Abstract
Heat shock factor 1 (HSF1) was discovered in 1984 as the master regulator of the heat shock response. In this classical role, HSF1 is activated following cellular stresses such as heat shock that ultimately lead to HSF1-mediated expression of heat shock proteins to protect the proteome and survive these acute stresses. However, it is now becoming clear that HSF1 also plays a significant role in several diseases, perhaps none more prominent than cancer. HSF1 appears to have a pleiotropic role in cancer by supporting multiple facets of malignancy including migration, invasion, proliferation, and cancer cell metabolism among others. Because of these functions, and others, of HSF1, it has been investigated as a biomarker for patient outcomes in multiple cancer types. HSF1 expression alone was predictive for patient outcomes in multiple cancer types but in other instances, markers for HSF1 activity were more predictive. Clearly, further work is needed to tease out which markers are most representative of the tumor promoting effects of HSF1. Additionally, there have been several attempts at developing small molecule inhibitors to reduce HSF1 activity. All of these HSF1 inhibitors are still in preclinical models but have shown varying levels of efficacy at suppressing tumor growth. The growth of research related to HSF1 in cancer has been enormous over the last decade with many new functions of HSF1 discovered along the way. In order for these discoveries to reach clinical impact, further development of HSF1 as a biomarker or therapeutic target needs to be continued.
Keywords: HSF1, metastasis, biomarker, therapy, EMT, invasion, migration.
Graphical Abstract
[1]
Ritossa, F. A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia, 1962, 18, 571-573.
[2]
Parker, C.S.; Topol, J. A drosophila RNA polymerase II transcription factor contains a promoter-region-specific DNA-binding activity. Cell, 1984, 36(2), 357-369.
[3]
Topol, J.; Ruden, D.M.; Parker, C.S. Sequences required for in vitro transcriptional activation of a Drosophila hsp 70 gene. Cell, 1985, 42(2), 527-537.
[4]
Amin, J.; Ananthan, J.; Voellmy, R. Key features of heat shock regulatory elements. Mol. Cell. Biol., 1988, 8(9), 3761-3769.
[5]
Dudler, R.; Travers, A.A. Upstream elements necessary for optimal function of the hsp 70 promoter in transformed flies. Cell, 1984, 38(2), 391-398.
[6]
Slater, M.R.; Craig, E.A. Transcriptional regulation of an hsp70 heat shock gene in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 1987, 7(5), 1906-1916.
[7]
Xiao, H.; Lis, J.T. Germline transformation used to define key features of heat-shock response elements. Science, 1988, 239(4844), 1139-1142.
[8]
Hoang, A.T.; Huang, J.; Rudra-Ganguly, N.; Zheng, J.; Powell, W.C.; Rabindran, S.K.; Wu, C.; Roy-Burman, P. A novel association between the human heat shock transcription factor 1 (HSF1) and prostate adenocarcinoma. Am. J. Pathol., 2000, 156(3), 857-864.
[9]
Cen, H.; Zheng, S.; Fang, Y.M.; Tang, X.P.; Dong, Q. Induction of HSF1 expression is associated with sporadic colorectal cancer. World J. Gastroenterol., 2004, 10(21), 3122-3126.
[10]
Cheng, Q.; Chang, J.T.; Geradts, J.; Neckers, L.M.; Haystead, T.; Spector, N.L.; Lyerly, H.K. Amplification and high-level expression of heat shock protein 90 marks aggressive phenotypes of human epidermal growth factor receptor 2 negative breast cancer. Breast Cancer Res., 2012, 14(2), R62.
[11]
Dai, C.; Whitesell, L.; Rogers, A.B.; Lindquist, S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell, 2007, 130(6), 1005-1018.
[12]
Mendillo, M.L.; Santagata, S.; Koeva, M.; Bell, G.W.; Hu, R.; Tamimi, R.M.; Fraenkel, E.; Ince, T.A.; Whitesell, L.; Lindquist, S. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell, 2012, 150(3), 549-562.
[13]
Santagata, S.; Hu, R.; Lin, N.U.; Mendillo, M.L.; Collins, L.C.; Hankinson, S.E.; Schnitt, S.J.; Whitesell, L.; Tamimi, R.M.; Lindquist, S.; Ince, T.A. High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc. Natl. Acad. Sci. USA, 2011, 108(45), 18378-18383.
[14]
Jego, G.; Lanneau, D.; De Thonel, A.; Berthenet, K.; Hazoumé, A.; Droin, N.; Hamman, A.; Girodon, F.; Bellaye, P.S.; Wettstein, G.; Jacquel, A. Dual regulation of SPI1/PU.1 transcription factor by heat shock factor 1 (HSF1) during macrophage differentiation of monocytes. Leukemia, 2014, 28(8), 1676-1686.
[15]
Min, J.N.; Huang, L.; Zimonjic, D.B.; Moskophidis, D.; Mivechi, N.F. Selective suppression of lymphomas by functional loss of Hsf1 in a p53-deficient mouse model for spontaneous tumors. Oncogene, 2007, 26(35), 5086-5097.
[16]
Chuma, M.; Sakamoto, N.; Nakai, A.; Hige, S.; Nakanishi, M.; Natsuizaka, M.; Suda, G.; Sho, T.; Hatanaka, K.; Matsuno, Y.; Yokoo, H. Heat shock factor 1 accelerates hepatocellular carcinoma development by activating nuclear factor-kappaB/mitogen-activated protein kinase. Carcinogenesis, 2014, 35(2), 272-281.
[17]
Fang, F.; Chang, R.; Yang, L. Heat shock factor 1 promotes invasion and metastasis of hepatocellular carcinoma in vitro and in vivo. Cancer, 2012, 118(7), 1782-1794.
[18]
Jin, X.; Moskophidis, D.; Mivechi, N.F. Heat shock transcription factor 1 is a key determinant of HCC development by regulating hepatic steatosis and metabolic syndrome. Cell Metab., 2011, 14(1), 91-103.
[19]
Li, S.; Ma, W.; Fei, T.; Lou, Q.; Zhang, Y.; Cui, X.; Qin, X.; Zhang, J.; Liu, G.; Dong, Z.; Ma, Y. Upregulation of heat shock factor 1 transcription activity is associated with hepatocellular carcinoma progression. Mol. Med. Rep., 2014, 10(5), 2313-2321.
[20]
Zhang, N.; Wu, Y.; Lyu, X.; Li, B.; Yan, X.; Xiong, H.; Li, X.; Huang, G.; Zeng, Y.; Zhang, Y.; Lian, J. HSF1 upregulates ATG4B expression and enhances epirubicin-induced protective autophagy in hepatocellular carcinoma cells. Cancer Lett., 2017, 409, 81-90.
[21]
Ishiwata, J.; Kasamatsu, A.; Sakuma, K.; Iyoda, M.; Yamatoji, M.; Usukura, K.; Ishige, S.; Shimizu, T.; Yamano, Y.; Ogawara, K.; Shiiba, M. State of heat shock factor 1 expression as a putative diagnostic marker for oral squamous cell carcinoma. Int. J. Oncol., 2012, 40(1), 47-52.
[22]
Kim, S.A.; Kwon, S.M.; Yoon, J.H.; Ahn, S.G. The antitumor effect of PLK1 and HSF1 double knockdown on human oral carcinoma cells. Int. J. Oncol., 2010, 36(4), 867-872.
[23]
Tsukao, Y.; Yamasaki, M.; Miyazaki, Y.; Makino, T.; Takahashi, T.; Kurokawa, Y.; Miyata, H.; Nakajima, K.; Takiguchi, S.; Mimori, K.; Mori, M.; Doki, Y. Overexpression of heat-shock factor 1 is associated with a poor prognosis in esophageal squamous cell carcinoma. Oncol. Lett., 2017, 13(3), 1819-1825.
[24]
Kourtis, N.; Moubarak, R.S.; Aranda-Orgilles, B.; Lui, K.; Aydin, I.T.; Trimarchi, T.; Darvishian, F.; Salvaggio, C.; Zhong, J.; Bhatt, K.; Chen, E.I. FBXW7 modulates cellular stress response and metastatic potential through HSF1 post-translational modification. Nat. Cell Biol., 2015, 17(3), 322-332.
[25]
Nakamura, Y.; Fujimoto, M.; Hayashida, N.; Takii, R.; Nakai, A.; Muto, M. Silencing HSF1 by short hairpin RNA decreases cell proliferation and enhances sensitivity to hyperthermia in human melanoma cell lines. J. Dermatol. Sci., 2010, 60(3), 187-192.
[26]
Dudeja, V.; Chugh, R.K.; Sangwan, V.; Skube, S.J.; Mujumdar, N.R.; Antonoff, M.B.; Dawra, R.K.; Vickers, S.M.; Saluja, A.K. Prosurvival role of heat shock factor 1 in the pathogenesis of pancreatobiliary tumors. Am. J. Physiol. Gastrointest. Liver Physiol., 2011, 300(6), G948-G955.
[27]
Chen, K.; Qian, W.; Li, J.; Jiang, Z.; Cheng, L.; Yan, B.; Cao, J.; Sun, L.; Zhou, C.; Lei, M.; Duan, W. Loss of AMPK activation promotes the invasion and metastasis of pancreatic cancer through an HSF1-dependent pathway. Mol. Oncol., 2017, 11(10), 1475-1492.
[28]
Liang, W.; Liao, Y.; Zhang, J.; Huang, Q.; Luo, W.; Yu, J.; Gong, J.; Zhou, Y.; Li, X.; Tang, B.; He, S. Heat shock factor 1 inhibits the mitochondrial apoptosis pathway by regulating second mitochondria-derived activator of caspase to promote pancreatic tumorigenesis. J. Exp. Clin. Cancer Res., 2017, 36(1), 64.
[29]
Chen, Y.F.; Wang, S.Y.; Yang, Y.H.; Zheng, J.; Liu, T.; Wang, L. Targeting HSF1 leads to an antitumor effect in human epithelial ovarian cancer. Int. J. Mol. Med., 2017, 39(6), 1564-1570.
[30]
Engerud, H.; Tangen, I.L.; Berg, A.; Kusonmano, K.; Halle, M.K.; Øyan, A.M.; Kalland, K.H.; Stefansson, I.; Trovik, J.; Salvesen, H.B.; Krakstad, C. High level of HSF1 associates with aggressive endometrial carcinoma and suggests potential for HSP90 inhibitors. Br. J. Cancer, 2014, 111(1), 78-84.
[31]
Powell, C.D.; Paullin, T.R.; Aoisa, C.; Menzie, C.J.; Ubaldini, A.; Westerheide, S.D. The heat shock transcription factor HSF1 induces ovarian cancer epithelial-mesenchymal transition in a 3D spheroid growth model. PLoS One, 2016, 11(12), e0168389.
[32]
Yasuda, K.; Hirohashi, Y.; Mariya, T.; Murai, A.; Tabuchi, Y.; Kuroda, T.; Kusumoto, H.; Takaya, A.; Yamamoto, E.; Kubo, T.; Nakatsugawa, M. Phosphorylation of HSF1 at serine 326 residue is related to the maintenance of gynecologic cancer stem cells through expression of HSP27. Oncotarget, 2017, 8(19), 31540-31553.
[33]
Cui, J.; Tian, H.; Chen, G. Upregulation of nuclear heat shock factor 1 contributes to tumor angiogenesis and poor survival in patients with non-small cell lung cancer. Ann. Thorac. Surg., 2015, 100(2), 465-472.
[34]
Wu, P.S.; Chang, Y.H.; Pan, C.C. High expression of heat shock proteins and heat shock factor-1 distinguishes an aggressive subset of clear cell renal cell carcinoma. Histopathology, 2017, 71(5), 711-718.
[35]
Zhou, Z.; Li, Y.; Jia, Q.; Wang, Z.; Wang, X.; Hu, J.; Xiao, J. Heat shock transcription factor 1 promotes the proliferation, migration and invasion of osteosarcoma cells. Cell Prolif., 2017, 50(4), e12346.
[36]
Fujimoto, M.; Nakai, A. The heat shock factor family and adaptation to proteotoxic stress. FEBS J., 2010, 277(20), 4112-4125.
[37]
Fujimoto, M.; Izu, H.; Seki, K.; Fukuda, K.; Nishida, T.; Yamada, S.I.; Kato, K.; Yonemura, S.; Inouye, S.; Nakai, A. HSF4 is required for normal cell growth and differentiation during mouse lens development. EMBO J., 2004, 23(21), 4297-4306.
[38]
Fujimoto, M.; Oshima, K.; Shinkawa, T.; Wang, B.B.; Inouye, S.; Hayashida, N.; Takii, R.; Nakai, A. Analysis of HSF4 binding regions reveals its necessity for gene regulation during development and heat shock response in mouse lenses. J. Biol. Chem., 2008, 283(44), 29961-29970.
[39]
Tessari, A.; Salata, E.; Ferlin, A.; Bartoloni, L.; Slongo, M.L.; Foresta, C. Characterization of HSFY, a novel AZFb gene on the Y chromosome with a possible role in human spermatogenesis. Mol. Hum. Reprod., 2004, 10(4), 253-258.
[40]
Fujimoto, M.; Hayashida, N.; Katoh, T.; Oshima, K.; Shinkawa, T.; Prakasam, R.; Tan, K.; Inouye, S.; Takii, R.; Nakai, A. A novel mouse HSF3 has the potential to activate nonclassical heat-shock genes during heat shock. Mol. Biol. Cell, 2010, 21(1), 106-116.
[41]
Zhang, Y.; Koushik, S.; Dai, R.; Mivechi, N.F. Structural organization and promoter analysis of murine heat shock transcription factor-1 gene. J. Biol. Chem., 1998, 273(49), 32514-32521.
[42]
Gokmen-Polar, Y.; Badve, S. Upregulation of HSF1 in estrogen receptor positive breast cancer. Oncotarget, 2016, 7(51), 84239-84245.
[43]
Hu, Y.; Mivechi, N.F. HSF-1 interacts with Ral-binding protein 1 in a stress-responsive, multiprotein complex with HSP90 in vivo. J. Biol. Chem., 2003, 278(19), 17299-17306.
[44]
Neef, D.W.; Jaeger, A.M.; Gomez-Pastor, R.; Willmund, F.; Frydman, J.; Thiele, D.J. A direct regulatory interaction between chaperonin TRiC and stress-responsive transcription factor HSF1. Cell Reports, 2014, 9(3), 955-966.
[45]
Shi, Y.; Mosser, D.D.; Morimoto, R.I. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev., 1998, 12(5), 654-666.
[46]
Zou, J.; Guo, Y.; Guettouche, T.; Smith, D.F.; Voellmy, R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell, 1998, 94(4), 471-480.
[47]
Morimoto, R.I. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev., 1998, 12(24), 3788-3796.
[48]
Hentze, N.; Le Breton, L.; Wiesner, J.; Kempf, G.; Mayer, M.P. Molecular mechanism of thermosensory function of human heat shock transcription factor Hsf1. eLife, 2016, 5, e11576.
[49]
Rabindran, S.K.; Haroun, R.I.; Clos, J.; Wisniewski, J.; Wu, C. Regulation of heat shock factor trimer formation: Role of a conserved leucine zipper. Science, 1993, 259(5092), 230-234.
[50]
Westwood, J.T.; Clos, J.; Wu, C. Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature, 1991, 353(6347), 822-827.
[51]
Guettouche, T.; Boellmann, F.; Lane, W.S.; Voellmy, R. Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem., 2005, 6, 4.
[52]
Larson, J.S.; Schuetz, T.J.; Kingston, R.E. Activation in vitro of sequence-specific DNA binding by a human regulatory factor. Nature, 1988, 335(6188), 372-375.
[53]
Sorger, P.K.; Pelham, H.R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell, 1988, 54(6), 855-864.
[54]
Carpenter, R.L.; Sirkisoon, S.; Zhu, D.; Rimkus, T.; Harrison, A.; Anderson, A.; Paw, I.; Qasem, S.; Xing, F.; Liu, Y.; Chan, M. Combined inhibition of AKT and HSF1 suppresses breast cancer stem cells and tumor growth. Oncotarget, 2017, 8(43), 73947-73963.
[55]
Xi, C.; Hu, Y.; Buckhaults, P.; Moskophidis, D.; Mivechi, N.F. Heat shock factor HSF1 cooperates with ErbB2 (Her2/Neu) protein to promote mammary tumorigenesis and metastasis. J. Biol. Chem., 2012, 287(42), 35646-35657.
[56]
Khaleque, M.A.; Bharti, A.; Sawyer, D.; Gong, J.; Benjamin, I.J.; Stevenson, M.A.; Calderwood, S.K. Induction of heat shock proteins by heregulin beta1 leads to protection from apoptosis and anchorage-independent growth. Oncogene, 2005, 24(43), 6564-3573.
[57]
O’Callaghan-Sunol, C.; Sherman, M.Y. Heat shock transcription factor (HSF1) plays a critical role in cell migration via maintaining MAP kinase signaling. Cell Cycle, 2006, 5(13), 1431-1437.
[58]
Nakamura, Y.; Fujimoto, M.; Fukushima, S.; Nakamura, A.; Hayashida, N.; Takii, R.; Takaki, E.; Nakai, A.; Muto, M. Heat shock factor 1 is required for migration and invasion of human melanoma in vitro and in vivo. Cancer Lett., 2014, 354(2), 329-335.
[59]
Meng, L.; Gabai, V.L.; Sherman, M.Y. Heat-shock transcription factor HSF1 has a critical role in human epidermal growth factor receptor-2-induced cellular transformation and tumorigenesis. Oncogene, 2010, 29(37), 5204-5213.
[60]
Toma-Jonik, A.; Widlak, W.; Korfanty, J.; Cichon, T.; Smolarczyk, R.; Gogler-Piglowska, A.; Widlak, P.; Vydra, N. Active heat shock transcription factor 1 supports migration of the melanoma cells via vinculin down-regulation. Cell. Signal., 2015, 27(2), 394-401.
[61]
Carpenter, R.L.; Paw, I.; Dewhirst, M.W.; Lo, H.W. Akt phosphorylates and activates HSF-1 independent of heat shock, leading to Slug overexpression and epithelial-mesenchymal transition (EMT) of HER2-overexpressing breast cancer cells. Oncogene, 2015, 34(5), 546-557.
[62]
Ye, X.; Tam, W.L.; Shibue, T.; Kaygusuz, Y.; Reinhardt, F.; Eaton, E.N.; Weinberg, R.A. Distinct EMT programs control normal mammary stem cells and tumour-initiating cells. Nature, 2015, 525(7568), 256-260.
[63]
Chou, S.D.; Murshid, A.; Eguchi, T.; Gong, J.; Calderwood, S.K. HSF1 regulation of beta-catenin in mammary cancer cells through control of HuR/elavL1 expression. Oncogene, 2015, 34(17), 2178-2188.
[64]
Lee, J.H.; Lee, Y.K.; Lim, J.J.; Byun, H.O.; Park, I.; Kim, G.H.; Xu, W.G.; Wang, H.J.; Yoon, G. Mitochondrial respiratory dysfunction induces claudin-1 expression via reactive oxygen species-mediated heat shock factor 1 activation, leading to hepatoma cell invasiveness. J. Biol. Chem., 2015, 290(35), 21421-21431.
[65]
Li, Y.; Xu, D.; Bao, C.; Zhang, Y.; Chen, D.; Zhao, F.; Ding, J.; Liang, L.; Wang, Q.; Liu, L.; Li, J. MicroRNA-135b, a HSF1 target, promotes tumor invasion and metastasis by regulating RECK and EVI5 in hepatocellular carcinoma. Oncotarget, 2015, 6(4), 2421-2433.
[66]
Khaleque, M.A.; Bharti, A.; Gong, J.; Gray, P.J.; Sachdev, V.; Ciocca, D.R.; Stati, A.; Fanelli, M.; Calderwood, S.K. Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene, 2008, 27(13), 1886-1893.
[67]
Kim, E.H.; Lee, Y.J.; Bae, S.; Lee, J.S.; Kim, J.; Lee, Y.S. Heat shock factor 1-mediated aneuploidy requires a defective function of p53. Cancer Res., 2009, 69(24), 9404-9412.
[68]
Lee, Y.J. Lee, H.J.; Lee, J.S.; Jeoung, D.; Kang, C.M.; Bae, S.; Lee, S.J.; Kwon, S.H.; Kang, D.; Lee, Y.S. A novel function for HSF1-induced mitotic exit failure and genomic instability through direct interaction between HSF1 and Cdc20. Oncogene, 2008, 27(21), 2999-3009.
[69]
Tang, Z.; Dai, S.; He, Y.; Doty, R.A.; Shultz, L.D.; Sampson, S.B.; Dai, C. MEK guards proteome stability and inhibits tumor-suppressive amyloidogenesis via HSF1. Cell, 2015, 160(4), 729-744.
[70]
Wang, B.; Lee, C.W.; Witt, A.; Thakkar, A.; Ince, T.A. Heat shock factor 1 induces cancer stem cell phenotype in breast cancer cell lines. Breast Cancer Res. Treat., 2015, 153(1), 57-66.
[71]
Bradley, E.; Bieberich, E.; Mivechi, N.F.; Tangpisuthipongsa, D.; Wang, G. Regulation of embryonic stem cell pluripotency by heat shock protein 90. Stem Cells, 2012, 30(8), 1624-1633.
[72]
Lee, Y.J.; Kim, E.H.; Lee, J.S.; Jeoung, D.; Bae, S.; Kwon, S.H.; Lee, Y.S. HSF1 as a mitotic regulator: Phosphorylation of HSF1 by Plk1 is essential for mitotic progression. Cancer Res., 2008, 68(18), 7550-7560.
[73]
Yang, X.; Wang, J.; Liu, S.; Yan, Q. HSF1 and Sp1 regulate FUT4 gene expression and cell proliferation in breast cancer cells. J. Cell. Biochem., 2014, 115(1), 168-178.
[74]
Antonietti, P.; Linder, B.; Hehlgans, S.; Mildenberger, I.C.; Burger, M.C.; Fulda, S.; Steinbach, J.P.; Gessler, F.; Rödel, F.; Mittelbronn, M.; Kögel, D. Interference with the HSF1/HSP70/BAG3 pathway primes glioma cells to matrix detachment and BH3 Mimetic-Induced Apoptosis. Mol. Cancer Ther., 2017, 16(1), 156-168.
[75]
Jacobs, A.T.; Marnett, L.J. Heat shock factor 1 attenuates 4-Hydroxynonenal-mediated apoptosis: critical role for heat shock protein 70 induction and stabilization of Bcl-XL. J. Biol. Chem., 2007, 282(46), 33412-33420.
[76]
Jacobs, A.T.; Marnett, L.J. HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. J. Biol. Chem., 2009, 284(14), 9176-9183.
[77]
Wang, J.; He, H.; Yu, L.; Xia, H.H.X.; Lin, M.C.; Gu, Q.; Li, M.; Zou, B.; An, X.; Jiang, B.; Kung, H.F. HSF1 down-regulates XAF1 through transcriptional regulation. J. Biol. Chem., 2006, 281(5), 2451-2459.
[78]
Desai, S.; Liu, Z.; Yao, J.; Patel, N.; Chen, J.; Wu, Y.; Ahn, E.E.Y.; Fodstad, O.; Tan, M. Heat shock factor 1 (HSF1) controls chemoresistance and autophagy through transcriptional regulation of autophagy-related protein 7 (ATG7). J. Biol. Chem., 2013, 288(13), 9165-9176.
[79]
Luo, T.; Fu, J.; Xu, A.; Su, B.; Ren, Y.; Li, N.; Zhu, J.; Zhao, X.; Dai, R.; Cao, J.; Wang, B. PSMD10/gankyrin induces autophagy to promote tumor progression through cytoplasmic interaction with ATG7 and nuclear transactivation of ATG7 expression. Autophagy, 2016, 12(8), 1355-1371.
[80]
Luan, Q.; Jin, L.; Jiang, C.C.; Tay, K.H.; Lai, F.; Liu, X.Y.; Liu, Y.L.; Guo, S.T.; Li, C.Y.; Yan, X.G.; Tseng, H.Y. RIPK1 regulates survival of human melanoma cells upon endoplasmic reticulum stress through autophagy. Autophagy, 2015, 11(7), 975-994.
[81]
Zhang, X. Expression, correlation and prognostic significance of CD133, P57 and HSF1 in meningioma. Eur. Rev. Med. Pharmacol. Sci., 2017, 21(20), 4600-4605.
[82]
Asgari, Y.; Zabihinpour, Z.; Salehzadeh-Yazdi, A.; Schreiber, F.; Masoudi-Nejad, A. Alterations in cancer cell metabolism: The Warburg effect and metabolic adaptation. Genomics, 2015, 105(5-6), 275-281.
[83]
Santagata, S.; Mendillo, M.L.; Tang, Y.C.; Subramanian, A.; Perley, C.C.; Roche, S.P.; Wong, B.; Narayan, R.; Kwon, H.; Koeva, M.; Amon, A. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science, 2013, 341(6143), 1238303.
[84]
Cigliano, A.; Wang, C.; Pilo, M.G.; Szydlowska, M.; Brozzetti, S.; Latte, G.; Pes, G.M.; Pascale, R.M.; Seddaiu, M.A.; Vidili, G.; Ribback, S. Inhibition of HSF1 suppresses the growth of hepatocarcinoma cell lines in vitro and AKT-driven hepatocarcinogenesis in mice. Oncotarget, 2017, 8(33), 54149-54159.
[85]
Zhao, Y.H.; Zhou, M.; Liu, H.; Ding, Y.; Khong, H.T.; Yu, D.; Fodstad, O.; Tan, M. Upregulation of lactate dehydrogenase A by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene, 2009, 28(42), 3689-3701.
[86]
Ma, W.; Zhang, Y.; Mu, H.; Qing, X.; Li, S.; Cui, X.; Lou, Q.; Ma, Y.; Pu, H.; Hu, Y. Glucose regulates heat shock factor 1 transcription activity via mTOR pathway in HCC cell lines. Cell Biol. Int., 2015, 39(11), 1217-1224.
[87]
Dai, S.; Tang, Z.; Cao, J.; Zhou, W.; Li, H.; Sampson, S.; Dai, C. Suppression of the HSF1-mediated proteotoxic stress response by the metabolic stress sensor AMPK. EMBO J., 2015, 34(3), 275-293.
[88]
Minsky, N.; Roeder, R.G. Direct link between metabolic regulation and the heat-shock response through the transcriptional regulator PGC-1alpha. Proc. Natl. Acad. Sci. USA, 2015, 112(42), E5669-E5678.
[89]
Wu, Z.; Puigserver, P.; Andersson, U.; Zhang, C.; Adelmant, G.; Mootha, V.; Troy, A.; Cinti, S.; Lowell, B.; Scarpulla, R.C.; Spiegelman, B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell, 1999, 98(1), 115-124.
[90]
Wan, T.; Shao, J.; Hu, B.; Liu, G.; Luo, P.; Zhou, Y. Prognostic role of HSF1 overexpression in solid tumors: A pooled analysis of 3,159 patients. OncoTargets Ther., 2018, 11, 383-393.
[91]
Liao, Y.; Xue, Y.; Zhang, L.; Feng, X.; Liu, W.; Zhang, G. Higher heat shock factor 1 expression in tumor stroma predicts poor prognosis in esophageal squamous cell carcinoma patients. J. Transl. Med., 2015, 13, 338.
[92]
Baler, R.; Dahl, G.; Voellmy, R. Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol., 1993, 13(4), 2486-2496.
[93]
Mercier, P.A.; Foksa, J.; Ovsenek, N.; Westwood, J.T. Xenopus heat shock factor 1 is a nuclear protein before heat stress. J. Biol. Chem., 1997, 272(22), 14147-14151.
[94]
Mercier, P.A.; Winegarden, N.A.; Westwood, J.T. Human heat shock factor 1 is predominantly a nuclear protein before and after heat stress. J. Cell Sci., 1999, 112(Pt 16), 2765-2774.
[95]
Wang, Y.; Theriault, J.R.; He, H.; Gong, J.; Calderwood, S.K. Expression of a dominant negative heat shock factor-1 construct inhibits aneuploidy in prostate carcinoma cells. J. Biol. Chem., 2004, 279(31), 32651-32659.
[96]
Im, C.N.; Yun, H.; Lee, J.H. Heat shock factor 1 depletion sensitizes A172 glioblastoma cells to temozolomide via suppression of cancer stem cell-like properties. Int. J. Mol. Sci., 2017, 18(2), 468.
[97]
Yokota, S.; Kitahara, M.; Nagata, K. Benzylidene lactam compound, KNK437, a novel inhibitor of acquisition of thermotolerance and heat shock protein induction in human colon carcinoma cells. Cancer Res., 2000, 60(11), 2942-2948.
[98]
Bustany, S.; Cahu, J.; Descamps, G.; Pellat-Deceunynck, C.; Sola, B. Heat shock factor 1 is a potent therapeutic target for enhancing the efficacy of treatments for multiple myeloma with adverse prognosis. J. Hematol. Oncol., 2015, 8, 40.
[99]
Lee, C.H.; Hong, H.M.; Chang, Y.Y.; Chang, W.W. Inhibition of heat shock protein (Hsp) 27 potentiates the suppressive effect of Hsp90 inhibitors in targeting breast cancer stem-like cells. Biochimie, 2012, 94(6), 1382-1389.
[100]
Taba, K.; Kuramitsu, Y.; Ryozawa, S.; Yoshida, K.; Tanaka, T.; Mori-Iwamoto, S.; Maehara, S.I.; Maehara, Y.; Sakaida, I.; Nakamura, K. KNK437 downregulates heat shock protein 27 of pancreatic cancer cells and enhances the cytotoxic effect of gemcitabine. Chemotherapy, 2011, 57(1), 12-16.
[101]
Koishi, M.; Yokota, S.I.; Mae, T.; Nishimura, Y.; Kanamori, S.; Horii, N.; Shibuya, K.; Sasai, K.; Hiraoka, M. The effects of KNK437, a novel inhibitor of heat shock protein synthesis, on the acquisition of thermotolerance in a murine transplantable tumor in vivo. Clin. Cancer Res., 2001, 7(1), 215-219.
[102]
Oommen, D.; Prise, K.M. KNK437, abrogates hypoxia-induced radioresistance by dual targeting of the AKT and HIF-1alpha survival pathways. Biochem. Biophys. Res. Commun., 2012, 421(3), 538-543.
[103]
Au, Q.; Zhang, Y.; Barber, J.R.; Ng, S.C.; Zhang, B. Identification of inhibitors of HSF1 functional activity by high-content target-based screening. J. Biomol. Screen., 2009, 14(10), 1165-1175.
[104]
Yoon, Y.J.; Kim, J.A.; Shin, K.D.; Shin, D.S.; Han, Y.M.; Lee, Y.J.; Lee, J.S.; Kwon, B.M.; Han, D.C. KRIBB11 inhibits HSP70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. J. Biol. Chem., 2011, 286(3), 1737-1747.
[105]
Fok, J.H.; Hedayat, S.; Zhang, L.; Aronson, L.I.; Mirabella, F.; Pawlyn, C.; Bright, M.D.; Wardell, C.P.; Keats, J.J.; De Billy, E.; Rye, C.S. HSF1 is essential for myeloma cell survival and a promising therapeutic target. Clin. Cancer Res., 2018, 24(10), 2395-2407.
[106]
Kang, M.J.; Yun, H.H.; Lee, J.H. KRIBB11 accelerates Mcl-1 degradation through an HSF1-independent, Mule-dependent pathway in A549 non-small cell lung cancer cells. Biochem. Biophys. Res. Commun., 2017, 492(3), 304-309.
[107]
Chen, Y.F.; Dong, Z.; Xia, Y.; Tang, J.; Peng, L.; Wang, S.; Lai, D. Nucleoside analog inhibits microRNA-214 through targeting heat-shock factor 1 in human epithelial ovarian cancer. Cancer Sci., 2013, 104(12), 1683-1689.
[108]
Xia, Y.; Liu, Y.; Rocchi, P.; Wang, M.; Fan, Y.; Qu, F.; Iovanna, J.L.; Peng, L. Targeting heat shock factor 1 with a triazole nucleoside analog to elicit potent anticancer activity on drug-resistant pancreatic cancer. Cancer Lett., 2012, 318(2), 145-153.
[109]
Cano, C.E.; Hamidi, T.; Garcia, M.N.; Grasso, D.; Loncle, C.; Garcia, S.; Calvo, E.; Lomberk, G.; Dusetti, N.; Bartholin, L.; Urrutia, R. Genetic inactivation of Nupr1 acts as a dominant suppressor event in a two-hit model of pancreatic carcinogenesis. Gut, 2014, 63(6), 984-995.
[110]
Agarwal, T.; Annamalai, N.; Khursheed, A.; Maiti, T.K.; Arsad, H.B.; Siddiqui, M.H. Molecular docking and dynamic simulation evaluation of Rohinitib - Cantharidin based novel HSF1 inhibitors for cancer therapy. J. Mol. Graph. Model., 2015, 61, 141-149.
[111]
Zhang, D.; Zhang, B. Selective killing of cancer cells by small molecules targeting heat shock stress response. Biochem. Biophys. Res. Commun., 2016, 478(4), 1509-1514.
[112]
Cheeseman, M.D.; Chessum, N.E.; Rye, C.S.; Pasqua, A.E.; Tucker, M.J.; Wilding, B.; Evans, L.E.; Lepri, S.; Richards, M.; Sharp, S.Y.; Ali, S. Discovery of a chemical probe bisamide (CCT251236): An orally bioavailable efficacious pirin ligand from a heat shock transcription factor 1 (HSF1) phenotypic screen. J. Med. Chem., 2017, 60(1), 180-201.
[113]
Vilaboa, N.; Boré, A.; Martin-Saavedra, F.; Bayford, M.; Winfield, N.; Firth-Clark, S.; Kirton, S.B.; Voellmy, R. New inhibitor targeting human transcription factor HSF1: Effects on the heat shock response and tumor cell survival. Nucleic Acids Res., 2017, 45(10), 5797-5817.
[114]
Salamanca, H.H.; Antonyak, M.A.; Cerione, R.A.; Shi, H.; Lis, J.T. Inhibiting heat shock factor 1 in human cancer cells with a potent RNA aptamer. PLoS One, 2014, 9(5), e96330.
[115]
Salamanca, H.H.; Fuda, N.; Shi, H.; Lis, J.T. An RNA aptamer perturbs heat shock transcription factor activity in Drosophila melanogaster. Nucleic Acids Res., 2011, 39(15), 6729-6740.
[116]
Wang, S.; Zhao, X.; Suran, R.; Vogt, V.M.; Lis, J.T.; Shi, H. Knocking down gene function with an RNA aptamer expressed as part of an intron. Nucleic Acids Res., 2010, 38(15), e154.
[117]
Zhao, X.; Shi, H.; Sevilimedu, A.; Liachko, N.; Nelson, H.C.; Lis, J.T. An RNA aptamer that interferes with the DNA binding of the HSF transcription activator. Nucleic Acids Res., 2006, 34(13), 3755-3761.
[118]
Nagai, N.; Nakai, A.; Nagata, K. Quercetin suppresses heat shock response by down regulation of HSF1. Biochem. Biophys. Res. Commun., 1995, 208(3), 1099-1105.
[119]
Westerheide, S.D.; Kawahara, T.L.; Orton, K.; Morimoto, R.I. Triptolide, an inhibitor of the human heat shock response that enhances stress-induced cell death. J. Biol. Chem., 2006, 281(14), 9616-9622.
[120]
Li, X.J.; Jiang, Z.Z.; Zhang, L.Y. Triptolide: Progress on research in pharmacodynamics and toxicology. J. Ethnopharmacol., 2014, 155(1), 67-79.
[121]
Fujimoto, M.; Takii, R.; Takaki, E.; Katiyar, A.; Nakato, R.; Shirahige, K.; Nakai, A. The HSF1-PARP13-PARP1 complex facilitates DNA repair and promotes mammary tumorigenesis. Nat. Commun., 2017, 8(1), 1638.
[122]
Gabai, V.L.; Meng, L.; Kim, G.; Mills, T.A.; Benjamin, I.J.; Sherman, M.Y. 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., 2012, 32(5), 929-940.
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