The role of FKBP5 in mood disorders: Action of FKBP5 on steroid hormone receptors leads to questions about its evolutionary importance

CNS and Neurological Disorders - Drug Targets

Volumn 12, Issue 8, 2013, Pages 1157-1162

  O'Leary III, John C ^a   Zhang, Bo ^a   Koren III, John ^a   Blair, Laura ^a   Dickey, Chad A ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Behavior; Depression; FK506 binding protein 51; FKBP5 gene; Genome wide association studies; Glucocorticoid receptor; Heat shock protein 90; Polymorphisms; Post traumatic stress disorder; Resilience; Stress; Suicide

Indexed keywords

CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; FK 506 BINDING PROTEIN; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 90; MESSENGER RNA; NEUROPSIN; PROGESTERONE RECEPTOR; STEROID RECEPTOR; TAU PROTEIN; CELL SURFACE RECEPTOR; TACROLIMUS BINDING PROTEIN 5;

AMYGDALOID NUCLEUS; CELL FUNCTION; DEPRESSION; ENZYME ACTIVITY; FKBP5 GENE; GENE; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HUMAN CELL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MOOD DISORDER; POSTTRAUMATIC STRESS DISORDER; PROTEIN EXPRESSION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TETRATRICOPEPTIDE REPEAT; ANIMAL; DISEASE MODEL; GENETICS; MENTAL STRESS; METABOLISM; MOLECULAR EVOLUTION; MOOD DISORDERS; PATHOLOGY; PHYSIOLOGY;

AMYGDALA; ANIMALS; DISEASE MODELS, ANIMAL; EVOLUTION, MOLECULAR; HUMANS; MOOD DISORDERS; RECEPTORS, CELL SURFACE; RECEPTORS, STEROID; STRESS, PSYCHOLOGICAL; TACROLIMUS BINDING PROTEINS;

EID: 84891676229     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: None     Document Type: Review

References (54)

1. de Kloet, E.R.; Joels, M.; Holsboer, F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci., 2005, 6 (6), 463-475.
2. Holsboer, F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology, 2000, 23 (5), 477-501.
3. Belelli, D.; Lambert, J.J. Neurosteroids: endogenous regulators of the GABA (A) receptor. Nat. Rev. Neurosci., 2005, 6 (7), 565-575.
4. De Kloet, E.R.; Vreugdenhil, E.; Oitzl, M.S.; Joels, M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev., 1998, 19 (3), 269-301.
5. Binder, E.B.; Salyakina, D.; Lichtner, P.; Wochnik, G.M.; Ising, M.; Putz, B.; Papiol, S.; Seaman, S.; Lucae, S.; Kohli, M.A.; Nickel, T.; Kunzel, H.E.; Fuchs, B.; Majer, M.; Pfennig, A.; Kern, N.; Brunner, J.; Modell, S.; Baghai, T.; Deiml, T.; Zill, P.; Bondy, B.; Rupprecht, R.; Messer, T.; Kohnlein, O.; Dabitz, H.; Bruckl, T.; Muller, N.; Pfister, H.; Lieb, R.; Mueller, J.C.; Lohmussaar, E.; Strom, T.M.; Bettecken, T.; Meitinger, T.; Uhr, M.; Rein, T.; Holsboer, F.; Muller-Myhsok, B. Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat. Genet., 2004, 36 (12), 1319-1325.
6. Tatro, E.T.; Nguyen, T.B.; Bousman, C.A.; Masliah, E.; Grant, I.; Atkinson, J.H.; Everall, I.P. Correlation of major depressive disorder symptoms with FKBP5 but not FKBP4 expression in human immunodeficiency virus-infected individuals. J. Neurovirol., 2010, 16 (5), 399-404.
7. Xie, P.; Kranzler, H.R.; Poling, J.; Stein, M.B.; Anton, R.F.; Farrer, L.A.; Gelernter, J. Interaction of FKBP5 with childhood adversity on risk for post-traumatic stress disorder. Neuropsychopharmacology, 2010, 35 (8), 1684-1692.
8. Willour, V.L.; Chen, H.; Toolan, J.; Belmonte, P.; Cutler, D.J.; Goes, F.S.; Zandi, P.P.; Lee, R.S.; MacKinnon, D.F.; Mondimore, F.M.; Schweizer, B.; DePaulo, J.R., Jr.; Gershon, E.S.; McMahon, F.J.; Potash, J.B. Family-based association of FKBP5 in bipolar disorder. Mol. Psychiatry, 2009, 14 (3), 261-268.
9. Koenen, K.C.; Saxe, G.; Purcell, S.; Smoller, J.W.; Bartholomew, D.; Miller, A.; Hall, E.; Kaplow, J.; Bosquet, M.; Moulton, S.; Baldwin, C. Polymorphisms in FKBP5 are associated with peritraumatic dissociation in medically injured children. Mol. Psychiatry, 2005, 10 (12), 1058-1059.
10. Roy, A.; Gorodetsky, E.; Yuan, Q.; Goldman, D.; Enoch, M.A. Interaction of FKBP5, a stress-related gene, with childhood trauma increases the risk for attempting suicide. Neuropsychopharmacology, 2010, 35 (8), 1674-1683.
11. Supriyanto, I.; Sasada, T.; Fukutake, M.; Asano, M.; Ueno, Y.; Nagasaki, Y.; Shirakawa, O.; Hishimoto, A. Association of FKBP5 gene haplotypes with completed suicide in the Japanese population. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2011, 35 (1), 252-256.
12. Roy, A.; Hodgkinson, C.A.; Deluca, V.; Goldman, D.; Enoch, M.A. Two HPA axis genes, CRHBP and FKBP5, interact with childhood trauma to increase the risk for suicidal behavior. J. Psychiatric Res., 2012, 46 (1), 72-79.
13. Brent, D.; Melhem, N.; Ferrell, R.; Emslie, G.; Wagner, K.D.; Ryan, N.; Vitiello, B.; Birmaher, B.; Mayes, T.; Zelazny, J.; Onorato, M.; Devlin, B.; Clarke, G.; DeBar, L.; Keller, M. Association of FKBP5 polymorphisms with suicidal events in the Treatment of Resistant Depression in Adolescents (TORDIA) study. Am. J. Psychiatry, 2010, 167 (2), 190-197.
14. Shibuya, N.; Suzuki, A.; Sadahiro, R.; Kamata, M.; Matsumoto, Y.; Goto, K.; Hozumi, Y.; Otani, K. Association study between a functional polymorphism of FK506-binding protein 51 (FKBP5) gene and personality traits in healthy subjects. Neurosci. Lett., 2010, 485 (3), 194-197.
15. Bevilacqua, L.; Carli, V.; Sarchiapone, M.; George, D.K.; Goldman, D.; Roy, A.; Enoch, M.A. Interaction between FKBP5 and childhood trauma and risk of aggressive behavior. Arch. Gen. Psychiatry, 2012, 69 (1), 62-70.
16. Binder, E.B. The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology, 2009, 34, S186-S195.
17. Lupien, S.J.; McEwen, B.S.; Gunnar, M.R.; Heim, C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci., 2009, 10 (6), 434-445.
18. Jaaskelainen, T.; Makkonen, H.; Palvimo, J.J. Steroid up-regulation of FKBP51 and its role in hormone signaling. Curr. Opin. Pharmacol., 2011, 11 (4), 326-331.
19. Chrousos, G.P.; Gold, P.W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA, 1992, 267 (9), 1244-1252.
20. Ulrich-Lai, Y.M.; Herman, J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci., 2009, 10 (6), 397-409.
21. Reul, J.M.; de Kloet, E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology, 1985, 117 (6), 2505-2511.
22. Arriza, J.L.; Simerly, R.B.; Swanson, L.W.; Evans, R.M. The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron, 1988, 1 (9), 887-900.
23. Datson, N.A.; van der Perk, J.; de Kloet, E.R.; Vreugdenhil, E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression. Eur. J. Neurosci., 2001, 14 (4), 675-689.
24. Sapolsky, R.M.; Romero, L.M.; Munck, A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev., 2000, 21 (1), 55-89.
25. Barik, S. Immunophilins: for the love of proteins. Cell. Mol. Life Sci., 2006, 63 (24), 2889-2900.
26. Wiederrecht, G.; Hung, S.; Chan, H.K.; Marcy, A.; Martin, M.; Calaycay, J.; Boulton, D.; Sigal, N.; Kincaid, R.L.; Siekierka, J.J. 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., 1992, 267 (30), 21753-21760.
27. rd; Jin, Y.; Buchner, J.; Cox, M.B.; Dickey, C.A. The Hsp90 cochaperone, FKBP51, increases Tau stability and polymerizes microtubules. J. Neurosci., 2010, 30 (2), 591-599.
28. Chen, M.S.; Silverstein, A.M.; Pratt, W.B.; Chinkers, M. The tetratricopeptide repeat domain of protein phosphatase 5 mediates binding to glucocorticoid receptor heterocomplexes and acts as a dominant negative mutant. J. Biol. Chem., 1996, 271 (50), 32315-32320.
29. 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. Biochemistry, 2005, 44 (6), 2030-2038.
30. 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. Endocrinology, 2000, 141 (11), 4107-4113.
31. 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. Endocrinology, 2003, 144 (6), 2380-2387.
32. Denny, W.B.; Prapapanich, V.; Smith, D.F.; Scammell, J.G. Structurefunction analysis of squirrel monkey FK506-binding protein 51, a potent inhibitor of glucocorticoid receptor activity. Endocrinology, 2005, 146 (7), 3194-3201.
33. 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. J. Biol. Chem., 2005, 280 (6), 4609-4616.
34. Ni, L.; Yang, C.S.; Gioeli, D.; Frierson, H.; Toft, D.O.; Paschal, B.M. FKBP51 promotes assembly of the Hsp90 chaperone complex and regulates androgen receptor signaling in prostate cancer cells. Mol. Cell Biol., 30 (5), 1243-1253.
35. Ising, M.; Depping, A.M.; Siebertz, A.; Lucae, S.; Unschuld, P.G.; Kloiber, S.; Horstmann, S.; Uhr, M.; Muller-Myhsok, B.; Holsboer, F. Polymorphisms in the FKBP5 gene region modulate recovery from psychosocial stress in healthy controls. Eur. J. Neurosci., 2008, 28 (2), 389-398.
36. Binder, E.B.; Bradley, R.G.; Liu, W.; Epstein, M.P.; Deveau, T.C.; Mercer, K.B.; Tang, Y.; Gillespie, C.F.; Heim, C.M.; Nemeroff, C.B.; Schwartz, A.C.; Cubells, J.F.; Ressler, K.J. Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA, 2008, 299 (11), 1291-1305.
37. Scharf, S.H.; Liebl, C.; Binder, E.B.; Schmidt, M.V.; Muller, M.B. Expression and regulation of the Fkbp5 gene in the adult mouse brain. PloS one, 2011, 6 (2), e16883.
38. Scammell, J.G.; Denny, W.B.; Valentine, D.L.; Smith, D.F. Overexpression of the FK506-binding immunophilin FKBP51 is the common cause of glucocorticoid resistance in three New World primates. Gen. Comp. Endocrinol., 2001, 124 (2), 152-165.
39. Clark, L.D.; Gay, P.E. Behavioral defeat in squirrel monkeys: an experimental model of reactive depression. Psychol. Rep., 1980, 47 (3 Pt 2), 1175-1184.
40. Petticrew, M.; Smith, D.G. The monkey puzzle: a systematic review of studies of stress, social hierarchies, and heart disease in monkeys. PloS One, 2012, 7 (3), e27939.
41. Touma, C.; Gassen, N.C.; Herrmann, L.; Cheung-Flynn, J.; Bull, D.R.; Ionescu, I.A.; Heinzmann, J.M.; Knapman, A.; Siebertz, A.; Depping, A.M.; Hartmann, J.; Hausch, F.; Schmidt, M.V.; Holsboer, F.; Ising, M.; Cox, M.B.; Schmidt, U.; Rein, T. FK506 binding protein 5 shapes stress responsiveness: modulation of neuroendocrine reactivity and coping behavior. Biol. Psychiatry, 2011, 70 (10), 928-936.
42. Hartmann, J.; Wagner, K.V.; Liebl, C.; Scharf, S.H.; Wang, X.D.; Wolf, M.; Hausch, F.; Rein, T.; Schmidt, U.; Touma, C.; Cheung-Flynn, J.; Cox, M.B.; Smith, D.F.; Holsboer, F.; Muller, M.B.; Schmidt, M.V. The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology, 2012, 62 (1), 332-339.
43. Ballatore, C.; Brunden, K.R.; Piscitelli, F.; James, M.J.; Crowe, A.; Yao, Y.; Hyde, E.; Trojanowski, J.Q.; Lee, V.M.; Smith, A.B., 3rd. Discovery of brain-penetrant, orally bioavailable aminothienopyridazine inhibitors of tau aggregation. J. Med. Chem., 2010, 53 (9), 3739-3747.
44. rd; Dharia, S.; Blair, L.J.; Brady, S.; Johnson, A.G.; Peters, M.; Cheung-Flynn, J.; Cox, M.B.; de Erausquin, G.; Weeber, E.J.; Jinwal, U.K.; Dickey, C.A. A New Anti-Depressive Strategy for the Elderly: Ablation of FKBP5/FKBP51. PloS One, 2011, 6 (9), e24840.
45. Sandi, C. Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci., 2004, 5 (12), 917-930.
46. de Quervain, D.J.F.; Roozendaal, B.; McGaugh, J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature, 1998, 394 (6695), 787-790.
47. Diamond, D.M.; Campbell, A.M.; Park, C.R.; Woodson, J.C.; Conrad, C.D.; Bachstetter, A.D.; Mervis, R.F. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus, 2006, 16 (7), 571-576.
48. Diamond, D.M.; Park, C.R.; Campbell, A.M.; Woodson, J.C. Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stressinduced amnesia. Hippocampus, 2005, 15 (8), 1006-1025.
49. Diamond, D.M.; Park, C.R.; Woodson, J.C. Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP. Hippocampus, 2004, 14 (3), 281-291.
50. Diamond, D.M.; Park, C.R.; Heman, K.L.; Rose, G.M. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus, 1999, 9 (5), 542-552.
51. Diamond, D.M.; Bennett, M.C.; Fleshner, M.; Rose, G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus, 1992, 2 (4), 421-430.
52. Attwood, B.K.; Bourgognon, J.M.; Patel, S.; Mucha, M.; Schiavon, E.; Skrzypiec, A.E.; Young, K.W.; Shiosaka, S.; Korostynski, M.; Piechota, M.; Przewlocki, R.; Pawlak, R. Neuropsin cleaves EphB2 in the amygdala to control anxiety. Nature, 2011, 473, 372-375.
53. Patterson, C.E.; Gao, J.; Rooney, A.P.; Davis, E.C. Genomic organization of mouse and human 65 kDa FK506-binding protein genes and evolution of the FKBP multigene family. Genomics, 2002, 79 (6), 881-889.
54. Trandinh, C.C.; Pao, G.M.; Saier, M.H., Jr. Structural and evolutionary relationships among the immunophilins: two ubiquitous families of peptidyl-prolyl cis-trans isomerases. FASEB J., 1992, 6 (15), 3410-3420.