Downregulation of a Dorsal Root Ganglion-Specifically Enriched Long Noncoding RNA is Required for Neuropathic Pain by Negatively Regulating RALY-Triggered Ehmt2 Expression.


Journal

Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569

Informations de publication

Date de publication:
07 2021
Historique:
revised: 19 03 2021
received: 23 11 2020
entrez: 12 8 2021
pubmed: 13 8 2021
medline: 6 1 2022
Statut: ppublish

Résumé

Nerve injury-induced maladaptive changes of gene expression in dorsal root ganglion (DRG) neurons contribute to neuropathic pain. Long non-coding RNAs (lncRNAs) are emerging as key regulators of gene expression. Here, a conserved lncRNA is reported, named DRG-specifically enriched lncRNA (DS-lncRNA) for its high expression in DRG neurons. Peripheral nerve injury downregulates DS-lncRNA in injured DRG due, in part, to silencing of POU domain, class 4, transcription factor 3, a transcription factor that interacts with the DS-lncRNA gene promoter. Rescuing DS-lncRNA downregulation blocks nerve injury-induced increases in the transcriptional cofactor RALY-triggered DRG Ehmt2 mRNA and its encoding G9a protein, reverses the G9a-controlled downregulation of opioid receptors and Kcna2 in injured DRG, and attenuates nerve injury-induced pain hypersensitivities in male mice. Conversely, DS-lncRNA downregulation increases RALY-triggered Ehmt2/G9a expression and correspondingly decreases opioid receptor and Kcna2 expression in DRG, leading to neuropathic pain symptoms in male mice in the absence of nerve injury. Mechanistically, downregulated DS-lncRNA promotes more binding of increased RALY to RNA polymerase II and the Ehmt2 gene promoter and enhances Ehmt2 transcription in injured DRG. Thus, downregulation of DS-lncRNA likely contributes to neuropathic pain by negatively regulating the expression of RALY-triggered Ehmt2/G9a, a key neuropathic pain player, in DRG neurons.

Identifiants

pubmed: 34383386
doi: 10.1002/advs.202004515
pmc: PMC8356248
doi:

Substances chimiques

Heterogeneous-Nuclear Ribonucleoprotein Group C 0
RNA, Long Noncoding 0
Raly protein, mouse 0
G9a protein, mouse EC 2.1.1.43
Histone-Lysine N-Methyltransferase EC 2.1.1.43

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2004515

Subventions

Organisme : NIH HHS
ID : RFNS113881
Pays : United States
Organisme : NIH HHS
ID : R01NS117484
Pays : United States
Organisme : NIH HHS
ID : 1S10OD025047-01
Pays : United States
Organisme : NIH HHS
ID : NS046593
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS117484
Pays : United States
Organisme : NIH HHS
ID : S10 OD025047
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS111553
Pays : United States
Organisme : NINDS NIH HHS
ID : P30 NS046593
Pays : United States
Organisme : NIH HHS
ID : R01NS111553
Pays : United States

Informations de copyright

© 2021 The Authors. Advanced Science published by Wiley‐VCH GmbH.

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Auteurs

Zhiqiang Pan (Z)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Shibin Du (S)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Kun Wang (K)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Xinying Guo (X)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Qingxiang Mao (Q)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Xiaozhou Feng (X)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Lina Huang (L)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Shaogen Wu (S)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Bailing Hou (B)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Yun-Juan Chang (YJ)

The Office of Advanced Research Computing, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Tong Liu (T)

Center for Advanced Proteomics Research, Departments of Biochemistry, Microbiology & Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Tong Chen (T)

Center for Advanced Proteomics Research, Departments of Biochemistry, Microbiology & Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Hong Li (H)

Center for Advanced Proteomics Research, Departments of Biochemistry, Microbiology & Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Thomas Bachmann (T)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Alex Bekker (A)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Huijuan Hu (H)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.
Department of Physiology, Pharmacology & Neuroscience, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

Yuan-Xiang Tao (YX)

Department of Anesthesiology, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.
Department of Physiology, Pharmacology & Neuroscience, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.
Department of Cell Biology & Molecular Medicine, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA.

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Classifications MeSH