Oligophrenin-1 (OPHN1), a gene involved in X-linked intellectual disability, undergoes RNA editing and alternative splicing during human brain development

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Barresi, Sabina ^a   Tomaselli, Sara ^a   Athanasiadis, Alekos ^b   Galeano, Federica ^a   Locatelli, Franco ^a,c   Bertini, Enrico ^a   Zanni, Ginevra ^a   Gallo, Angela ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; ADENOSINE DEAMINASE ACTING ON RNA 1; ADENOSINE DEAMINASE ACTING ON RNA 2; MESSENGER RNA PRECURSOR; UNCLASSIFIED DRUG; ADARB1 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NUCLEAR PROTEIN; OPHN1 PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA ISOFORM; RNA PRECURSOR;

ALTERNATIVE RNA SPLICING; ALU SEQUENCE; ARTICLE; ASTROCYTOMA CELL; BRAIN; BRAIN DEVELOPMENT; CEREBELLUM; CHILD; FETUS; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTELLECTUAL IMPAIRMENT; OLIGOPHRENIN 1 GENE; RNA EDITING; X CHROMOSOME LINKED DISORDER; X LINKED INTELLECTUAL DISABILITY; CELL LINE; CHEMISTRY; CONFORMATION; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENE ORDER; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; X LINKED MENTAL RETARDATION;

ADENOSINE DEAMINASE; ALTERNATIVE SPLICING; BASE SEQUENCE; BRAIN; CELL LINE; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; GTPASE-ACTIVATING PROTEINS; HUMANS; MENTAL RETARDATION, X-LINKED; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; ORGANOGENESIS; RNA EDITING; RNA ISOFORMS; RNA PRECURSORS; RNA-BINDING PROTEINS;

EID: 84898655795     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091351     Document Type: Article

References (67)

1. Billuart P, Bienvenu T, Ronce N, des Portes V, Vinet MC, et al. (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392: 923-926. (Pubitemid 28232063)
2. Ramakers GJ (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends in neurosciences 25: 191-199. (Pubitemid 34615536)
3. Bergmann C, Zerres K, Senderek J, Rudnik-Schoneborn S, Eggermann T, et al. (2003) Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cerebellar hypoplasia. Brain 126: 1537-1544. (Pubitemid 36834930)
4. Rocas D, Alix E, Michel J, Cordier MP, Labalme A, et al. (2013) Neuropathological features in a female fetus with OPHN1 deletion and cerebellar hypoplasia. European journal of medical genetics 56: 270-273.
5. Khelfaoui M, Denis C, van Galen E, de Bock F, Schmitt A, et al. (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J Neurosci 27: 9439-9450. (Pubitemid 47358207)
6. Khelfaoui M, Pavlowsky A, Powell AD, Valnegri P, Cheong KW, et al. (2009) Inhibition of RhoA pathway rescues the endocytosis defects in Oligophrenin1 mouse model of mental retardation. Human molecular genetics 18: 2575-2583.
7. Valnegri P, Khelfaoui M, Dorseuil O, Bassani S, Lagneaux C, et al. (2011) A circadian clock in hippocampus is regulated by interaction between oligophrenin-1 and Rev-erbalpha. Nature neuroscience 14: 1293-1301.
8. Nishikura K (2006) Editor meets silencer: crosstalk between RNA editing and RNA interference. Nat Rev Mol Cell Biol 7: 919-931. (Pubitemid 44871418)
9. Nishikura K (2010) Functions and regulation of RNA editing by ADAR deaminases. Annual review of biochemistry 79: 321-349.
10. Gallo A, Locatelli F (2011) ADARs: allies or enemies? The importance of A-to-I RNA editing in human disease: from cancer to HIV-1. Biological reviews of the Cambridge Philosophical Society 87: 95-110.
11. Athanasiadis A, Rich A, Maas S (2004) Widespread A-to-I RNA editing of Alucontaining mRNAs in the human transcriptome. PLoS biology 2: 2144-2158
12. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, et al. (2004) Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nature biotechnology 22: 1001-1005. (Pubitemid 39014477)
13. Blow M, Futreal PA, Wooster R, Stratton MR (2004) A survey of RNA editing in human brain. Genome research 14: 2379-2387. (Pubitemid 40012220)
14. Kim DD, Kim TT, Walsh T, Kobayashi Y, Matise TC, et al. (2004) Widespread RNA editing of embedded alu elements in the human transcriptome. Genome research 14: 1719-1725. (Pubitemid 39276429)
15. Chen LL, Carmichael GG (2008) Gene regulation by SINES and inosines: biological consequences of A-to-I editing of Alu element inverted repeats. Cell cycle 7: 3294-3301.
16. Wahlstedt H, Daniel C, Enstero M, Ohman M (2009) Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome research 19: 978-986.
17. Higuchi M, Maas S, Single FN, Hartner J, Rozov A, et al. (2000) Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406: 78-81. (Pubitemid 30460214)
18. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA (2000) A-to-I premRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102: 437-449.
19. Stapleton M, Carlson JW, Celniker SE (2006) RNA editing in Drosophila melanogaster: new targets and functional consequences. RNA 12: 1922-1932. (Pubitemid 44771752)
20. Seeburg PH, Higuchi M, Sprengel R (1998) RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res Brain Res Rev 26: 217-229. (Pubitemid 28318077)
21. Werry TD, Loiacono R, Sexton PM, Christopoulos A (2008) RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacology & therapeutics 119: 7-23.
22. Levanon EY, Hallegger M, Kinar Y, Shemesh R, Djinovic-Carugo K, et al. (2005) Evolutionarily conserved human targets of adenosine to inosine RNA editing. Nucleic acids research 33: 1162-1168. (Pubitemid 41439909)
23. Gallo A, Galardi S (2008) A-to-I RNA editing and cancer: From pathology to basic science. RNA biology 5: 135-139.
24. Galeano F, Rossetti C, Tomaselli S, Cifaldi L, Lezzerini M, et al. (2012) ADAR2-editing activity inhibits glioblastoma growth through the modulation of the CDC14B/Skp2/p21/p27 axis. Oncogene 32: 998-1009.
25. Cenci C, Barzotti R, Galeano F, Corbelli S, Rota R, et al. (2008) Downregulation of RNA editing in pediatric astrocytomas: ADAR2 editing activity inhibits cell migration and proliferation. The Journal of biological chemistry 283: 7251-7260.
26. Larder BA, Kohli A, Kellam P, Kemp SD, Kronick M, et al. (1993) Quantitative detection of HIV-1 drug resistance mutations by automated DNA sequencing. Nature 365: 671-673.
27. Kiran A, Baranov PV (2010) DARNED: a DAtabase of RNa EDiting in humans. Bioinformatics 26: 1772-1776.
28. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic acids research 31: 3406-3415. (Pubitemid 37442169)
29. Ljubimova JY, Khazenzon NM, Chen Z, Neyman YI, Turner L, et al. (2001) Gene expression abnormalities in human glial tumors identified by gene array. International journal of oncology 18: 287-295.
30. Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proceedings of the National Academy of Sciences of the United States of America 98: 14687-14692. (Pubitemid 33121452)
31. Nadif Kasri N, Nakano-Kobayashi A, Malinow R, Li B, Van Aelst L (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes & development 23: 1289-1302.
32. Ba W, van der Raadt J, Nadif Kasri N (2013) Rho GTPase signaling at the synapse: implications for intellectual disability. Experimental cell research 319: 2368-2374.
33. Mallela A and Nishikura K (2012) A-to-I editing of protein coding and noncoding RNAs. Critical reviews in biochemistry and molecular biology 47: 493-501.
34. Jepson JE, Reenan RA (2008) RNA editing in regulating gene expression in the brain. Biochimica et biophysica acta 1779: 459-470.
35. Morabito MV, Abbas AI, Hood JL, Kesterson RA, Jacobs MM, et al. (2010) Mice with altered serotonin 2C receptor RNA editing display characteristics of Prader-Willi syndrome. Neurobiology of disease 39: 169-180.
36. Rice GI, Kasher PR, Forte GM, Mannion NM, Greenwood SM, et al. (2012) Mutations in ADAR1 cause Aicardi-Goutieres syndrome associated with a type I interferon signature. Nature genetics 44: 1243-1248.
37. Morse DP, Bass BL (1997) Detection of inosine in messenger RNA by inosinespecific cleavage. Biochemistry 36: 8429-8434. (Pubitemid 27305124)
38. Paul MS, Bass BL (1998) Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. The EMBO journal 17: 1120-1127. (Pubitemid 28077665)
39. Greger IH, Khatri L, Ziff EB (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34: 759-772. (Pubitemid 34628738)
40. Li JB, Levanon EY, Yoon JK, Aach J, Xie B, et al. (2009) Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210-1213.
41. Zanni G, Saillour Y, Nagara M, Billuart P, Castelnau L, et al. (2005) Oligophrenin 1 mutations frequently cause X-linked mental retardation with cerebellar hypoplasia. Neurology 65: 1364-1369. (Pubitemid 41552762)
42. Bedeschi MF, Novelli A, Bernardini L, Parazzini C, Bianchi V, et al. (2008) Association of syndromic mental retardation with an Xq12q13.1 duplication encompassing the oligophrenin 1 gene. American journal of medical genetics 146A: 1718-1724. (Pubitemid 351975483)
43. Morse DP, Aruscavage PJ, Bass BL (2002) RNA hairpins in noncoding regions of human brain and Caenorhabditis elegans mRNA are edited by adenosine deaminases that act on RNA. Proceedings of the National Academy of Sciences of the United States of America 99: 7906-7911. (Pubitemid 34650978)
44. Lev-Maor G, Ram O, Kim E, Sela N, Goren A, et al. (2008) Intronic Alus influence alternative splicing. PLoS genetics 4: e1000204.
45. Lev-Maor G, Sorek R, Levanon EY, Paz N, Eisenberg E, et al. (2007) RNA-editing-mediated exon evolution. Genome biology 8: R29.
46. Lev-Maor G, Sorek R, Shomron N, Ast G (2003) The birth of an alternatively spliced exon: 39 splice-site selection in Alu exons. Science 300: 1288-1291. (Pubitemid 36618239)
47. Sakurai M, Yano T, Kawabata H, Ueda H, Suzuki T (2010) Inosine cyanoethylation identifies A-to-I RNA editing sites in the human transcriptome. Nature chemical biology 6: 733-740.
48. Yang L, Zhao L, Gan Z, He Z, Xu J, et al. (2010) Deficiency in RNA editing enzyme ADAR2 impairs regulated exocytosis. Faseb J.
49. Wang Q, Zhang Z, Blackwell K, Carmichael GG (2005) Vigilins bind to promiscuously A-to-I-edited RNAs and are involved in the formation of heterochromatin. Curr Biol 15: 384-391. (Pubitemid 40263374)
50. Greenberger S, Levanon EY, Paz-Yaacov N, Barzilai A, Safran M, et al. (2010) Consistent levels of A-to-I RNA editing across individuals in coding sequences and non-conserved Alu repeats. BMC genomics 11: 608.
51. Rueter SM, Dawson TR, Emeson RB (1999) Regulation of alternative splicing by RNA editing. Nature 399: 75-80.
52. Farajollahi S, Maas S (2010) Molecular diversity through RNA editing: a balancing act. Trends Genet 26: 221-230.
53. Beghini A, Ripamonti CB, Peterlongo P, Roversi G, Cairoli R, et al. (2000) RNA hyperediting and alternative splicing of hematopoietic cell phosphatase (PTPN6) gene in acute myeloid leukemia. Human molecular genetics 9: 2297-2304.
54. Veno MT, Bramsen JB, Bendixen C, Panitz F, Holm IE, et al. (2012) Spatiotemporal regulation of ADAR editing during development in porcine neural tissues. RNA biology 9: 1054-1065.
55. Greger IH, Khatri L, Kong X, Ziff EB (2003) AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40: 763-774. (Pubitemid 37431036)
56. Eberth A, Lundmark R, Gremer L, Dvorsky R, Koessmeier KT, et al. (2009) A BAR domain-mediated autoinhibitory mechanism for RhoGAPs of the GRAF family. The Biochemical journal 417: 371-377.
57. Fauchereau F, Herbrand U, Chafey P, Eberth A, Koulakoff A, et al. (2003) The RhoGAP activity of OPHN1, a new F-actin-binding protein, is negatively controlled by its amino-terminal domain. Molecular and cellular neurosciences 23: 574-586. (Pubitemid 36970219)
58. Santos-Reboucas CB, Belet S, Guedes de Almeida L, Ribeiro MG, Medina-Acosta E, et al. (2013) A novel in-frame deletion affecting the BAR domain of OPHN1 in a family with intellectual disability and hippocampal alterations. Eur J Hum Genet. doi: 10.1038/ejhg.2013.216.
59. Pirozzi F, Di Raimo FR, Zanni G, Bertini E, Billuart P, et al. (2011) Insertion of 16 amino acids in the BAR domain of the oligophrenin 1 protein causes mental retardation and cerebellar hypoplasia in an Italian family. Human mutation 32: E2294-2307.
60. Al-Owain M, Kaya N, Al-Zaidan H, Al-Hashmi N, Al-Bakheet A, et al. (2011) Novel intragenic deletion in OPHN1 in a family causing XLMR with cerebellar hypoplasia and distinctive facial appearance. Clinical genetics 79: 363-370.
61. Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35: 147-168.
62. Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neuroscience and biobehavioral reviews 27: 3-18. (Pubitemid 36535387)
63. Bhogal B, Jepson JE, Savva YA, Pepper AS, Reenan RA, et al. (2011) Modulation of dADAR-dependent RNA editing by the Drosophila fragile X mental retardation protein. Nature neuroscience 14: 1517-1524.
64. Doe CM, Relkovic D, Garfield AS, Dalley JW, Theobald DE, et al. (2009) Loss of the imprinted snoRNA mbii-52 leads to increased 5htr2c pre-RNA editing and altered 5HT2CR-mediated behaviour. Human molecular genetics 18: 2140-2148.
65. Grohmann M, Hammer P, Walther M, Paulmann N, Buttner A, et al. (2010) Alternative splicing and extensive RNA editing of human TPH2 transcripts. PloS one 5: e8956.
66. Silberberg G, Lundin D, Navon R, Ohman M (2012) Deregulation of the A-to-I RNA editing mechanism in psychiatric disorders. Human molecular genetics 21: 311-321.
67. Tojo K, Sekijima Y, Suzuki T, Suzuki N, Tomita Y, et al. (2006) Dystonia, mental deterioration, and dyschromatosis symmetrica hereditaria in a family with ADAR1 mutation. Mov Disord 21: 1510-1513. (Pubitemid 44613313)