Regulation of the glucocorticoid response to stress-related disorders by the Hsp90-binding immunophilin FKBP51

Journal of Neurochemistry

Volumn 122, Issue 1, 2012, Pages 4-18

  Galigniana, Natalia M ^a   Ballmer, Luzia T ^a   Toneatto, Judith ^a   Erlejman, Alejandra G ^b   Lagadari, Mariana ^a   Galigniana, Mario D ^a,b  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

depression; glucocorticoid receptor; Hsp90; Hypothalamic Pituitary Adrenal axis; immunophilin; tetratricopeptide repeat domain

Indexed keywords

CHAPERONE; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 51; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 90; IMMUNOPHILIN; MINERALOCORTICOID RECEPTOR; PEPTIDYLPROLYL ISOMERASE; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ANXIETY DISORDER; CUSHING DISEASE; DEPRESSION; DISEASE ASSOCIATION; DISEASE COURSE; DRUG RESISTANCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HORMONE RESPONSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; MENTAL STRESS; MOOD DISORDER; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; ANXIETY DISORDERS; GLUCOCORTICOIDS; HUMANS; MOOD DISORDERS; PEPTIDYLPROLYL ISOMERASE; RECEPTORS, STEROID; STRESS DISORDERS, POST-TRAUMATIC; TACROLIMUS BINDING PROTEINS;

EID: 84862219142     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07775.x     Document Type: Review

References (159)

1. Ansai T., Dupuy L. C., and, Barik S., (1996) Interactions between a minimal protein serine/threonine phosphatase and its phosphopeptide substrate sequence. J. Biol. Chem. 271, 24401-24407. (Pubitemid 26333172)
2. Bain D. L., Heneghan A. F., Connaghan-Jones K. D., and, Miura M. T., (2007) Nuclear receptor structure: implications for function. Annu. Rev. Physiol. 69, 201-220. (Pubitemid 46457641)
3. Balbach J., Steegborn C., Schindler T., and, Schmid F. X., (1999) A protein folding intermediate of ribonuclease T1 characterized at high resolution by 1D and 2D real-time NMR spectroscopy. J. Mol. Biol. 285, 829-842. (Pubitemid 29041811)
4. Barden N., Stec I. S., Montkowski A., Holsboer F., and, Reul J. M., (1997) Endocrine profile and neuroendocrine challenge tests in transgenic mice expressing antisense RNA against the glucocorticoid receptor. Neuroendocrinology 66, 212-220. (Pubitemid 27356903)
5. Baughman G., Wiederrecht G. J., Chang F., Martin M. M., and, Bourgeois S., (1997) Tissue distribution and abundance of human FKBP51, and FK506-binding protein that can mediate calcineurin inhibition. Biochem. Biophys. Res. Commun. 232, 437-443. (Pubitemid 27216235)
6. Billing A. M., Fack F., Renaut J., Olinger C. M., Schote A. B., Turner J. D., and, Muller C. P., (2007) Proteomic analysis of the cortisol-mediated stress response in THP-1 monocytes using DIGE technology. J. Mass Spectrom. 42, 1433-1444. (Pubitemid 350113461)
7. Billing A. M., Fack F., Turner J. D., and, Muller C. P., (2011) Cortisol is a potent modulator of lipopolysaccharide-induced interferon signaling in macrophages. Innate Immun 17, 302-320.
8. Binder E. B., (2009) The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 34, S186-S195.
9. Binder E. B., Salyakina D., and, Lichtner P., et al. (2004) Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat. Genet. 36, 1319-1325. (Pubitemid 39577942)
10. Binder E. B., Bradley R. G., and, Liu W., et al. (2008) Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA 299, 1291-1305. (Pubitemid 351439075)
11. Binder E. B., Kunzel H. E., Nickel T., Kern N., Pfennig A., Majer M., Uhr M., Ising M., and, Holsboer F., (2009) HPA-axis regulation at in-patient admission is associated with antidepressant therapy outcome in male but not in female depressed patients. Psychoneuroendocrinology 34, 99-109.
12. Boyle M. P., Brewer J. A., Funatsu M., Wozniak D. F., Tsien J. Z., Izumi Y., and, Muglia L. J., (2005) Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc. Natl Acad. Sci. USA 102, 473-478. (Pubitemid 40116791)
13. Brent D., Melhem N., Ferrell R., et al. (2010) Association of FKBP5 polymorphisms with suicidal events in the Treatment of Resistant Depression in Adolescents (TORDIA) study. Am. J. Psychiatry 167, 190-197.
14. Buchanan T. W., (2007) Retrieval of emotional memories. Psychol. Bull. 133, 761-779.
15. Carrasco G. A., and, Van de Kar L. D., (2003) Neuroendocrine pharmacology of stress. Eur. J. Pharmacol. 463, 235-272. (Pubitemid 36205084)
16. Chambraud B., Belabes H., Fontaine-Lenoir V., Fellous A., and, Baulieu E. E., (2007) The immunophilin FKBP52 specifically binds to tubulin and prevents microtubule formation. Faseb J. 21, 2787-2797. (Pubitemid 47372746)
17. Cheng R., Juo S. H., and, Loth J. E., et al. (2006) Genome-wide linkage scan in a large bipolar disorder sample from the National Institute of Mental Health genetics initiative suggests putative loci for bipolar disorder, psychosis, suicide, and panic disorder. Mol Psychiatry 11, 252-260.
18. Cheung-Flynn J., Prapapanich V., Cox M. B., Riggs D. L., Suarez-Quian C., and, Smith D. F., (2005) Physiological role for the cochaperone FKBP52 in androgen receptor signaling. Mol. Endocrinol. 19, 1654-1666. (Pubitemid 41002993)
19. Cioffi D. L., Hubler T. R., and, Scammell J. G,. (2011) Organization and function of the FKBP52 and FKBP51 genes. Curr. Opin. Pharmacol. 11, 308-313.
20. Claes S., (2009) Glucocorticoid receptor polymorphisms in major depression. Ann. NY Acad. Sci. 1179, 216-228.
21. Colo G. P., Rubio M. F., Nojek I. M., Werbajh S. E., Echeverria P. C., Alvarado C. V., Nahmod V. E., Galigniana M. D., and, Costas M. A., (2008) The p160 nuclear receptor co-activator RAC3 exerts an anti-apoptotic role through a cytoplasmatic action. Oncogene 27, 2430-2444. (Pubitemid 351521102)
22. Consortium W. T. C. C. (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447, 661-678.
23. Cox M. B., and, Smith D. F,. (2007) Functions of the Hsp90-Binding FKBP Immunophilins, in The Networking of Chaperones by Cochaperones (, Blatch G. L,. ed.), pp. 13-25. Austin, Texas. Eurekah.com.
24. Cox M. B., Riggs D. L., Hessling M., Schumacher F., Buchner J., and, Smith D. F., (2007) FK506-binding protein 52 phosphorylation: a potential mechanism for regulating steroid hormone receptor activity. Mol. Endocrinol. 21, 2956-2967. (Pubitemid 350223507)
25. Czar M. J., Owens-Grillo J. K., Yem A. W., Leach K. L., Deibel Jr M. R., Welsh M. J., and, Pratt W. B., (1994) The hsp56 immunophilin component of untransformed steroid receptor complexes is localized both to microtubules in the cytoplasm and to the same nonrandom regions within the nucleus as the steroid receptor. Mol. Endocrinol. 8, 1731-1741.
26. Das A. K., Helps N. R., Cohen P. T., and, Barford D., (1996) Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J. 15, 6798-6809.
27. Davies T. H., and, Sanchez E. R,. (2005) Fkbp52. Int. J. Biochem. Cell Biol. 37, 42-47. (Pubitemid 39286022)
28. Davies T. H., Ning Y. M., and, Sanchez E. R., (2002) A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J. Biol. Chem. 277, 4597-4600. (Pubitemid 34968486)
29. Davies T. H., Ning Y. M., and, Sanchez E. R., (2005) Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506. Biochemistry 44, 2030-2038. (Pubitemid 40223631)
30. De Iudicibus S., Franca R., Martelossi S., Ventura A., and, Decorti G., (2011) Molecular mechanism of glucocorticoid resistance in inflammatory bowel disease. World J. Gastroenterol. 17, 1095-1108.
31. De Kloet E. R., Vreugdenhil E., Oitzl M. S., and, Joels M., (1998) Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269-301. (Pubitemid 29117816)
32. Denny W. B., Valentine D. L., Reynolds P. D., Smith D. F., and, Scammell J. G., (2000) Squirrel monkey immunophilin FKBP51 is a potent inhibitor of glucocorticoid receptor binding. Endocrinology 141, 4107-4113.
33. Denny W. B., Prapapanich V., Smith D. F., and, Scammell J. G., (2005) Structure-function analysis of squirrel monkey FK506-binding protein 51, a potent inhibitor of glucocorticoid receptor activity. Endocrinology 146, 3194-3201. (Pubitemid 41002828)
34. 2+-induced permeability transition in brain mitochondria, with relation to the bioenergetic state. J. Biol. Chem. 286, 6345-6353.
35. Echeverria P. C., and, Picard D., (2010) Molecular chaperones, essential partners of steroid hormone receptors for activity and mobility. Biochim. Biophys. Acta. 1803, 641-649.
36. Echeverria P. C., Mazaira G., Erlejman A., Gomez-Sanchez C., Piwien Pilipuk G., and, Galigniana M. D., (2009) Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta. Mol. Cell. Biol. 29, 4788-4797.
37. Escriva H., Bertrand S., and, Laudet V., (2004) The evolution of the nuclear receptor superfamily. Essays Biochem. 40, 11-26. (Pubitemid 38901165)
38. Evans R. M., (1988) The steroid and thyroid hormone receptor superfamily. Science 240, 889-895.
39. Fischer G., and, Aumuller T., (2003) Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. Rev. Physiol. Biochem. Pharmacol. 148, 105-150.
40. Fischer G., Wittmann-Liebold B., Lang K., Kiefhaber T., and, Schmid F. X., (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337, 476-478.
41. Friedman D. B., and, Lilley K. S., (2008) Optimizing the difference gel electrophoresis (DIGE) technology. Methods Mol. Biol. 428, 93-124.
42. Fusco D., Vargiolu M., Vidone M., et al. (2010) The RET51/FKBP52 complex and its involvement in Parkinson disease. Hum. Mol. Genet. 19, 2804-2816.
43. Galat A., (2004) A note on clustering the functionally-related paralogues and orthologues of proteins: a case of the FK506-binding proteins (FKBPs). Comput. Biol. Chem. 28, 129-140.
44. Galigniana M. D., (1998) Native rat kidney mineralocorticoid receptor is a phosphoprotein whose transformation to a DNA-binding form is induced by phosphatases. Biochem. J. 333, 555-563. (Pubitemid 28398521)
45. Galigniana M. D., and, Piwien Pilipuk G., (2004) Activation of the ligand-mineralocorticoid receptor functional unit by ancient, classical, and novel ligands. Structure-activity relationship Vitam. Horm. 69, 31-68. (Pubitemid 39753686)
46. Galigniana M. D., and, Piwien-Pilipuk G., (1999) Comparative inhibition by hard and soft metal ions of steroid-binding capacity of renal mineralocorticoid receptor cross-linked to the 90-kDa heat-shock protein heterocomplex. Biochem. J. 341, 585-592. (Pubitemid 29389188)
47. Galigniana M. D., Housley P. R., DeFranco D. B., and, Pratt W. B., (1999) Inhibition of glucocorticoid receptor nucleocytoplasmic shuttling by okadaic acid requires intact cytoskeleton. J. Biol. Chem. 274, 16222-16227.
48. Galigniana M. D., Vicent G. P., Piwien-Pilipuk G., Burton G., and, Lantos C. P., (2000) Mechanism of action of the potent sodium-retaining steroid 11, 19-oxidoprogesterone. Mol. Pharmacol. 58, 58-70. (Pubitemid 30452528)
49. Galigniana M. D., Radanyi C., Renoir J. M., Housley P. R., and, Pratt W. B., (2001) 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. J. Biol. Chem. 276, 14884-14889.
50. Galigniana M. D., Harrell J. M., Murphy P. J., Chinkers M., Radanyi C., Renoir J. M., Zhang M., and, Pratt W. B., (2002) Binding of hsp90-associated immunophilins to cytoplasmic dynein: direct binding and in vivo evidence that the peptidylprolyl isomerase domain is a dynein interaction domain. Biochemistry 41, 13602-13610. (Pubitemid 35332696)
51. Galigniana M. D., Harrell J. M., O'Hagen H. M., Ljungman M., and, Pratt W. B., (2004a) Hsp90-binding immunophilins link p53 to dynein during p53 transport to the nucleus. J. Biol. Chem. 279, 22483-22489. (Pubitemid 38679447)
52. Galigniana M. D., Morishima Y., Gallay P. A., and, Pratt W. B., (2004b) Cyclophilin-A is bound through its peptidylprolyl isomerase domain to the cytoplasmic dynein motor protein complex. J. Biol. Chem. 279, 55754-55759. (Pubitemid 40066582)
53. Galigniana M. D., Piwien Pilipuk G., Kanelakis K. C., Burton G., and, Lantos C. P., (2004c) Molecular mechanism of activation and nuclear translocation of the mineralocorticoid receptor upon binding of pregnanesteroids. Mol. Cell. Endocrinol. 217, 167-179. (Pubitemid 38596641)
54. Galigniana M. D., Erlejman A. G., Monte M., Gomez-Sanchez C., and, 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. Mol. Cell. Biol. 30, 1285-1298.
55. Gallo L. I., Ghini A. A., Pilipuk G. P., and, 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, 14044-14057. (Pubitemid 350250300)
56. Gallo L. I., Lagadari M., Piwien-Pilipuk G., and, Galigniana M. D,. (2011) TPR-domain immunophilin FKBP51 is a major mitochondrial protein that protects cells from oxidative stress. J. Biol. Chem. 286, 30152-30160.
57. Groeneweg F. L., Karst H., de Kloet E. R., and, Joels M., (2011) Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol. 209, 153-167.
58. Groeneweg F. L., Karst H., de Kloet E. R., and, Joels M,. (2012) Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol. Cell. Endocrinol. 350, 299-309.
59. Handschumacher R. E., Harding M. W., Rice J., Drugge R. J., and, Speicher D. W., (1984) Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226, 544-547. (Pubitemid 14018525)
60. Hartmann J., Wagner K. V., Liebl C., et al. (2012) The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 62, 332-339.
61. Hawkins G. A., Lazarus R., Smith R. S., Tantisira K. G., Meyers D. A., Peters S. P., Weiss S. T., and, Bleecker E. R., (2009) The glucocorticoid receptor heterocomplex gene STIP1 is associated with improved lung function in asthmatic subjects treated with inhaled corticosteroids. J. Allergy Clin. Immunol. 123, 1376-1383.
62. Heim C., and, Nemeroff C. B., (2009) Neurobiology of posttraumatic stress disorder. CNS Spectr. 14, 13-24.
63. Hilser V. J., and, Thompson E. B., (2011) Structural dynamics, intrinsic disorder, and allostery in nuclear receptors as transcription factors. J. Biol. Chem. 286, 39675-39682.
64. Hirota Y., Acar N., Tranguch S., et al. (2010) Uterine FK506-binding protein 52 (FKBP52)-peroxiredoxin-6 (PRDX6) signaling protects pregnancy from overt oxidative stress. Proc. Natl Acad. Sci. USA 107, 15577-15582.
65. Holsboer F., (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23, 477-501.
66. Hong J., Kim S. T., Tranguch S., Smith D. F., and, Dey S. K., (2007) Deficiency of co-chaperone immunophilin FKBP52 compromises sperm fertilizing capacity. Reproduction 133, 395-403. (Pubitemid 46359527)
67. Horstmann S., Lucae S., Menke A., Hennings J. M., Ising M., Roeske D., Muller-Myhsok B., Holsboer F., and, Binder E. B., (2010) Polymorphisms in GRIK4, HTR2A, and FKBP5 show interactive effects in predicting remission to antidepressant treatment. Neuropsychopharmacology 35, 727-740.
68. Hubler T. R., and, Scammell J. G., (2004) Intronic hormone response elements mediate regulation of FKBP5 by progestins and glucocorticoids. Cell Stress Chaperones 9, 243-252. (Pubitemid 39457428)
69. Hubler T. R., Denny W. B., Valentine D. L., Cheung-Flynn J., Smith D. F., and, Scammell J. G., (2003) The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness. Endocrinology 144, 2380-2387. (Pubitemid 36629888)
70. Ising M., Depping A. M., Siebertz A., et al. (2008) Polymorphisms in the FKBP5 gene region modulate recovery from psychosocial stress in healthy controls. Eur. J. Neurosci. 28, 389-398.
71. Kam J. C., Szefler S. J., Surs W., Sher E. R., and, Leung D. Y., (1993) Combination IL-2 and IL-4 reduces glucocorticoid receptor-binding affinity and T cell response to glucocorticoids. J. Immunol. 151, 3460-3466. (Pubitemid 23282658)
72. Kang C. B., Hong Y., Dhe-Paganon S., and, Yoon H. S., (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals 16, 318-325.
73. Kato T., (2007) Molecular genetics of bipolar disorder and depression. Psychiatry Clin. Neurosci. 61, 3-19. (Pubitemid 46089400)
74. Kato T., (2008) Role of mitochondrial DNA in calcium signaling abnormality in bipolar disorder. Cell Calcium 44, 92-102.
75. de Kloet E. R., (2003) Hormones, brain and stress. Endocr. Regul. 37, 51-68. (Pubitemid 37420023)
76. de Kloet E. R., Joels M., and, Holsboer F., (2005) Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. (Pubitemid 40769171)
77. Klok M. D., Vreeburg S. A., Penninx B. W., Zitman F. G., de Kloet E. R., and, DeRijk R. H., (2011) Common functional mineralocorticoid receptor polymorphisms modulate the cortisol awakening response: interaction with SSRIs. Psychoneuroendocrinology 36, 484-494.
78. Koenen K. C., Saxe G., Purcell S., et al. (2005) Polymorphisms in FKBP5 are associated with peritraumatic dissociation in medically injured children. Mol Psychiatry 10, 1058-1059. (Pubitemid 43251094)
79. Kokras N., Dalla C., and, Papadopoulou-Daifoti Z., (2011) Sex differences in pharmacokinetics of antidepressants. Expert Opin. Drug Metab. Toxicol. 7, 213-226.
80. Kuhlmann S., Piel M., and, Wolf O. T., (2005) Impaired memory retrieval after psychosocial stress in healthy young men. J. Neurosci. 25, 2977-2982. (Pubitemid 40389255)
81. Lee R. S., Tamashiro K. L., Yang X., et al. (2010) Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 151, 4332-4343.
82. Lekman M., Laje G., Charney D., et al. (2008) The FKBP5-gene in depression and treatment response - an association study in the Sequenced Treatment Alternatives to Relieve Depression (STARD) Cohort. Biol. Psychiatry, 63, 1103-1110.
83. Li T. K., Baksh S., Cristillo A. D., and, Bierer B. E., (2002) Calcium- and FK506-independent interaction between the immunophilin FKBP51 and calcineurin. J. Cell. Biochem. 84, 460-471. (Pubitemid 34111181)
84. Li H., Rao A., and, Hogan P. G., (2011) Interaction of calcineurin with substrates and targeting proteins. Trends Cell Biol. 21, 91-103.
85. Lovas K., Gjesdal C. G., Christensen M., et al. (2009) Glucocorticoid replacement therapy and pharmacogenetics in Addison's disease: effects on bone. Eur. J. Endocrinol. 160, 993-1002.
86. Makkonen H., Kauhanen M., Paakinaho V., Jaaskelainen T., and, Palvimo J. J., (2009) Long-range activation of FKBP51 transcription by the androgen receptor via distal intronic enhancers. Nucleic Acids Res. 37, 4135-4148.
87. Marques A. H., Silverman M. N., and, Sternberg E. M., (2009) Glucocorticoid dysregulations and their clinical correlates. From receptors to therapeutics. Ann. N. Y. Acad. Sci. 1179, 1-18.
88. Massol N., Lebeau M. C., Schumacher M., and, Baulieu E. E., (2003) Promoter activity and gene structure of rabbit FKBP52. DNA Cell Biol. 22, 505-511. (Pubitemid 37174749)
89. Nestler E. J., Barrot M., DiLeone R. J., Eisch A. J., Gold S. J., and, Monteggia L. M., (2002) Neurobiology of depression. Neuron 34, 13-25. (Pubitemid 34270695)
90. Oishi K., Miyazaki K., Kadota K., et al. (2003) Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 278, 41519-41527. (Pubitemid 37280981)
91. Oitzl M. S., Reichardt H. M., Joels M., and, de Kloet E. R., (2001) Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl Acad. Sci. USA 98, 12790-12795. (Pubitemid 33020023)
92. Oitzl M. S., Champagne D. L., van der Veen R., and, de Kloet E. R., (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 34, 853-866.
93. Ozer E. J., Best S. R., Lipsey T. L., and, Weiss D. S., (2003) Predictors of posttraumatic stress disorder and symptoms in adults: a meta-analysis. Psychol. Bull. 129, 52-73. (Pubitemid 41103268)
94. Paakinaho V., Makkonen H., Jaaskelainen T., and, Palvimo J. J., (2010) Glucocorticoid receptor activates poised FKBP51 locus through long-distance interactions. Mol. Endocrinol. 24, 511-525.
95. Pariante C. M., and, Miller A. H., (2001) Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol. Psychiatry 49, 391-404. (Pubitemid 32234301)
96. Pariante C. M., Makoff A., Lovestone S., Feroli S., Heyden A., Miller A. H., and, Kerwin R. W., (2001) Antidepressants enhance glucocorticoid receptor function in vitro by modulating the membrane steroid transporters. Br. J. Pharmacol. 134, 1335-1343. (Pubitemid 33097265)
97. Periyasamy S., Hinds Jr T., Shemshedini L., Shou W., and, Sanchez E. R., (2010) FKBP51 and Cyp40 are positive regulators of androgen-dependent prostate cancer cell growth and the targets of FK506 and cyclosporin A. Oncogene 29, 1691-1701.
98. Perrot-Applanat M., Cibert C., Geraud G., Renoir J. M., and, Baulieu E. E., (1995) The 59 kDa FK506-binding protein, a 90 kDa heat shock protein binding immunophilin (FKBP59-HBI), is associated with the nucleus, the cytoskeleton and mitotic apparatus. J. Cell Sci. 108, 2037-2051.
99. Piwien Pilipuk G., Vinson G. P., Sanchez C. G., and, Galigniana M. D., (2007) Evidence for NL1-independent nuclear translocation of the mineralocorticoid receptor. Biochemistry 46, 1389-1397. (Pubitemid 46208486)
100. Piwien-Pilipuk G., and, Galigniana M. D., (1998) Tautomycin inhibits phosphatase-dependent transformation of the rat kidney mineralocorticoid receptor. Mol. Cell. Endocrinol. 144, 119-130. (Pubitemid 28491307)
101. Piwien-Pilipuk G., and, Galigniana M. D., (2000) Oxidative stress induced by L-buthionine-(S,R)-sulfoximine, a selective inhibitor of glutathione metabolism, abrogates mouse kidney mineralocorticoid receptor function. Biochim. Biophys. Acta 1495, 263-280. (Pubitemid 30103547)
102. Piwien-Pilipuk G., Ayala A., Machado A., and, Galigniana M. D., (2002) 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. J. Biol. Chem. 277, 11896-11903. (Pubitemid 34952747)
103. Pratt W. B., and, Toft D. O., (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18, 306-360. (Pubitemid 27246880)
104. Quintá H. R., and, Galigniana M. D,. (2012) The Neuroregenerative Mechanism Mediated by the Hsp90-Binding Immunophilin Fkbp52 Resembles the Early Steps of Neuronal Differentiation. Br. J. Pharmacol. 166, 637-649.
105. Quintá H. R., Maschi D., Gomez-Sanchez C., Piwien Pilipuk G., and, Galigniana M. D., (2010) Subcellular rearrangement of hsp90-binding immunophilins accompanies neuronal differentiation and neurite outgrowth. J. Neurochem. 115, 716-734.
106. Quintá H. R., Galigniana N. M., Erlejman A. G., Lagadari M., Piwien-Pilipuk G., and, Galigniana M. D., (2011) Management of cytoskeleton architecture by molecular chaperones and immunophilins. Cell. Signal. 23, 1907-1920.
107. Raddatz D., Middel P., Bockemuhl M., Benohr P., Wissmann C., Schworer H., and, Ramadori G., (2004) Glucocorticoid receptor expression in inflammatory bowel disease: evidence for a mucosal down-regulation in steroid-unresponsive ulcerative colitis. Aliment. Pharmacol. Ther. 19, 47-61. (Pubitemid 38125637)
108. Reiche E. M., Nunes S. O., and, Morimoto H. K., (2004) Stress, depression, the immune system, and cancer. Lancet Oncol 5, 617-625. (Pubitemid 39303129)
109. Reynolds P. D., Roveda K. P., Tucker J. A., Moore C. M., Valentine D. L., and, Scammell J. G., (1998) Glucocorticoid-resistant B-lymphoblast cell line derived from the Bolivian squirrel monkey (Saimiri boliviensis boliviensis). Lab. Anim. Sci. 48, 364-370.
110. Ridder S., Chourbaji S., Hellweg R., et al. (2005) Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions. J. Neurosci. 25, 6243-6250. (Pubitemid 40923491)
111. Riggs D. L., Roberts P. J., Chirillo S. C., Cheung-Flynn J., Prapapanich V., Ratajczak T., Gaber R., Picard D., and, Smith D. F., (2003) The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J. 22, 1158-1167. (Pubitemid 36313599)
112. Riggs D. L., Cox M. B., Tardif H. L., Hessling M., Buchner J., and, Smith D. F., (2007) Noncatalytic role of the FKBP52 peptidyl-prolyl isomerase domain in the regulation of steroid hormone signaling. Mol. Cell. Biol. 27, 8658-8669. Epub 20070Oct 8615.
113. van Rossum E. F., Binder E. B., Majer M., Koper J. W., Ising M., Modell S., Salyakina D., Lamberts S. W., and, Holsboer F., (2006) Polymorphisms of the glucocorticoid receptor gene and major depression. Biol. Psychiatry 59, 681-688.
114. Roy A., Gorodetsky E., Yuan Q., Goldman D., and, Enoch M. A., (2010) Interaction of FKBP5, a stress-related gene, with childhood trauma increases the risk for attempting suicide. Neuropsychopharmacology 35, 1674-1683.
115. Sapolsky R. M., Krey L. C., and, McEwen B. S., (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 7, 284-301.
116. Sarginson J. E., Lazzeroni L. C., Ryan H. S., Schatzberg A. F., and, Murphy Jr G. M., (2010) FKBP5 polymorphisms and antidepressant response in geriatric depression. Am J. Med. Genet. B Neuropsychiatr. Genet. 153B, 554-560.
117. Scammell J. G., Denny W. B., Valentine D. L., and, Smith D. F., (2001) Overexpression of the FK506-binding immunophilin FKBP51 is the common cause of glucocorticoid resistance in three New World primates. Gen. Comp. Endocrinol. 124, 152-165. (Pubitemid 33065587)
118. Scammell J. G., Hubler T. R., Denny W. B., and, Valentine D. L., (2003) Organization of the human FK506-binding immunophilin FKBP52 protein gene (FKBP4). Genomics 81, 640-643. (Pubitemid 36627507)
119. Schiene-Fischer C., Aumuller T., and, Fischer G,. (2012) Peptide Bond cis/trans Isomerases: a Biocatalysis Perspective of Conformational Dynamics in Proteins. Top. Curr. Chem. 1-33.
120. Schmidt U., Holsboer F., and, Rein T., (2011) Epigenetic aspects of posttraumatic stress disorder. Dis. Markers 30, 77-87.
121. Schule C., Baghai T. C., Eser D., Hafner S., Born C., Herrmann S., and, Rupprecht R., (2009) The combined dexamethasone/CRH Test (DEX/CRH test) and prediction of acute treatment response in major depression. PLoS ONE 4, e4324.
122. Segman R. H., Shefi N., Goltser-Dubner T., Friedman N., Kaminski N., and, Shalev A. Y., (2005) Peripheral blood mononuclear cell gene expression profiles identify emergent post-traumatic stress disorder among trauma survivors. Mol Psychiatry 10, 500-513, 42, 500-513, 425. (Pubitemid 40646438)
123. Sherry B., Zybarth G., Alfano M., et al. (1998) Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes. Proc. Natl Acad. Sci. USA 95, 1758-1763. (Pubitemid 28103467)
124. Shibuya N., Suzuki A., Sadahiro R., Kamata M., Matsumoto Y., Goto K., Hozumi Y., and, Otani K., (2010) Association study between a functional polymorphism of FK506-binding protein 51 (FKBP5) gene and personality traits in healthy subjects. Neurosci. Lett. 485, 194-197.
125. Shim S., Yuan J. P., Kim J. Y., et al. (2009) Peptidyl-prolyl isomerase FKBP52 controls chemotropic guidance of neuronal growth cones via regulation of TRPC1 channel opening. Neuron 64, 471-483.
126. Silverstein A. M., Galigniana M. D., Kanelakis K. C., Radanyi C., Renoir J. M., and, Pratt W. B., (1999) Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, hsp90, and cytoplasmic dynein. J. Biol. Chem. 274, 36980-36986.
127. Sinars C. R., Cheung-Flynn J., Rimerman R. A., Scammell J. G., Smith D. F., and, Clardy J., (2003) Structure of the large FK506-binding protein FKBP51, an Hsp90-binding protein and a component of steroid receptor complexes. Proc. Natl Acad. Sci. USA 100, 868-873. (Pubitemid 36183922)
128. Sivils J. C., Storer C. L., Galigniana M. D., and, Cox M. B,. (2011) Regulation of steroid hormone receptor function by the 52-kDa FK506-binding protein (FKBP52). Curr. Opin. Pharmacol. 11, 314-319.
129. Soontornniyomkij V., Everall I. P., and, Moore D. J,. et al. (2012) Increased cortical expression of FK506 binding protein-51 in HIV-associated neurocognitive disorders. J. Neurovirol. DOI:.
130. Stechschulte L. A., and, Sanchez E. R,. (2011) FKBP51-a selective modulator of glucocorticoid and androgen sensitivity. Curr. Opin. Pharmacol. 11, 332-337.
131. Szymanska M., Budziszewska B., Jaworska-Feil L., Basta-Kaim A., Kubera M., Leskiewicz M., Regulska M., and, Lason W., (2009) The effect of antidepressant drugs on the HPA axis activity, glucocorticoid receptor level and FKBP51 concentration in prenatally stressed rats. Psychoneuroendocrinology 34, 822-832.
132. Takahashi N., Hayano T., and, Suzuki M., (1989) Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337, 473-475.
133. Tamura M., Sajo M., Kakita A., Matsuki N., and, Koyama R., (2011) Prenatal stress inhibits neuronal maturation through downregulation of mineralocorticoid receptors. J. Neurosci. 31, 11505-11514.
134. Tatro E. T., Everall I. P., Kaul M., and, Achim C. L., (2009a) Modulation of glucocorticoid receptor nuclear translocation in neurons by immunophilins FKBP51 and FKBP52: implications for major depressive disorder. Brain Res. 1286, 1-12.
135. Tatro E. T., Everall I. P., Masliah E., Hult B. J., Lucero G., Chana G., Soontornniyomkij V., and, Achim C. L., (2009b) Differential expression of immunophilins FKBP51 and FKBP52 in the frontal cortex of HIV-infected patients with major depressive disorder. J. Neuroimmune. Pharmacol. 4, 218-226.
136. Thomas M., Harrell J. M., Morishima Y., Peng H. M., Pratt W. B., and, Lieberman A. P., (2006) Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction. Hum. Mol. Genet. 15, 1876-1883. (Pubitemid 43821778)
137. Touma C., Gassen N. C., Herrmann L., et al. (2011) FK506 binding protein 5 shapes stress responsiveness: modulation of neuroendocrine reactivity and coping behavior. Biol. Psychiatry 70, 928-936.
138. Tranguch S., Cheung-Flynn J., Daikoku T., et al. (2005) Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc. Natl Acad. Sci. USA 102, 14326-14331, Epub 12005 Sep 14321. (Pubitemid 41429697)
139. Tranguch S., Wang H., Daikoku T., Xie H., Smith D. F., and, Dey S. K., (2007) FKBP52 deficiency-conferred uterine progesterone resistance is genetic background and pregnancy stage specific. J. Clin. Invest. 117, 1824-1834. (Pubitemid 47036316)
140. Ulrich-Lai Y. M., and, Herman J. P., (2009) Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10, 397-409.
141. Vermeer H., Hendriks-Stegeman B. I., van der Burg B., van Buul-Offers S. C., and, Jansen M., (2003) Glucocorticoid-induced increase in lymphocytic FKBP51 messenger ribonucleic acid expression: a potential marker for glucocorticoid sensitivity, potency, and bioavailability. J. Clin. Endocrinol. Metab. 88, 277-284. (Pubitemid 36115178)
142. Vicent G. P., Monteserin M. C., Veleiro A. S., Burton G., Lantos C. P., and, Galigniana M. D., (1997) 21-Hydroxy-6,19-oxidoprogesterone: a novel synthetic steroid with specific antiglucocorticoid properties in the rat. Mol. Pharmacol. 52, 749-753. (Pubitemid 27443998)
143. Vicent G. P., Pecci A., Ghini A., Piwien-Pilipuk G., and, Galigniana M. D., (2002) Differences in nuclear retention characteristics of agonist-activated glucocorticoid receptor may determine specific responses. Exp. Cell Res. 276, 142-154. (Pubitemid 34969309)
144. Warrier M., Hinds Jr T. D., Ledford K. J., et al. (2010) Susceptibility to diet-induced hepatic steatosis and glucocorticoid resistance in FK506-binding protein 52-deficient mice. Endocrinology 151, 3225-3236.
145. Watson S., Gallagher P., Del-Estal D., Hearn A., Ferrier I. N., and, Young A. H., (2002) Hypothalamic-pituitary-adrenal axis function in patients with chronic depression. Psychol. Med. 32, 1021-1028.
146. Weiwad M., Edlich F., Kilka S., Erdmann F., Jarczowski F., Dorn M., Moutty M. C., and, Fischer G., (2006) Comparative analysis of calcineurin inhibition by complexes of immunosuppressive drugs with human FK506 binding proteins. Biochemistry 45, 15776-15784. (Pubitemid 46032498)
147. Wiederrecht G., Hung S., Chan H. K., et al. (1992) Characterization of high molecular weight FK-506 binding activities reveals a novel FK-506-binding protein as well as a protein complex. J. Biol. Chem. 267, 21753-21760.
148. Willour V. L., Chen H., Toolan J., et al. (2009) Family-based association of FKBP5 in bipolar disorder. Mol. Psychiatry 14, 261-268.
149. Wochnik G. M., Ruegg J., Abel G. A., Schmidt U., Holsboer F., and, Rein T., (2005) FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. 280, 4609-4616. (Pubitemid 40288629)
150. Wohleb E. S., Hanke M. L., Corona A. W., Powell N. D., Stiner L. M., Bailey M. T., Nelson R. J., Godbout J. P., and, Sheridan J. F., (2011) beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31, 6277-6288.
151. Wolf O. T., (2009) Stress and memory in humans: twelve years of progress? Brain Res. 1293, 142-154.
152. Wu B., Li P., Liu Y., et al. (2004) 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex. Proc. Natl Acad. Sci. USA 101, 8348-8353. (Pubitemid 38736578)
153. Xie P., Kranzler H. R., Poling J., Stein M. B., Anton R. F., Farrer L. A., and, Gelernter J., (2010) Interaction of FKBP5 with childhood adversity on risk for post-traumatic stress disorder. Neuropsychopharmacology 35, 1684-1692.
154. Xu X., Su B., Barndt R. J., et al. (2002) FKBP12 is the only FK506 binding protein mediating T-cell inhibition by the immunosuppressant FK506. Transplantation 73, 1835-1838. (Pubitemid 34655263)
155. Yang Z., Wolf I. M., Chen H., et al. (2006) FK506-binding protein 52 is essential to uterine reproductive physiology controlled by the progesterone receptor A isoform. Mol. Endocrinol. 20, 2682-2694, Epub 2006 Jul 2627. (Pubitemid 44833530)
156. Yehuda R., and, LeDoux J., (2007) Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56, 19-32. (Pubitemid 47484180)
157. Yehuda R., Golier J. A., Yang R. K., and, Tischler L., (2004) Enhanced sensitivity to glucocorticoids in peripheral mononuclear leukocytes in posttraumatic stress disorder. Biol. Psychiatry 55, 1110-1116. (Pubitemid 38680564)
158. Yong W., Yang Z., Periyasamy S., et al. (2007) Essential role for Co-chaperone Fkbp52 but not Fkbp51 in androgen receptor-mediated signaling and physiology. J. Biol. Chem. 282, 5026-5036, Epub 2006 Dec 5021. (Pubitemid 47100995)
159. Zhao W., Zhong L., Wu J., et al. (2006) Role of cellular FKBP52 protein in intracellular trafficking of recombinant adeno-associated virus 2 vectors. Virology, 353, 283-293. (Pubitemid 44397129)