MED12 interacts with the heat-shock transcription factor HSF1 and recruits CDK8 to promote the heat-shock response in mammalian cells.
Animals
Cyclin-Dependent Kinase 8
/ genetics
Cyclin-Dependent Kinases
/ genetics
Fibroblasts
Gene Expression Regulation
HEK293 Cells
HSP70 Heat-Shock Proteins
/ genetics
HeLa Cells
Heat Shock Transcription Factors
/ genetics
Heat-Shock Response
/ genetics
Humans
Mediator Complex
/ genetics
Mice
Multiprotein Complexes
/ genetics
Neurons
Osteoblasts
Phosphorylation
Protein Binding
Proteostasis
/ genetics
Signal Transduction
Transcription, Genetic
CDK8
HSF1
MED12
heat shock
phosphorylation
transcription
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
16
05
2021
received:
25
01
2021
accepted:
21
05
2021
pubmed:
1
6
2021
medline:
5
8
2021
entrez:
31
5
2021
Statut:
ppublish
Résumé
Activated and promoter-bound heat-shock transcription factor 1 (HSF1) induces RNA polymerase II recruitment upon heat shock, and this is facilitated by the core Mediator in Drosophila and yeast. Another Mediator module, CDK8 kinase module (CKM), consisting of four subunits including MED12 and CDK8, plays a negative or positive role in the regulation of transcription; however, its involvement in HSF1-mediated transcription remains unclear. We herein demonstrated that HSF1 interacted with MED12 and recruited MED12 and CDK8 to the HSP70 promoter during heat shock in mammalian cells. The kinase activity of CDK8 (and its paralog CDK19) promoted HSP70 expression partly by phosphorylating HSF1-S326 and maintained proteostasis capacity. These results indicate an important role for CKM in the protection of cells against proteotoxic stress.
Identifiants
pubmed: 34056708
doi: 10.1002/1873-3468.14139
doi:
Substances chimiques
HSF1 protein, human
0
HSP70 Heat-Shock Proteins
0
Heat Shock Transcription Factors
0
MED12 protein, human
0
Mediator Complex
0
Multiprotein Complexes
0
CDK19 protein, human
EC 2.7.11.22
CDK8 protein, human
EC 2.7.11.22
Cyclin-Dependent Kinase 8
EC 2.7.11.22
Cyclin-Dependent Kinases
EC 2.7.11.22
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1933-1948Informations de copyright
© 2021 Federation of European Biochemical Societies.
Références
Balch WE, Morimoto RI, Dillin A and Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319, 916-919.
Labbadia J and Morimoto RI (2015) The biology of proteostasis in aging and disease. Annu Rev Biochem 84, 435-464.
Parsell DA and Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27, 437-496.
Gomez-Pastor R, Burchfiel ET and Thiele DJ (2018) Regulation of heat shock transcription factors and their roles in physiology and disease. Nat Rev Mol Cell Biol 19, 4-19.
Nakai A, ed (2016) Heat shock factor. Springer, Tokyo, Japan.
Fujimoto M, Takaki E, Takii R, Prakasam R, Hayashida N, Iemura S, Natsume T and Nakai A (2012) RPA assists HSF1 access to nucleosomal DNA by recruiting histone chaperone FACT. Mol Cell 48, 182-194.
Fujimoto M, Takii R, Katiyar A, Srivastava P and Nakai A (2018) Poly(ADP-Ribose) polymerase 1 promotes the human heat shock response by facilitating heat shock transcription factor 1 binding to DNA. Mol Cell Biol 38, e0005-18.
Corey LL, Weirich CS, Benjamin IJ and Kingston RE (2003) Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev 17, 1392-1401.
Xu D, Zalmas LP and La Thangue NB (2008) A transcription cofactor required for the heat-shock response. EMBO Rep 9, 662-669.
Hong S, Kim SH, Heo MA, Choi YH, Park MJ, Yoo MA, Kim HD, Kang HS and Cheong J (2004) Coactivator ASC-2 mediates heat shock factor 1-mediated transactivation dependent on heat shock. FEBS Lett 559, 165-170.
Chen Y, Chen J, Yu J, Yang G, Temple E, Harbinski F, Gao H, Wilson C, Pagliarini R and Zhou W (2014) Identification of mixed lineage leukemia 1 (MLL1) protein as a coactivator of heat shock factor 1(HSF1) protein in response to heat shock protein 90 (HSP90) inhibition. J Biol Chem 289, 18914-18927.
Takii R, Fujimoto M, Matsumoto M, Srivastava P, Katiyar A, Nakayama KI and Nakai A (2019) The pericentromeric protein shugoshin 2 cooperates with HSF1 in heat shock response and RNA Pol II recruitment. EMBO J 38, e102566.
Cramer P (2019) Organization and regulation of gene transcription. Nature 573, 45-54.
Park JM, Werner J, Kim JM, Lis JT and Kim YJ (2001) Mediator, not holoenzyme, is directly recruited to the heat shock promoter by HSF upon heat shock. Mol Cell 8, 9-19.
Mason PB Jr and Lis JT (1997) Cooperative and competitive protein interactions at the hsp70 promoter. J Biol Chem 272, 33227-33233.
Soutourina J (2018) Transcription regulation by the Mediator complex. Nat Rev Mol Cell Biol 19, 262-274.
Schier AC and Taatjes DJ (2020) Structure and mechanism of the RNA polymerase II transcription machinery. Genes Dev 34, 465-488.
Knuesel MT, Meyer KD, Bernecky C and Taatjes DJ (2009) The human CDK8 subcomplex is a molecular switch that controls mediator coactivator function. Genes Dev 23, 439-451.
Tsai KL, Sato S, Tomomori-Sato C, Conaway RC, Conaway JW and Asturias FJ (2013) A conserved mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat Struct Mol Biol 20, 611-619.
Knuesel MT, Meyer KD, Donner AJ, Espinosa JM and Taatjes DJ (2009) The human CDK8 subcomplex is a histone kinase that requires MED12 for activity and can function independently of Mediator. Mol Cell Biol 29, 650-661.
Klatt F, Leitner A, Kim IV, Ho-Xuan H, Schneider EV, Langhammer F, Weinmann R, Müller MR, Huber R, Meister G et al. (2020) A precisely positioned MED12 activation helix stimulates CDK8 kinase activity. Proc Natl Acad Sci USA 117, 2894-2905.
Hengartner CJ, Myer VE, Liao SM, Wilson CJ, Koh SS and Young RA (1998) Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol Cell 2, 43-53.
Akoulitchev S, Chuikov S and Reinberg D (2000) TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 407, 102-106.
Donner AJ, Szostek S, Hoover JM and Espinosa JM (2007) CDK8 is a stimulus-specific positive coregulator of p53 target genes. Mol Cell 27, 121-133.
Donner AJ, Ebmeier CC, Taatjes DJ and Espinosa JM (2010) CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17, 194-201.
Galbraith MD, Allen MA, Bensard CL, Wang X, Schwinn MK, Qin B, Long HW, Daniels DL, Hahn WC, Dowell RD et al. (2013) HIF1A employs CDK8-mediator to stimulate RNAPII elongation in response to hypoxia. Cell 153, 1327-1339.
Chen M, Liang J, Ji H, Yang Z, Altilia S, Hu B, Schronce A, McDermott MSJ, Schools GP, Lim CU et al. (2017) CDK8/19 Mediator kinases potentiate induction of transcription by NFκB. Proc Natl Acad Sci USA 114, 10208-10213.
Bancerek J, Poss ZC, Steinparzer I, Sedlyarov V, Pfaffenwimmer T, Mikulic I, Dölken L, Strobl B, Müller M, Taatjes DJ et al. (2013) CDK8 kinase phosphorylates transcription factor STAT1 to selectively regulate the interferon response. Immunity 38, 250-262.
Steinparzer I, Sedlyarov V, Rubin JD, Eislmayr K, Galbraith MD, Levandowski CB, Vcelkova T, Sneezum L, Wascher F, Amman F et al. (2019) Transcriptional responses to IFN-γ require mediator kinase-dependent pause release and mechanistically distinct CDK8 and CDK19 functions. Mol Cell 76, 485-499.
Anandhakumar J, Moustafa YW, Chowdhary S, Kainth AS and Gross DS (2016) Evidence for multiple mediator complexes in yeast independently recruited by activated heat shock factor. Mol Cell Biol 36, 1943-1960.
Kim S and Gross D (2013) Mediator recruitment to heat shock genes requires dual Hsf1 activation domains and mediator tail subunits Med15 and Med16. J Biol Chem 288, 12197-12213.
Miozzo F, Sabéran-Djoneidi D and Mezger V (2015) HSFs, stress sensors and sculptors of transcription compartments and epigenetic landscapes. J Mol Biol 427, 3793-3816.
Takahashi H, Parmely TJ, Sato S, Tomomori-Sato C, Banks CA, Kong SE, Szutorisz H, Swanson SK, Martin-Brown S, Washburn MP et al. (2011) Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146, 92-104.
Clos J, Rabindran S, Wisniewski J and Wu C (1993) Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment. Nature 364, 252-255.
Liu XD, Liu PC, Santoro N and Thiele DJ (1997) Conservation of a stress response: human heat shock transcription factors functionally substitute for yeast HSF. EMBO J 16, 6466-6477.
Inouye S, Katsuki K, Izu H, Fujimoto M, Sugahara K, Yamada S, Shinkai Y, Oka Y, Katoh Y and Nakai A (2003) Activation of heat shock genes is not necessary for protection by heat shock transcription factor 1 against cell death due to a single exposure to high temperatures. Mol Cell Biol 23, 5882-5895.
El Khattabi L, Zhao H, Kalchschmidt J, Young N, Jung S, Van Blerkom P, Kieffer-Kwon P, Kieffer-Kwon KR, Park S, Wang X et al. (2019) A pliable mediator acts as a functional rather than an architectural bridge between promoters and enhancers. Cell 178, 1145-1158.
Kim TW, Kwon YJ, Kim JM, Song YH, Kim SN and Kim YJ (2004) MED16 and MED23 of Mediator are coactivators of lipopolysaccharide- and heat-shock-induced transcriptional activators. Proc Natl Acad Sci USA 101, 12153-12158.
Takii R, Fujimoto M, Tan K, Takaki E, Hayashida N, Nakato R, Shirahige K and Nakai A (2015) ATF1 modulates the heat shock response by regulating the stress-inducible heat shock factor 1 transcription complex. Mol Cell Biol 35, 11-25.
Zhou R, Bonneaud N, Yuan CX, de Santa BP, Boizet B, Schomber T, Scherer G, Roeder RG, Poulat F and Berta P (2002) SOX9 interacts with a component of the human thyroid hormone receptor-associated protein complex. Nucleic Acids Res 30, 3245-3252.
Kim S, Xu X, Hecht A and Boyer TG (2006) Mediator is a transducer of Wnt/beta-catenin signaling. J Biol Chem 281, 14066-14075.
Kuuluvainen E, Domènech-Moreno E, Niemelä EH and Mäkelä TP (2018) Depletion of mediator kinase module subunits represses superenhancer-associated genes in colon cancer cells. Mol Cell Biol 38, e00573-e617.
Li N, Fassl A, Chick J, Inuzuka H, Li X, Mansour MR, Liu L, Wang H, King B, Shaik S et al. (2014) Cyclin C is a haploinsufficient tumour suppressor. Nat Cell Biol 16, 1080-1091.
Porter DC, Farmaki E, Altilia S, Schools GP, West DK, Chen M, Chang BD, Puzyrev AT, Lim CU, Rokow-Kittell R et al. (2012) Cyclin-dependent kinase 8 mediates chemotherapy-induced tumor-promoting paracrine activities. Proc Natl Acad Sci USA 109, 13799-13804.
Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES and Young RA (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728.
Fant CB and Taatjes DJ (2019) Regulatory functions of the mediator kinases CDK8 and CDK19. Transcription 10, 76-90.
Guettouche T, Boellmann F, Lane WS and Voellmy R (2005) Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 6, 4.
Jonkers I and Lis JT (2015) Getting up to speed with transcription elongation by RNA polymerase II. Nat Rev Mol Cell Biol 16, 167-177.
Cooper KF, Mallory MJ, Smith JB and Strich R (1997) Stress and developmental regulation of the yeast C-type cyclin Ume3p (Srb11p/Ssn8p). EMBO J 16, 4665-4675.
Galbraith MD, Donner AJ and Espinosa JM (2010) CDK8: a positive regulator of transcription. Transcription 1, 4-12.
Jeronimo C, Langelier MF, Bataille AR, Pascal JM, Pugh BF and Robert F (2016) Tail and kinase modules differently regulate core mediator recruitment and function in vivo. Mol Cell 64, 455-466.
Poss ZC, Ebmeier CC, Odell AT, Tangpeerachaikul A, Lee T, Pelish HE, Shair MD, Dowell RD, Old WM and Taatjes DJ (2016) Identification of mediator kinase substrates in human cells using cortistatin A and quantitative phosphoproteomics. Cell Rep 15, 436-450.
Zhao X, Feng D, Wang Q, Abdulla A, Xie XJ, Zhou J, Sun Y, Yang ES, Liu LP, Vaitheesvaran B et al. (2012) Regulation of lipogenesis by cyclin-dependent kinase 8-mediated control of SREBP-1. J Clin Invest 122, 2417-2427.
Tang Z, Dai S, He Y, Doty RA, Shultz LD, Sampson SB and Dai C (2015) MEK guards proteome stability and inhibits tumor-suppressive amyloidogenesis via HSF1. Cell 160, 729-744.
Dayalan Naidu S, Sutherland C, Zhang Y, Risco A, de la Vega L, Caunt CJ, Hastie CJ, Lamont DJ, Torrente L, Chowdhry S et al. (2016) Heat shock factor 1 Is a substrate for p38 mitogen-activated protein kinases. Mol Cell Biol 36, 2403-2417.
Chou SD, Prince T, Gong J and Calderwood SK (2012) mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS ONE 7, e39679.
Moreno R, Banerjee S, Jackson AW, Quinn J, Baillie G, Dixon JE, Dinkova-Kostova AT, Edwards J and de la Vega L (2020) The stress-responsive kinase DYRK2 activates heat shock factor 1 promoting resistance to proteotoxic stress. Cell Death Differ 28, 1563-1578.
Clark AD, Oldenbroek M and Boyer TG (2015) Mediator kinase module and human tumorigenesis. Crit Rev Biochem Mol Biol 50, 393-426.
Turunen M, Spaeth JM, Keskitalo S, Park MJ, Kivioja T, Clark AD, Mäkinen N, Gao F, Palin K, Nurkkala H et al. (2014) Uterine leiomyoma-linked MED12 mutations disrupt mediator-associated CDK activity. Cell Rep 7, 654-660.
Park MJ, Shen H, Spaeth JM, Tolvanen JH, Failor C, Knudtson JF, McLaughlin J, Halder SK, Yang Q, Bulun SE et al. (2018) Oncogenic exon 2 mutations in mediator subunit MED12 disrupt allosteric activation of cyclin C-CDK8/19. J Biol Chem 293, 4870-4882.