Home LiteratureArticle Details
PMID: 15163683 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Visualization of glucocorticoid receptor and mineralocorticoid receptor interactions in living cells with GFP-based fluorescence resonance energy transfer.

Nishi M, Tanaka M, Matsuda K, Sunaguchi M, Kawata M

Abstract

Adrenal corticosteroids readily enter the brain and exert markedly diverse effects, including stress responses in the target neural cells via two receptor systems, the mineralocorticoid receptor (MR) and the glucocorticoid receptor (GR). It has been shown that the GR and MR are highly colocalized in the hippocampus. Given the differential action of the MR and GR in the hippocampal region, it is important to elucidate how these receptors interact with each other in response to corticosteroids. We investigated the heterodimerization of the MR and GR with green fluorescent protein-based fluorescence resonance energy transfer (FRET) microscopy in living cells with spatiotemporal manner. FRET was evaluated in three ways: (1) ratio imaging; (2) emission spectra; and (3) acceptor photobleaching. FRET analysis demonstrated that cyan fluorescent protein-GR and yellow fluorescent protein-MR form heterodimers after corticosterone (CORT) treatment both in the nucleus of cultured hippocampal neurons and COS-1 cells, whereas they do not form heterodimers in the cytoplasm. The content of the GR-MR heterodimer was higher at 10(-6) m CORT than at 10(-9) m CORT and reached a maximum level after 60 min of CORT treatment in both cultured hippocampal neurons and COS-1 cells. The distribution pattern of heterodimers in the nucleus of cultured hippocampal neurons was more restricted than that in COS-1 cells. The present study using mutant fusion proteins in nuclear localization signal showed that these corticosteroid receptors are not translocated into the nucleus in the form of heterodimers even after treatment with ligand and thus allow no heterodimerization to take place in the cytoplasm. These results obtained with FRET analyses give new insights into the sites, time course, and effects of ligand concentration on heterodimersization of the GR and MR.

MeSH Terms
Animals COS Cells/cytology Cell Nucleus/ultrastructure Cells, Cultured Fluorescence Resonance Energy Transfer/methods Hippocampus/cytology,metabolism Image Processing, Computer-Assisted Neurons/metabolism Protein Transport/physiology Rats Rats, Sprague-Dawley Receptors, Glucocorticoid/metabolism Receptors, Mineralocorticoid/metabolism Transfection
Chemicals
Receptors, Glucocorticoid Receptors, Mineralocorticoid
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Nishi Mayumi
Department of Anatomy and Neurobiology, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan. nmayumi@koto.kpu-m.ac.jp
Tanaka Masayuki
Matsuda Ken-ichi
Sunaguchi Masataka
Kawata Mitsuhiro
References (53)
53 references, click to expand
  1. Real-time imaging of glucocorticoid receptor dynamics in living neurons and glial cells in comparison with non-neural cells.
    Eur J Neurosci. 1999 Jun;11(6):1927-36 PMID: 10336661
  2. Mechanisms of Glucocorticoid-receptor-mediated Repression of Gene Expression.
    Trends Endocrinol Metab. 1999 Dec;10(10):396-402 PMID: 10542396
  3. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells.
    Science. 2000 Feb 18;287(5456):1262-5 PMID: 10678832
  4. In vitro and in vivo immunocytochemistry for the distribution of mineralocorticoid receptor with the use of specific antibody.
    Neurosci Res. 2000 Jul;37(3):173-82 PMID: 10940451
  5. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein.
    Methods Enzymol. 2000;327:472-500 PMID: 11045004
  6. FRAP reveals that mobility of oestrogen receptor-alpha is ligand- and proteasome-dependent.
    Nat Cell Biol. 2001 Jan;3(1):15-23 PMID: 11146621
  7. Glucocorticoid receptor homodimers and glucocorticoid-mineralocorticoid receptor heterodimers form in the cytoplasm through alternative dimerization interfaces.
    Mol Cell Biol. 2001 Feb;21(3):781-93 PMID: 11154266
  8. Heterodimerization of mineralocorticoid and glucocorticoid receptors at a novel negative response element of the 5-HT1A receptor gene.
    J Biol Chem. 2001 Apr 27;276(17):14299-307 PMID: 11278286
  9. From fixed to FRAP: measuring protein mobility and activity in living cells.
    Nat Cell Biol. 2001 Jun;3(6):E145-7 PMID: 11389456
  10. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1.
    Nature. 2001 Jun 28;411(6841):1065-8 PMID: 11429608
  11. 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.
    Mol Endocrinol. 2001 Jul;15(7):1077-92 PMID: 11435609
  12. Resolution of multiple green fluorescent protein color variants and dyes using two-photon microscopy and imaging spectroscopy.
    J Biomed Opt. 2001 Jul;6(3):311-8 PMID: 11516321
  13. Demonstration by fluorescence resonance energy transfer of two sites of interaction between the low-density lipoprotein receptor-related protein and the amyloid precursor protein: role of the intracellular adapter protein Fe65.
    J Neurosci. 2001 Nov 1;21(21):8354-61 PMID: 11606623
  14. Navigating steroid hormone receptors through the nuclear compartment.
    Mol Endocrinol. 2002 Jul;16(7):1449-55 PMID: 12089341
  15. Colocalization and ligand-dependent discrete distribution of the estrogen receptor (ER)alpha and ERbeta.
    Mol Endocrinol. 2002 Oct;16(10):2215-30 PMID: 12351687
  16. Multispectral imaging fluorescence microscopy for living cells.
    Cell Struct Funct. 2002 Oct;27(5):367-74 PMID: 12502891
  17. Subcellular localization and mechanisms of nucleocytoplasmic trafficking of steroid receptor coactivator-1.
    J Biol Chem. 2003 Aug 22;278(34):32195-203 PMID: 12791702
  18. Yellow fluorescent protein-tagged and cyan fluorescent protein-tagged imaging analysis of glucocorticoid receptor and importins in single living cells.
    Endocrinology. 2003 Sep;144(9):4070-9 PMID: 12933681
  19. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling.
    Nature. 1992 Jan 30;355(6359):446-9 PMID: 1310351
  20. Coordinative mineralocorticoid and glucocorticoid receptor-mediated control of responses to serotonin in rat hippocampus.
    Neuroendocrinology. 1992 Mar;55(3):344-50 PMID: 1323803
  21. New insights into activation of the steroid hormone receptor superfamily.
    Trends Pharmacol Sci. 1992 Aug;13(8):318-23 PMID: 1413090
  22. Differential regulation of mouse mammary tumor virus-bacterial chloramphenicol acetyltransferase chimeric gene by human mineralocorticoid hormone-receptor complexes.
    J Steroid Biochem Mol Biol. 1991 Jul;39(1):91-103 PMID: 1648951
  23. Non-genomic and genomic effects of steroids on neural activity.
    Trends Pharmacol Sci. 1991 Apr;12(4):141-7 PMID: 2063480
  24. Interactions among a subfamily of nuclear hormone receptors: the regulatory zipper model.
    Mol Endocrinol. 1990 Sep;4(9):1293-301 PMID: 2172797
  25. ICV infusion of corticosterone antagonizes ICV-aldosterone hypertension.
    Am J Physiol. 1990 Apr;258(4 Pt 1):E649-53 PMID: 2333961
  26. Determinants of target gene specificity for steroid/thyroid hormone receptors.
    Cell. 1989 Jun 30;57(7):1139-46 PMID: 2500251
  27. High level expression in Escherichia coli of the DNA-binding domain of the glucocorticoid receptor in a functional form utilizing domain-specific cleavage of a fusion protein.
    J Biol Chem. 1989 Jan 15;264(2):804-9 PMID: 2642905
  28. A molecular framework for the actions of glucocorticoid hormones in the nervous system.
    Neuron. 1989 Feb;2(2):1105-12 PMID: 2696502
  29. The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response.
    Neuron. 1988 Nov;1(9):887-900 PMID: 2856104
  30. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation.
    Endocrinology. 1985 Dec;117(6):2505-11 PMID: 2998738
  31. Adrenal steroid receptors and actions in the nervous system.
    Physiol Rev. 1986 Oct;66(4):1121-88 PMID: 3532143
  32. Characterization of rat brain aldosterone receptors reveals high affinity for corticosterone.
    Endocrinology. 1983 Dec;113(6):2043-51 PMID: 6227474
  33. Renal mineralocorticoid receptors and hippocampal corticosterone-binding species have identical intrinsic steroid specificity.
    Proc Natl Acad Sci U S A. 1983 Oct;80(19):6056-60 PMID: 6310613
  34. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems.
    Prog Neurobiol. 1994 May;43(1):1-36 PMID: 7526416
  35. Unique response pathways are established by allosteric interactions among nuclear hormone receptors.
    Cell. 1995 May 19;81(4):541-50 PMID: 7758108
  36. In vitro studies of glucocorticoid effects on neurons and astrocytes.
    Ann N Y Acad Sci. 1994 Nov 30;746:243-58; discussion 258-9, 289-93 PMID: 7825881
  37. Heterodimerization between mineralocorticoid and glucocorticoid receptor: a new principle of glucocorticoid action in the CNS.
    Neuron. 1994 Dec;13(6):1457-62 PMID: 7993637
  38. Pharmacological and functional characterization of human mineralocorticoid and glucocorticoid receptor ligands.
    Eur J Pharmacol. 1993 Oct 15;247(2):145-54 PMID: 8282004
  39. Physical association and functional antagonism between the p65 subunit of transcription factor NF-kappa B and the glucocorticoid receptor.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):752-6 PMID: 8290595
  40. Mineralocorticoid and glucocorticoid receptor activities distinguished by nonreceptor factors at a composite response element.
    Science. 1993 Feb 19;259(5098):1161-5 PMID: 8382376
  41. Steroid receptor heterodimerization demonstrated in vitro and in vivo.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12480-4 PMID: 8618925
  42. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews.
    J Neurosci. 1996 May 15;16(10):3534-40 PMID: 8627386
  43. Visualization of glucocorticoid receptor translocation and intranuclear organization in living cells with a green fluorescent protein chimera.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4845-50 PMID: 8643491
  44. Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons.
    J Cell Sci. 1996 Apr;109 ( Pt 4):787-92 PMID: 8718670
  45. Negative glucorticoid regulation of cyclic adenosine 3', 5'-monophosphate-stimulated corticotropin-releasing hormone-reporter expression in AtT-20 cells.
    Mol Endocrinol. 1996 Mar;10(3):317-29 PMID: 8833660
  46. Roles of steroid hormones and their receptors in structural organization in the nervous system.
    Neurosci Res. 1995 Dec;24(1):1-46 PMID: 8848287
  47. Heterodimerization between mineralocorticoid and glucocorticoid receptors increases the functional diversity of corticosteroid action.
    Trends Pharmacol Sci. 1996 Apr;17(4):145-9 PMID: 8984741
  48. Mineralocorticoid receptors and glucocorticoid receptors.
    Clin Endocrinol (Oxf). 1996 Dec;45(6):651-6 PMID: 9039329
  49. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study.
    Neurosci Res. 1996 Nov;26(3):235-69 PMID: 9121734
  50. Activation of the type 2 adrenal steroid receptor can rescue granule cells from death during development.
    Brain Res Dev Brain Res. 1997 Jul 18;101(1-2):265-8 PMID: 9263599
  51. Subcellular localization of mineralocorticoid receptors in living cells: effects of receptor agonists and antagonists.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2973-8 PMID: 9501200
  52. Brain corticosteroid receptor balance in health and disease.
    Endocr Rev. 1998 Jun;19(3):269-301 PMID: 9626555
  53. Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor.
    Mol Cell Biol. 1999 Feb;19(2):1025-37 PMID: 9891038
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-05-26
Pages
4918-27
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6729363
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com