Exosome-encapsulated microRNAs as promising biomarkers for Alzheimer’s disease

References

Aksoy-Aksel, A., Zampa, F., and Schratt, G. (2014). MicroRNAs and synaptic plasticity – a mutual relationship. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130515.10.1098/rstb.2013.0515Suche in Google Scholar PubMed PubMed Central

Alzheimer Association. (2016). Alzheimer’s disease facts and figures. Alzheimers Dement. 12, 459–509.10.1016/j.jalz.2016.03.001Suche in Google Scholar PubMed

Cai, M., Wang, Y.W., Xu, S.H., Qiao, S., Shu, Q.F., Du, J.Z., Li, Y.G., and Liu, X.L. (2018). Regulatory effects of the long noncoding RNA RP11543N12.1 and microRNA3243p axis on the neuronal apoptosis induced by the inflammatory reactions of microglia. Int. J. Mol. Med. 42, 1741–1755.10.3892/ijmm.2018.3736Suche in Google Scholar

Canter, R., Penney, J., and Tsai, L. (2016). The road to restoring neural circuits for the treatment of Alzheimer’s disease. Nature. 539, 187–196.10.1038/nature20412Suche in Google Scholar PubMed

Chen, J.J., Zhao, B., Zhao, J., and Li, S. (2017). Potential roles of exosomal microRNAs as diagnostic biomarkers and therapeutic application in Alzheimer’s disease. Neural Plast. 2017, 1–12.10.1155/2017/7027380Suche in Google Scholar PubMed PubMed Central

Cheng, L., Quek, C., Sun, X., Bellingham, S., and Hill, A. (2013). The detection of microRNA associated with Alzheimer’s disease in biological fluids using next-generation sequencing technologies. Front Genet. 4, 150.10.3389/fgene.2013.00150Suche in Google Scholar PubMed PubMed Central

Cheng, L., Doecke, J.D., Sharples, R.A., Villemagne, V.L., Fowler, C.J., Rembach, A., Martins, R.N., Rowe, C.C., Macaulay, S.L., Masters, C.L. et al. (2015). Prognostic serum miRNA biomarkers associated with Alzheimer’s disease shows concordance with neuropsychological and neuroimaging assessment. Mol. Psychiatry. 20, 1188–1196.10.1038/mp.2014.127Suche in Google Scholar PubMed

Cogoni, C., Ruberti, F., and Barbato, C. (2015). MicroRNA landscape in Alzheimer’s disease. CNS Neurol. Disord. Drug Targets. 14, 168–175.10.2174/1871527314666150116123305Suche in Google Scholar PubMed

Dehghani, R., Rahmani, F., and Rezaei, N. (2018). MicroRNA in Alzheimer’s disease revisited: implications for major neuropathological mechanisms. Rev. Neurosci. 29, 161–182.10.1515/revneuro-2017-0042Suche in Google Scholar PubMed

Deng, Y., Ding, Y., and Hou, D. (2014). Research status of the regulation of miRNA on BACE1. Int. J. Neurosci. 124, 474–477.10.3109/00207454.2013.858249Suche in Google Scholar PubMed

Faridani, O., Abdullayev, I., Hagemann-Jensen, M., Schell, J., Lanner, F., and Sandberg, R. (2016). Single-cell sequencing of the small-RNA transcriptome. Nat. Biotechnol. 34, 1264–1266.10.1038/nbt.3701Suche in Google Scholar PubMed

Fernandes, A., Ribeiro, A.R., Monteiro, M., Garcia, G., Vaz, A.R., and Brites, D. (2018). Secretome from SH-SY5Y APPSwe cells trigger time-dependent CHME3 microglia activation phenotypes, ultimately leading to miR-21 exosome shuttling. Biochimie 155, 67–82.10.1016/j.biochi.2018.05.015Suche in Google Scholar

Fiandaca, M.S., Kapogiannis, D., Mapstone, M., Boxer, A., Eitan, E., Schwartz, J.B., Abner, E.L., Petersen, R.C., Federoff, H.J., Miller, B.L., et al. (2015). Identification of preclinical Alzheimer’s disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study. Alzheimers Dement. 11, 600–607.e601.10.1016/j.jalz.2014.06.008Suche in Google Scholar

Frisoni, G., Boccardi, M., Barkhof, F., Blennow, K., Cappa, S., Chiotis, K., Démonet, J., Garibotto, V., Giannakopoulos, P., Gietl, A., et al. (2017). Strategic roadmap for an early diagnosis of Alzheimer’s disease based on biomarkers. Lancet Neurol. 16, 661–676.10.1016/S1474-4422(17)30159-XSuche in Google Scholar

Goetzl, E., Mustapic, M., Kapogiannis, D., Eitan, E., Lobach, I., Goetzl, L., Schwartz, J., and Miller, B. (2016). Cargo proteins of plasma astrocyte-derived exosomes in Alzheimer’s disease. FASEB J. 30, 3853–3859.10.1096/fj.201600756RSuche in Google Scholar PubMed PubMed Central

Goetzl, E.J., Schwartz, J.B., Abner, E.L., Jicha, G.A., and Kapogiannis, D. (2018). High complement levels in astrocyte-derived exosomes of Alzheimer disease. Ann. Neurol. 83, 544–552.10.1002/ana.25172Suche in Google Scholar PubMed PubMed Central

Higa, G., de Sousa, E., Walter, L., Kinjo, E., Resende, R., and Kihara, A. (2014). MicroRNAs in neuronal communication. Mol. Neurobiol. 49, 1309–1326.10.1007/s12035-013-8603-7Suche in Google Scholar PubMed

Huang, W. and Li, M. (2009). Differential allelic expression of dopamine D1 receptor gene (DRD1) is modulated by microRNA miR-504. Biol. Psychiatry 65, 702–705.10.1016/j.biopsych.2008.11.024Suche in Google Scholar PubMed PubMed Central

Iranifar, E., Seresht, B.M., Momeni, F., Fadaei, E., Mehr, M.H., Ebrahimi, Z., Rahmati, M., Kharazinejad, E., and Mirzaei, H. (2019). Exosomes and microRNAs: new potential therapeutic candidates in Alzheimer disease therapy. J. Cell Physiol. 234, 2296–2305.10.1002/jcp.27214Suche in Google Scholar PubMed

Jo, S., Yarishkin, O., Hwang, Y., Chun, Y., Park, M., Woo, D., Bae, J., Kim, T., Lee, J., Chun, H., et al. (2014). GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat. Med. 20, 886–896.10.1038/nm.3639Suche in Google Scholar PubMed PubMed Central

Kiko, T., Nakagawa, K., Tsuduki, T., Furukawa, K., Arai, H., and Miyazawa, T. (2014). MicroRNAs in plasma and cerebrospinal fluid as potential markers for Alzheimer’s disease. J. Alzheimers Dis. 39, 253–259.10.3233/JAD-130932Suche in Google Scholar PubMed

Kim, D. and Tsai, L. (2009). Bridging physiology and pathology in AD. Cell. 137, 997–1000.10.1016/j.cell.2009.05.042Suche in Google Scholar PubMed

Kumar, S. and Reddy, P. (2016). Are circulating microRNAs peripheral biomarkers for Alzheimer’s disease? Biochim. Biophys. Acta. 1862, 1617–1627.10.1016/j.bbadis.2016.06.001Suche in Google Scholar PubMed PubMed Central

Kumar, S., Vijayan, M., Bhatti, J., and Reddy, P. (2017). MicroRNAs as peripheral biomarkers in aging and age-related diseases. Prog. Mol. Biol. Transl. Sci. 146, 47–94.10.1016/bs.pmbts.2016.12.013Suche in Google Scholar PubMed

Lambert, T., Storm, D., and Sullivan, J. (2010). MicroRNA132 modulates short-term synaptic plasticity but not basal release probability in hippocampal neurons. PLoS One 5, e15182.10.1371/journal.pone.0015182Suche in Google Scholar PubMed PubMed Central

Lei, X., Lei, L., Zhang, Z., Zhang, Z., and Cheng, Y. (2015). Down-regulated miR-29c correlates with increased BACE1 expression in sporadic Alzheimer’s disease. Int. J. Clin. Exp. Pathol. 8, 1565–1574.Suche in Google Scholar

Li, X., Wang, Z., Tan, L., Wang, Y., Lu, C., Chen, R., Zhang, S., Gao, Y., Liu, Y., Yin, Y., et al. (2017). Correcting miR92a-vGAT-mediated GABAergic dysfunctions rescues human tau-induced anxiety in mice. Mol. Ther. 25, 140–152.10.1016/j.ymthe.2016.10.010Suche in Google Scholar PubMed PubMed Central

Li, W.Y., Zhang, W.T., Cheng, Y.X., Liu, Y.C., Zhai, F.G., Sun, P., Li, H.T., Deng, L.X., Zhu, X.F., and Wang, Y. (2018). Inhibition of KLF7-targeting microRNA 146b promotes sciatic nerve regeneration. Neurosci. Bull. 34, 419–437.10.1007/s12264-018-0206-xSuche in Google Scholar PubMed PubMed Central

Liu, C.G., Song, J., Zhang, Y.Q., and Wang, P.C. (2014). MicroRNA-193b is a regulator of amyloid precursor protein in the blood and cerebrospinal fluid derived exosomal microRNA-193b is a biomarker of Alzheimer’s disease. Mol. Med. Rep. 10, 2395–2400.10.3892/mmr.2014.2484Suche in Google Scholar PubMed

Lugli, G., Cohen, A.M., Bennett, D.A., Shah, R.C., Fields, C.J., Hernandez, A.G., and Smalheiser, N.R. (2015). Plasma exosomal miRNAs in persons with and without Alzheimer disease: altered expression and prospects for biomarkers. PLoS One 10, e0139233.10.1371/journal.pone.0139233Suche in Google Scholar PubMed PubMed Central

Miller, P. and Aricescu, A. (2014). Crystal structure of a human GABAA receptor. Nature 512, 270–275.10.1038/nature13293Suche in Google Scholar PubMed PubMed Central

Nadim, W., Simion, V., Benedetti, H., Pichon, C., Baril, P., and Morisset-Lopez, S. (2017). MicroRNAs in neurocognitive dysfunctions: new molecular targets for pharmacological treatments? Curr. Neuropharmacol. 15, 260–275.10.2174/1570159X14666160709001441Suche in Google Scholar PubMed PubMed Central

Nigro, A., Colombo, F., Casella, G., Finardi, A., Verderio, C., and Furlan, R. (2016). Myeloid extracellular vesicles: messengers from the demented brain. Front. Immunol. 7, 17.10.3389/fimmu.2016.00017Suche in Google Scholar PubMed PubMed Central

Nolte-’t Hoen, E., van der Vlist, E., Aalberts, M., Mertens, H., Bosch, B., Bartelink, W., Mastrobattista, E., van Gaal, E., Stoorvogel, W., Arkesteijn, G., et al. (2012). Quantitative and qualitative flow cytometric analysis of nanosized cell-derived membrane vesicles. Nanomedicine 8, 712–720.10.1016/j.nano.2011.09.006Suche in Google Scholar PubMed PubMed Central

Pant, S., Hilton, H., and Burczynski, M. (2012). The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem. Pharmacol. 83, 1484–1494.10.1016/j.bcp.2011.12.037Suche in Google Scholar PubMed PubMed Central

Pogue, A.I. and Lukiw, W.J. (2018). Up-regulated pro-inflammatory microRNAs (miRNAs) in Alzheimer’s disease (AD) and age-related macular degeneration (AMD). Cell Mol. Neurobiol. 38, 1021–1031.10.1007/s10571-017-0572-3Suche in Google Scholar PubMed

Prasad, K.N. (2017). Oxidative stress and pro-inflammatory cytokines may act as one of the signals for regulating microRNAs expression in Alzheimer’s disease. Mech. Ageing Dev. 162, 63–71.10.1016/j.mad.2016.12.003Suche in Google Scholar PubMed

Properzi, F., Ferroni, E., Poleggi, A., and Vinci, R. (2015). The regulation of exosome function in the CNS: implications for neurodegeneration. Swiss Med. Wkly. 145, w14204.10.4414/smw.2015.14204Suche in Google Scholar PubMed

Rahman, M., Islam, R., Islam, S., Mondal, S., and Amin, M. (2012). MiRANN: a reliable approach for improved classification of precursor microRNA using Artificial Neural Network model. Genomics 99, 189–194.10.1016/j.ygeno.2012.02.001Suche in Google Scholar PubMed

Riancho, J., Vazquez-Higuera, J.L., Pozueta, A., Lage, C., Kazimierczak, M., Bravo, M., Calero, M., Gonalezalez, A., Rodriguez, E., Lleo, A., et al. (2017). MicroRNA profile in patients with Alzheimer’s disease: analysis of miR-9-5p and miR-598 in raw and exosome enriched cerebrospinal fluid samples. J. Alzheimers Dis. 57, 483–491.10.3233/JAD-161179Suche in Google Scholar PubMed

Saba, R., Störchel, P., Aksoy-Aksel, A., Kepura, F., Lippi, G., Plant, T., and Schratt, G. (2012). Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons. Mol. Cell. Biol. 32, 619–632.10.1128/MCB.05896-11Suche in Google Scholar PubMed PubMed Central

Scott, H., Tamagnini, F., Narduzzo, K., Howarth, J., Lee, Y., Wong, L., Brown, M., Warburton, E., Bashir, Z., and Uney, J. (2012). MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci. 36, 2941–2948.10.1111/j.1460-9568.2012.08220.xSuche in Google Scholar PubMed PubMed Central

Sengupta, J., Pochiraju, S., Pochiraju, S., Kannampalli, P., Bruckert, M., Addya, S., Yadav, P., Miranda, A., Shaker, R., and Banerjee, B. (2013). MicroRNA-mediated GABA Aα-1 receptor subunit down-regulation in adult spinal cord following neonatal cystitis-induced chronic visceral pain in rats. Pain. 154, 59–70.10.1016/j.pain.2012.09.002Suche in Google Scholar

Sierksma, A., Lu, A., Salta, E., Vanden Eynden, E., Callaerts-Vegh, Z., D’Hooge, R., Blum, D., Buee, L., Fiers, M., and De Strooper, B. (2018). Deregulation of neuronal miRNAs induced by amyloid-beta or TAU pathology. Mol. Neurodegener. 13, 54.10.1186/s13024-018-0285-1Suche in Google Scholar

Tabaraud, F., Leman, J., Milor, A., Roussie, J., Barrière, G., Tartary, M., Boutros-Toni, F., and Rigaud, M. (2012). Alzheimer CSF biomarkers in routine clinical setting. Acta Neurol. Scand. 125, 416–423.10.1111/j.1600-0404.2011.01592.xSuche in Google Scholar

Tan, L., Yu, J., Liu, Q., Tan, M., Zhang, W., Hu, N., Wang, Y., Sun, L., Jiang, T., and Tan, L. (2014a). Circulating miR-125b as a biomarker of Alzheimer’s disease. J. Neurol. Sci. 336, 52–56.10.1016/j.jns.2013.10.002Suche in Google Scholar

Tan, L., Yu, J., Tan, M., Liu, Q., Wang, H., Zhang, W., Jiang, T., and Tan, L. (2014b). Genome-wide serum microRNA expression profiling identifies serum biomarkers for Alzheimer’s disease. J. Alzheimers Dis. 40, 1017–1027.10.3233/JAD-132144Suche in Google Scholar

Thery, C., Witwer, K.W., Aikawa, E., Alcaraz, M.J., Anderson, J.D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G.K., et al. (2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 7, 1535750.10.1080/20013078.2018.1535750Suche in Google Scholar

Van Giau, V. and An, S.S. (2016). Emergence of exosomal miRNAs as a diagnostic biomarker for Alzheimer’s disease. J. Neurol. Sci. 360, 141–152.10.1016/j.jns.2015.12.005Suche in Google Scholar

Vella, L., Hill, A., and Cheng, L. (2016). Focus on extracellular vesicles: exosomes and their role in protein trafficking and biomarker potential in Alzheimer’s and Parkinson’s disease. Int. J. Mol. Sci. 17, 173.10.3390/ijms17020173Suche in Google Scholar

Villemagne, V., Burnham, S., Bourgeat, P., Brown, B., Ellis, K., Salvado, O., Szoeke, C., Macaulay, S., Martins, R., Maruff, P., et al. (2013). Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer’s disease: a prospective cohort study. Lancet Neurol. 12, 357–367.10.1016/S1474-4422(13)70044-9Suche in Google Scholar

Wang, Y., Balaji, V., Kaniyappan, S., Krüger, L., Irsen, S., Tepper, K., Chandupatla, R., Maetzler, W., Schneider, A., Mandelkow, E., et al. (2017). The release and trans-synaptic transmission of Tau via exosomes. Mol. Neurodegener. 12, 5.10.1186/s13024-016-0143-ySuche in Google Scholar PubMed PubMed Central

Wang, D., Zhang, X., Wang, M., Zhou, D., Pan, H., Shu, Q., and Sun,B. (2018). Early Activation of astrocytes does not affect amyloid plaque load in an animal model of Alzheimer’s disease. Neurosci. Bull. 34, 912–920.10.1007/s12264-018-0262-2Suche in Google Scholar PubMed PubMed Central

Wayman, G., Davare, M., Ando, H., Fortin, D., Varlamova, O., Cheng, H., Marks, D., Obrietan, K., Soderling, T., Goodman, R., et al. (2008). An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl. Acad. Sci. U.S.A. 105, 9093–9098.10.1073/pnas.0803072105Suche in Google Scholar PubMed PubMed Central

Whitehead, G., Regan, P., Whitcomb, D., and Cho, K. (2017). Ca(2+)-permeable AMPA receptor: A new perspective on amyloid-beta mediated pathophysiology of Alzheimer’s disease. Neuropharmacology 112, 221–227.10.1016/j.neuropharm.2016.08.022Suche in Google Scholar PubMed

Winston, C.N., Goetzl, E.J., Akers, J.C., Carter, B.S., Rockenstein, E.M., Galasko, D., Masliah, E., and Rissman, R.A. (2016). Prediction of conversion from mild cognitive impairment to dementia with neuronally derived blood exosome protein profile. Alzheimers Dement (Amst.) 3, 63–72.10.1016/j.dadm.2016.04.001Suche in Google Scholar PubMed PubMed Central

Wu, H., Ong, K., Seeher, K., Armstrong, N., Thalamuthu, A., Brodaty, H., Sachdev, P., and Mather, K. (2016). Circulating microRNAs as biomarkers of Alzheimer’s disease: a systematic review. J. Alzheimers Dis. 49, 755–766.10.3233/JAD-150619Suche in Google Scholar PubMed

Wu, X., Zheng, T., and Zhang, B. (2017). Exosomes in Parkinson’s disease. Neurosci. Bull. 33, 331–338.10.1007/s12264-016-0092-zSuche in Google Scholar PubMed PubMed Central

Yang, T.T., Liu, C.G., Gao, S.C., Zhang, Y., and Wang, P.C. (2018). The serum exosome derived microRNA-135a, -193b, and -384 were potential Alzheimer’s disease biomarkers. Biomed. Environ. Sci. 31, 87–96.Suche in Google Scholar

Zhang, Y., Tang, C., Yu, T., Zhang, R., Zheng, H., and Yan, W. (2017). MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells. Genome Biol. 18, 105.10.1186/s13059-017-1243-xSuche in Google Scholar PubMed PubMed Central