Does the interplay between human endogenous retrovirus K and extracellular vesicles contribute to aging?

Catherine DeMarino , Avindra Nath , Zhengping Zhuang , Tara T. Doucet-O’Hare

Extracellular Vesicles and Circulating Nucleic Acids ›› 2023, Vol. 4 ›› Issue (4) : 548 -56.

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Extracellular Vesicles and Circulating Nucleic Acids ›› 2023, Vol. 4 ›› Issue (4) :548 -56. DOI: 10.20517/evcna.2023.45
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Does the interplay between human endogenous retrovirus K and extracellular vesicles contribute to aging?

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Abstract

The role of extracellular vesicles (EVs), including retroviral-like particles (RVLPs), in pathogenic processes is currently a subject of active investigation. Several studies have identified mechanistic links between the increased presence of EVs and the process of senescence. A recent study reveals that the reverse transcribed complementary DNA (cDNA) of a human endogenous retroviral sequence can activate the innate immune system and result in tissue damage and/or the spread of cellular senescence to distant tissues. Several studies have linked EVs to age-related diseases, such as Alzheimer’s disease and Parkinson’s disease, and have included isolation of EVs from individuals with these diseases. Loss of epigenetic regulation, immune activation, and environmental stimuli can all lead to the expression of endogenous retroviruses and the incorporation of their proteins and transcripts into EVs. In addition, EVs disseminating these endogenous retroviral components have now been shown to act in a paracrine manner in multiple human diseases. Further investigation of the connection between EVs containing endogenous retroviral protein products or nucleotides should be pursued in models of age-related diseases.

Keywords

HML-2 / human endogenous retrovirus / aging / senescence / repetitive elements / mobile DNA / transposable elements

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Catherine DeMarino, Avindra Nath, Zhengping Zhuang, Tara T. Doucet-O’Hare. Does the interplay between human endogenous retrovirus K and extracellular vesicles contribute to aging?. Extracellular Vesicles and Circulating Nucleic Acids, 2023, 4(4): 548-56 DOI:10.20517/evcna.2023.45

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References

[1]

Luan DD,Jakubczak JL.Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition.Cell1993;72:595-605

[2]

De Cecco M,Petrashen AP.L1 drives IFN in senescent cells and promotes age-associated inflammation.Nature2019;566:73-8

[3]

Della Valle F,Yamamoto M.LINE-1 RNA causes heterochromatin erosion and is a target for amelioration of senescent phenotypes in progeroid syndromes.Sci Transl Med2022;14:eabl6057

[4]

Liu X,Wu Z.Resurrection of endogenous retroviruses during aging reinforces senescence.Cell2023;186:287-304.e26

[5]

Johnson WE.Origins and evolutionary consequences of ancient endogenous retroviruses.Nat Rev Microbiol2019;17:355-70

[6]

Blikstad V,Sperber GO.Evolution of human endogenous retroviral sequences: a conceptual account.Cell Mol Life Sci2008;65:3348-65

[7]

Marchi E,Magiorkinis G.Unfixed endogenous retroviral insertions in the human population.J Virol2014;88:9529-37 PMCID:PMC4136357

[8]

Subramanian RP,Russo C.Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses.Retrovirology2011;8:90 PMCID:PMC3228705

[9]

Stoye JP.Studies of endogenous retroviruses reveal a continuing evolutionary saga.Nat Rev Microbiol2012;10:395-406

[10]

Doucet-O'Hare TT,DeMarino C.SMARCB1 deletion in atypical teratoid rhabdoid tumors results in human endogenous retrovirus K (HML-2) expression.Sci Rep2021;11:12893 PMCID:PMC8213802

[11]

Wang T,Johnson KR.Regulation of stem cell function and neuronal differentiation by HERV-K via mTOR pathway.Proc Natl Acad Sci U S A2020;117:17842-53 PMCID:PMC7395438

[12]

Steiner JP,Malik N.Human endogenous retrovirus k envelope in spinal fluid of amyotrophic lateral sclerosis is toxic.Ann Neurol2022;92:545-61 PMCID:PMC9489628

[13]

Shah AH,Doucet-O'Hare TT.Human endogenous retrovirus K contributes to a stem cell niche in glioblastoma.J Clin Invest2023;133:e167929. PMCID:PMC10313366

[14]

Grow EJ,Chavez SL.Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells.Nature2015;522:221-5 PMCID:PMC4503379

[15]

Pastuzyn ED,Kearns RB.The neuronal gene arc encodes a repurposed retrotransposon gag protein that mediates intercellular RNA transfer.Cell2018;172:275-88.e18 PMCID:PMC5884693

[16]

Frendo JL,Cheynet V.Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation.Mol Cell Biol2003;23:3566-74 PMCID:PMC164757

[17]

Mangeney M,Schlecht-Louf G.Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins.Proc Natl Acad Sci U S A2007;104:20534-9 PMCID:PMC2154466

[18]

Knerr I,Weigel C.Endogenous retroviral syncytin: compilation of experimental research on syncytin and its possible role in normal and disturbed human placentogenesis.Mol Hum Reprod2004;10:581-8

[19]

Bolze P,Mallet F.Contribution of syncytins and other endogenous retroviral envelopes to human placenta pathologies.Prog Mol Biol Transl Sci2017;145:111-62.

[20]

Cornelis G,Carradec Q.Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials.Proc Natl Acad Sci U S A2015;112:E487-96. PMCID:PMC4321253

[21]

Frendo JL,Guibourdenche J.Defect of villous cytotrophoblast differentiation into syncytiotrophoblast in Down's syndrome.J Clin Endocrinol Metab2000;85:3700-7

[22]

Massin N,Guibourdenche J.Defect of syncytiotrophoblast formation and human chorionic gonadotropin expression in Down's syndrome.Placenta2001;22 Suppl A:S93-7

[23]

Vargas A,LeBellego F,Lafond J.Reduced expression of both syncytin 1 and syncytin 2 correlates with severity of preeclampsia.Reprod Sci2011;18:1085-91.

[24]

Lee X,Stumm N.Downregulation of placental syncytin expression and abnormal protein localization in pre-eclampsia.Placenta2001;22:808-12

[25]

Soygur B,Demir R.Altered expression of human endogenous retroviruses syncytin-1, syncytin-2 and their receptors in human normal and gestational diabetic placenta.Histol Histopathol2016;31:1037-47

[26]

Shah AH,Doucet-O'Hare TT.Differential expression of an endogenous retroviral element [HERV-K(HML-6)] is associated with reduced survival in glioblastoma patients.Sci Rep2022;12:6902 PMCID:PMC9046263

[27]

Liu S,Hossinger A.Reactivated endogenous retroviruses promote protein aggregate spreading.Nat Commun2023;14:5034 PMCID:PMC10439213

[28]

Vargas A,Éthier-Chiasson M.Syncytin proteins incorporated in placenta exosomes are important for cell uptake and show variation in abundance in serum exosomes from patients with preeclampsia.FASEB J2014;28:3703-19

[29]

Contreras-Galindo R,Dube D.Human endogenous retrovirus type K (HERV-K) particles package and transmit HERV-K-related sequences.J Virol2015;89:7187-201 PMCID:PMC4473553

[30]

Lötvall J,Hochberg F.Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the international society for extracellular vesicles.J Extracell Vesicles2014;3:26913 PMCID:PMC4275645

[31]

Li Y,Zhang N.Human endogenous retrovirus K (HERV-K) env in neuronal extracellular vesicles: a new biomarker of motor neuron disease.Amyotroph Lateral Scler Frontotemporal Degener2022;23:100-7

[32]

Record M.Intercellular communication by exosomes in placenta: a possible role in cell fusion?.Placenta2014;35:297-302

[33]

Ovadya Y,Leins H.Impaired immune surveillance accelerates accumulation of senescent cells and aging.Nat Commun2018;9:5435 PMCID:PMC6303397

[34]

Yin Y,Wang Y,Wang X.Roles of extracellular vesicles in the aging microenvironment and age-related diseases.J Extracell Vesicles2021;10:e12154 PMCID:PMC8491204

[35]

Wood JG.Chromatin structure and transposable elements in organismal aging.Front Genet2013;4:274 PMCID:PMC3849598

[36]

Manghera M.Endogenous retrovirus-K promoter: a landing strip for inflammatory transcription factors?.Retrovirology2013;10:16 PMCID:PMC3598470

[37]

Levine KS,Blauwendraat C.Virus exposure and neurodegenerative disease risk across national biobanks.Neuron2023;111:1086-93.e2 PMCID:PMC10079561

[38]

Franceschi C,Valensin S.Inflamm-aging. An evolutionary perspective on immunosenescence.Ann N Y Acad Sci2000;908:244-54

[39]

O'Carroll IP,Kroupa T.Structural mimicry drives HIV-1 Rev-mediated HERV-K expression.J Mol Biol2020;432:166711 PMCID:PMC7842262

[40]

Petrone V,Giudice M.Expression profile of HERVs and inflammatory mediators detected in nasal mucosa as a predictive biomarker of COVID-19 severity.Front Microbiol2023;14:1155624 PMCID:PMC10239953

[41]

Wang D,Mo Y.Human endogenous retrovirus, SARS-CoV-2, and HIV promote PAH via inflammation and growth stimulation.Int J Mol Sci2023;24:7472 PMCID:PMC10138839

[42]

Temerozo JR,Dos Santos MC.Human endogenous retrovirus K in the respiratory tract is associated with COVID-19 physiopathology.Microbiome2022;10:65

[43]

Wildschutte JH,Montesion M,Kidd JM.Discovery of unfixed endogenous retrovirus insertions in diverse human populations.Proc Natl Acad Sci U S A2016;113:E2326-34 PMCID:PMC4843416

[44]

Burn A,Freeman M.Widespread expression of the ancient HERV-K (HML-2) provirus group in normal human tissues.PLoS Biol2022;20:e3001826 PMCID:PMC9578601

[45]

Büscher K,Hofmann M.Expression of the human endogenous retrovirus-K transmembrane envelope, Rec and Np9 proteins in melanomas and melanoma cell lines.Melanoma Res2006;16:223-34

[46]

Temin HM.Viral RNA-dependent DNA Polymerase: RNA-dependent DNA polymerase in virions of rous sarcoma virus.Nature1970;226:1211-3

[47]

Baltimore D.Viral RNA-dependent DNA Polymerase: RNA-dependent DNA polymerase in virions of RNA tumour viruses.Nature1970;226:1209-11

[48]

Berkhout B,Zsíros J.Identification of an active reverse transcriptase enzyme encoded by a human endogenous HERV-K retrovirus.J Virol1999;73:2365-75 PMCID:PMC104482

[49]

Ono M,Miyata T.Nucleotide sequence of human endogenous retrovirus genome related to the mouse mammary tumor virus genome.J Virol1986;60:589-98. PMCID:PMC288930

[50]

Cortopassi G.Genotypic selection of mitochondrial and oncogenic mutations in human tissue suggests mechanisms of age-related pathophysiology.Mutat Res1995;338:151-9

[51]

Seth RB,Ea CK.Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3.Cell2005;122:669-82

[52]

Schoggins JW,Imanaka N.Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity.Nature2014;505:691-5 PMCID:PMC4077721

[53]

Horn MD.Extracellular vesicles as a means of viral immune evasion, CNS invasion, and glia-induced neurodegeneration.Front Cell Neurosci2021;15:695899 PMCID:PMC8287503

[54]

Kritsilis M,Koutsoudaki PN,Gorgoulis VG.Ageing, cellular senescence and neurodegenerative disease.Int J Mol Sci2018;19:2937 PMCID:PMC6213570

[55]

Ruan Z,Venkatesan Kalavai S.Alzheimer's disease brain-derived extracellular vesicles spread tau pathology in interneurons.Brain2021;144:288-309 PMCID:PMC7880668

[56]

Herman S,Mollenhauer B.CSF-derived extracellular vesicles from patients with Parkinson's disease induce symptoms and pathology.Brain2023;146:209-24

[57]

Komurian-Pradel F,Bedin F.Molecular cloning and characterization of MSRV-related sequences associated with retrovirus-like particles.Virology1999;260:1-9

[58]

Sun W,Gamez M,Frost B.Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies.Nat Neurosci2018;21:1038-48 PMCID:PMC6095477

[59]

Hardy MP,Migneault F.Apoptotic endothelial cells release small extracellular vesicles loaded with immunostimulatory viral-like RNAs.Sci Rep2019;9:7203 PMCID:PMC6510763

[60]

Bowers EC,Knox K,Ramos KS.LINE-1 cargo and reverse transcriptase activity profiles in extracellular vesicles from lung cancer cells and human plasma.Int J Mol Sci2022;23:3461 PMCID:PMC8998977

[61]

Keswani RK,Pack DW.Design of hybrid lipid/retroviral-like particle gene delivery vectors.Mol Pharm2013;10:1725-35 PMCID:PMC3646931

[62]

Dang DD,Shah AH,Doucet-O'Hare TT.Epigenetic regulation in primary CNS tumors: an opportunity to bridge old and new WHO classifications.Cancers2023;15:2511 PMCID:PMC10177493

[63]

Zhang J,Maruyama A.BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress.Mol Cell Biol2006;26:7942-52 PMCID:PMC1636732

[64]

Doucet-O'Hare TT,Shah AH,Zhuang Z.Endogenous retroviral elements in human development and central nervous system embryonal tumors.J Pers Med2021;11:1332 PMCID:PMC8708524

[65]

Li W,Henderson L.Human endogenous retrovirus-K contributes to motor neuron disease.Sci Transl Med2015;7:307ra153 PMCID:PMC6344353

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