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Basic Research Papers

MicroRNA expression profiling of Leishmania donovani-infected host cells uncovers the regulatory role of MIR30A-3p in host autophagy

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Pages 1817-1831 | Received 27 Jul 2015, Accepted 15 Jun 2016, Published online: 19 Aug 2016

References

  • Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 2005; 18:293-305; PMID:15831826; http://dx.doi.org/10.1128/CMR.18.2.293-305.2005
  • Shadab M, Ali N. Evasion of Host Defence by Leishmania donovani: Subversion of Signaling Pathways. Mol Biol Int 2011; 2011:343961; PMID:22091401; http://dx.doi.org/10.4061/2011/343961
  • Naderer T, McConville MJ. The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 2008; 10:301-8; PMID:18070117; http://dx.doi.org/10.1111/j.1462-5822.2007.01096.x
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013; 13:722-37; PMID:24064518; http://dx.doi.org/10.1038/nri3532
  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
  • Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90:1383-435; PMID:20959619; http://dx.doi.org/10.1152/physrev.00030.2009
  • Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, et al. Autophagy defends cells against invading group A Streptococcus. Science 2004; 306:1037-40; PMID:15528445; http://dx.doi.org/10.1126/science.1103966
  • Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 2006; 281:11374-83; PMID:16495224; http://dx.doi.org/10.1074/jbc.M509157200
  • Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66; PMID:15607973; http://dx.doi.org/10.1016/j.cell.2004.11.038
  • Py BF, Lipinski MM, Yuan J. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 2007; 3:117-25; PMID:17204850; http://dx.doi.org/10.4161/auto.3618
  • Rikihisa Y. Glycogen autophagosomes in polymorphonuclear leukocytes induced by rickettsiae. Anat Rec 1984; 208:319-27; PMID:6721227; http://dx.doi.org/10.1002/ar.1092080302
  • Tallóczy Z, Virgin HW, Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2006; 2:24-9; PMID:Can't; http://dx.doi.org/10.4161/auto.2176
  • Smith JD, de Harven E. Herpes simplex virus and human cytomegalovirus replication in WI-38 cells. III. Cytochemical localization of lysosomal enzymes in infected cells. J Virol 1978; 26:102-9; PMID:206717
  • Wang Y, Weiss LM, Orlofsky A. Host cell autophagy is induced by Toxoplasma gondii and contributes to parasite growth. J Biol Chem 2009; 284:1694-701; PMID:19028680; http://dx.doi.org/10.1074/jbc.M807890200
  • Schaible UE, Schlesinger PH, Steinberg TH, Mangel WF, Kobayashi T, Russell DG. Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J Cell Sci 1999; 112(Pt 5):681-93; PMID:9973603
  • Jaramillo M, Gomez MA, Larsson O, Shio MT, Topisirovic I, Contreras I, Luxenburg R, Rosenfeld A, Colina R, McMaster RW, et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe 2011; 9:331-41; PMID:21501832; http://dx.doi.org/10.1016/j.chom.2011.03.008
  • Pinheiro RO, Nunes MP, Pinheiro CS, D'Avila H, Bozza PT, Takiya CM, Côrte-Real S, Freire-de-Lima CG, DosReis GA. Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages. Microbes Infect Inst Pasteur 2009; 11:181-90; PMID:19070676; http://dx.doi.org/10.1016/j.micinf.2008.11.006
  • Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40:280-93; PMID:20965422; http://dx.doi.org/10.1016/j.molcel.2010.09.023
  • Orvedahl A, Levine B. Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 2009; 16:57-69; PMID:18772897; http://dx.doi.org/10.1038/cdd.2008.130
  • Sinha S, Levine B. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 2008; 27(Suppl 1):S137-48; PMID:19641499; http://dx.doi.org/10.1038/onc.2009.51
  • Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-80; PMID:21311563; http://dx.doi.org/10.1038/cdd.2010.191
  • Su Z, Yang Z, Xu Y, Chen Y, Yu Q. MicroRNAs in apoptosis, autophagy and necroptosis. Oncotarget 2015; 6:8474-90; PMID:25893379; http://dx.doi.org/10.18632/oncotarget.3523
  • Xu J, Wang Y, Tan X, Jing H. MicroRNAs in autophagy and their emerging roles in crosstalk with apoptosis. Autophagy 2012; 8:873-82; PMID:22441107; http://dx.doi.org/10.4161/auto.19629
  • He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5:522-31; PMID:15211354; http://dx.doi.org/10.1038/nrg1379
  • O'Connell RM, Rao DS, Baltimore D. microRNA regulation of inflammatory responses. Annu Rev Immunol 2012; 30:295-312; PMID:Can't; http://dx.doi.org/10.1146/annurev-immunol-020711-075013
  • Schulte LN, Eulalio A, Mollenkopf H-J, Reinhardt R, Vogel J. Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J 2011; 30:1977-89; PMID:21468030; http://dx.doi.org/10.1038/emboj.2011.94
  • Shwetha S, Gouthamchandra K, Chandra M, Ravishankar B, Khaja MN, Das S. Circulating miRNA profile in HCV infected serum: novel insight into pathogenesis. Sci Rep 2013; 3:1555; PMID:23549102; http://dx.doi.org/10.1038/srep01555
  • Chen X-M, Splinter PL, O'Hara SP, LaRusso NF. A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J Biol Chem 2007; 282:28929-38; PMID:17660297; http://dx.doi.org/10.1074/jbc.M702633200
  • Cai Y, Chen H, Mo X, Tang Y, Xu X, Zhang A, Lun Z, Lu F, Wang Y, Shen J. Toxoplasma gondii inhibits apoptosis via a novel STAT3-miR-17-92-Bim pathway in macrophages. Cell Signal 2014; 26:1204-12; PMID:24583285; http://dx.doi.org/10.1016/j.cellsig.2014.02.013
  • Lemaire J, Mkannez G, Guerfali FZ, Gustin C, Attia H, Sghaier RM, Sysco-Consortium, Dellagi K, Laouini D, Renard P. MicroRNA expression profile in human macrophages in response to Leishmania major infection. PLoS Negl Trop Dis 2013; 7:e2478; PMID:24098824; http://dx.doi.org/10.1371/journal.pntd.0002478
  • Geraci NS, Tan JC, McDowell MA. Characterization of microRNA expression profiles in Leishmania-infected human phagocytes. Parasite Immunol 2015; 37:43-51; PMID:25376316; http://dx.doi.org/10.1111/pim.12156
  • Mitroulis I, Kourtzelis I, Papadopoulos VP, Mimidis K, Speletas M, Ritis K. In vivo induction of the autophagic machinery in human bone marrow cells during Leishmania donovani complex infection. Parasitol Int 2009; 58:475-7; PMID:19591960; http://dx.doi.org/10.1016/j.parint.2009.07.002
  • Cyrino LT, Araújo AP, Joazeiro PP, Vicente CP, Giorgio S. In vivo and in vitro Leishmania amazonensis infection induces autophagy in macrophages. Tissue Cell 2012; 44:401-8; PMID:22939777; http://dx.doi.org/10.1016/j.tice.2012.08.003
  • Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, Liu C-G, Yang J-M. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 2009; 5:816-23; PMID:19535919; http://dx.doi.org/10.4161/auto.9064
  • Zou Z, Wu L, Ding H, Wang Y, Zhang Y, Chen X, Chen X, Zhang C-Y, Zhang Q, Zen K. MicroRNA-30a sensitizes tumor cells to cis-platinum via suppressing beclin 1-mediated autophagy. J Biol Chem 2012; 287:4148-56; PMID:22157765; http://dx.doi.org/10.1074/jbc.M111.307405
  • Chen Z, Wang T, Liu Z, Zhang G, Wang J, Feng S, Liang J. Inhibition of Autophagy by MiR-30A Induced by Mycobacteria tuberculosis as a Possible Mechanism of Immune Escape in Human Macrophages. Jpn J Infect Dis 2015; 68:420-4; PMID:25866116; http://dx.doi.org/10.7883/yoken.JJID.2014.466
  • Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j.cell.2010.01.028
  • Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-9; PMID:17909521; http://dx.doi.org/10.1038/ncb1007-1102
  • Wang J, Yang K, Zhou L, Minhaowu null, Wu Y, Zhu M, Lai X, Chen T, Feng L, Li M, et al. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog 2013; 9:e1003697; PMID:24130493; http://dx.doi.org/10.1371/journal.ppat.1003697
  • Kim JK, Yuk J-M, Kim SY, Kim TS, Jin HS, Yang C-S, Jo E-K. MicroRNA-125a inhibits autophagy activation and antimicrobial responses during mycobacterial infection. J Immunol Baltim Md 1950 2015; 194:5355-65; PMID:25917095
  • Cramer EM, Shao Y, Wang Y, Yuan Y. miR-190 is upregulated in Epstein-Barr Virus type I latency and modulates cellular mRNAs involved in cell survival and viral reactivation. Virology 2014; 464-465:184-95; PMID:25086243
  • Zhai H, Fesler A, Ju J. MicroRNA: a third dimension in autophagy. Cell Cycle Georget Tex 2013; 12:246-50; PMID:23255136; http://dx.doi.org/10.4161/cc.23273
  • Wang B, Ling S, Lin W-C. 14-3-3Tau regulates Beclin 1 and is required for autophagy. PloS One 2010; 5:e10409; PMID:20454448; http://dx.doi.org/10.1371/journal.pone.0010409
  • Ghosh J, Bose M, Roy S, Bhattacharyya SN. Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe 2013; 13:277-88; PMID:23498953; http://dx.doi.org/10.1016/j.chom.2013.02.005
  • Crauwels P, Bohn R, Thomas M, Gottwalt S, Jäckel F, Krämer S, Bank E, Tenzer S, Walther P, Bastian M, et al. Apoptotic-like Leishmania exploit the host's autophagy machinery to reduce T-cell-mediated parasite elimination. Autophagy 2015; 11:285-97; PMID:25801301; http://dx.doi.org/10.1080/15548627.2014.998904
  • Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, Jacob S, Majumder S. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 2008; 283:29897-903; PMID:18708351; http://dx.doi.org/10.1074/jbc.M804612200
  • Frankel LB, Wen J, Lees M, Høyer-Hansen M, Farkas T, Krogh A, Jäättelä M, Lund AH. microRNA-101 is a potent inhibitor of autophagy. EMBO J 2011; 30:4628-41; PMID:21915098; http://dx.doi.org/10.1038/emboj.2011.331
  • Jing Z, Han W, Sui X, Xie J, Pan H. Interaction of autophagy with microRNAs and their potential therapeutic implications in human cancers. Cancer Lett 2015; 356:332-8; PMID:25304373; http://dx.doi.org/10.1016/j.canlet.2014.09.039
  • Garofalo M, Croce CM. microRNAs: Master regulators as potential therapeutics in cancer. Annu Rev Pharmacol Toxicol 2011; 51:25-43; PMID:20809797; http://dx.doi.org/10.1146/annurev-pharmtox-010510-100517
  • Singh AK, Pandey RK, Siqueira-Neto JL, Kwon Y-J, Freitas-Junior LH, Shaha C, Madhubala R. Proteomic-based approach to gain insight into reprogramming of THP-1 cells exposed to Leishmania donovani over an early temporal window. Infect Immun 2015; 83:1853-68; PMID:25690103; http://dx.doi.org/10.1128/IAI.02833-14
  • Dweep H, Gretz N, Sticht C. miRWalk database for miRNA-target interactions. Methods Mol Biol Clifton NJ 2014; 1182:289-305; PMID:NOT_FOUND; http://dx.doi.org/10.1007/978-1-4939-1062-5_25
  • Subramanian M, Shaha C. Up-regulation of Bcl-2 through ERK phosphorylation is associated with human macrophage survival in an estrogen microenvironment. J Immunol Baltim Md 1950 2007; 179:2330-8; PMID:17675494
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods San Diego Calif 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
  • Siqueira-Neto JL, Moon S, Jang J, Yang G, Lee C, Moon HK, Chatelain E, Genovesio A, Cechetto J, Freitas-Junior LH. An image-based high-content screening assay for compounds targeting intracellular Leishmania donovani amastigotes in human macrophages. PLoS Negl Trop Dis 2012; 6:e1671; PMID:22720099; http://dx.doi.org/10.1371/journal.pntd.0001671
  • Anand S, Madhubala R. Genetically Engineered Ascorbic acid-deficient Live Mutants of Leishmania donovani induce long lasting Protective Immunity against Visceral Leishmaniasis. Sci Rep 2015; 5:10706; PMID:26035062; http://dx.doi.org/10.1038/srep10706

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