Interaction of the Tau2 Transcriptional Activation Domain of Glucocorticoid Receptor with a Novel Steroid Receptor Coactivator, Hic-5, Which Localizes to Both Focal Adhesions and the Nuclear Matrix

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2000 Jun 10

PMID 10848625

Citations 46

Authors

L Yang

J Guerrero

H Hong

D B DeFranco

M R Stallcup

Affiliations

Soon will be listed here.

Abstract

Hic-5 (hydrogen peroxide-inducible clone-5) is a focal adhesion protein that is involved in cellular senescence. In the present study, a yeast two-hybrid screen identified Hic-5 as a protein that interacts with a region of the glucocorticoid receptor that includes a nuclear matrix-targeting signal and the tau2 transcriptional activation domain. In transiently transfected mammalian cells, overexpression of Hic-5 potentiated the activation of reporter genes by all steroid receptors, excluding the estrogen receptor. The activity of the estrogen receptor and the thyroid hormone receptor was stimulated by Hic-5 in the presence but not in the absence of coexpressed coactivator GRIP1. In biochemical fractionations and indirect immunofluorescence assays, a fraction of endogenous Hic-5 in REF-52 cells and transiently expressed Hic-5 in Cos-1 cells was associated with the nuclear matrix. The C-terminal region of Hic-5, which contains seven zinc fingers arranged in four LIM domains, was required for interaction with focal adhesions, the nuclear matrix, steroid receptors, and the tau2 domain of glucocorticoid receptor. The N-terminal region of Hic-5 possesses a transcriptional activation domain and was essential for the coactivator activity of Hic-5. Given the coexisting cytoplasmic and nuclear distributions of Hic-5 and its role in steroid receptor-mediated transcriptional activation, it is proposed that Hic-5 might transmit signals that emanate at cell attachment sites and regulate transcription factors, such as steroid receptors.

Citing Articles

A comparative analysis of paxillin and Hic-5 proximity interactomes.

Brock K, Alpha K, Brennan G, De Jong E, Luke E, Turner C Cytoskeleton (Hoboken). 2024; 82(1-2):12-31.

PMID: 38801098 PMC: 11599474. DOI: 10.1002/cm.21878.

Physiological and pathological roles of Hic‑5 in several organs (Review).

Yao S, Tu Z, Yang X, Zhang L, Zhong Y, Zheng L Int J Mol Med. 2022; 50(5).

PMID: 36222304 PMC: 9558762. DOI: 10.3892/ijmm.2022.5194.

Characterisation of a nucleo-adhesome.

Byron A, Griffith B, Herrero A, Loftus A, Koeleman E, Kogerman L Nat Commun. 2022; 13(1):3053.

PMID: 35650196 PMC: 9160004. DOI: 10.1038/s41467-022-30556-5.

Manipulation of Focal Adhesion Signaling by Pathogenic Microbes.

Murphy K, Brinkworth A Int J Mol Sci. 2021; 22(3).

PMID: 33572997 PMC: 7866387. DOI: 10.3390/ijms22031358.

Paxillin family of focal adhesion adaptor proteins and regulation of cancer cell invasion.

Alpha K, Xu W, Turner C Int Rev Cell Mol Biol. 2020; 355:1-52.

PMID: 32859368 PMC: 7737098. DOI: 10.1016/bs.ircmb.2020.05.003.

References

Barrack E, Coffey D . The specific binding of estrogens and androgens to the nuclear matrix of sex hormone responsive tissues. J Biol Chem. 1980; 255(15):7265-75. View

Hong H, Yang L, Stallcup M . Hormone-independent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J Biol Chem. 1999; 274(32):22618-26. DOI: 10.1074/jbc.274.32.22618. View

Hollenberg S, Evans R . Multiple and cooperative trans-activation domains of the human glucocorticoid receptor. Cell. 1988; 55(5):899-906. DOI: 10.1016/0092-8674(88)90145-6. View

Getzenberg R, Coffey D . Tissue specificity of the hormonal response in sex accessory tissues is associated with nuclear matrix protein patterns. Mol Endocrinol. 1990; 4(9):1336-42. DOI: 10.1210/mend-4-9-1336. View

Schuchard M, Subramaniam M, Ruesink T, Spelsberg T . Nuclear matrix localization and specific matrix DNA binding by receptor binding factor 1 of the avian oviduct progesterone receptor. Biochemistry. 1991; 30(39):9516-22. DOI: 10.1021/bi00103a019. View

Partin A, Getzenberg R, Carmichael M, Vindivich D, Yoo J, Epstein J . Nuclear matrix protein patterns in human benign prostatic hyperplasia and prostate cancer. Cancer Res. 1993; 53(4):744-6. View

Pearce D, Yamamoto K . Mineralocorticoid and glucocorticoid receptor activities distinguished by nonreceptor factors at a composite response element. Science. 1993; 259(5098):1161-5. DOI: 10.1126/science.8382376. View

van Wijnen A, Bidwell J, Fey E, Penman S, Lian J, Stein J . Nuclear matrix association of multiple sequence-specific DNA binding activities related to SP-1, ATF, CCAAT, C/EBP, OCT-1, and AP-1. Biochemistry. 1993; 32(33):8397-402. DOI: 10.1021/bi00084a003. View

Fackelmayer F, DAHM K, Renz A, Ramsperger U, Richter A . Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear-matrix protein which binds DNA and RNA in vivo and in vitro. Eur J Biochem. 1994; 221(2):749-57. DOI: 10.1111/j.1432-1033.1994.tb18788.x. View

10.

Schmidhauser C, Casperson G, Bissell M . Transcriptional activation by viral enhancers: critical dependence on extracellular matrix-cell interactions in mammary epithelial cells. Mol Carcinog. 1994; 10(2):66-71. DOI: 10.1002/mc.2940100203. View

11.

Sun J, Chen H, Davie J . Nuclear factor 1 is a component of the nuclear matrix. J Cell Biochem. 1994; 55(2):252-63. DOI: 10.1002/jcb.240550212. View

12.

Shibanuma M, Mashimo J, Kuroki T, Nose K . Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J Biol Chem. 1994; 269(43):26767-74. View

13.

Milhon J, Kohli K, Stallcup M . Genetic analysis of the N-terminal end of the glucocorticoid receptor hormone binding domain. J Steroid Biochem Mol Biol. 1994; 51(1-2):11-9. DOI: 10.1016/0960-0760(94)90110-4. View

14.

Schmeichel K, Beckerle M . The LIM domain is a modular protein-binding interface. Cell. 1994; 79(2):211-9. DOI: 10.1016/0092-8674(94)90191-0. View

15.

van Steensel B, Jenster G, Damm K, Brinkmann A, VAN Driel R . Domains of the human androgen receptor and glucocorticoid receptor involved in binding to the nuclear matrix. J Cell Biochem. 1995; 57(3):465-78. DOI: 10.1002/jcb.240570312. View

16.

Wurtz J, Bourguet W, Renaud J, Vivat V, Chambon P, Moras D . A canonical structure for the ligand-binding domain of nuclear receptors. Nat Struct Biol. 1996; 3(1):87-94. DOI: 10.1038/nsb0196-87. View

17.

Tang Y, DeFranco D . ATP-dependent release of glucocorticoid receptors from the nuclear matrix. Mol Cell Biol. 1996; 16(5):1989-2001. PMC: 231186. DOI: 10.1128/MCB.16.5.1989. View

18.

Tremblay L, Hauck W, Nguyen L, Allard P, Landry F, CHAPDELAINE A . Regulation and activation of focal adhesion kinase and paxillin during the adhesion, proliferation, and differentiation of prostatic epithelial cells in vitro and in vivo. Mol Endocrinol. 1996; 10(8):1010-20. DOI: 10.1210/mend.10.8.8843417. View

19.

Guan J, Chen H . Signal transduction in cell-matrix interactions. Int Rev Cytol. 1996; 168:81-121. View

20.

Tremblay L, Hauck W, Aprikian A, Begin L, CHAPDELAINE A, Chevalier S . Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int J Cancer. 1996; 68(2):164-71. DOI: 10.1002/(sici)1097-0215(19961009)68:2<169::aid-ijc4>3.0.co;2-w. View