Home LiteratureArticle Details
PMID: 20826656 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Induced loss of ADAR2 engenders slow death of motor neurons from Q/R site-unedited GluR2.

Hideyama T, Yamashita T, Suzuki T, Tsuji S, Higuchi M, Seeburg PH, Takahashi R, Misawa H, Kwak S

Abstract

GluR2 is a subunit of the AMPA receptor, and the adenosine for the Q/R site of its pre-mRNA is converted to inosine (A-to-I conversion) by the enzyme called adenosine deaminase acting on RNA 2 (ADAR2). Failure of A-to-I conversion at this site affects multiple AMPA receptor properties, including the Ca(2+) permeability of the receptor-coupled ion channel, thereby inducing fatal epilepsy in mice (Brusa et al., 1995; Feldmeyer et al., 1999). In addition, inefficient GluR2 Q/R site editing is a disease-specific molecular dysfunction found in the motor neurons of sporadic amyotrophic lateral sclerosis (ALS) patients (Kawahara et al., 2004). Here, we generated genetically modified mice (designated as AR2) in which the ADAR2 gene was conditionally targeted in motor neurons using the Cre/loxP system. These AR2 mice showed a decline in motor function commensurate with the slow death of ADAR2-deficient motor neurons in the spinal cord and cranial motor nerve nuclei. Notably, neurons in nuclei of oculomotor nerves, which often escape degeneration in ALS, were not decreased in number despite a significant decrease in GluR2 Q/R site editing. All cellular and phenotypic changes in AR2 mice were prevented when the mice carried endogenous GluR2 alleles engineered to express edited GluR2 without ADAR2 activity (Higuchi et al., 2000). Thus, loss of ADAR2 activity causes AMPA receptor-mediated death of motor neurons.

MeSH Terms
Adenosine Deaminase/deficiency Age Factors Amyotrophic Lateral Sclerosis/genetics,pathology,physiopathology Animals Behavior, Animal Brain Stem/cytology Calcium/metabolism Cell Death/genetics Disease Models, Animal Electromyography/methods Extracellular Matrix Proteins/genetics,metabolism Hyperkinesis/genetics,pathology,physiopathology Mice Mice, Inbred C57BL Mice, Knockout Motor Neurons/physiology Muscle, Skeletal/physiopathology Protein-Lysine 6-Oxidase/genetics,metabolism RNA Editing/physiology RNA, Messenger/metabolism RNA-Binding Proteins Reaction Time/genetics,physiology Receptors, AMPA/genetics,metabolism Rotarod Performance Test/methods Spinal Cord/cytology Vesicular Acetylcholine Transport Proteins/metabolism
Chemicals
Extracellular Matrix Proteins RNA, Messenger RNA-Binding Proteins Receptors, AMPA Slc18a3 protein, mouse Vesicular Acetylcholine Transport Proteins Lox protein, mouse Protein-Lysine 6-Oxidase ADARB1 protein, human Adenosine Deaminase glutamate receptor ionotropic, AMPA 2 Calcium
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Hideyama Takuto
Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, University of Tokyo, Bunkyo-ku, Tokyo, Japan.
Yamashita Takenari
Suzuki Takeshi
Tsuji Shoji
Higuchi Miyoko
Seeburg Peter H
Takahashi Ryosuke
Misawa Hidemi
Kwak Shin
References (40)
40 references, click to expand
  1. Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis.
    N Engl J Med. 1992 May 28;326(22):1464-8 PMID: 1349424
  2. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice.
    Science. 1995 Dec 8;270(5242):1677-80 PMID: 7502080
  3. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia.
    Neuron. 2006 Mar 2;49(5):719-33 PMID: 16504947
  4. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration.
    Mol Neurobiol. 2008 Aug;38(1):78-100 PMID: 18686046
  5. Glutamate receptors: RNA editing and death of motor neurons.
    Nature. 2004 Feb 26;427(6977):801 PMID: 14985749
  6. Genetics of sporadic amyotrophic lateral sclerosis.
    Hum Mol Genet. 2007 Oct 15;16 Spec No. 2:R233-42 PMID: 17911166
  7. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro.
    J Neurosci. 1996 Jul 1;16(13):4069-79 PMID: 8753869
  8. Genetic studies of amyotrophic lateral sclerosis: controversies and perspectives.
    Amyotroph Lateral Scler. 2009 Feb;10(1):1-14 PMID: 19110986
  9. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B.
    Nat Neurosci. 1999 Jan;2(1):57-64 PMID: 10195181
  10. GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis.
    J Neuropathol Exp Neurol. 2005 Jul;64(7):605-12 PMID: 16042312
  11. Modulation of RNA editing by functional nucleolar sequestration of ADAR2.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14018-23 PMID: 14612560
  12. Calcium signaling and neurodegenerative diseases.
    Trends Mol Med. 2009 Mar;15(3):89-100 PMID: 19230774
  13. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels.
    Cell. 1991 Oct 4;67(1):11-9 PMID: 1717158
  14. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum.
    Neuron. 2002 May 30;34(5):759-72 PMID: 12062022
  15. Low editing efficiency of GluR2 mRNA is associated with a low relative abundance of ADAR2 mRNA in white matter of normal human brain.
    Eur J Neurosci. 2003 Jul;18(1):23-33 PMID: 12859334
  16. Determination of editors at the novel A-to-I editing positions.
    Neurosci Res. 2008 Jun;61(2):201-6 PMID: 18407364
  17. A mammalian RNA editing enzyme.
    Nature. 1996 Feb 1;379(6564):460-4 PMID: 8559253
  18. Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit.
    Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5826-31 PMID: 15827116
  19. Systematic identification of abundant A-to-I editing sites in the human transcriptome.
    Nat Biotechnol. 2004 Aug;22(8):1001-5 PMID: 15258596
  20. Molecular identification and characterization of a family of kinases with homology to Ca2+/calmodulin-dependent protein kinases I/IV.
    J Biol Chem. 2006 Jul 21;281(29):20427-39 PMID: 16684769
  21. Regulation of dendritogenesis via a lipid-raft-associated Ca2+/calmodulin-dependent protein kinase CLICK-III/CaMKIgamma.
    Neuron. 2007 Jun 7;54(5):755-70 PMID: 17553424
  22. The AMPA receptor subunit GluR-B in its Q/R site-unedited form is not essential for brain development and function.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13777-82 PMID: 9811877
  23. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit.
    Neuron. 1992 Jan;8(1):189-98 PMID: 1370372
  24. Underediting of GluR2 mRNA, a neuronal death inducing molecular change in sporadic ALS, does not occur in motor neurons in ALS1 or SBMA.
    Neurosci Res. 2006 Jan;54(1):11-4 PMID: 16225946
  25. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing.
    Science. 2009 May 29;324(5931):1210-3 PMID: 19478186
  26. Altered RNA editing in mice lacking ADAR2 autoregulation.
    Mol Cell Biol. 2006 Jan;26(2):480-8 PMID: 16382140
  27. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2.
    Nature. 2000 Jul 6;406(6791):78-81 PMID: 10894545
  28. Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis.
    J Mol Med (Berl). 2005 Feb;83(2):110-20 PMID: 15624111
  29. VAChT-Cre. Fast and VAChT-Cre.Slow: postnatal expression of Cre recombinase in somatomotor neurons with different onset.
    Genesis. 2003 Sep;37(1):44-50 PMID: 14502577
  30. RNA editing of the glutamate receptor subunits GluR2 and GluR6 in human brain tissue.
    J Neurochem. 1994 Nov;63(5):1596-602 PMID: 7523595
  31. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia.
    Brain Res. 1995 Nov 20;699(2):297-304 PMID: 8616634
  32. Human spinal motoneurons express low relative abundance of GluR2 mRNA: an implication for excitotoxicity in ALS.
    J Neurochem. 2003 May;85(3):680-9 PMID: 12694394
  33. AMPA receptor tetramerization is mediated by Q/R editing.
    Neuron. 2003 Nov 13;40(4):763-74 PMID: 14622580
  34. A-to-I editing: new and old sites, functions and speculations.
    Neuron. 2002 Jul 3;35(1):17-20 PMID: 12123604
  35. Recent advances in the study of AMPA receptors.
    Nihon Yakurigaku Zasshi. 2003 Dec;122(6):515-26 PMID: 14639006
  36. Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease.
    Neuropathol Appl Neurobiol. 1993 Aug;19(4):291-9 PMID: 8232749
  37. Protective effect of parvalbumin on excitotoxic motor neuron death.
    Exp Neurol. 2002 Apr;174(2):150-61 PMID: 11922657
  38. Excitotoxicity and ALS: what is unique about the AMPA receptors expressed on spinal motor neurons?
    Amyotroph Lateral Scler Other Motor Neuron Disord. 2005 Sep;6(3):131-44 PMID: 16183555
  39. Editing of glutamate receptor subunit B pre-mRNA in vitro by site-specific deamination of adenosine.
    Nature. 1995 Mar 2;374(6517):77-81 PMID: 7870177
  40. Reduction of GluR2 RNA editing, a molecular change that increases calcium influx through AMPA receptors, selective in the spinal ventral gray of patients with amyotrophic lateral sclerosis.
    Ann Neurol. 1999 Dec;46(6):806-15 PMID: 10589532
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2010-09-08
Pages
11917-25
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6633551
Subset
IM
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]