Target Gene Specificity of USF-1 is Directed Via P38-mediated Phosphorylation-dependent Acetylation

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2009 Apr 25

PMID 19389701

Citations 24

Authors

Sebastien Corre

Aline Primot

Yorann Baron

Jacques Le Seyec

Colin Goding

Marie-Dominique Galibert

Affiliations

Soon will be listed here.

Abstract

How transcription factors interpret the output from signal transduction pathways to drive distinct programs of gene expression is a key issue that underpins development and disease. The ubiquitously expressed basic-helix-loop-helix leucine zipper upstream stimulating factor-1 binds E-box regulatory elements (CANNTG) to regulate a wide number of gene networks. In particular, USF-1 is a key component of the tanning process. Following UV irradiation, USF-1 is phosphorylated by the p38 stress-activated kinase on threonine 153 and directly up-regulates expression of the POMC, MC1R, TYR, TYRP-1 and DCT genes. However, how phosphorylation on Thr-153 might affect the activity of USF-1 is unclear. Here we show that, in response to DNA damage, oxidative stress and cellular infection USF-1 is acetylated in a phospho-Thr-153-dependent fashion. Phospho-acetylated USF-1 is nuclear and interacts with DNA but displays altered gene regulatory properties. Phospho-acetylated USF-1 is thus proposed to be associated with loss of transcriptional activation properties toward several target genes implicated in pigmentation process and cell cycle regulation. The identification of this critical stress-dependent USF-1 modification gives new insights into understanding USF-1 gene expression modulation associated with cancer development.

Citing Articles

Acetylation reprograms MITF target selectivity and residence time.

Louphrasitthiphol P, Loffreda A, Pogenberg V, Picaud S, Schepsky A, Friedrichsen H Nat Commun. 2023; 14(1):6051.

PMID: 37770430 PMC: 10539308. DOI: 10.1038/s41467-023-41793-7.

Upstream Stimulatory Factors Regulate HIV-1 Latency and Are Required for Robust T Cell Activation.

Horvath R, Sadowski I Viruses. 2023; 15(7).

PMID: 37515158 PMC: 10384547. DOI: 10.3390/v15071470.

Targeting radiation-induced upstream stimulatory factor-1 by histone deacetylase inhibitors to reverse radioresistance in prostate cancer.

Gupta S, Ahmed M Cancer Rep (Hoboken). 2021; 5(12):e1553.

PMID: 34533293 PMC: 9780427. DOI: 10.1002/cnr2.1553.

Sulfuretin exerts diversified functions in the processing of amyloid precursor protein.

Chen J, Luo B, Zhong B, Li K, Wen Q, Song L Genes Dis. 2021; 8(6):867-881.

PMID: 34522714 PMC: 8427253. DOI: 10.1016/j.gendis.2020.11.008.

Molecular mechanism of FSHR expression induced by BMP15 in human granulosa cells.

Shimizu K, Nakamura T, Bayasula , Nakanishi N, Kasahara Y, Nagai T J Assist Reprod Genet. 2019; 36(6):1185-1194.

PMID: 31079267 PMC: 6603124. DOI: 10.1007/s10815-019-01469-y.

References

Kawaguchi Y, Ito A, Appella E, Yao T . Charge modification at multiple C-terminal lysine residues regulates p53 oligomerization and its nucleus-cytoplasm trafficking. J Biol Chem. 2005; 281(3):1394-400. DOI: 10.1074/jbc.M505772200. View

Zachos G, Clements B, Conner J . Herpes simplex virus type 1 infection stimulates p38/c-Jun N-terminal mitogen-activated protein kinase pathways and activates transcription factor AP-1. J Biol Chem. 1999; 274(8):5097-103. DOI: 10.1074/jbc.274.8.5097. View

Liu M, Whetstine J, Payton S, Ge Y, Flatley R, Matherly L . Roles of USF, Ikaros and Sp proteins in the transcriptional regulation of the human reduced folate carrier B promoter. Biochem J. 2004; 383(Pt 2):249-57. PMC: 1134065. DOI: 10.1042/BJ20040414. View

Rahaus M, Desloges N, Yang M, Ruyechan W, Wolff M . Transcription factor USF, expressed during the entire phase of varicella-zoster virus infection, interacts physically with the major viral transactivator IE62 and plays a significant role in virus replication. J Gen Virol. 2003; 84(Pt 11):2957-2967. DOI: 10.1099/vir.0.19335-0. View

Nowak M, Helleboid-Chapman A, Jakel H, Martin G, Duran-Sandoval D, Staels B . Insulin-mediated down-regulation of apolipoprotein A5 gene expression through the phosphatidylinositol 3-kinase pathway: role of upstream stimulatory factor. Mol Cell Biol. 2005; 25(4):1537-48. PMC: 548024. DOI: 10.1128/MCB.25.4.1537-1548.2005. View

Wu Y, Wiltbank M . Transcriptional regulation of the cyclooxygenase-2 gene changes from protein kinase (PK) A- to PKC-dependence after luteinization of granulosa cells. Biol Reprod. 2002; 66(5):1505-14. DOI: 10.1095/biolreprod66.5.1505. View

Andrews G . Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol. 1999; 59(1):95-104. DOI: 10.1016/s0006-2952(99)00301-9. View

Baxevanis A, Vinson C . Interactions of coiled coils in transcription factors: where is the specificity?. Curr Opin Genet Dev. 1993; 3(2):278-85. DOI: 10.1016/0959-437x(93)90035-n. View

Corre S, Primot A, Sviderskaya E, Bennett D, Vaulont S, Goding C . UV-induced expression of key component of the tanning process, the POMC and MC1R genes, is dependent on the p-38-activated upstream stimulating factor-1 (USF-1). J Biol Chem. 2004; 279(49):51226-33. DOI: 10.1074/jbc.M409768200. View

10.

Polesskaya A, Duquet A, Naguibneva I, Weise C, Vervisch A, Bengal E . CREB-binding protein/p300 activates MyoD by acetylation. J Biol Chem. 2000; 275(44):34359-64. DOI: 10.1074/jbc.M003815200. View

11.

Huang S, Li X, Yusufzai T, Qiu Y, Felsenfeld G . USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol Cell Biol. 2007; 27(22):7991-8002. PMC: 2169148. DOI: 10.1128/MCB.01326-07. View

12.

Cogswell J, Godlevski M, Bonham M, Bisi J, Babiss L . Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter. Mol Cell Biol. 1995; 15(5):2782-90. PMC: 230509. DOI: 10.1128/MCB.15.5.2782. View

13.

Sirito M, Lin Q, Deng J, Behringer R, Sawadogo M . Overlapping roles and asymmetrical cross-regulation of the USF proteins in mice. Proc Natl Acad Sci U S A. 1998; 95(7):3758-63. PMC: 19910. DOI: 10.1073/pnas.95.7.3758. View

14.

Kelly D, Rizzino A . Transcriptional regulation of the transforming growth factor-beta2 promoter by cAMP-responsive element-binding protein (CREB) and activating transcription factor-1 (ATF-1) is modulated by protein kinases and the coactivators p300 and CREB-binding.... J Biol Chem. 1999; 274(48):34020-8. DOI: 10.1074/jbc.274.48.34020. View

15.

Xiao Q, Kenessey A, Ojamaa K . Role of USF1 phosphorylation on cardiac alpha-myosin heavy chain promoter activity. Am J Physiol Heart Circ Physiol. 2002; 283(1):H213-9. DOI: 10.1152/ajpheart.01085.2001. View

16.

Barlev N, Liu L, Chehab N, Mansfield K, Harris K, Halazonetis T . Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol Cell. 2002; 8(6):1243-54. DOI: 10.1016/s1097-2765(01)00414-2. View

17.

Deininger M, Meyermann R, Trautmann K, Duffner F, Grote E, Wickboldt J . Heme oxygenase (HO)-1 expressing macrophages/microglial cells accumulate during oligodendroglioma progression. Brain Res. 2000; 882(1-2):1-8. DOI: 10.1016/s0006-8993(00)02594-4. View

18.

Corre S, Galibert M . Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res. 2005; 18(5):337-48. DOI: 10.1111/j.1600-0749.2005.00262.x. View

19.

Carreira S, Liu B, Goding C . The gene encoding the T-box factor Tbx2 is a target for the microphthalmia-associated transcription factor in melanocytes. J Biol Chem. 2000; 275(29):21920-7. DOI: 10.1074/jbc.M000035200. View

20.

Galibert M, Boucontet L, Goding C, Meo T . Recognition of the E-C4 element from the C4 complement gene promoter by the upstream stimulatory factor-1 transcription factor. J Immunol. 1998; 159(12):6176-83. View