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Research Article

HIV-1 Tat and Cocaine Coexposure Impacts Pirnas to Affect Astrocyte Energy Metabolism

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 261-278 | Received 11 Jul 2021, Accepted 27 Jan 2022, Published online: 16 Feb 2022

References

  • US Department of Health&Human Services . US Statistics: HIV (2012). www.hiv.gov/hiv-basics/overview/data-and-trends/statistics
  • US Department of Health&Human Services . Global Statistics: HIV (2017). www.hiv.gov/hiv-basics/overview/data-and-trends/global-statistics
  • Hernán MA . The effect of combined antiretroviral therapy on the overall mortality of HIV-infected individuals. AIDS24(1), 123–137 (2010).
  • Sacktor N , McArthurJ. Prospects for therapy of HIV-associated neurologic diseases. J. Neurovirol.3(2), 89–101 (1997).
  • Trujillo JR , Jaramillo-RangelG , Ortega-MartinezMet al. International NeuroAIDS: prospects of HIV-1 associated neurological complications. Cell Res.15(11–12), 962–969 (2005).
  • Cherner M , MasliahE , EllisRJet al. Neurocognitive dysfunction predicts postmortem findings of HIV encephalitis. Neurology59(10), 1563–1567 (2002).
  • Tsegaw M , AndargieG , AlemG , TarekeM. Screening HIV-associated neurocognitive disorders (HAND) among HIV positive patients attending antiretroviral therapy in South Wollo, Ethiopia. J. Psychiatr. Res.85, 37–41 (2017).
  • Gaskill PJ , CalderonTM , ColeyJS , BermanJW. Drug induced increases in CNS dopamine alter monocyte, macrophage and T cell functions: implications for HAND. J. Neuroimmune Pharmacol.8, 621–642 (2013).
  • Arce Rentería M , ByrdD , CoulehanKet al. Neurocognitive intra-individual variability within HIV+ adults with and without current substance use. Neuropsychology34(3), 321–330 (2020).
  • Doke M , JeganathanV , McLaughlinJP , SamikkannuT. HIV-1 Tat and cocaine impact mitochondrial epigenetics: effects on DNA methylation. Epigenetics16(9), 980–999 (2020).
  • Bloomquist A , VaidyaNK. Modelling the risk of HIV infection for drug abusers. J. Biol. Dyn.15(suppl. 1), 1–24 (2020).
  • Shu C , JusticeAC , ZhangXet al. DNA methylation mediates the effect of cocaine use on HIV severity. Clin. Epigenetics12(1), 140 (2020).
  • Sivalingam K , CirinoTJ , McLaughlinJP , SamikkannuT. HIV-Tat and cocaine impact brain energy metabolism: redox modification and mitochondrial biogenesis influence NRF transcription-mediated neurodegeneration. Mol. Neurobiol.58(2), 490–504 (2020).
  • Stoccoro A , CoppedèF. Mitochondrial dna methylation and human diseases. Int. J. Mol. Sci.22(9), 4594 (2021).
  • Handy DE , CastroR , LoscalzoJ. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation123(19), 2145–2156 (2011).
  • Centers for Disease Control and Prevention . What is epigenetics? (2020). www.cdc.gov/genomics/disease/epigenetics.htm
  • Chuang JC , JonesPA. Epigenetics and microRNAs. Pediatr. Res.61(5 Pt. 2), 24–29 (2007).
  • Dash S , BalasubramaniamM , Martínez-RiveraFJet al. Cocaine-regulated microRNA miR-124 controls poly (ADP-ribose) polymerase-1 expression in neuronal cells. Sci. Rep.10(1), 11197 (2020).
  • Modai S , FarberovL , HerzigE , IsakovO , HiziA , ShomronN. HIV-1 infection increases microRNAs that inhibit Dicer1, HRB and HIV-EP2, thereby reducing viral replication. PLoS ONE14(1), e0211111 (2019).
  • He K , GuoC , HeL , ShiY. MiRNAs of peripheral blood as the biomarker of schizophrenia. Hereditas155, 9 (2018).
  • Kim VN . Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev.20(15), 1993–1997 (2006).
  • Zhao K , ChengS , MiaoNet al. A Pandas complex adapted for piRNA-guided transcriptional silencing and heterochromatin formation. Nat. Cell Biol.21, 1261–1272 (2019).
  • Klattenhoff C , TheurkaufW. Biogenesis and germline functions of piRNAs. Development135(1), 3–9 (2008).
  • Tian Y , SimanshuDK , MaJB , PatelDJ. Structural basis for piRNA 2′-O-methylated 3′-end recognition by Piwi PAZ (Piwi/Argonaute/Zwille) domains. Proc. Natl Acad. Sci. USA108(3), 903–910 (2011).
  • Wu X , PanY , FangYet al. The biogenesis and functions of piRNAs in human diseases. Mol. Ther. Nucleic Acids21, 108–120 (2020).
  • Roy J , SarkarA , ParidaS , GhoshZ , MallickB. Small RNA sequencing revealed dysregulated piRNAs in Alzheimer’s disease and their probable role in pathogenesis. Mol. Biosyst.13(3), 565–576 (2017).
  • Qiu W , GuoX , LinXet al. Transcriptome-wide piRNA profiling in human brains of Alzheimer’s disease. Neurobiol. Aging57, 170–177 (2017).
  • Huang G , HuH , XueXet al. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin. Transl. Oncol.15(7), 563–568 (2013).
  • Hashim A , RizzoF , MarcheseGet al. RNA sequencing identifies specific PIWI-interacting small noncoding RNA expression patterns in breast cancer. Oncotarget5(20), 9901–9910 (2014).
  • Rizzo F , RinaldiA , MarcheseGet al. Specific patterns of PIWI-interacting small noncoding RNA expression in dysplastic liver nodules and hepatocellular carcinoma. Oncotarget7(34), 54650–54661 (2016).
  • Busch J , RallaB , JungMet al. Piwi-interacting RNAs as novel prognostic markers in clear cell renal cell carcinomas. J. Exp. Clin. Cancer Res.34(1), 61 (2015).
  • Bélanger M , MagistrettiPJ. The role of astroglia in neuroprotection. Dialogues Clin. Neurosci.11(3), 281–295 (2009).
  • Deitmer JW , TheparambilSM , RuminotI , NoorSI , BeckerHM. Energy dynamics in the brain: contributions of astrocytes to metabolism and pH homeostasis. Front. Neurosci.13, 1301 (2019).
  • Dayton AI , SodroskiJG , RosenCA , GohWC , HaseltineWA. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell44(6), 941–947 (1986).
  • Fields J , DumaopW , CrewsLet al. Mechanisms of HIV-1 Tat neurotoxicity via CDK5 translocation and hyper-activation: role in HIV-associated neurocognitive disorders. Curr. HIV Res.13(1), 43–54 (2015).
  • Natarajaseenivasan K , CottoB , ShanmughapriyaSet al. Astrocytic metabolic switch is a novel etiology for cocaine and HIV-1 Tat-mediated neurotoxicity. Cell Death Dis.9(4), 415 (2018).
  • Afgan E , BakerD , BatutBet al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res.46(W1), W537–W544 (2018).
  • Wingett SW , AndrewsS. FastQ Screen: a tool for multi-genome mapping and quality control. F1000Research7, 1338 (2018).
  • Krueger F . Babraham bioinformatics – trim galore! (2017). www.bioinformatics.babraham.ac.uk/projects/trim_galore/
  • Langmead B , TrapnellC , PopM , SalzbergSL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol.10(3), R25 (2009).
  • PIWI-interacting RNA (piRNA) Database – piRNAdb. www.pirnadb.org/index
  • Shen EZ , ChenH , OzturkARet al. Identification of piRNA binding sites reveals the argonaute regulatory landscape of the C. elegans germline. Cell172(5), 937–951.e18 (2018).
  • Wu WS , HuangWC , BrownJSet al. PirScan: a webserver to predict piRNA targeting sites and to avoid transgene silencing in C. elegans. Nucleic Acids Res.46(W1), W43–W48 (2018).
  • Zhang D , TuS , StubnaMet al. The piRNA targeting rules and the resistance to piRNA silencing in endogenous genes. Science359(6375), 587–592 (2018).
  • Rosenkranz D , HanCT , RooversEF , ZischlerH , KettingRF. Piwi proteins and piRNAs in mammalian oocytes and early embryos: from sample to sequence. Genomics Data5, 309–313 (2015).
  • GitHub – mzytnicki/srnaMapper’. https://github.com/mzytnicki/srnaMapper
  • Kanehisa M . Toward understanding the origin and evolution of cellular organisms. Protein Sci.28(11), 1947–1951 (2019).
  • Kanehisa M , FurumichiM , SatoY , Ishiguro-WatanabeM , TanabeM. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res.49(D1), D545–D551 (2020).
  • Kanehisa M , GotoS. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res.28(1), 27–30 (2000).
  • Friedländer MR , MacKowiakSD , LiN , ChenW , RajewskyN. MiRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res.40(1), 37–52 (2012).
  • Liu Q , DingC , LangX , GuoG , ChenJ , SuX. Small noncoding RNA discovery and profiling with sRNAtools based on high-throughput sequencing. Brief. Bioinform.22(1), 463–473 (2021).
  • Smyth GK . Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol.3, 3 (2004).
  • Phipson B , LeeS , MajewskiIJ , AlexanderWS , SmythGK. Robust hyperparameter estimation protects against hypervariable genes and improves power to detect differential expression. Ann. Appl. Stat.10(2), 946–963 (2016).
  • Ritchie ME , PhipsonB , WuDet al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res.43(7), e47 (2015).
  • Law CW , ChenY , ShiW , SmythGK. Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol.15(2), R29 (2014).
  • Chan PP , LoweTM. GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes. Nucleic Acids Res.44(D1), D184–D189 (2016).
  • Wang J , ZhangP , LuYet al. PiRBase: a comprehensive database of piRNA sequences. Nucleic Acids Res.47(D1), D175–D180 (2019).
  • Rosenkranz D . piRNA cluster database: a web resource for piRNA producing loci. Nucleic Acids Res.44(D1), D223–D230 (2016).
  • Mi H , MuruganujanA , ThomasPD. PANTHER in 2013: Modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res.41(D1), (2013).
  • Thomas PD , CampbellMJ , KejariwalAet al. PANTHER: A library of protein families and subfamilies indexed by function. Genome Res.13(9), 2129–2141 (2003).
  • Doke M , KashanchiF , KhanMA , SamikkannuT. HIV-1 Tat and cocaine impact astrocytic energy reservoir influence on miRNA epigenetic regulation. Genomics113(6), 3461–3475 (2021).
  • Samikkannu T , AtluriVSR , NairMPN. HIV and cocaine impact glial metabolism: energy sensor AMP-activated protein kinase role in mitochondrial biogenesis and epigenetic remodeling. Sci. Rep.6(1), 1–11 (2016).
  • Sivalingam K , DokeM , KhanMA , SamikkannuT. Influence of psychostimulants and opioids on epigenetic modification of class III histone deacetylase (HDAC)-sirtuins in glial cells. Sci. Rep.11(1), 1–16 (2021).
  • Juliano C , WangJ , LinH. Uniting germline and stem cells: the function of piwi proteins and the pirna pathway in diverse organisms. Annu. Rev. Genet.45, 447–469 (2011).
  • Guo M , WuY. Fighting an old war with a new weapon – silencing transposons by Piwi-interacting RNA. IUBMB Life65(9), 739–747 (2013).
  • Yang G , SauC , LaiW , CichonJ , LiW. piRNAs and their functions in the brain. Int. J. Hum. Genet.344(6188), 1173–1178 (2015).
  • Perera BPU , TsaiZTY , ColwellMLet al. Somatic expression of piRNA and associated machinery in the mouse identifies short, tissue-specific piRNA. Epigenetics14(5), 504–521 (2019).
  • Lee EJ , BanerjeeS , ZhouHet al. Identification of piRNAs in the central nervous system. RNA17(6), 1090–1099 (2011).
  • Qi Y , HuH , GuoHet al. MicroRNA profiling in plasma of HIV-1 infected patients: potential markers of infection and immune status. J. Public Health Emergency1, 65–65 (2017).
  • Xu Z , AsahchopEL , BrantonWG , GelmanBB , PowerC , HobmanTC. MicroRNAs upregulated during HIV infection target peroxisome biogenesis factors: implications for virus biology, disease mechanisms and neuropathology. PLoS Pathog.13(6), e1006360 (2017).
  • Bali P , KennyPJ. MicroRNAs and drug addiction. Front Genet.4, 43 (2013).
  • Peterlin BM , LiuP , WangXet al. Hili inhibits HIV replication in activated T cells. J. Virol.91(11), e00237-17 (2017).
  • He Z , JingS , YangTet al. PIWIL4 maintains HIV-1 latency by enforcing epigenetically suppressive modifications on the 5′ long terminal repeat. J. Virol.94(10), (2020).
  • Ramat A , SimoneligM. Functions of PIWI proteins in gene regulation: new arrows added to the piRNA quiver. Trends Genet.37(2), 188–200 (2021).
  • Huang X , WongG. An old weapon with a new function: PIWI-interacting RNAs in neurodegenerative diseases. Transl. Neurodegener.10(1), 9 (2021).
  • Yin H , LinH. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature450(7167), 304–308 (2007).
  • Watanabe T , LinH. Posttranscriptional regulation of gene expression by piwi proteins and piRNAs. Mol. Cell56(1), 18–27 (2014).
  • Sai lakshmi S , AgrawalS. piRNABank: a web resource on classified and clustered Piwi-interacting RNAs. Nucleic Acids Res.36(Database issue), D173–D177 (2008).
  • Seto AG , KingstonRE , LauNC. The coming of age for Piwi proteins. Mol. Cell26(5), 603–609 (2007).
  • Wang J , ShiY , ZhouHet al. piRBase: integrating piRNA annotation in all aspects. Nucleic Acids Res.50(D1), D265–D272 (2022).
  • Zhang P , SiX , SkogerbøGet al. PiRBase: a web resource assisting piRNA functional study. Database (1), 10 (2014).
  • Rosenkranz D . piRNA cluster database: a web resource for piRNA producing loci. Nucleic Acids Res.44(D1), D223–D230 (2016).
  • Sarkar A , MajiRK , SahaS , GhoshZ. PiRNAQuest: searching the piRNAome for silencers. BMC Genomics15(1), 1–17 (2014).
  • Wu WS , BrownJS , ChenTTet al. piRTarBase: a database of piRNA targeting sites and their roles in gene regulation. Nucleic Acids Res.47(D1), D181–D187 (2019).
  • Uhrig S , KleinH. PingPongPro: a tool for the detection of piRNA-mediated transposon-silencing in small RNA-Seq data. Bioinformatics35(2), 335–336 (2019).
  • Wu WS , HuangWC , BrownJSet al. PirScan: a webserver to predict piRNA targeting sites and to avoid transgene silencing in C. elegans. Nucleic Acids Res.46(W1), W43–W48 (2018).

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