MicroRNAs in blood and cerebrospinal fluid as diagnostic biomarkers of multiple sclerosis and to monitor disease progression

Martinez, Bridget; Peplow, PhilipV

doi:10.4103/1673-5374.266905

Title: MicroRNAs in blood and cerebrospinal fluid as diagnostic biomarkers of multiple sclerosis and to monitor disease progression

Journal Article · Fri Oct 18 00:00:00 EDT 2019 · Neural Regeneration Research

DOI:https://doi.org/10.4103/1673-5374.266905· OSTI ID:1628702

Martinez, Bridget ^[1]; Peplow, PhilipV ^[2]

University of California, Merced, CA (United States); St. Georges University (Grenada); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
University of Otago, Dunedin (New Zealand)

Multiple sclerosis is a chronic autoimmune disease of the central nervous system. It is the main cause of non-traumatic neurological disability in young adults. Multiple sclerosis mostly affects people aged 20–50 years; however, it can occur in young children and much older adults. Factors identified in the distribution of MS include age, gender, genetics, environment, and ethnic background. Multiple sclerosis is usually associated with progressive degrees of disability. The disease involves demyelination of axons of the central nervous system and causes brain and spinal cord neuronal loss and atrophy. Diagnosing multiple sclerosis is based on a patient’s medical history including symptoms, physical examination, and various tests such as magnetic resonance imaging, cerebrospinal fluid and blood tests, and electrophysiology. The disease course of multiple sclerosis is not well correlated with the biomarkers presently used in clinical practice. Blood-derived biomarkers that can detect and distinguish the different phenotypes in multiple sclerosis may be advantageous in personalized treatment with disease-modifying drugs and to predict response to treatment. The studies reviewed have shown that the expression levels of a large number of miRNAs in peripheral blood, serum, exosomes isolated from serum, and cerebrospinal fluid are altered in multiple sclerosis and can distinguish the disease phenotypes from each other. Further studies are warranted to independently validate these findings so that individual or pairs of miRNAs in serum or cerebrospinal fluid can be used as potential diagnostic markers for adult and pediatric multiple sclerosis and for monitoring disease progression and response to therapy.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1628702

Journal Information:: Neural Regeneration Research, Vol. 15, Issue 4; ISSN 1673-5374

Publisher:: Chinese Association of Rehabilitation Medicine (CARM)Copyright Statement

Country of Publication:: United States

Language:: English

References (91)

Deregulation of microRNA-181c in cerebrospinal fluid of patients with clinically isolated syndrome is associated with early conversion to relapsing–remitting multiple sclerosis Ahlbrecht, Jonas; Martino, Filippo; Pul, Refik Multiple Sclerosis Journal, Vol. 22, Issue 9 https://doi.org/10.1177/1352458515613641	journal	July 2016
Pediatric multiple sclerosis: a review Alroughani, Raed; Boyko, Alexey BMC Neurology, Vol. 18, Issue 1 https://doi.org/10.1186/s12883-018-1026-3	journal	March 2018
Integration of MicroRNA Databases to Study MicroRNAs Associated with Multiple Sclerosis Angerstein, Charlotte; Hecker, Michael; Paap, Brigitte Katrin Molecular Neurobiology, Vol. 45, Issue 3 https://doi.org/10.1007/s12035-012-8270-0	journal	May 2012
MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components Asirvatham, Ananthi J.; Gregorie, Christopher J.; Hu, Zihua Molecular Immunology, Vol. 45, Issue 7 https://doi.org/10.1016/j.molimm.2007.10.035	journal	April 2008
Decreased Dicer expression is linked to increased expression of co-stimulatory molecule CD80 on B cells in multiple sclerosis Aung, Latt Latt; Balashov, Konstantin E. Multiple Sclerosis Journal, Vol. 21, Issue 9 https://doi.org/10.1177/1352458514560923	journal	December 2014
Specific miRNA Disease Biomarkers in Blood, Serum and Plasma: Challenges and Prospects Backes, Christina; Meese, Eckart; Keller, Andreas Molecular Diagnosis & Therapy, Vol. 20, Issue 6 https://doi.org/10.1007/s40291-016-0221-4	journal	July 2016
Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses Belbasis, Lazaros; Bellou, Vanesa; Evangelou, Evangelos The Lancet Neurology, Vol. 14, Issue 3 https://doi.org/10.1016/S1474-4422(14)70267-4	journal	March 2015
Elevated relapse rates in pediatric compared to adult MS persist for at least 6 years Benson, L. A.; Healy, B. C.; Gorman, M. P. Multiple Sclerosis and Related Disorders, Vol. 3, Issue 2 https://doi.org/10.1016/j.msard.2013.06.004	journal	March 2014
A Viral microRNA Cluster Regulates the Expression of PTEN, p27 and of a bcl-2 Homolog Bernhardt, Katharina; Haar, Janina; Tsai, Ming-Han PLOS Pathogens, Vol. 12, Issue 1 https://doi.org/10.1371/journal.ppat.1005405	journal	January 2016
MicroRNA in Control of Gene Expression: An Overview of Nuclear Functions Catalanotto, Caterina; Cogoni, Carlo; Zardo, Giuseppe International Journal of Molecular Sciences, Vol. 17, Issue 10 https://doi.org/10.3390/ijms17101712	journal	October 2016
Dicer Insufficiency and MicroRNA-155 Overexpression in Lupus Regulatory T Cells: An Apparent Paradox in the Setting of an Inflammatory Milieu Divekar, Anagha A.; Dubey, Shweta; Gangalum, Pallavi R. The Journal of Immunology, Vol. 186, Issue 2 https://doi.org/10.4049/jimmunol.1002218	journal	December 2010
MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis Du, Changsheng; Liu, Chang; Kang, Jiuhong Nature Immunology, Vol. 10, Issue 12 https://doi.org/10.1038/ni.1798	journal	October 2009
Dicer1 and miR-219 Are Required for Normal Oligodendrocyte Differentiation and Myelination Dugas, Jason C.; Cuellar, Trinna L.; Scholze, Anja Neuron, Vol. 65, Issue 5 https://doi.org/10.1016/j.neuron.2010.01.027	journal	March 2010
The contribution of oligodendrocytes and oligodendrocyte progenitor cells to central nervous system repair in multiple sclerosis: perspectives for remyelination therapeutic strategies Dulamea, AdrianaOctaviana Neural Regeneration Research, Vol. 12, Issue 12 https://doi.org/10.4103/1673-5374.221146	journal	January 2017
Exosomal microRNA signatures in multiple sclerosis reflect disease status Ebrahimkhani, Saeideh; Vafaee, Fatemeh; Young, Paul E. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14301-3	journal	October 2017
Non-coding RNAs in human disease Esteller, Manel Nature Reviews Genetics, Vol. 12, Issue 12 https://doi.org/10.1038/nrg3074	journal	November 2011
Neuroproteomics and microRNAs studies in multiple sclerosis: transforming research and clinical knowledge in biomarker research Fawaz, Cherine N.; Makki, Iman S.; Kazan, Jalal M. Expert Review of Proteomics, Vol. 12, Issue 6 https://doi.org/10.1586/14789450.2015.1099435	journal	October 2015
Downregulation of microRNA-24 and -181 parallels the upregulation of IFN-γ secreted by activated human CD4 lymphocytes Fayyad-Kazan, Hussein; Hamade, Eva; Rouas, Redouane Human Immunology, Vol. 75, Issue 7 https://doi.org/10.1016/j.humimm.2014.01.007	journal	July 2014
Decreased circulating miRNA levels in patients with primary progressive multiple sclerosis Fenoglio, Chiara; Ridolfi, Elisa; Cantoni, Claudia Multiple Sclerosis Journal, Vol. 19, Issue 14 https://doi.org/10.1177/1352458513485654	journal	November 2013
The Majority of MicroRNAs Detectable in Serum and Saliva Is Concentrated in Exosomes Gallo, Alessia; Tandon, Mayank; Alevizos, Ilias PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0030679	journal	March 2012
Circulating MicroRNAs as biomarkers for disease staging in multiple sclerosis Gandhi, Roopali; Healy, Brian; Gholipour, Taha Annals of Neurology, Vol. 73, Issue 6 https://doi.org/10.1002/ana.23880	journal	June 2013
Cause or Effect: Misregulation of microRNA Pathways in Neurodegeneration Gascon, Eduardo; Gao, Fen-Biao Frontiers in Neuroscience, Vol. 6 https://doi.org/10.3389/fnins.2012.00048	journal	January 2012
Uncoupling Malt1 Threshold Function from Paracaspase Activity Results in Destructive Autoimmune Inflammation Gewies, Andreas; Gorka, Oliver; Bergmann, Hanna Cell Reports, Vol. 9, Issue 4 https://doi.org/10.1016/j.celrep.2014.10.044	journal	November 2014
Regulated microRNAs in the CSF of patients with multiple sclerosis: A case-control study Haghikia, A.; Haghikia, A.; Hellwig, K. Neurology, Vol. 79, Issue 22 https://doi.org/10.1212/WNL.0b013e3182759621	journal	October 2012
Biomarkers of multiple sclerosis: current findings Harris, Violaine; Tuddenham, John; Sadiq, Saud Degenerative Neurological and Neuromuscular Disease, Vol. Volume 7 https://doi.org/10.2147/DNND.S98936	journal	January 2017
MicroRNA Expression Changes during Interferon-Beta Treatment in the Peripheral Blood of Multiple Sclerosis Patients Hecker, Michael; Thamilarasan, Madhan; Koczan, Dirk International Journal of Molecular Sciences, Vol. 14, Issue 8 https://doi.org/10.3390/ijms140816087	journal	August 2013
Biomarkers in multiple sclerosis Housley, William J.; Pitt, David; Hafler, David A. Clinical Immunology, Vol. 161, Issue 1 https://doi.org/10.1016/j.clim.2015.06.015	journal	November 2015
MicroRNAs associated with the pathogenesis of multiple sclerosis Huang, Qingrong; Xiao, Bo; Ma, Xinting Journal of Neuroimmunology, Vol. 295-296 https://doi.org/10.1016/j.jneuroim.2016.04.014	journal	June 2016
Overexpression of microRNA biogenesis machinery: Drosha, DGCR8 and Dicer in multiple sclerosis patients Jafari, Naser; Shaghaghi, Hassan; Mahmoodi, Davood Journal of Clinical Neuroscience, Vol. 22, Issue 1 https://doi.org/10.1016/j.jocn.2014.06.106	journal	January 2015
Malt1 protease inactivation efficiently dampens immune responses but causes spontaneous autoimmunity Jaworski, Maike; Marsland, Ben J.; Gehrig, Jasmine The EMBO Journal, Vol. 33, Issue 23 https://doi.org/10.15252/embj.201488987	journal	October 2014
MicroRNA regulate immune pathways in T-cells in multiple sclerosis (MS) Jernås, Margareta; Malmeström, Clas; Axelsson, Markus BMC Immunology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2172-14-32	journal	July 2013
Pathophysiology of translational regulation by microRNAs in multiple sclerosis Junker, Andreas FEBS Letters, Vol. 585, Issue 23 https://doi.org/10.1016/j.febslet.2011.03.052	journal	March 2011
MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47 Junker, Andreas; Krumbholz, Markus; Eisele, Sylvia Brain, Vol. 132, Issue 12 https://doi.org/10.1093/brain/awp300	journal	December 2009
Selected Extracellular microRNA as Potential Biomarkers of Multiple Sclerosis Activity—Preliminary Study Kacperska, Magdalena Justyna; Jastrzebski, Karol; Tomasik, Bartlomiej Journal of Molecular Neuroscience, Vol. 56, Issue 1 https://doi.org/10.1007/s12031-014-0476-3	journal	December 2014
Treatment with interferon beta-1b delays conversion to clinically definite and McDonald MS in patients with clinically isolated syndromes Kappos, L.; Polman, C. H.; Freedman, M. S. Neurology, Vol. 67, Issue 7 https://doi.org/10.1212/01.wnl.0000237641.33768.8d	journal	August 2006
Systematic review of genome-wide expression studies in multiple sclerosis Kemppinen, A. K.; Kaprio, J.; Palotie, A. BMJ Open, Vol. 1, Issue 1 https://doi.org/10.1136/bmjopen-2011-000053	journal	July 2011
Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions Koning, Nathalie; Bö, Lars; Hoek, Robert M. Annals of Neurology, Vol. 62, Issue 5 https://doi.org/10.1002/ana.21220	journal	November 2007
Epigenetics of Multiple Sclerosis: An Updated Review Küçükali, Cem İsmail; Kürtüncü, Murat; Çoban, Arzu NeuroMolecular Medicine, Vol. 17, Issue 2 https://doi.org/10.1007/s12017-014-8298-6	journal	March 2014
On the origin of EDSS Kurtzke, John F. Multiple Sclerosis and Related Disorders, Vol. 4, Issue 2 https://doi.org/10.1016/j.msard.2015.02.003	journal	March 2015
Circulating exosomes from patients with systemic lupus erythematosus induce a proinflammatory immune response Lee, Joo Youn; Park, Jin Kyun; Lee, Eun Young Arthritis Research & Therapy, Vol. 18, Issue 1 https://doi.org/10.1186/s13075-016-1159-y	journal	November 2016
Combined microRNA and mRNA expression analysis in pediatric multiple sclerosis: an integrated approach to uncover novel pathogenic mechanisms of the disease Liguori, Maria; Nuzziello, Nicoletta; Licciulli, Flavio Human Molecular Genetics, Vol. 27, Issue 1 https://doi.org/10.1093/hmg/ddx385	journal	October 2017
Dysregulation of microRNAs in autoimmune diseases: Pathogenesis, biomarkers and potential therapeutic targets Long, Hai; Wang, Xin; Chen, Yongjian Cancer Letters, Vol. 428 https://doi.org/10.1016/j.canlet.2018.04.016	journal	August 2018
Defining the clinical course of multiple sclerosis: Results of an international survey Lublin, F. D.; Reingold, S. C. Neurology, Vol. 46, Issue 4 https://doi.org/10.1212/WNL.46.4.907	journal	April 1996
Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR Lytle, J. R.; Yario, T. A.; Steitz, J. A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 23 https://doi.org/10.1073/pnas.0703820104	journal	May 2007
Dicer and microRNA expression in multiple sclerosis and response to interferon therapy Magner, William J.; Weinstock-Guttman, Bianca; Rho, Mina Journal of Neuroimmunology, Vol. 292 https://doi.org/10.1016/j.jneuroim.2016.01.009	journal	March 2016
A MicroRNA Targeting Dicer for Metastasis Control Martello, Graziano; Rosato, Antonio; Ferrari, Francesco Cell, Vol. 141, Issue 7 https://doi.org/10.1016/j.cell.2010.05.017	journal	June 2010
Increased number of circulating exosomes and their microRNA cargos are potential novel biomarkers in alcoholic hepatitis Momen-Heravi, Fatemeh; Saha, Banishree; Kodys, Karen Journal of Translational Medicine, Vol. 13, Issue 1 https://doi.org/10.1186/s12967-015-0623-9	journal	August 2015
Evaluation of Selected MicroRNAs Expression in Remission Phase of Multiple Sclerosis and Their Potential Link to Cognition, Depression, and Disability Niwald, Marta; Migdalska-Sęk, Monika; Brzeziańska-Lasota, Ewa Journal of Molecular Neuroscience, Vol. 63, Issue 3-4 https://doi.org/10.1007/s12031-017-0977-y	journal	October 2017
Investigating the Role of MicroRNA and Transcription Factor Co-regulatory Networks in Multiple Sclerosis Pathogenesis Nuzziello, Nicoletta; Vilardo, Laura; Pelucchi, Paride International Journal of Molecular Sciences, Vol. 19, Issue 11 https://doi.org/10.3390/ijms19113652	journal	November 2018
microRNA Regulation of Inflammatory Responses O'Connell, Ryan M.; Rao, Dinesh S.; Baltimore, David Annual Review of Immunology, Vol. 30, Issue 1 https://doi.org/10.1146/annurev-immunol-020711-075013	journal	April 2012
Multiple sclerosis genetics—is the glass half full, or half empty? Oksenberg, Jorge R.; Baranzini, Sergio E. Nature Reviews Neurology, Vol. 6, Issue 8 https://doi.org/10.1038/nrneurol.2010.91	journal	July 2010
Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis Olsson, Tomas; Barcellos, Lisa F.; Alfredsson, Lars Nature Reviews Neurology, Vol. 13, Issue 1 https://doi.org/10.1038/nrneurol.2016.187	journal	December 2016
Biomarkers in Multiple Sclerosis Paul, Anu; Comabella, Manuel; Gandhi, Roopali Cold Spring Harbor Perspectives in Medicine, Vol. 9, Issue 3 https://doi.org/10.1101/cshperspect.a029058	journal	March 2018
Integrated systems for exosome investigation Peterson, Maureen F.; Otoc, Nicole; Sethi, Jasmine K. Methods, Vol. 87 https://doi.org/10.1016/j.ymeth.2015.04.015	journal	October 2015
Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria Polman, Chris H.; Reingold, Stephen C.; Banwell, Brenda Annals of Neurology, Vol. 69, Issue 2 https://doi.org/10.1002/ana.22366	journal	February 2011
MicroRNAs 24 and 27 Suppress Allergic Inflammation and Target a Network of Regulators of T Helper 2 Cell-Associated Cytokine Production Pua, Heather H.; Steiner, David F.; Patel, Sana Immunity, Vol. 44, Issue 4 https://doi.org/10.1016/j.immuni.2016.01.003	journal	April 2016
What are exosomes and how can they be used in multiple sclerosis therapy? Pusic, Aya D.; Pusic, Kae M.; Kraig, Richard P. Expert Review of Neurotherapeutics, Vol. 14, Issue 4 https://doi.org/10.1586/14737175.2014.890893	journal	February 2014
miRNAs in cerebrospinal fluid identify patients with MS and specifically those with lipid-specific oligoclonal IgM bands Quintana, Ester; Ortega, Francisco José; Robles-Cedeño, René Multiple Sclerosis Journal, Vol. 23, Issue 13 https://doi.org/10.1177/1352458516684213	journal	January 2017
Association Between Serum MicroRNAs and Magnetic Resonance Imaging Measures of Multiple Sclerosis Severity Regev, Keren; Healy, Brian C.; Khalid, Fariha JAMA Neurology, Vol. 74, Issue 3 https://doi.org/10.1001/jamaneurol.2016.5197	journal	March 2017
Comprehensive evaluation of serum microRNAs as biomarkers in multiple sclerosis Regev, Keren; Paul, Anu; Healy, Brian Neurology - Neuroimmunology Neuroinflammation, Vol. 3, Issue 5 https://doi.org/10.1212/NXI.0000000000000267	journal	August 2016
Multiple Sclerosis Severity Score: Using disability and disease duration to rate disease severity Roxburgh, R. H. S. R.; Seaman, S. R.; Masterman, T. Neurology, Vol. 64, Issue 7 https://doi.org/10.1212/01.WNL.0000156155.19270.F8	journal	April 2005
Global exosome transcriptome profiling reveals biomarkers for multiple sclerosis Selmaj, Igor; Cichalewska, Maria; Namiecinska, Magdalena Annals of Neurology, Vol. 81, Issue 5 https://doi.org/10.1002/ana.24931	journal	May 2017
Extracellular miR-145, miR-223 and miR-326 expression signature allow for differential diagnosis of immune-mediated neuroinflammatory diseases Sharaf-Eldin, Wessam E.; Kishk, Nirmeen A.; Gad, Yehia Z. Journal of the Neurological Sciences, Vol. 383 https://doi.org/10.1016/j.jns.2017.11.014	journal	December 2017
Dicerablation in oligodendrocytes provokes neuronal impairment in mice Shin, Daesung; Shin, Ji-Yeon; McManus, Michael T. Annals of Neurology, Vol. 66, Issue 6 https://doi.org/10.1002/ana.21927	journal	December 2009
The role of miRNA in inflammation and autoimmunity Singh, Ram Pyare; Massachi, Israel; Manickavel, Sudhir Autoimmunity Reviews, Vol. 12, Issue 12 https://doi.org/10.1016/j.autrev.2013.07.003	journal	October 2013
Differential microRNA expression in blood in multiple sclerosis Søndergaard, Helle Bach; Hesse, Dan; Krakauer, Martin Multiple Sclerosis Journal, Vol. 19, Issue 14 https://doi.org/10.1177/1352458513490542	journal	June 2013
Interleukin-17 Production in Central Nervous System-Infiltrating T Cells and Glial Cells Is Associated with Active Disease in Multiple Sclerosis Tzartos, John S.; Friese, Manuel A.; Craner, Matthew J. The American Journal of Pathology, Vol. 172, Issue 1 https://doi.org/10.2353/ajpath.2008.070690	journal	January 2008
Circulating microRNAs as biomarkers in progressive multiple sclerosis Vistbakka, Julia; Elovaara, Irina; Lehtimäki, Terho Multiple Sclerosis Journal, Vol. 23, Issue 3 https://doi.org/10.1177/1352458516651141	journal	July 2016
Evaluation of serum miR-191-5p, miR-24-3p, miR-128-3p, and miR-376c-3 in multiple sclerosis patients Vistbakka, J.; Sumelahti, M. -L.; Lehtimäki, T. Acta Neurologica Scandinavica, Vol. 138, Issue 2 https://doi.org/10.1111/ane.12921	journal	March 2018
The identification of up-regulated ebv-miR-BHRF1-2-5p targeting MALT1 and ebv-miR-BHRF1-3 in the circulation of patients with multiple sclerosis Wang, Y. F.; He, D. D.; Liang, H. W. Clinical and Experimental Immunology, Vol. 189, Issue 1 https://doi.org/10.1111/cei.12954	journal	March 2017
MicroRNA-Mediated Control of Oligodendrocyte Differentiation Zhao, Xianghui; He, Xuelian; Han, Xiaolei Neuron, Vol. 65, Issue 5 https://doi.org/10.1016/j.neuron.2010.02.018	journal	March 2010
Identification of miRNA-21 and miRNA-24 in plasma as potential early stage markers of acute cerebral infarction Zhou, Jiansuo; Zhang, Jie Molecular Medicine Reports, Vol. 10, Issue 2 https://doi.org/10.3892/mmr.2014.2245	journal	May 2014
Further to the origin of EDSS (Response to: L. Kappos et al: “On the origin of Neurostatus” Multiple Sclerosis and Related Disorders 2015; 4: 186) Kurtzke, John F. Multiple Sclerosis and Related Disorders, Vol. 4, Issue 3 https://doi.org/10.1016/j.msard.2015.04.007	journal	May 2015
Oligodendrocytes and the “Micro Brake” of Progenitor Cell Proliferation Nave, Klaus-Armin Neuron, Vol. 65, Issue 5 https://doi.org/10.1016/j.neuron.2010.02.026	journal	March 2010
Measurement and clinical effect of grey matter pathology in multiple sclerosis Geurts, Jeroen JG; Calabrese, Massimiliano; Fisher, Elizabeth The Lancet Neurology, Vol. 11, Issue 12 https://doi.org/10.1016/s1474-4422(12)70230-2	journal	December 2012
The systematic search for risk factors in multiple sclerosis McKay, Kyla A.; Tremlett, Helen The Lancet Neurology, Vol. 14, Issue 3 https://doi.org/10.1016/s1474-4422(15)70015-3	journal	March 2015
Do patients with clinically isolated syndrome benefit from treatment with interferon β1b? Panitch, Hillel Nature Clinical Practice Neurology, Vol. 3, Issue 2 https://doi.org/10.1038/ncpneuro0397	journal	February 2007
Natural History of Multiple Sclerosis with Childhood Onset Renoux, Christel; Vukusic, Sandra; Mikaeloff, Yann New England Journal of Medicine, Vol. 356, Issue 25 https://doi.org/10.1056/nejmoa067597	journal	June 2007
The MicroRNA miR-191 Supports T Cell Survival Following Common γ Chain Signaling Lykken, Erik Allen; Li, Qi-Jing Journal of Biological Chemistry, Vol. 291, Issue 45 https://doi.org/10.1074/jbc.m116.741264	journal	November 2016
Classification, diagnosis, and differential diagnosis of multiple sclerosis Katz Sand, Ilana Current Opinion in Neurology, Vol. 28, Issue 3 https://doi.org/10.1097/wco.0000000000000206	journal	June 2015
Cerebrospinal fluid - physiology, analysis and interpretation of protein patterns for diagnosis of neurological diseases Reiber, Hansotto Multiple Sclerosis Journal, Vol. 4, Issue 3 https://doi.org/10.1177/135245859800400302	journal	June 1998
Correction to: Circulating exosomes from patients with systemic lupus erythematosus induce an proinflammatory immune response Lee, Joo Youn; Park, Jin Kyun; Lee, Eun Young Arthritis Research & Therapy, Vol. 22, Issue 1 https://doi.org/10.1186/s13075-020-02206-y	journal	May 2020
Circulating miR-150 in CSF is a novel candidate biomarker for multiple sclerosis Bergman, Petra; Piket, Eliane; Khademi, Mohsen Neurology - Neuroimmunology Neuroinflammation, Vol. 3, Issue 3 https://doi.org/10.1212/nxi.0000000000000219	journal	April 2016
Identification of MS-specific serum miRNAs in an international multicenter study Regev, Keren; Healy, Brian C.; Paul, Anu Neurology - Neuroimmunology Neuroinflammation, Vol. 5, Issue 5 https://doi.org/10.1212/nxi.0000000000000491	journal	August 2018
MicroRNAs in the CSF: Macro-advance in MS? Meinl, E.; Meister, G. Neurology, Vol. 79, Issue 22 https://doi.org/10.1212/wnl.0b013e31827597d1	journal	October 2012
Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS) Kurtzke, J. F. Neurology, Vol. 33, Issue 11 https://doi.org/10.1212/wnl.33.11.1444	journal	November 1983
Early onset multiple sclerosis: A longitudinal study Boiko, A.; Vorobeychik, G.; Paty, D. Neurology, Vol. 59, Issue 7 https://doi.org/10.1212/wnl.59.7.1006	journal	October 2002
MALT 1 protease: equilibrating immunity versus tolerance Bertossi, Arianna; Krappmann, Daniel The EMBO Journal, Vol. 33, Issue 23 https://doi.org/10.15252/embj.201490217	journal	October 2014
Interleukin-17—Extended Features of a Key Player in Multiple Sclerosis Gold, Ralf; Lühder, Fred The American Journal of Pathology, Vol. 172, Issue 1 https://doi.org/10.2353/ajpath.2008.070862	journal	January 2008
MicroRNA dysregulation in multiple sclerosis Jr, Omar de Faria; Moore, Craig S.; Kennedy, Timothy E. Frontiers in Genetics, Vol. 3 https://doi.org/10.3389/fgene.2012.00311	journal	January 2013
Circulating cell-free microRNA as biomarkers for screening, diagnosis and monitoring of neurodegenerative diseases and other neurologic pathologies Sheinerman, Kira S.; Umansky, Samuil R. Frontiers in Cellular Neuroscience, Vol. 7 https://doi.org/10.3389/fncel.2013.00150	journal	January 2013

Similar Records

MicroRNAs as disease progression biomarkers and therapeutic targets in experimental autoimmune encephalomyelitis model of multiple sclerosis

Journal Article · Fri Apr 03 00:00:00 EDT 2020 · Neural Regeneration Research · OSTI ID:1628702

Martinez, Bridget; Peplow, PhilipV

Increased frequency of {gamma}{delta} T cells in cerebrospinal fluid and peripheral blood of patients with multiple sclerosis: Reactivity, cytotoxicity, and T cell receptor V gene rearrangements

Journal Article · Mon May 01 00:00:00 EDT 1995 · Journal of Immunology · OSTI ID:1628702

Stinissen, P; Vandevyver, C; Medaer, R

Protective effects of pharmacological therapies in animal models of multiple sclerosis: a review of studies 2014–2019

Journal Article · Thu Jan 09 00:00:00 EST 2020 · Neural Regeneration Research · OSTI ID:1628702

Martinez, Bridget; Peplow, Philip V.

Related Subjects

60 APPLIED LIFE SCIENCES
cell biology
neurosciences
neurology
clinically isolated syndrome
CSF
disease progression
exosomes
humans
microRNA
multiple sclerosis
peripheral blood
phenotypes
serum

Title: MicroRNAs in blood and cerebrospinal fluid as diagnostic biomarkers of multiple sclerosis and to monitor disease progression

Citation Formats

References (91)

Similar Records

Related Subjects