progesterone derivative; spironolactone; tacrolimus; unclassified drug; animal cell; article; binding affinity; biological activity; controlled study; drug effect; drug potentiation; fibroblast; hormone binding; human; human cell; immunofluorescence; ligand binding; mouse; nonhuman; priority journal; protein degradation; receptor binding; steroid binding; tetratricopeptide repeat; Western blotting; Aldosterone; Animals; Benzoquinones; Desoxycorticosterone; Dynein ATPase; Fibroblasts; HSP90 Heat-Shock Proteins; Humans; Lactams, Macrocyclic; Male; Mice; NIH 3T3 Cells; Progesterone; Protein Conformation; Protein Transport; Rats; Receptors, Mineralocorticoid; Repetitive Sequences, Amino Acid; Tacrolimus Binding Proteins; Transcription, Genetic
Año:2007
Volumen:46
Número:49
Página de inicio:14044
Página de fin:14057
DOI: http://dx.doi.org/10.1021/bi701372c
Título revista:Biochemistry
Título revista abreviado:Biochemistry
ISSN:00062960
CODEN:BICHA
CAS:aldosterone, 52-39-1, 6251-69-0; geldanamycin, 30562-34-6; spironolactone, 52-01-7; tacrolimus, 104987-11-3; 11,19-oxidoprogesterone, 1913-28-6; 6,19-oxidoprogesterone; Aldosterone, 52-39-1; Benzoquinones; Desoxycorticosterone, 64-85-7; Dynein ATPase, 3.6.4.2; HSP90 Heat-Shock Proteins; Lactams, Macrocyclic; Progesterone, 57-83-0; Receptors, Mineralocorticoid; Tacrolimus Binding Proteins, 5.2.1.-; geldanamycin, 30562-34-6; tacrolimus binding protein 4, 5.2.1.-; tacrolimus binding protein 5, 5.2.1.8
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00062960_v46_n49_p14044_Gallo

Referencias:

  • Evans, R.M., The steroid and thyroid hormone receptor superfamily (1988) Science, 240, pp. 889-895
  • Escriva, H., Bertrand, S., Laudet, V., The evolution of the nuclear receptor superfamily (2004) Essays Biochem, 40, pp. 11-26
  • Nollen, E.A., Morimoto, R.I., Chaperoning signaling pathways: Molecular chaperones as stress-sensing 'heat shock' proteins (2002) J. Cell Sci, 115, pp. 2809-2816
  • 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
  • Ratajczak, T., Ward, B.K., Minchin, R.F., Immunophilin chaperones in steroid receptor signalling (2003) Curr. Top. Med. Chem, 3, pp. 1348-1357
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • Burton, G., Galigniana, M., De Lavallaz, S., Brachet-Cota, A.L., Sproviero, E.M., Ghini, A.A., Lantos, C.P., Damasco, M.C., Sodium-retaining activity of some natural and synthetic 21-deoxysteroids (1995) Mol. Pharmacol, 47, pp. 535-543
  • 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
  • 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
  • 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., 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., 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
  • Galigniana, M.D., Morishima, Y., Gallay, P.A., Pratt, W.B., Cyclophilin-A is bound through its peptidylprolyl isomerase domain to the cytoplasmic dynein motor protein complex (2004) J. Biol. Chem, 279, pp. 55754-55759
  • 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
  • Piwien-Pilipuk, G., Ayala, A., Machado, A., Galigniana, M.D., Impairment of mineralocorticoid receptor (MR)-dependent biological response by oxidative stress and aging: Correlation with post-translational modification of MR and decreased ADP-ribosylatable level of elongating factor 2 in kidney cells (2002) J. Biol. Chem, 277, pp. 11896-11903
  • Galigniana, M.D., Stability study on renal type I mineralocorticoid receptor (1996) Life Sci, 59, pp. 511-521
  • Galigniana, M.D., Piwien Pilipuk, G., Activation of the ligand-mineralocorticoid receptor functional unit by ancient, classical, and novel ligands. Structure-activity relationship (2004) Vitam. Horm. (San Diego), 69, pp. 31-68
  • 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
  • Hultman, M.L., Krasnoperova, N.V., Li, S., Du, S., Xia, C., Dietz, J.D., Lala, D.S., Hu, X., The ligand-dependent interaction of mineralocorticoid receptor with coactivator and corepressor peptides suggests multiple activation mechanisms (2005) Mol. Endocrinol, 19, pp. 1460-1473
  • Fuse, H., Kitagawa, H., Kato, S., Characterization of transactivational property and coactivator mediation of rat mineralocorticoid receptor activation function-1 (AF-1) (2000) Mol. Endocrinol, 14, pp. 889-899
  • 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
  • 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
  • Housley, P.R., Forsthoefel, A.M., Isolation and characterization of a mouse L cell variant deficient in glucocorticoid receptors (1989) Biochem. Biophys. Res. Commun, 164, pp. 480-487
  • Hubler, T.R., Denny, W.B., Valentine, D.L., Cheung-Flynn, J., Smith, D.F., Scammell, J.G., The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness (2003) Endocrinology, 144, pp. 2380-2387
  • Denny, W.B., Valentine, D.L., Reynolds, P.D., Smith, D.F., Scammell, J.G., Squirrel monkey immunophilin FKBP51 is a potent inhibitor of glucocorticoid receptor binding (2000) Endocrinology, 141, pp. 4107-4113
  • 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
  • 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
  • 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
  • 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
  • Zhao, W., Zhong, L., Wu, J., Chen, L., Qing, K., Weigel-Kelley, K.A., Larsen, S.H., Srivastava, A., Role of cellular FKBP52 protein in intracellular trafficking of recombinant adeno-associated virus 2 vectors (2006) Virology, 353, pp. 283-293
  • 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
  • Li, P., Ding, Y., Wu, B., Shu, C., Shen, B., Rao, Z., Structure of the N-terminal domain of human FKBP52 (2003) Acta Crystallogr. D: Biol. Crystallogr, 59, pp. 16-22
  • 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
  • Deppe, C.E., Heering, P.J., Viengchareun, S., Grabensee, B., Farman, N., Lombes, M., Cyclosporine a and FK506 inhibit transcriptional activity of the human mineralocorticoid receptor: A cell-based model to investigate partial aldosterone resistance in kidney transplantation (2002) Endocrinology, 143, pp. 1932-1941
  • Wiebe, J.P., Souter, L., Zhang, G., Dutasteride affects progesterone metabolizing enzyme activity/expression in human breast cell lines resulting in suppression of cell proliferation and detachment (2006) J. Steroid Biochem. Mol. Biol, 100, pp. 129-140
  • Funder, J.W., Aldosterone and mineralocorticoid receptors: Orphan questions (2000) Kidney Int, 57, pp. 1358-1363

Citas:

---------- APA ----------
Gallo, L.I., Ghini, A.A., Pilipuk, G.P. & Galigniana, M.D. (2007) . Differential recruitment of tetratricorpeptide repeat domain immunophilins to the mineralocorticoid receptor influences both heat-shock protein 90-dependent retrotransport and hormone-dependent transcriptional activity. Biochemistry, 46(49), 14044-14057.
http://dx.doi.org/10.1021/bi701372c
---------- CHICAGO ----------
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" . Biochemistry 46, no. 49 (2007) : 14044-14057.
http://dx.doi.org/10.1021/bi701372c
---------- MLA ----------
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" . Biochemistry, vol. 46, no. 49, 2007, pp. 14044-14057.
http://dx.doi.org/10.1021/bi701372c
---------- VANCOUVER ----------
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. Biochemistry. 2007;46(49):14044-14057.
http://dx.doi.org/10.1021/bi701372c