Heat Shock Factor 1 Is a Substrate for p38 Mitogen-Activated Protein Kinases

REFERENCES

• Morimoto RI. 2011. The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harbor Symp Quant Biol 76:91–99. http://dx.doi.org/10.1101/sqb.2012.76.010637.
   PubMedGoogle Scholar
• Anckar J, Sistonen L. 2011. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80:1089–1115. http://dx.doi.org/10.1146/annurev-biochem-060809-095203.
   PubMed Web of Science ®Google Scholar
• Vihervaara A, Sistonen L. 2014. HSF1 at a glance. J Cell Sci 127:261–266. http://dx.doi.org/10.1242/jcs.132605.
   PubMed Web of Science ®Google Scholar
• Richter K, Haslbeck M, Buchner J. 2010. The heat shock response: life on the verge of death. Mol Cell 40:253–266. http://dx.doi.org/10.1016/j.molcel.2010.10.006.
   PubMed Web of Science ®Google Scholar
• Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, Fraenkel E, Ince TA, Whitesell L, Lindquist S. 2012. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150:549–562. http://dx.doi.org/10.1016/j.cell.2012.06.031.
   PubMed Web of Science ®Google Scholar
• Dai C, Santagata S, Tang Z, Shi J, Cao J, Kwon H, Bronson RT, Whitesell L, Lindquist S. 2012. Loss of tumor suppressor NF1 activates HSF1 to promote carcinogenesis. J Clin Invest 122:3742–3754. http://dx.doi.org/10.1172/JCI62727.
   PubMed Web of Science ®Google Scholar
• Calderwood SK. 2012. HSF1, a versatile factor in tumorigenesis. Curr Mol Med 12:1102–1107. http://dx.doi.org/10.2174/156652412803306675.
   PubMedGoogle Scholar
• Gabai VL, Meng L, Kim G, Mills TA, Benjamin IJ, Sherman MY. 2012. Heat shock transcription factor Hsf1 is involved in tumor progression via regulation of hypoxia-inducible factor 1 and RNA-binding protein HuR. Mol Cell Biol 32:929–940. http://dx.doi.org/10.1128/MCB.05921-11.
   PubMed Web of Science ®Google Scholar
• Chou SD, Murshid A, Eguchi T, Gong J, Calderwood SK. 2014. HSF1 regulation of beta-catenin in mammary cancer cells through control of HuR/elavL1 expression. Oncogene 34:2178–2188. http://dx.doi.org/10.1038/onc.2014.177.
   PubMedGoogle Scholar
• Santagata S, Mendillo ML, Tang YC, Subramanian A, Perley CC, Roche SP, Wong B, Narayan R, Kwon H, Koeva M, Amon A, Golub TR, Porco JA, Jr, Whitesell L, Lindquist S. 2013. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 341:1238303. http://dx.doi.org/10.1126/science.1238303.
   PubMed Web of Science ®Google Scholar
• Westerheide SD, Anckar J, Stevens SM, Jr, Sistonen L, Morimoto RI. 2009. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323:1063–1066. http://dx.doi.org/10.1126/science.1165946.
   PubMed Web of Science ®Google Scholar
• Raychaudhuri S, Loew C, Korner R, Pinkert S, Theis M, Hayer-Hartl M, Buchholz F, Hartl FU. 2014. Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell 156:975–985. http://dx.doi.org/10.1016/j.cell.2014.01.055.
   PubMedGoogle Scholar
• Budzynski MA, Puustinen MC, Joutsen J, Sistonen L. 2015. Uncoupling stress-inducible phosphorylation of heat shock factor 1 from its activation. Mol Cell Biol 35:2530–2540. http://dx.doi.org/10.1128/MCB.00816-14.
   PubMed Web of Science ®Google Scholar
• Kline MP, Morimoto RI. 1997. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol Cell Biol 17:2107–2115. http://dx.doi.org/10.1128/MCB.17.4.2107.
   PubMed Web of Science ®Google Scholar
• Chu B, Zhong R, Soncin F, Stevenson MA, Calderwood SK. 1998. Transcriptional activity of heat shock factor 1 at 37°C is repressed through phosphorylation on two distinct serine residues by glycogen synthase kinase 3 and protein kinases Cα and Cζ. J Biol Chem 273:18640–18646. http://dx.doi.org/10.1074/jbc.273.29.18640.
   PubMed Web of Science ®Google Scholar
• Xavier IJ, Mercier PA, McLoughlin CM, Ali A, Woodgett JR, Ovsenek N. 2000. Glycogen synthase kinase 3β negatively regulates both DNA-binding and transcriptional activities of heat shock factor 1. J Biol Chem 275:29147–29152. http://dx.doi.org/10.1074/jbc.M002169200.
   PubMedGoogle Scholar
• Knauf U, Newton EM, Kyriakis J, Kingston RE. 1996. Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev 10:2782–2793. http://dx.doi.org/10.1101/gad.10.21.2782.
   PubMed Web of Science ®Google Scholar
• Wang X, Khaleque MA, Zhao MJ, Zhong R, Gaestel M, Calderwood SK. 2006. Phosphorylation of HSF1 by MAPK-activated protein kinase 2 on serine 121, inhibits transcriptional activity and promotes HSP90 binding. J Biol Chem 281:782–791. http://dx.doi.org/10.1074/jbc.M505822200.
   PubMed Web of Science ®Google Scholar
• Guettouche T, Boellmann F, Lane WS, Voellmy R. 2005. Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 6:4. http://dx.doi.org/10.1186/1471-2091-6-4.
   PubMedGoogle Scholar
• Chou SD, Prince T, Gong J, Calderwood SK. 2012. mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS One 7:e39679. http://dx.doi.org/10.1371/journal.pone.0039679.
   PubMed Web of Science ®Google Scholar
• Kristal AR, Lampe JW. 2002. Brassica vegetables and prostate cancer risk: a review of the epidemiological evidence. Nutr Cancer 42:1–9. http://dx.doi.org/10.1207/S15327914NC421_1.
   PubMed Web of Science ®Google Scholar
• Fahey JW, Zalcmann AT, Talalay P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51. http://dx.doi.org/10.1016/S0031-9422(00)00316-2.
   PubMed Web of Science ®Google Scholar
• Mithen R, Bennett R, Marquez J. 2010. Glucosinolate biochemical diversity and innovation in the Brassicales. Phytochemistry 71:2074–2086. http://dx.doi.org/10.1016/j.phytochem.2010.09.017.
   PubMed Web of Science ®Google Scholar
• Hu R, Xu C, Shen G, Jain MR, Khor TO, Gopalkrishnan A, Lin W, Reddy B, Chan JY, Kong AN. 2006. Identification of Nrf2-regulated genes induced by chemopreventive isothiocyanate PEITC by oligonucleotide microarray. Life Sci 79:1944–1955. http://dx.doi.org/10.1016/j.lfs.2006.06.019.
   PubMed Web of Science ®Google Scholar
• Cheung KL, Khor TO, Yu S, Kong AN. 2008. PEITC induces G1 cell cycle arrest on HT-29 cells through the activation of p38 MAPK signaling pathway. AAPS J 10:277–281. http://dx.doi.org/10.1208/s12248-008-9032-9.
   PubMedGoogle Scholar
• Calamini B, Silva MC, Madoux F, Hutt DM, Khanna S, Chalfant MA, Saldanha SA, Hodder P, Tait BD, Garza D, Balch WE, Morimoto RI. 2012. Small-molecule proteostasis regulators for protein conformational diseases. Nat Chem Biol 8:185–196. http://dx.doi.org/10.1038/nchembio.763.
   Web of Science ®Google Scholar
• Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, Richardson JA, Benjamin IJ. 1999. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J 18:5943–5952. http://dx.doi.org/10.1093/emboj/18.21.5943.
   PubMed Web of Science ®Google Scholar
• Zur R, Garcia-Ibanez L, Nunez-Buiza A, Aparicio N, Liappas G, Escos A, Risco A, Page A, Saiz-Ladera C, Alsina-Beauchamp D, Montans J, Paramio JM, Cuenda A. 2015. Combined deletion of p38γ and p38δ reduces skin inflammation and protects from carcinogenesis. Oncotarget 6:12920–12935. http://dx.doi.org/10.18632/oncotarget.4320.
   PubMedGoogle Scholar
• Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K. 2010. REAP: a two minute cell fractionation method. BMC Res Notes 3:294. http://dx.doi.org/10.1186/1756-0500-3-294.
   PubMedGoogle Scholar
• Zhang Y, Ahn YH, Benjamin IJ, Honda T, Hicks RJ, Calabrese V, Cole PA, Dinkova-Kostova AT. 2011. HSF1-dependent upregulation of Hsp70 by sulfhydryl-reactive inducers of the KEAP1/NRF2/ARE pathway. Chem Biol 18:1355–1361. http://dx.doi.org/10.1016/j.chembiol.2011.09.008.
   PubMedGoogle Scholar
• Dinkova-Kostova AT. 2012. Chemoprotection against cancer by isothiocyanates: a focus on the animal models and the protective mechanisms. Top Curr Chem 329:179–201. http://dx.doi.org/10.1007/128_2012_337.
   Web of Science ®Google Scholar
• Dinkova-Kostova AT, Kostov RV. 2012. Glucosinolates and isothiocyanates in health and disease. Trends Mol Med 18:337–347. http://dx.doi.org/10.1016/j.molmed.2012.04.003.
   PubMed Web of Science ®Google Scholar
• Kensler TW, Egner PA, Agyeman AS, Visvanathan K, Groopman JD, Chen JG, Chen TY, Fahey JW, Talalay P. 2012. Keap1-Nrf2 signaling: a target for cancer prevention by sulforaphane. Top Curr Chem 329:163–177. http://dx.doi.org/10.1007/128_2012_339.
   Google Scholar
• Sorger PK, Nelson HC. 1989. Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell 59:807–813. http://dx.doi.org/10.1016/0092-8674(89)90604-1.
   PubMed Web of Science ®Google Scholar
• Perisic O, Xiao H, Lis JT. 1989. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5-bp recognition unit. Cell 59:797–806. http://dx.doi.org/10.1016/0092-8674(89)90603-X.
   PubMed Web of Science ®Google Scholar
• Peteranderl R, Nelson HC. 1992. Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry 31:12272–12276. http://dx.doi.org/10.1021/bi00163a042.
   PubMedGoogle Scholar
• Rabindran SK, Haroun RI, Clos J, Wisniewski J, Wu C. 1993. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259:230–234. http://dx.doi.org/10.1126/science.8421783.
   PubMed Web of Science ®Google Scholar
• Jhaveri K, Taldone T, Modi S, Chiosis G. 2012. Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim Biophys Acta 1823:742–755. http://dx.doi.org/10.1016/j.bbamcr.2011.10.008.
   PubMed Web of Science ®Google Scholar
• Taipale M, Krykbaeva I, Koeva M, Kayatekin C, Westover KD, Karras GI, Lindquist S. 2012. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150:987–1001. http://dx.doi.org/10.1016/j.cell.2012.06.047.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Dayalan Naidu S, Samarasinghe K, Van Hecke GC, Pheely A, Boronina TN, Cole RN, Benjamin IJ, Cole PA, Ahn YH, Dinkova-Kostova AT. 2014. Sulphoxythiocarbamates modify cysteine residues in HSP90 causing degradation of client proteins and inhibition of cancer cell proliferation. Br J Cancer 110:71–82. http://dx.doi.org/10.1038/bjc.2013.710.
   PubMed Web of Science ®Google Scholar
• Ubersax JA, Ferrell JE, Jr. 2007. Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8:530–541. http://dx.doi.org/10.1038/nrm2203.
   PubMed Web of Science ®Google Scholar
• Park J, Liu AY. 2001. JNK phosphorylates the HSF1 transcriptional activation domain: role of JNK in the regulation of the heat shock response. J Cell Biochem 82:326–338. http://dx.doi.org/10.1002/jcb.1163.
   PubMed Web of Science ®Google Scholar
• Zhang T, Inesta-Vaquera F, Niepel M, Zhang J, Ficarro SB, Machleidt T, Xie T, Marto JA, Kim N, Sim T, Laughlin JD, Park H, LoGrasso PV, Patricelli M, Nomanbhoy TK, Sorger PK, Alessi DR, Gray NS. 2012. Discovery of potent and selective covalent inhibitors of JNK. Chem Biol 19:140–154. http://dx.doi.org/10.1016/j.chembiol.2011.11.010.
   PubMed Web of Science ®Google Scholar
• Kuma Y, Sabio G, Bain J, Shpiro N, Marquez R, Cuenda A. 2005. BIRB796 inhibits all p38 MAPK isoforms in vitro and in vivo. J Biol Chem 280:19472–19479. http://dx.doi.org/10.1074/jbc.M414221200.
   PubMed Web of Science ®Google Scholar
• Tang Z, Dai S, He Y, Doty RA, Shultz LD, Sampson SB, Dai C. 2015. MEK guards proteome stability and inhibits tumor-suppressive amyloidogenesis via HSF1. Cell 160:729–744. http://dx.doi.org/10.1016/j.cell.2015.01.028.
   PubMed Web of Science ®Google Scholar
• Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623–18632. http://dx.doi.org/10.1074/jbc.273.29.18623.
   PubMed Web of Science ®Google Scholar
• Goedert M, Cuenda A, Craxton M, Jakes R, Cohen P. 1997. Activation of the novel stress-activated protein kinase SAPK4 by cytokines and cellular stresses is mediated by SKK3 (MKK6); comparison of its substrate specificity with that of other SAP kinases. EMBO J 16:3563–3571. http://dx.doi.org/10.1093/emboj/16.12.3563.
   PubMedGoogle Scholar
• Morley JF, Morimoto RI. 2004. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15:657–664.
   PubMed Web of Science ®Google Scholar
• Chiang WC, Ching TT, Lee HC, Mousigian C, Hsu AL. 2012. HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148:322–334. http://dx.doi.org/10.1016/j.cell.2011.12.019.
   PubMed Web of Science ®Google Scholar
• Xu YM, Huang DY, Chiu JF, Lau AT. 2012. Posttranslational modification of human heat shock factors and their functions: a recent update by proteomic approach. J Proteome Res 11:2625–2634. http://dx.doi.org/10.1021/pr201151a.
   PubMedGoogle Scholar
• Soncin F, Zhang X, Chu B, Wang X, Asea A, Ann Stevenson M, Sacks DB, Calderwood SK. 2003. Transcriptional activity and DNA binding of heat shock factor-1 involve phosphorylation on threonine 142 by CK2. Biochem Biophys Res Commun 303:700–706. http://dx.doi.org/10.1016/S0006-291X(03)00398-X.
   PubMed Web of Science ®Google Scholar
• Lee YJ, Kim EH, Lee JS, Jeoung D, Bae S, Kwon SH, Lee YS. 2008. HSF1 as a mitotic regulator: phosphorylation of HSF1 by Plk1 is essential for mitotic progression. Cancer Res 68:7550–7560. http://dx.doi.org/10.1158/0008-5472.CAN-08-0129.
   PubMedGoogle Scholar
• Kim SA, Yoon JH, Lee SH, Ahn SG. 2005. Polo-like kinase 1 phosphorylates heat shock transcription factor 1 and mediates its nuclear translocation during heat stress. J Biol Chem 280:12653–12657. http://dx.doi.org/10.1074/jbc.M411908200.
   PubMed Web of Science ®Google Scholar
• Murshid A, Chou SD, Prince T, Zhang Y, Bharti A, Calderwood SK. 2010. Protein kinase A binds and activates heat shock factor 1. PLoS One 5:e13830. http://dx.doi.org/10.1371/journal.pone.0013830.
   PubMed Web of Science ®Google Scholar
• Holmberg CI, Hietakangas V, Mikhailov A, Rantanen JO, Kallio M, Meinander A, Hellman J, Morrice N, MacKintosh C, Morimoto RI, Eriksson JE, Sistonen L. 2001. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J 20:3800–3810. http://dx.doi.org/10.1093/emboj/20.14.3800.
   PubMed Web of Science ®Google Scholar
• Cavell BE, Syed Alwi SS, Donlevy AM, Proud CG, Packham G. 2012. Natural product-derived antitumor compound phenethyl isothiocyanate inhibits mTORC1 activity via TSC2. J Nat Prod 75:1051–1057. http://dx.doi.org/10.1021/np300049b.
   PubMed Web of Science ®Google Scholar
• Cohen P. 2009. Targeting protein kinases for the development of anti-inflammatory drugs. Curr Opin Cell Biol 21:317–324. http://dx.doi.org/10.1016/j.ceb.2009.01.015.
   PubMed Web of Science ®Google Scholar
• Banerjee Mustafi S, Chakraborty PK, Dey RS, Raha S. 2009. Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperones 14:579–589. http://dx.doi.org/10.1007/s12192-009-0109-x.
   PubMed Web of Science ®Google Scholar
• Sugimoto N, Shido O, Matsuzaki K, Ohno-Shosaku T, Hitomi Y, Tanaka M, Sawaki T, Fujita Y, Kawanami T, Masaki Y, Okazaki T, Nakamura H, Koizumi S, Yachie A, Umehara H. 2012. Cellular heat acclimation regulates cell growth, cell morphology, mitogen-activated protein kinase activation, and expression of aquaporins in mouse fibroblast cells. Cell Physiol Biochem 30:450–457. http://dx.doi.org/10.1159/000339038.
   PubMedGoogle Scholar
• Seo MS, Oh SY, Park MJ, Kim SM, Kim MY, Han SI, Park HG, Kang HS. 2005. Implication of reactive oxygen species, ERK1/2, and p38MAPK in sodium salicylate-induced heat shock protein 72 expression in C6 glioma cells. Int J Mol Med 16:841–849.
   PubMedGoogle Scholar
• Westerheide SD, Bosman JD, Mbadugha BN, Kawahara TL, Matsumoto G, Kim S, Gu W, Devlin JP, Silverman RB, Morimoto RI. 2004. Celastrols as inducers of the heat shock response and cytoprotection. J Biol Chem 279:56053–56060. http://dx.doi.org/10.1074/jbc.M409267200.
   PubMed Web of Science ®Google Scholar
• Dayalan Naidu S, Kostov RV, Dinkova-Kostova AT. 2015. Transcription factors Hsf1 and Nrf2 engage in crosstalk for cytoprotection. Trends Pharmacol Sci 36:6–14. http://dx.doi.org/10.1016/j.tips.2014.10.011.
   PubMed Web of Science ®Google Scholar
• Trott A, West JD, Klaic L, Westerheide SD, Silverman RB, Morimoto RI, Morano KA. 2008. Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol Biol Cell 19:1104–1112.
   PubMed Web of Science ®Google Scholar
• Escos A, Risco A, Alsina-Beauchamp D, Cuenda A. 2016. p38γ and p38δ mitogen-activated protein kinases (MAPKs), new stars in the MAPK galaxy. Front Cell Dev Biol 4:31. http://dx.doi.org/10.3389/fcell.2016.00031.
   PubMed Web of Science ®Google Scholar