HCMV miR-UL70-3p downregulates the rapamycin-induced autophagy by targeting the autophagy-related protein 9A (ATG9A)

References

• Dunn W, Chou C, Li H, et al. Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci USA. 2003;100(24):14223–14228. doi:10.1073/pnas.2334032100.
   PubMed Web of Science ®Google Scholar
• Griffiths P, Reeves M. Pathogenesis of human cytomegalovirus in the immunocompromised host. Nat Rev Microbiol. 2021;19(12):759–773. doi:10.1038/s41579-021-00582-z.
   PubMed Web of Science ®Google Scholar
• Revello MG, Gerna G. Diagnosis and management of human cytomegalovirus infection in the mother, fetus, and newborn infant. Clin Microbiol Rev. 2002; 15(4):680–715. doi:10.1128/CMR.15.4.680-715.2002.
   PubMed Web of Science ®Google Scholar
• McGeoch DJ, Cook S, Dolan A, et al. Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J Mol Biol. 1995; 247(3):443–458. doi:10.1006/jmbi.1995.0152.
   PubMed Web of Science ®Google Scholar
• Chaumorcel M, Lussignol M, Mouna L, et al. The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. J Virol. 2012; 86(5):2571–2584. doi:10.1128/JVI.05746-11.
   PubMed Web of Science ®Google Scholar
• Diggins NL, Hancock MH. HCMV miRNA targets reveal important cellular pathways for viral replication, latency, and reactivation. Noncoding RNA. 2018; 4(4):29. doi:10.3390/ncrna4040029.
   PubMedGoogle Scholar
• Fan J, Zhang W, Liu Q. Human cytomegalovirus-encoded miR-US25-1 aggravates the oxidised low density lipoprotein-induced apoptosis of endothelial cells. Biomed Res Int. 2014;2014:531979–531913. doi:10.1155/2014/531979.
   PubMed Web of Science ®Google Scholar
• Guo X, Huang Y, Qi Y, et al. Human cytomegalovirus miR-UL36-5p inhibits apoptosis via downregulation of adenine nucleotide translocator 3 in cultured cells. Arch Virol. 2015;160(10):2483–2490. doi:10.1007/s00705-015-2498-8.
   PubMed Web of Science ®Google Scholar
• Kim S, Lee S, Shin J, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 2011;12(10):984–991. doi:10.1038/ni.2097.
   PubMed Web of Science ®Google Scholar
• Kim S, Seo D, Kim D, et al. Temporal landscape of microRNA-mediated host-virus crosstalk during productive human cytomegalovirus infection. Cell Host Microbe. 2015; 17(6):838–851. doi:10.1016/j.chom.2015.05.014.
   PubMed Web of Science ®Google Scholar
• Shao Y, Qi Y, Huang Y, et al. Human cytomegalovirus miR-US4-5p promotes apoptosis via downregulation of p21-activated kinase 2 in cultured cells. Mol Med Rep. 2017;16(4):4171–4178. doi:10.3892/mmr.2017.7108.
   PubMed Web of Science ®Google Scholar
• Wang Y-P, Qi Y, Huang Y-J, et al. Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int J Mol Med. 2013;31(4):959–966. doi:10.3892/ijmm.2013.1271.
   PubMed Web of Science ®Google Scholar
• Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13(10):722–737. doi:10.1038/nri3532.
   PubMed Web of Science ®Google Scholar
• Richetta C, Faure M. Autophagy in antiviral innate immunity. Cell Microbiol. 2013;15(3):368–376. doi:10.1111/cmi.12043.
   PubMed Web of Science ®Google Scholar
• Lussignol M, Esclatine A. Herpesvirus and autophagy:“All right, everybody be cool, this is a robbery. !Viruses. 2017;9(12):372. doi:10.3390/v9120372.
   PubMed Web of Science ®Google Scholar
• McFarlane S, Aitken J, Sutherland JS, et al. Early induction of autophagy in human fibroblasts after infection with human cytomegalovirus or herpes simplex virus 1. J Virol. 2011;85(9):4212–4221. doi:10.1128/JVI.02435-10.
   PubMed Web of Science ®Google Scholar
• Mouna L, Hernandez E, Bonte D, et al. Analysis of the role of autophagy inhibition by two complementary human cytomegalovirus BECN1/Beclin 1-binding proteins. Autophagy. 2016;12(2):327–342. doi:10.1080/15548627.2015.1125071.
   PubMed Web of Science ®Google Scholar
• Chaumorcel M, Souquère S, Pierron G, et al. Human cytomegalovirus controls a new autophagy-dependent cellular antiviral defense mechanism. Autophagy. 2008;4(1):46–53. doi:10.4161/auto.5184.
   PubMed Web of Science ®Google Scholar
• Pfeffer S, Sewer A, Lagos-Quintana M, et al. Identification of microRNAs of the herpesvirus family. Nat Methods. 2005;2(4):269–276. doi:10.1038/nmeth746.
   PubMed Web of Science ®Google Scholar
• Grey F, Antoniewicz A, Allen E, et al. Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol. 2005;79(18):12095–12099. doi:10.1128/JVI.79.18.12095-12099.2005.
   PubMed Web of Science ®Google Scholar
• Babu SG, Pandeya A, Verma N, et al. Role of HCMV miR-UL70-3p and miR-UL148D in overcoming the cellular apoptosis. Mol Cell Biochem. 2014;393(1-2):89–98. doi:10.1007/s11010-014-2049-8.
   PubMed Web of Science ®Google Scholar
• Pandeya A, Khalko RK, Mishra A, et al. Human cytomegalovirus miR-UL70-3p downregulates the H2O2-induced apoptosis by targeting the modulator of apoptosis-1 (MOAP1). Int J Mol Sci. 2021;23(1):18. doi:10.3390/ijms23010018.
   PubMed Web of Science ®Google Scholar
• Pandeya A, Khalko RK, Singh S, et al. Hcmv-miR-UL148D regulates the staurosporine-induced apoptosis by targeting the Endoplasmic Reticulum to Nucleus signaling 1(ERN1). PLoS One. 2022;17(9):e0275072. doi:10.1371/journal.pone.0275072.
   PubMed Web of Science ®Google Scholar
• Sotthibundhu A, McDonagh K, von Kriegsheim A, et al. Rapamycin regulates autophagy and cell adhesion in induced pluripotent stem cells. Stem Cell Res Ther. 2016;7(1):166. doi:10.1186/s13287-016-0425-x.
   PubMed Web of Science ®Google Scholar
• Jiang CY, Yang BY, Zhao S, et al. Deregulation of ATG9A by impaired AR signaling induces autophagy in prostate stromal fibroblasts and promotes BPH progression. Cell Death Dis. 2018;9(4):431. doi:10.1038/s41419-018-0415-2.
   PubMedGoogle Scholar
• Shimada H, Hata S, Yamazaki Y, et al. YM750, an ACAT inhibitor, acts on adrenocortical cells to inhibit aldosterone secretion due to depolarization. Int J Mol Sci. 2022;23(21):12803. doi:10.3390/ijms232112803.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Ravikumar B, Floto RA, et al. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies. Cell Death Differ. 2009;16(1):46–56. doi:10.1038/cdd.2008.110.
   PubMed Web of Science ®Google Scholar
• Wu J, Dang Y, Su W, et al. Molecular cloning and characterization of rat LC3A and LC3B—two novel markers of autophagosome. Biochem Biophys Res Commun. 2006;339(1):437–442. doi:10.1016/j.bbrc.2005.10.211.
   PubMed Web of Science ®Google Scholar
• Koukourakis MI, Kalamida D, Giatromanolaki A, et al. Autophagosome proteins LC3A, LC3B and LC3C have distinct subcellular distribution kinetics and expression in cancer cell lines. PLoS One. 2015;10(9):e0137675. doi:10.1371/journal.pone.0137675.
   PubMed Web of Science ®Google Scholar
• Kirkegaard K, Taylor MP, Jackson WT. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol. 2004;2(4):301–314. doi:10.1038/nrmicro865.
   PubMed Web of Science ®Google Scholar
• Deretic V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol Rev. 2011;240(1):92–104. doi:10.1111/j.1600-065X.2010.00995.x.
   PubMed Web of Science ®Google Scholar
• Cavignac Y, Esclatine AJV. Herpesviruses and autophagy: catch me if you can! Viruses 2010;2(1):314–333. doi:10.3390/v2010314.
   PubMed Web of Science ®Google Scholar
• Delcour C, Amazit L, Patino LC, et al. ATG7 and ATG9A loss-of-function variants trigger autophagy impairment and ovarian failure. Genet Med. 2019;21(4):930–938. doi:10.1038/s41436-018-0287-y.
   PubMed Web of Science ®Google Scholar
• Pang J, Xiong H, Lin P, et al. Activation of miR-34a impairs autophagic flux and promotes cochlear cell death via repressing ATG9A: implications for age-related hearing loss. Cell Death Dis. 2017;8(10):e3079–e3079. doi:10.1038/cddis.2017.462.
   PubMedGoogle Scholar
• Mari M, Griffith J, Rieter E, et al. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J Cell Biol. 2010;190(6):1005–1022. doi:10.1083/jcb.200912089.
   PubMed Web of Science ®Google Scholar
• Orsi A, Razi M, Dooley HC, et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell. 2012;23(10):1860–1873. doi:10.1091/mbc.E11-09-0746.
   PubMed Web of Science ®Google Scholar
• Young AR, Chan EY, Hu XW, et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci. 2006;119(Pt 18):3888–3900. doi:10.1242/jcs.03172.
   PubMed Web of Science ®Google Scholar
• Yamada T, Carson AR, Caniggia I, et al. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem. 2005;280(18):18283–18290. doi:10.1074/jbc.M413957200.
   PubMed Web of Science ®Google Scholar
• Claude-Taupin A, Jia J, Bhujabal Z, et al. ATG9A protects the plasma membrane from programmed and incidental permeabilization. Nat Cell Biol. 2021;23(8):846–858. doi:10.1038/s41556-021-00706-w.
   PubMed Web of Science ®Google Scholar
• Reggiori F, Tucker KA, Stromhaug PE, et al. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell. 2004;6(1):79–90. doi:10.1016/s1534-5807(03)00402-7.
   PubMed Web of Science ®Google Scholar
• Kanda T, Yoshida A, Ikebuchi Y, et al. Autophagy‑related 16‑like 1 is influenced by human herpes virus 1‑encoded microRNAs in biopsy samples from the lower esophageal sphincter muscle during per‑oral endoscopic myotomy for esophageal achalasia. Biomed Rep. 2021;14(1):7–1. J doi:10.3892/br.2020.1383.
   PubMed Web of Science ®Google Scholar
• Shen ZZ, Pan X, Miao LF, et al. Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One. 2014;9(2):e88531. doi:10.1371/journal.pone.0088531.
   PubMed Web of Science ®Google Scholar
• Ulasov IV, Kaverina NV, Ghosh D, et al. CMV70-3P miRNA contributes to the CMV mediated glioma stemness and represents a target for glioma experimental therapy. Oncotarget. 2017;8(16):25989–25999. doi:10.18632/oncotarget.11175.
   PubMedGoogle Scholar
• Lee JS, Li Q, Lee JY, et al. FLIP-mediated autophagy regulation in cell death control. Nat Cell Biol. 2009;11(11):1355–1362. doi:10.1038/ncb1980.
   PubMed Web of Science ®Google Scholar
• Leib DA, Alexander DE, Cox D, et al. Interaction of ICP34. 5 with Beclin 1 modulates herpes simplex virus type 1 pathogenesis through control of CD4+ T-cell responses. J Virol. 2009;83(23):12164–12171. doi:10.1128/JVI.01676-09.
   PubMed Web of Science ®Google Scholar