Cited by 119

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Identification of a circulating miRNA signature in extracellular vesicles collected from amyotrophic lateral sclerosis patients

Saucier, Daniel, Wajnberg, Gabriel, Roy, Jeremy, Beauregard, Annie-Pier, Chacko, Simi, Crapoulet, Nicolas, Fournier, Sébastien, Ghosh, Anirban, Lewis, Stephen M., Marrero, Alier, O'Connell, Colleen, Ouellette, Rodney J., Morin, Pier Jr·2019·Brain Research

Abstract

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder associated with the progressive death of motor neurons. Mean survival for a patient diagnosed with ALS is between 2 and 5 years. Early and efficient diagnosis of the various forms of ALS remains a significant challenge, resulting in a need to identify clinically-relevant biomarkers in readily accessible body fluids. microRNAs (miRNAs) are short, evolutionarily conserved non-coding RNA molecules involved in post-transcriptional regulation of gene expression that have received interest as disease biomarkers. This study was undertaken to identify an ALS-associated miRNA signature in extracellular vesicles (EVs), which can cross the blood-brain barrier and enter the circulatory system, obtained from plasma samples of persons diagnosed and living with ALS (PALS). Next-generation sequencing was used to identify differentially expressed miRNAs recovered from EVs of PALS and healthy controls. High-throughput sequencing data for select miRNA targets was subsequently validated by droplet digital PCR (ddPCR). This approach revealed elevated levels of 5 miRNAs and reduced levels of 22 miRNAs in EVs collected from PALS as compared with healthy controls subjects. miRNAs with relevance to ALS were found to be deregulated, including miR-9-5p, miR-183-5p, miR-338-3p and miR-1246. MiR-15a-5p and miR-193a-5p were identified for their diagnostic potential of ALS and association with disability progression, respectively. Function…

Overview

Integrity signals

Registry

Crossref · 10.1016/j.brainres.2018.12.016

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Show all 6 references

Research works printed but not linked: 46

  1. Agarwal, 2015, Predicting effective microRNA target sites in mammalian mRNAs, Elife, 12
  2. Belsh, 1996, The amyotrophic lateral sclerosis (ALS) patient perspective on misdiagnosis and its repercussions, J. Neurol. Sci., 139, 110, 10.1016/0022-510X(96)00088-3 · DOI
  3. Blandford, 2018, The roles of extracellular vesicle microRNAs in the central nervous system, Glia, 10.1002/glia.23445 · DOI
  4. Boylan, 2015, Familial amyotrophic lateral sclerosis, Neurol. Clin., 33, 807, 10.1016/j.ncl.2015.07.001 · DOI
  5. Byrne, 2011, Rate of familial amyotrophic lateral sclerosis: a systematic review and meta-analysis, J. Neurol. Neurosurg. Psychiatry, 82, 623, 10.1136/jnnp.2010.224501 · DOI
  6. Campos-Melo, 2013, Altered microRNA expression profile in Amyotrophic Lateral Sclerosis: a role in the regulation of NFL mRNA levels, Mol. Brain, 6, 26, 10.1186/1756-6606-6-26 · DOI
  7. Chai, 2016, Octamer 4/microRNA-1246 signaling axis drives Wnt/β-catenin activation in liver cancer stem cells, Hepatology, 64, 2062, 10.1002/hep.28821 · DOI
  8. Cheng, 2014, Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood, J. Extracell. Vesicles, 3, 23743, 10.3402/jev.v3.23743 · DOI · Paper page
  9. Cleveland, 2001, From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS, Nat. Rev. Neurosci., 2, 806, 10.1038/35097565 · DOI
  10. De Felice, 2014, miR-338-3p is over-expressed in blood, CFS, serum and spinal cord from sporadic amyotrophic lateral sclerosis patients, Neurogenetics, 15, 243, 10.1007/s10048-014-0420-2 · DOI
  11. Emde, 2015, Dysregulated miRNA biogenesis downstream of cellular stress and ALS-causing mutations: a new mechanism for ALS, EMBO J., 34, 2633, 10.15252/embj.201490493 · DOI · Paper page
  12. Freischmidt, 2013, Systemic dysregulation of TDP-43 binding microRNAs in amyotrophic lateral sclerosis, Acta Neuropathol. Commun., 1, 42, 10.1186/2051-5960-1-42 · DOI
  13. Ghosh, 2014, Rapid isolation of extracellular vesicles from cell culture and biological fluids using a synthetic peptide with specific affinity for heat shock proteins, PLoS One, 9, 10.1371/journal.pone.0110443 · DOI
  14. Goode, 2016, ALS-FTLD associated mutations of SQSTM1 impact on Keap1-Nrf2 signalling, Mol. Cell. Neurosci., 76, 52, 10.1016/j.mcn.2016.08.004 · DOI
  15. Guo, 2017, A 9-microRNA signature in serum serves as a noninvasive biomarker in early diagnosis of Alzheimer's Disease, J. Alzheimers Dis., 60, 1365, 10.3233/JAD-170343 · DOI
  16. Hogden, 2017, Amyotrophic lateral sclerosis: improving care with a multidisciplinary approach, J. Multidiscip. Healthc., 10, 205, 10.2147/JMDH.S134992 · DOI
  17. Holm, 2018, Extracellular vesicles: multimodal envoys in neural maintenance and repair, Trends Neurosci., 41, 360, 10.1016/j.tins.2018.03.006 · DOI
  18. Huang da, 2009, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc., 4, 44, 10.1038/nprot.2008.211 · DOI · Paper page
  19. Ishii, 2000, Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages, J. Biol. Chem., 275, 16023, 10.1074/jbc.275.21.16023 · DOI
  20. John, 2004, Human MicroRNA Targets, PLoS Biol., 2, 10.1371/journal.pbio.0020363 · DOI · Paper page
  21. Johnson, 2018, Association of salivary MicroRNA changes with prolonged concussion symptoms, JAMA Pediatr., 172, 65, 10.1001/jamapediatrics.2017.3884 · DOI
  22. Kozomara, 2011, miRBase: integrating microRNA annotation and deep-sequencing data, Nucl. Acids Res., 39, D152, 10.1093/nar/gkq1027 · DOI · Paper page
  23. Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 · DOI · Paper page
  24. Lewis, 2003, Prediction of mammalian microRNA targets, Cell, 115, 787, 10.1016/S0092-8674(03)01018-3 · DOI · Paper page
  25. Li, 2013, The FTD/ALS-associated RNA-binding protein TDP-43 regulates the robustness of neuronal specification through microRNA-9a in Drosophila, Hum. Mol. Genet., 22, 218, 10.1093/hmg/dds420 · DOI
  26. Ling, 2010, ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS, Proc. Natl. Acad. Sci. U.S.A., 107, 13318, 10.1073/pnas.1008227107 · DOI
  27. Mall, 2013, Stability of miRNA in human urine supports its biomarker potential, Biomark. Med., 7, 623, 10.2217/bmm.13.44 · DOI
  28. Marcuzzo, 2015, Up-regulation of neural and cell cycle-related microRNAs in brain of amyotrophic lateral sclerosis mice at late disease stage, Mol. Brain, 8, 5, 10.1186/s13041-015-0095-0 · DOI
  29. Martin, 2012, Cutadapt removes adapter sequences from high-throughput sequencing reads, Bioinform. Action, 17, 10
  30. Matamala, 2018, Genome-wide circulating microRNA expression profiling reveals potential biomarkers for amyotrophic lateral sclerosis, Neurobiol. Aging, 64, 123, 10.1016/j.neurobiolaging.2017.12.020 · DOI
  31. Mitchell, 2008, Circulating microRNAs as stable blood-based markers for cancer detection, PNAS, 105, 10513, 10.1073/pnas.0804549105 · DOI · Paper page
  32. Paganoni, 2014, Diagnostic timelines and delays in diagnosing amyotrophic lateral sclerosis (ALS), Amyotroph. Lateral. Scler. Frontotemporal. Degener., 15, 453, 10.3109/21678421.2014.903974 · DOI
  33. Raheja, 2018, Correlating serum micrornas and clinical parameters in amyotrophic lateral sclerosis, Muscle Nerve, 58, 261, 10.1002/mus.26106 · DOI
  34. Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 · DOI · Paper page
  35. Robinson, 2010, A scaling normalization method for differential expression analysis of RNA-seq data, Genome Biol., 11, R25, 10.1186/gb-2010-11-3-r25 · DOI · Paper page
  36. Selmaj, 2017, Global exosome transcriptome profiling reveals biomarkers for multiple sclerosis, Ann. Neurol., 81, 703, 10.1002/ana.24931 · DOI
  37. Sproviero, 2018, Pathological proteins are transported by extracellular vesicles of sporadic amyotrophic lateral sclerosis patients, Front. Neurosci., 12, 487, 10.3389/fnins.2018.00487 · DOI
  38. Toivonen, 2014, MicroRNA-206: a potential circulating biomarker candidate for amyotrophic lateral sclerosis, PLoS One, 9, 10.1371/journal.pone.0089065 · DOI
  39. Vallelunga, 2014, Identification of circulating microRNAs for the differential diagnosis of Parkinson's disease and Multiple System Atrophy, Front. Cell. Neurosci., 8, 156, 10.3389/fncel.2014.00156 · DOI
  40. Venugopal, 1998, Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes, Oncogene, 17, 3145, 10.1038/sj.onc.1202237 · DOI
  41. Wakabayashi, 2014, Analysis of microRNA from archived formalin-fixed paraffin-embedded specimens of amyotrophic lateral sclerosis, Acta Neuropathol. Commun., 2, 173, 10.1186/s40478-014-0173-z · DOI
  42. Waller, 2018, Small RNA sequencing of sporadic amyotrophic lateral sclerosis cerebrospinal fluid reveals differentially expressed miRNAs related to neural and glial activity, Front. Neurosci., 11, 731, 10.3389/fnins.2017.00731 · DOI
  43. Wang, 2014, Effect of the human SOD1-G93A gene on the Nrf2/ARE signaling pathway in NSC-34 cells, Mol. Med. Rep., 9, 2453, 10.3892/mmr.2014.2087 · DOI
  44. Witte, 2016, A systematic investigation of parameters influencing droplet rain in the listeria monocytogenes prfA assay - reduction of ambiguous results in ddPCR, PLoS One, 11, 10.1371/journal.pone.0168179 · DOI
  45. Yu, 2013, Wnt Signaling is altered by spinal cord neuronal dysfunction in amyotrophic lateral sclerosis transgenic mice, Neurochem. Res., 38, 1904, 10.1007/s11064-013-1096-y · DOI
  46. Zhou, 2013, miRNA-9 expression is upregulated in the spinal cord of G93A-SOD1 transgenic mice, Int. J. Clin. Exp. Pathol., 6, 1826

Cited by

Sorted by citations

See all 119

Metadata

Authors
Saucier, D., Wajnberg, G., Roy, J., Beauregard, A.-P., Chacko, S., Crapoulet, N., Fournier, S., Ghosh, A., Lewis, S. M., Marrero, A., O'Connell, C., Ouellette, R. J., & Morin, P. J.
Venue
Brain Research
Publisher
Elsevier BV
Published
2019-04
Volume
1708
Pages
100-108
ISSN
0006-8993
Cited by
119
References
6
Language
en
Funders
  • ALS Canada
  • Brain Canada

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review