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No specific antiviral drug is available in the clinic against these flavivirus infections. Heat-shock protein 70 (HSP70) has recently been proven to be a promising antiviral target against Zika virus and Dengue virus. Here, we report that Apoptozole, a small molecule inhibitor of ATPase activity of HSP70, has broad-spectrum anti-flavivirus potential. The mode of action analysis revealed that Apoptozole acted at the post-entry step. Transcriptome analysis revealed that genes related to cholesterol metabolism, fatty acid synthesis, and innate immunity were differentially expressed after treatment with Apoptozole. In vivo data suggested Apoptozole exerted protection effects against Zika virus (ZIKV) infection in a mouse model by enhancing the innate immune response, which suggested a novel anti-ZIKV mechanism of HSP70 inhibitors.<\/jats:p>","DOI":"10.1021\/acsinfecdis.9b00376","type":"journal-article","created":{"date-parts":[[2020,1,22]],"date-time":"2020-01-22T14:56:45Z","timestamp":1579705005000},"page":"832-843","source":"Crossref","is-referenced-by-count":40,"title":["Small Molecule Inhibitor of ATPase Activity of HSP70\nas a Broad-Spectrum Inhibitor against Flavivirus Infections"],"prefix":"10.1021","volume":"6","author":[{"given":"Jingjing","family":"Yang","sequence":"first","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongfen","family":"Xu","sequence":"additional","affiliation":[{"name":"Institut Pasteur of Shanghai, Chinese Academy of Sciences , , ,","place":["Shanghai, China, 200031"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunzheng","family":"Yan","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Li","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Zhao","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingsong","family":"Dai","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuexiang","family":"Li","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Song","family":"Li","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Zhong","sequence":"additional","affiliation":[{"name":"Institut Pasteur of Shanghai, Chinese Academy of Sciences , , ,","place":["Shanghai, China, 200031"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruiyuan","family":"Cao","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0536-620X","authenticated-orcid":true,"given":"Wu","family":"Zhong","sequence":"additional","affiliation":[{"name":"Beijing Institute of Pharmacology and Toxicology , , ,","place":["Beijing, China, 100850"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,1,22]]},"reference":[{"issue":"6","key":"2026081806122948900_cit1","doi-asserted-by":"publisher","first-page":"e12744","DOI":"10.1111\/cmi.12744","article-title":"Zika\ninfection and the development of neurological defects","volume":"19","author":"Russo","year":"2017","journal-title":"Cellular microbiology"},{"key":"2026081806122948900_cit2","doi-asserted-by":"publisher","first-page":"593","DOI":"10.3389\/fimmu.2018.00593","article-title":"A New In Vivo Model to Study Protective\nImmunity to Zika Virus Infection in Mice With Intact Type I Interferon\nSignaling","volume":"9","author":"Nazerai","year":"2018","journal-title":"Front. Immunol."},{"issue":"7446","key":"2026081806122948900_cit3","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1038\/nature12060","article-title":"The global distribution and burden\nof dengue","volume":"496","author":"Bhatt","year":"2013","journal-title":"Nature"},{"issue":"9966","key":"2026081806122948900_cit4","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1016\/S0140-6736(14)60572-9","article-title":"Dengue","volume":"385","author":"Guzman","year":"2015","journal-title":"Lancet"},{"issue":"10","key":"2026081806122948900_cit5","doi-asserted-by":"publisher","first-page":"766","DOI":"10.2471\/BLT.10.085233","article-title":"Estimated\nglobal incidence of Japanese encephalitis: a systematic review","volume":"89","author":"Campbell","year":"2011","journal-title":"Bulletin of the World Health Organization"},{"issue":"6405","key":"2026081806122948900_cit6","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1126\/science.aau8225","article-title":"The reemergence of yellow fever","volume":"361","author":"Barrett","year":"2018","journal-title":"Science"},{"key":"2026081806122948900_cit7","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/j.antiviral.2016.03.017","article-title":"An inducible heat\nshock protein 70 small molecule inhibitor demonstrates anti-dengue\nvirus activity, validating Hsp70 as a host antiviral target","volume":"130","author":"Howe","year":"2016","journal-title":"Antiviral Res."},{"issue":"3","key":"2026081806122948900_cit8","doi-asserted-by":"publisher","first-page":"404","DOI":"10.2174\/138161213804143699","article-title":"Hsp70 Protein Complexes as Drug Targets","volume":"19","author":"Assimon","year":"2013","journal-title":"Curr. Pharm. Des."},{"issue":"5","key":"2026081806122948900_cit9","doi-asserted-by":"publisher","first-page":"1108","DOI":"10.1016\/j.cell.2015.10.046","article-title":"Defining Hsp70 Subnetworks\nin Dengue Virus Replication Reveals Key Vulnerability in Flavivirus\nInfection","volume":"163","author":"Taguwa","year":"2015","journal-title":"Cell"},{"issue":"4","key":"2026081806122948900_cit10","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1016\/j.celrep.2018.12.095","article-title":"Zika Virus Dependence on Host Hsp70\nProvides a Protective Strategy against Infection and Disease","volume":"26","author":"Taguwa","year":"2019","journal-title":"Cell Rep."},{"issue":"1","key":"2026081806122948900_cit11","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1080\/22221751.2018.1557988","article-title":"Heat shock protein 70 (Hsp70) mediates Zika virus entry,\nreplication, and egress from host cells","volume":"8","author":"Pujhari","year":"2019","journal-title":"Emerging\nMicrobes Infect."},{"issue":"6","key":"2026081806122948900_cit12","doi-asserted-by":"publisher","first-page":"e02274-16","DOI":"10.1128\/JVI.02274-16","article-title":"GRP78 Is an Important Host Factor for Japanese Encephalitis Virus\nEntry and Replication in Mammalian Cells","volume":"91","author":"Nain","year":"2017","journal-title":"J.\nVirol."},{"issue":"Pt 4","key":"2026081806122948900_cit13","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1099\/jgv.0.000015","article-title":"Heat shock\ncognate protein 70 isoform D is required for clathrin-dependent endocytosis\nof Japanese encephalitis virus in C6\/36 cells","volume":"96","author":"Chuang","year":"2015","journal-title":"J. Gen. Virol."},{"issue":"9","key":"2026081806122948900_cit14","doi-asserted-by":"publisher","first-page":"e75188","DOI":"10.1371\/journal.pone.0075188","article-title":"Heat shock protein 70 is associated with replicase complex of Japanese\nencephalitis virus and positively regulates viral genome replication","volume":"8","author":"Ye","year":"2013","journal-title":"PLoS One"},{"issue":"6","key":"2026081806122948900_cit15","doi-asserted-by":"publisher","first-page":"3212","DOI":"10.1128\/JVI.03077-15","article-title":"Chaperone-Assisted\nProtein Folding Is Critical for Yellow Fever Virus NS3\/4A Cleavage\nand Replication","volume":"90","author":"Bozzacco","year":"2016","journal-title":"J. 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Rep."},{"issue":"5","key":"2026081806122948900_cit24","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1016\/0035-9203(52)90042-4","article-title":"Zika Virus\n(I). Isolations and serological specificity","volume":"46","author":"Dick","year":"1952","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"issue":"2","key":"2026081806122948900_cit25","doi-asserted-by":"publisher","first-page":"263","DOI":"10.4161\/hv.26902","article-title":"Japanese encephalitis:\nthe virus and vaccines","volume":"10","author":"Yun","year":"2014","journal-title":"Hum. Vaccines Immunother."},{"key":"2026081806122948900_cit26","doi-asserted-by":"publisher","first-page":"2463","DOI":"10.1360\/N972016-00665","article-title":"Genetic and Biological Characterization for Zika Viruses Imported\nthrough Shenzhen Port","volume":"61","author":"Wang","year":"2016","journal-title":"Chin. Sci. Bull."},{"issue":"14","key":"2026081806122948900_cit27","doi-asserted-by":"publisher","first-page":"11979","DOI":"10.1074\/jbc.M210914200","article-title":"Inhibition\nof Hepatitis C Virus RNA Replication by 2\u2032-Modified Nucleoside\nAnalogs","volume":"278","author":"Carroll","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2026081806122948900_cit28","doi-asserted-by":"publisher","first-page":"6605","DOI":"10.2147\/OTT.S155930","article-title":"Asparagine\nsynthetase expression is associated with the sensitivity to asparaginase\nin extranodal natural killer\/T-cell lymphoma in vivo and in vitro","volume":"11","author":"Liu","year":"2018","journal-title":"OncoTargets Ther."},{"issue":"3","key":"2026081806122948900_cit29","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1002\/2211-5463.12373","article-title":"ULBP1 is induced by hepatitis C virus infection and is the target\nof the NK cell-mediated innate immune response in human hepatocytes","volume":"8","author":"Dansako","year":"2018","journal-title":"FEBS Open Bio"},{"key":"2026081806122948900_cit30","doi-asserted-by":"publisher","first-page":"388","DOI":"10.3389\/fcimb.2018.00388","article-title":"The Role of Host Cholesterol During\nFlavivirus Infection","volume":"8","author":"Osuna-Ramos","year":"2018","journal-title":"Front. Cell. Infect. Microbiol."},{"issue":"12","key":"2026081806122948900_cit31","doi-asserted-by":"publisher","first-page":"6793","DOI":"10.1128\/JVI.00045-14","article-title":"Rab18 facilitates dengue virus infection by targeting\nfatty acid synthase to sites of viral replication","volume":"88","author":"Tang","year":"2014","journal-title":"J. Virol."},{"issue":"1","key":"2026081806122948900_cit32","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1186\/s12985-017-0685-9","article-title":"Involvement of fatty acid synthase in dengue virus\ninfection","volume":"14","author":"Tongluan","year":"2017","journal-title":"Virol. J."},{"issue":"1\u20132","key":"2026081806122948900_cit33","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.virol.2009.03.025","article-title":"Cholesterol biosynthesis\nmodulation regulates dengue viral replication","volume":"389","author":"Rothwell","year":"2009","journal-title":"Virology"},{"issue":"4","key":"2026081806122948900_cit34","doi-asserted-by":"publisher","first-page":"2920","DOI":"10.1002\/jcp.26040","article-title":"PCSK9 and infection: A potentially\nuseful or dangerous association?","volume":"233","author":"Khademi","year":"2018","journal-title":"J. Cell. Physiol."},{"issue":"9","key":"2026081806122948900_cit35","doi-asserted-by":"publisher","first-page":"2330","DOI":"10.1002\/jcp.25767","article-title":"PCSK9 at the\ncrossroad of cholesterol metabolism and immune function during infections","volume":"232","author":"Paciullo","year":"2017","journal-title":"J. Cell. Physiol."},{"key":"2026081806122948900_cit36","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.antiviral.2019.03.002","article-title":"Stearoyl-CoA desaturase-1 is required for flavivirus\nRNA replication","volume":"165","author":"Hishiki","year":"2019","journal-title":"Antiviral Res."},{"issue":"5","key":"2026081806122948900_cit37","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1210\/me.2008-0412","article-title":"FSH and\nFOXO1 regulate genes in the sterol\/steroid and lipid biosynthetic\npathways in granulosa cells","volume":"23","author":"Liu","year":"2009","journal-title":"Mol. Endocrinol."},{"issue":"4","key":"2026081806122948900_cit38","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1080\/09168451.2018.1559719","article-title":"RNA-Seq analysis reveals\na negative role of MSMO1 with a synergized NSDHL expression during\nadipogenesis of 3T3-L1","volume":"83","author":"Xin","year":"2019","journal-title":"Biosci., Biotechnol.,\nBiochem."},{"issue":"3","key":"2026081806122948900_cit39","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1016\/j.immuni.2017.02.012","article-title":"25-Hydroxycholesterol\nProtects Host against Zika Virus Infection and Its Associated Microcephaly\nin a Mouse Model","volume":"46","author":"Li","year":"2017","journal-title":"Immunity"},{"issue":"6","key":"2026081806122948900_cit40","doi-asserted-by":"publisher","first-page":"1362","DOI":"10.4269\/ajtmh.16-0111","article-title":"Characterization\nof a Novel Murine Model to Study Zika Virus","volume":"94","author":"Rossi","year":"2016","journal-title":"Am. J. Trop. Med. Hyg."},{"issue":"8","key":"2026081806122948900_cit41","doi-asserted-by":"publisher","first-page":"e1007261","DOI":"10.1371\/journal.ppat.1007261","article-title":"Stearoly-CoA desaturase\n1 differentiates early and advanced dengue virus infections and determines\nvirus particle infectivity","volume":"14","author":"Gullberg","year":"2018","journal-title":"PLoS Pathog."},{"issue":"Pt 9","key":"2026081806122948900_cit42","doi-asserted-by":"publisher","first-page":"1900","DOI":"10.1099\/vir.0.065300-0","article-title":"Hepatitis C virus infection mediates\ncholesteryl ester synthesis to facilitate infectious particle production","volume":"95","author":"Read","year":"2014","journal-title":"J. Gen. Virol."},{"issue":"3","key":"2026081806122948900_cit43","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1097\/01.shk.0000223134.17877.ad","article-title":"The inhibition of LPS-induced production of inflammatory cytokines\nby HSP70 involves inactivation of the NF-kappaB pathway but not the\nMAPK pathways","volume":"26","author":"Shi","year":"2006","journal-title":"Shock"},{"key":"2026081806122948900_cit44","doi-asserted-by":"publisher","first-page":"7478","DOI":"10.1038\/sj.onc.1204948","article-title":"Selective depletion of inducible\nHSP70 enhances immunogenicity of rat colon cancer cells","volume":"20","author":"Gurbuxani","year":"2001","journal-title":"Oncogene"},{"issue":"17","key":"2026081806122948900_cit45","doi-asserted-by":"publisher","first-page":"7942","DOI":"10.1158\/0008-5472.CAN-05-0377","article-title":"Chaperon and adjuvant activity of\nhsp70: different natural killer requirement for cross-priming of chaperoned\nand bystander antigens","volume":"65","author":"Massa","year":"2005","journal-title":"Cancer Res."},{"key":"2026081806122948900_cit46","doi-asserted-by":"publisher","first-page":"17642","DOI":"10.1038\/srep17642","article-title":"A small molecule inhibitor for ATPase activity of Hsp70 and Hsc70\nenhances the immune response to protein antigens","volume":"5","author":"Baek","year":"2015","journal-title":"Sci. Rep."},{"issue":"7","key":"2026081806122948900_cit47","doi-asserted-by":"publisher","first-page":"1716","DOI":"10.1016\/j.cell.2015.11.045","article-title":"Limiting cholesterol biosynthetic flux spontaneously\nengages type I IFN signaling","volume":"163","author":"York","year":"2015","journal-title":"Cell"},{"key":"2026081806122948900_cit48","doi-asserted-by":"publisher","first-page":"7377","DOI":"10.1038\/s41598-017-07620-y","article-title":"Highly Sensitive, Engineered\nMagnetic Nanosensors to Investigate the Ambiguous Activity of Zika\nVirus and Binding Receptors","volume":"7","author":"Shelby","year":"2017","journal-title":"Sci. Rep."},{"key":"2026081806122948900_cit49","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.antiviral.2017.12.017","article-title":"Development of a replicon cell line-based high throughput antiviral\nassay for screening inhibitors of Zika virus","volume":"150","author":"Li","year":"2018","journal-title":"Antiviral Res."}],"container-title":["ACS Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acsinfecdis.9b00376","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article-pdf\/6\/5\/832\/12725164\/id9b00376.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article-pdf\/6\/5\/832\/12725164\/id9b00376.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T10:53:39Z","timestamp":1787050419000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article\/6\/5\/832\/1292702\/Small-Molecule-Inhibitor-of-ATPase-Activity-of"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,22]]},"references-count":49,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,1,22]]},"published-print":{"date-parts":[[2020,5,8]]}},"URL":"https:\/\/doi.org\/10.1021\/acsinfecdis.9b00376","relation":{},"ISSN":["2373-8227"],"issn-type":[{"value":"2373-8227","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,22]]}}}