Cited by 41RNA Interference and Gene DeliveryNeuroinflammation and Neurodegeneration MechanismsCancer-related molecular mechanisms research

Role of piRNA biogenesis and its neuronal function in the development of neurodegenerative diseases

Open access
Sato, Kaoru, Takayama, Ken-ichi, Inoue, Satoshi·2023·Frontiers in Aging Neuroscience

Abstract

Neurodegenerative diseases, such as Alzheimer’s disease (AD), Parkinson’s disease (PD), and amyotrophic lateral sclerosis (ALS), are caused by neuronal loss and dysfunction. Despite remarkable improvements in our understanding of these pathogeneses, serious worldwide problems with significant public health burdens are remained. Therefore, new efficient diagnostic and therapeutic strategies are urgently required. PIWI-interacting RNAs (piRNAs) are a major class of small non-coding RNAs that silence gene expression through transcriptional and post-transcriptional processes. Recent studies have demonstrated that piRNAs, originally found in the germ line, are also produced in non-gonadal somatic cells, including neurons, and further revealed the emerging roles of piRNAs, including their roles in neurodevelopment, aging, and neurodegenerative diseases. In this review, we aimed to summarize the current knowledge regarding the piRNA roles in the pathophysiology of neurodegenerative diseases. In this context, we first reviewed on recent updates on neuronal piRNA functions, including biogenesis, axon regeneration, behavior, and memory formation, in humans and mice. We also discuss the aberrant expression and dysregulation of neuronal piRNAs in neurodegenerative diseases, such as AD, PD, and ALS. Moreover, we review pioneering preclinical studies on piRNAs as biomarkers and therapeutic targets. Elucidation of the mechanisms underlying piRNA biogenesis and their functions in the brain would provide new perspectives for the clinical diagnosis and treatment of AD and various neurodegenerative diseases.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fnagi.2023.1157818

Cites

11 of 11 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Numerous reports have detected small RNAs with piRNA length and sequence features in the brain via small RNA sequencing, including in postnatal mouse brain development.

    “There are numerous reports of small RNAs with piRNA length and sequence features being detected in the brain via small RNA sequencing, including in postnatal mouse brain development”

    From The Role of Retrotransposons and Endogenous Retroviruses in Age-Dependent Neurodegenerative Disorders (2024) · cites this paper as Sato et al. 2023

    The Introduction and “Neuronal expression of piRNAs” section (pages unavailable) describe piRNA length and report multiple studies detecting piRNAs in brains. The Introduction links small-RNA discovery generally to next-generation sequencing, but our copy does not establish that the cited brain detections used small RNA sequencing or describe detection during postnatal mouse brain development. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 86

  1. Abdelhamid R. F. Ogawa K. Beck G. Ikenaka K. Takeuchi E. Yasumizu Y.. (2022). piRNA/PIWI protein complex as a potential biomarker in sporadic amyotrophic lateral sclerosis. Mol. Neurobiol. 59, 1693– 1705. doi: 10.1007/s12035-021-02686-2, PMID: 35015250 PMC8882100 · DOI
  2. Andrews P. W. (1984). Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev. Biol. 103, 285– 293. doi: 10.1016/0012-1606(84)90316-6, PMID: 6144603 · DOI · Paper page
  3. Aravin A. Gaidatzis D. Pfeffer S. Lagos-Quintana M. Landgraf P. Iovino N.. (2006). A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203– 207. doi: 10.1038/nature04916 16751777 · DOI · Paper page
  4. Bartels A. L. Leenders K. L. (2010). Cyclooxygenase and neuroinflammation in Parkinson’s disease neurodegeneration. Curr. Neuropharmacol. 8, 62– 68. doi: 10.2174/157015910790909485, PMID: 20808546 PMC2866462 · DOI
  5. Bernheimer H. Birkmayer W. Hornykiewicz O. Jellinger K. Seitelberger F. (1973). Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 20, 415– 455. doi: 10.1016/0022-510x(73)90175-5, PMID: 4272516 · DOI
  6. Bhatheja K. Field J. (2006). Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell Biol. 38, 1995– 1999. doi: 10.1016/j.biocel.2006.05.007, PMID: 16807057 · DOI
  7. Braak H. Braak E. (1990). Alzheimer’s disease: striatal amyloid deposits and neurofibrillary changes. J. Neuropathol. Exp. Neurol. 49, 215– 224. doi: 10.1097/00005072-199005000-00003 1692337 · DOI
  8. Braak H. Braak E. (1996). Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol. 92, 197– 201. doi: 10.1007/s004010050508, PMID: 8841666 · DOI · Paper page
  9. Brennecke J. Aravin A. A. Stark A. Dus M. Kellis M. Sachidanandam R.. (2007). Discrete small RNA-generating loci as master regulators of transposon activity in drosophila. Cells 128, 1089– 1103. doi: 10.1016/j.cell.2007.01.043, PMID: 17346786 · DOI · Paper page
  10. Brown R. H. Al-Chalabi A. (2017). Amyotrophic lateral sclerosis. N. Engl. J. Med. 377, 162– 172. doi: 10.1056/NEJMra1603471 28700839 · DOI
  11. Campbell M. R. Ashrafzadeh-Kian S. Petersen R. C. Mielke M. M. Syrjanen J. A. van Harten A. C.. (2021). P-tau/Aβ42 and Aβ42/40 ratios in CSF are equally predictive of amyloid PET status. Alzheimers Dement. 13: e12190. doi: 10.1002/dad2.12190, PMID: 34027020 PMC8129859 · DOI
  12. Ching Y. P. Pang A. S. Lam W. H. Qi R. Z. Wang J. H. (2002). Identification of a neuronal Cdk5 activator-binding protein as Cdk5 inhibitor. J. Biol. Chem. 277, 15237– 15240. doi: 10.1074/jbc.C200032200, PMID: 11882646 · DOI
  13. Choong C. J. Okuno T. Ikenaka K. Baba K. Hayakawa H. Koike M.. (2021). Alternative mitochondrial quality control mediated by extracellular release. Autophagy 17, 2962– 2974. doi: 10.1080/15548627.2020.1848130, PMID: 33218272 PMC8525996 · DOI
  14. Croce N. Gelfo F. Ciotti M. T. Federici G. Caltagirone C. Bernardini S.. (2013). NPY modulates miR-30a-5p and BDNF in opposite direction in an in vitro model of Alzheimer disease: a possible role in neuroprotection. Mol. Cell. Biochem. 376, 189– 195. doi: 10.1007/s11010-013-1567-0, PMID: 23358924 · DOI
  15. Czech B. Munafò M. Ciabrelli F. Eastwood E. L. Fabry M. H. Kneuss E.. (2018). piRNA-guided genome defense: from biogenesis to silencing. Annu. Rev. Genet. 52, 131– 157. doi: 10.1146/annurev-genet-120417-031441, PMID: 30476449 PMC10784713 · DOI
  16. Dharap A. Nakka V. P. Vemuganti R. (2011). Altered expression of PIWI RNA in the rat brain after transient focal ischemia. Stroke 42, 1105– 1109. doi: 10.1161/STROKEAHA.110.598391, PMID: 21311060 PMC3566794 · DOI
  17. Ding Y. Zhang Y. Xu C. Tao Q. H. Chen Y. G. (2013). HECT domain-containing E3 ubiquitin ligase NEDD4L negatively regulates Wnt signaling by targeting dishevelled for proteasomal degradation. J. Biol. Chem. 288, 8289– 8298. doi: 10.1074/jbc.M112.433185, PMID: 23396981 PMC3605647 · DOI
  18. Fang-Hu Zhang H. H. Yang B. X. Huang J. L. Shun J. L. Kong F. J.. (2015). Cdk5 contributes to inflammation-induced thermal hyperalgesia mediated by the p38 MAPK pathway in microglia. Brain Res. 1619, 166– 175. doi: 10.1016/j.brainres.2015.01.056 25819553 · DOI
  19. Ferrari K. J. Scelfo A. Jammula S. Cuomo A. Barozzi I. Stützer A.. (2014). Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol. Cell 53, 49– 62. doi: 10.1016/j.molcel.2013.10.030, PMID: 24289921 · DOI
  20. Foti S. C. Hargreaves I. Carrington S. Kiely A. P. Houlden H. Holton J. L. (2019). Cerebral mitochondrial electron transport chain dysfunction in multiple system atrophy and Parkinson’s disease. Sci. Rep. 9: 6559. doi: 10.1038/s41598-019-42902-7, PMID: 31024027 PMC6484105 · DOI
  21. Ghildiyal M. Seitz H. Horwich M. D. Li C. Du T. Lee S.. (2008). Endogenous siRNAs derived from transposons and mRNAs in drosophila somatic cells. Science 320, 1077– 1081. doi: 10.1126/science.1157396 18403677 PMC2953241 · DOI · Paper page
  22. Girard A. Sachidanandam R. Hannon G. J. Carmell M. A. (2006). A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199– 202. doi: 10.1038/nature04917, PMID: 16751776 · DOI · Paper page
  23. Goldman J. G. Postuma R. (2014). Premotor and nonmotor features of Parkinson’s disease. Curr. Opin. Neurol. 27, 434– 441. doi: 10.1097/WCO.0000000000000112, PMID: 24978368 PMC4181670 · DOI
  24. Goriaux C. Desset S. Renaud Y. Vaury C. Brasset E. (2014). Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep. 15, 411– 418. doi: 10.1002/embr.201337898, PMID: 24562610 PMC3989672 · DOI
  25. Hampel H. Hardy J. Blennow K. Chen C. Perry G. Kim S. H.. (2021). The amyloid-β pathway in Alzheimer’s disease. Mol. Psychiatry 26, 5481– 5503. doi: 10.1038/s41380-021-01249-0, PMID: 34456336 PMC8758495 · DOI · Paper page
  26. Hardiman O. Al-Chalabi A. Chio A. Corr E. M. Logroscino G. Robberecht W.. (2017). Amyotrophic lateral sclerosis. Nat. Rev. Dis. Primers. 3: 17071. doi: 10.1038/nrdp.2017.71 28980624 · DOI
  27. Hill E. J. Jiménez-González C. Tarczyluk M. Nagel D. A. Coleman M. D. Parri H. R. (2012). NT2 derived neuronal and astrocytic network signalling. PLoS One 7: e36098. doi: 10.1371/journal.pone.0036098, PMID: 22567128 PMC3342170 · DOI
  28. Huang X. Wong G. (2021). An old weapon with a new function: PIWI-interacting RNAs in neurodegenerative diseases. Transl. Neurodegener. 10: 9. doi: 10.1186/s40035-021-00233-6, PMID: 33685517 PMC7938595 · DOI
  29. Illarioshkin S. N. Klyushnikov S. A. Vigont V. A. Seliverstov Y. A. Kaznacheyeva E. V. (2018). Molecular pathogenesis in Huntington’s disease. Biochemistry 83, 1030– 1039. doi: 10.1134/S0006297918090043 30472941 · DOI
  30. Jain G. Stuendl A. Rao P. Berulava T. Pena Centeno T. Kaurani L.. (2019). A combined miRNA-piRNA signature to detect Alzheimer’s disease. Transl. Psychiatry 9: 250. doi: 10.1038/s41398-019-0579-2, PMID: 31591382 PMC6779890 · DOI · Paper page
  31. Julien C. L. Thompson J. C. Wild S. Yardumian P. Snowden J. S. Turner G.. (2007). Psychiatric disorders in preclinical Huntington’s disease. J. Neurol. Neurosurg. Psychiatry 78, 939– 943. doi: 10.1136/jnnp.2006.103309, PMID: 17178819 PMC2117854 · DOI
  32. Kalia L. V. Lang A. E. (2015). Parkinson’s disease. Lancet 386, 896– 912. doi: 10.1016/S0140-6736(14)61393-3 25904081 · DOI
  33. Kim K. W. (2019). PIWI proteins and piRNAs in the nervous system. Mol. Cells 42, 828– 835. doi: 10.14348/molcells.2019.0241, PMID: 31838836 PMC6939654 · DOI
  34. Kim V. N. Han J. Siomi M. C. (2009). Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126– 139. doi: 10.1038/nrm2632 19165215 · DOI
  35. Kozomara A. Birgaoanu M. Griffiths-Jones S. (2019). miRBase: from microRNA sequences to function. Nucleic Acids Res. 47, D155– D162. doi: 10.1093/nar/gky1141, PMID: 30423142 PMC6323917 · DOI · Paper page
  36. Ku H. Y. Lin H. (2014). PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression. Natl. Sci. Rev. 1, 205– 218. doi: 10.1093/nsr/nwu014, PMID: 25512877 PMC4265212 · DOI
  37. Lauretti E. Dabrowski K. Praticò D. (2021). The neurobiology of non-coding RNAs and Alzheimer’s disease pathogenesis: pathways, mechanisms and translational opportunities. Ageing Res. Rev. 71: 101425. doi: 10.1016/j.arr.2021.101425, PMID: 34384901 · DOI
  38. Lee E. J. Banerjee S. Zhou H. Jammalamadaka A. Arcila M. Manjunath B. S.. (2011). Identification of piRNAs in the central nervous system. RNA 17, 1090– 1099. doi: 10.1261/rna.2565011, PMID: 21515829 PMC3096041 · DOI · Paper page
  39. Leighton L. J. Wei W. Marshall P. R. Ratnu V. S. Li X. Zajaczkowski E. L.. (2019). Disrupting the hippocampal Piwi pathway enhances contextual fear memory in mice. Neurobiol. Learn. Mem. 161, 202– 209. doi: 10.1016/j.nlm.2019.04.002, PMID: 30965112 · DOI
  40. Liu K. C. Leuckx G. Sakano D. Seymour P. A. Mattsson C. L. Rautio L.. (2018). Inhibition of Cdk5 promotes β-cell differentiation from ductal progenitors. Diabetes 67, 58– 70. doi: 10.2337/db16-1587, PMID: 28986398 PMC6463766 · DOI
  41. MacDonald M. E. Ambrose C. M. Duyao M. P. Myers R. H. Lin C. Srinidhi L.. (1993). A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cells 72, 971– 983. doi: 10.1016/0092-8674(93)90585-e 8458085 · DOI · Paper page
  42. Mao Q. Fan L. Wang X. Lin X. Cao Y. Zheng C.. (2019). Transcriptome-wide piRNA profiling in human brains for aging genetic factors. Jacobs J. Genet. 4: 14. PMC7059831 32149191
  43. Masters C. L. Bateman R. Blennow K. Rowe C. C. Sperling R. A. Cummings J. L. (2015). Alzheimer’s disease. Nat. Rev. Dis. Primers. 1: 15056. doi: 10.1038/nrdp.2015.56 27188934 · DOI · Paper page
  44. McKhann G. Drachman D. Folstein M. Katzman R. Price D. Stadlan E. M. (1984). Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology 34, 939– 944. doi: 10.1212/wnl.34.7.939, PMID: 6610841 · DOI · Paper page
  45. Moody J. D. Levy S. Mathieu J. Xing Y. Kim W. Dong C.. (2017). First critical repressive H3K27me3 marks in embryonic stem cells identified using designed protein inhibitor. Proc. Natl. Acad. Sci. U. S. A. 114, 10125– 10130. doi: 10.1073/pnas.1706907114, PMID: 28864533 PMC5617284 · DOI
  46. Moutal A. Luo S. Largent-Milnes T. M. Vanderah T. W. Khanna R. (2019). Cdk5-mediated CRMP2 phosphorylation is necessary and sufficient for peripheral neuropathic pain. Neurobiol. Pain 5: 100022. doi: 10.1016/j.ynpai.2018.07.003, PMID: 31080913 PMC6505708 · DOI
  47. Müller M. Kuiperij H. B. Claassen J. A. Küsters B. Verbeek M. M. (2014). MicroRNAs in Alzheimer’s disease: differential expression in hippocampus and cell-free cerebrospinal fluid. Neurobiol. Aging 35, 152– 158. doi: 10.1016/j.neurobiolaging.2013.07.005 23962497 · DOI
  48. Nandi S. Chandramohan D. Fioriti L. Melnick A. M. Hébert J. M. Mason C. E.. (2016). Roles for small noncoding RNAs in silencing of retrotransposons in the mammalian brain. Proc. Natl. Acad. Sci. USA 113, 12697– 12702. doi: 10.1073/pnas.1609287113 27791114 PMC5111663 · DOI
  49. Nguyen H. P. Van Broeckhoven C. van der Zee J. (2018). ALS genes in the genomic era and their implications for FTD. Trends Genet. 34, 404– 423. doi: 10.1016/j.tig.2018.03.001, PMID: 29605155 · DOI
  50. Panero R. Rinaldi A. Memoli D. Nassa G. Ravo M. Rizzo F.. (2017). iSmaRT: a toolkit for a comprehensive analysis of small RNA-Seq data. Bioinformatics 33, 938– 940. doi: 10.1093/bioinformatics/btw734, PMID: 28057684 · DOI
  51. Parhad S. S. Theurkauf W. E. (2019). Rapid evolution and conserved function of the piRNA pathway. Open Biol. 9: 180181. doi: 10.1098/rsob.180181, PMID: 30958115 PMC6367137 · DOI
  52. Perera B. P. U. Tsai Z. T. Colwell M. L. Jones T. R. Goodrich J. M. Wang K.. (2019). Somatic expression of piRNA and associated machinery in the mouse identifies short, tissue-specific piRNA. Epigenetics 14, 504– 521. doi: 10.1080/15592294.2019.1600389, PMID: 30955436 PMC6557559 · DOI
  53. Phay M. Kim H. H. Yoo S. (2018). Analysis of piRNA-like small non-coding RNAs present in axons of adult sensory neurons. Mol. Neurobiol. 55, 483– 494. doi: 10.1007/s12035-016-0340-2, PMID: 27966078 PMC5901696 · DOI
  54. Pleasure S. J. Lee V. M. (1993). NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res. 35, 585– 602. doi: 10.1002/jnr.490350603 8411264 · DOI
  55. Prasad A. Bharathi V. Sivalingam V. Girdhar A. Patel B. K. (2019). Molecular mechanisms of TDP-43 Misfolding and pathology in amyotrophic lateral sclerosis. Front. Mol. Neurosci. 12: 25. doi: 10.3389/fnmol.2019.00025, PMID: 30837838 PMC6382748 · DOI
  56. Rajasethupathy P. Antonov I. Sheridan R. Frey S. Sander C. Tuschl T.. (2012). A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cells 149, 693– 707. doi: 10.1016/j.cell.2012.02.057, PMID: 22541438 PMC3442366 · DOI
  57. Rojas-Ríos P. Simonelig M. (2018). piRNAs and PIWI proteins: regulators of gene expression in development and stem cells. Development 145: dev161786. doi: 10.1242/dev.161786 30194260 · DOI
  58. Roy J. Sarkar A. Parida S. Ghosh Z. Mallick B. (2017). Small RNA sequencing revealed dysregulated piRNAs in Alzheimer’s disease and their probable role in pathogenesis. Mol. Biosyst. 13, 565– 576. doi: 10.1039/c6mb00699j, PMID: 28127595 · DOI · Paper page
  59. Sasaki T. Shiohama A. Minoshima S. Shimizu N. (2003). Identification of eight members of the Argonaute family in the human genome. Genomics 82, 323– 330. doi: 10.1016/s0888-7543(03)00129-0, PMID: 12906857 · DOI
  60. Sato K. Siomi M. C. (2018). Two distinct transcriptional controls triggered by nuclear Piwi-piRISCs in the drosophila piRNA pathway. Curr. Opin. Struct. Biol. 53, 69– 76. doi: 10.1016/j.sbi.2018.06.005, PMID: 29990672 · DOI
  61. Sato K. Siomi M. C. (2020). The piRNA pathway in drosophila ovarian germ and somatic cells. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 96, 32– 42. doi: 10.2183/pjab.96.003, PMID: 31932527 PMC6974405 · DOI
  62. Sato K. Takayama K. I. Hashimoto M. Inoue S. (2021). Transcriptional and post-transcriptional regulations of amyloid-β precursor protein (APP) mRNA. Front. Aging 2: 721579. doi: 10.3389/fragi.2021.721579, PMID: 35822056 PMC9261399 · DOI
  63. Siomi M. C. Sato K. Pezic D. Aravin A. A. (2011). PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12, 246– 258. doi: 10.1038/nrm3089, PMID: 21427766 · DOI · Paper page
  64. Sohn E. J. Jo Y. R. Park H. T. (2019). Downregulation MIWI-piRNA regulates the migration of Schwann cells in peripheral nerve injury. Biochem. Biophys. Res. Commun. 519, 605– 612. doi: 10.1016/j.bbrc.2019.09.008, PMID: 31540693 · DOI
  65. Soria Lopez J. A. González H. M. Léger G. C. (2019). Alzheimer’s disease. Handb. Clin. Neurol. 167, 231– 255. doi: 10.1016/B978-0-12-804766-8.00013-3 31753135 · DOI
  66. Strand A. D. Aragaki A. K. Shaw D. Bird T. Holton J. Turner C.. (2005). Gene expression in Huntington’s disease skeletal muscle: a potential biomarker. Hum. Mol. Genet. 14, 1863– 1876. doi: 10.1093/hmg/ddi192, PMID: 15888475 · DOI
  67. Subhramanyam C. S. Cao Q. Wang C. Heng Z. S. L. Zhou Z. Hu Q. (2020). Role of PIWI-like 4 in modulating neuronal differentiation from human embryonal carcinoma cells. RNA Biol. 17, 1613– 1624. doi: 10.1080/15476286.2020.1757896, PMID: 32372724 PMC7567516 · DOI
  68. Subhramanyam C. S. Cao Q. Wang C. Heng Z. S. Zhou Z. Hu Q. (2022). piRNAs interact with cold-shock domain-containing RNA binding proteins and regulate neuronal gene expression during differentiation. Mol. Neurobiol. 59, 1285– 1300. doi: 10.1007/s12035-021-02678-2, PMID: 34982407 · DOI
  69. Tabrizi S. J. Flower M. D. Ross C. A. Wild E. J. (2020). Huntington disease: new insights into molecular pathogenesis and therapeutic opportunities. Nat. Rev. Neurol. 16, 529– 546. doi: 10.1038/s41582-020-0389-4, PMID: 32796930 · DOI
  70. Talbott E. O. Malek A. M. Lacomis D. (2016). The epidemiology of amyotrophic lateral sclerosis. Handb. Clin. Neurol. 138, 225– 238. doi: 10.1016/B978-0-12-802973-2.00013-6 27637961 · DOI · Paper page
  71. Vagin V. V. Sigova A. Li C. Seitz H. Gvozdev V. Zamore P. D. (2006). A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320– 324. doi: 10.1126/science.1129333, PMID: 16809489 · DOI
  72. van Es M. A. Hardiman O. Chio A. Al-Chalabi A. Pasterkamp R. J. Veldink J. H.. (2017). Amyotrophic lateral sclerosis. Lancet 390, 2084– 2098. doi: 10.1016/S0140-6736(17)31287-4 28552366 · DOI
  73. Wakisaka K. T. Tanaka R. Hirashima T. Muraoka Y. Azuma Y. Yoshida H.. (2019). Novel roles of drosophila FUS and Aub responsible for piRNA biogenesis in neuronal disorders. Brain Res. 1708, 207– 219. doi: 10.1016/j.brainres.2018.12.028, PMID: 30578769 · DOI
  74. Walker F. O. (2007). Huntington’s disease. Lancet 369, 218– 228. doi: 10.1016/S0140-6736(07)60111-1 17240289 · DOI
  75. Waller R. Wyles M. Heath P. R. Kazoka M. Wollff H. Shaw P. J.. (2017). Small RNA sequencing of sporadic amyotrophic lateral sclerosis cerebrospinal fluid reveals differentially expressed miRNAs related to neural and glial activity. Front. Neurosci. 11: 731. doi: 10.3389/fnins.2017.00731, PMID: 29375285 PMC5767269 · DOI
  76. Wang C. Lin H. (2021). Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAs. Genome Biol. 22: 27. doi: 10.1186/s13059-020-02221-x, PMID: 33419460 PMC7792047 · DOI
  77. Wang J. Shi Y. Zhou H. Zhang P. Song T. Ying Z.. (2022). piRBase: integrating piRNA annotation in all aspects. Nucleic Acids Res. 50, D265– D272. doi: 10.1093/nar/gkab1012, PMID: 34871445 PMC8728152 · DOI
  78. Wang X. Ramat A. Simonelig M. Liu M. F. (2022). Emerging roles and functional mechanisms of PIWI-interacting RNAs. Nat. Rev. Mol. Cell Biol. 24, 123– 141. doi: 10.1038/s41580-022-00528-0, PMID: 36104626 · DOI
  79. Weil R. S. Lashley T. L. Bras J. Schrag A. E. Schott J. M. (2017). Current concepts and controversies in the pathogenesis of Parkinson’s disease dementia and dementia with Lewy bodies. F1000Res 6: 1604. doi: 10.12688/f1000research.11725.1, PMID: 28928962 PMC5580419 · DOI
  80. Wu P. H. Zamore P. D. (2021). Defining the functions of PIWI-interacting RNAs. Nat. Rev. Mol. Cell Biol. 22, 239– 240. doi: 10.1038/s41580-021-00336-y, PMID: 33483697 · DOI
  81. Yan Y. Wang C. (2006). Abeta42 is more rigid than Abeta40 at the C terminus: implications for Abeta aggregation and toxicity. J. Mol. Biol. 364, 853– 862. doi: 10.1016/j.jmb.2006.09.046, PMID: 17046788 · DOI
  82. Zhang C. Sha H. Peng Y. Wang Y. Liu C. Zhou X. (2019). PiRNA-DQ541777 contributes to neuropathic pain via targeting Cdk5rap1. J. Neurosci. 39, 9028– 9039. doi: 10.1523/JNEUROSCI.1602-19.2019, PMID: 31519819 PMC6832687 · DOI
  83. Zhang P. Si X. Skogerbø G. Wang J. Cui D. Li Y.. (2014). piRBase: A web resource assisting piRNA functional study. Database 2014, 2014: bau110. doi: 10.1093/database/bau110, PMID: 25425034 PMC4243270 · DOI
  84. Zhang T. Wong G. (2022). Dysregulation of human somatic piRNA expression in Parkinson’s disease subtypes and stages. Int. J. Mol. Sci. 23: 2469. doi: 10.3390/ijms23052469, PMID: 35269612 PMC8910154 · DOI
  85. Zovoilis A. Agbemenyah H. Y. Agis-Balboa R. C. Stilling R. M. Edbauer D. Rao P.. (2011). microRNA-34c is a novel target to treat dementias. EMBO J. 30, 4299– 4308. doi: 10.1038/emboj.2011.327, PMID: 21946562 PMC3199394 · DOI · Paper page
  86. Zucchi E. Bonetto V. Sorarù G. Martinelli I. Parchi P. Liguori R.. (2020). Neurofilaments in motor neuron disorders: towards promising diagnostic and prognostic biomarkers. Mol. Neurodegener. 15: 58. doi: 10.1186/s13024-020-00406-3, PMID: 33059698 PMC7559190 · DOI

Cited by

Sorted by citations

Authors
Sato, K., Takayama, K.-I., & Inoue, S.
Affiliations
Tokyo Metropolitan Institute of Gerontology (JP)
Corresponding author
Inoue, Satoshi
Venue
Frontiers in Aging Neuroscience
Published
2023-05-03
Volume
15
Pages
1157818-1157818
ISSN
1663-4365 (ISSN-L)
OpenAlex
W4368405210
Cited by
41
References
11
Citations by year
2026: 7 · 2025: 17 · 2024: 14 · 2023: 3
FWCI
1.08
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Aging Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Kowa Company
  • Kowa Life Science Foundation
  • Japan Society for the Promotion of Science (21H04829, 20K06596, 20K07350, 23K06408)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Keywords
piRNA biogenesis, piRNA, neurodegenerative diseases, Alzheimer's disease, Parkinson's disease, amyotrophic lateral sclerosis, small RNA, axon regeneration, memory formation, biomarkers, therapeutic target

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