Antisense-mediated isoform switching of steroid receptor coactivator-1 in the central nucleus of the amygdala of the mouse brain

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Zalachoras, Ioannis ^a,b,c   Grootaers, Gwendolynn ^a   van Weert, Lisa T C M ^a   Aubert, Yves ^a   de Kreij, Suzanne R ^a   Datson, Nicole A ^a,b   van Roon Mom, Willeke M C ^b   Aartsma Rus, Annemieke ^b   Meijer, Onno C ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Postzone C4 R ^*  (Netherlands)

Author keywords

Antisense oligonucleotide; Brain; Exon skipping; Glucocorticoid receptor; Steroid receptor coactivator 1

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CORTICOTROPIN RELEASING FACTOR; DYSTROPHIN; MESSENGER RNA; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 1A; STEROID RECEPTOR COACTIVATOR 1E; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTISENSE THERAPY; ARTICLE; CELL NUCLEUS; CELL TYPE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; DRUG EFFICACY; EXON; EXON SKIPPING; FEASIBILITY STUDY; GENE TARGETING; GENETIC VARIABILITY; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; IMMUNOSTIMULATION; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RNA SPLICING;

AMYGDALA; ANIMALS; ANTIGENS, CD45; GLIAL FIBRILLARY ACIDIC PROTEIN; LASER CAPTURE MICRODISSECTION; MALE; MICE; MICE, INBRED C57BL; NUCLEAR RECEPTOR COACTIVATOR 1; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PHOSPHOPYRUVATE HYDRATASE; PROTEIN ISOFORMS; RNA SPLICING; TIME FACTORS;

EID: 84871896697     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-5     Document Type: Article

References (56)

1. Fagnani M, Barash Y, Ip JY, Misquitta C, Pan Q, Saltzman AL, Shai O, Lee L, Rozenhek A, Mohammad N, et al. Functional coordination of alternative splicing in the mammalian central nervous system. Genome Biol 2007, 8(6):R108. 10.1186/gb-2007-8-6-r108, 2394768, 17565696.
2. Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, Wang H, Clark T, Fraser C, Ruggiu M, et al. Nova regulates brain-specific splicing to shape the synapse. Nat Genet 2005, 37(8):844-852. 10.1038/ng1610, 16041372.
3. Vallone D, Picetti R, Borrelli E. Structure and function of dopamine receptors. Neurosci Biobehav R 2000, 24(1):125-132.
4. Zmijewski MA, Slominski AT. Modulation of corticotropin releasing factor (CRF) signaling through receptor splicing in mouse pituitary cell line AtT-20-emerging role of soluble isoforms. J Physiol Pharmacol 2009, 60(Suppl 4):39-46. 2814449, 20083850.
5. Ryberg E, Vu HK, Larsson N, Groblewski T, Hjorth S, Elebring T, Sjogren S, Greasley PJ. Identification and characterisation of a novel splice variant of the human CB1 receptor. FEBS Lett 2005, 579(1):259-264. 10.1016/j.febslet.2004.11.085, 15620723.
6. Liu QR, Pan CH, Hishimoto A, Li CY, Xi ZX, Llorente-Berzal A, Viveros MP, Ishiguro H, Arinami T, Onaivi ES, et al. Species differences in cannabinoid receptor 2 (CNR2 gene): identification of novel human and rodent CB2 isoforms, differential tissue expression and regulation by cannabinoid receptor ligands. Genes Brain Behav 2009, 8(5):519-530. 10.1111/j.1601-183X.2009.00498.x, 3389515, 19496827.
7. Zalachoras I, Evers MM, van Roon-Mom WM, Aartsma-Rus AM, Meijer OC. Antisense-mediated RNA targeting: versatile and expedient genetic manipulation in the brain. Front Mol Neurosci 2011, 4:10. 3142880, 21811437.
8. Evers MM, Pepers BA, van Deutekom JC, Mulders SA, den Dunnen JT, Aartsma-Rus A, van Ommen GJ, van Roon-Mom WM. Targeting several CAG expansion diseases by a single antisense oligonucleotide. PLoS One 2011, 6(9):e24308. 10.1371/journal.pone.0024308, 3164722, 21909428.
9. Yang J, Fuller PJ. Interactions of the mineralocorticoid receptor - Within and without. Mol Cell Endocrinol 2012, 350(2):196-205. 10.1016/j.mce.2011.07.001, 21784126.
10. Hua Y, Sahashi K, Hung G, Rigo F, Passini MA, Bennett CF, Krainer AR. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev 2010, 24(15):1634-1644. 10.1101/gad.1941310, 2912561, 20624852.
11. Zakharov MN, Pillai BK, Bhasin S, Ulloor J, Istomin AY, Guo C, Godzik A, Kumar R, Jasuja R. Dynamics of coregulator-induced conformational perturbations in androgen receptor ligand binding domain. Mol Cell Endocrinol 2011, 341(1-2):1-8.
12. Dobrovolna J, Chinenov Y, Kennedy MA, Liu B, Rogatsky I. Glucocorticoid-dependent phosphorylation of the transcriptional coregulator GRIP1. Mol Cell Biol 2012, 32(4):730-739. 10.1128/MCB.06473-11, 3272970, 22158970.
13. Goemans NM, Tulinius M, van den Akker JT, Burm BE, Ekhart PF, Heuvelmans N, Holling T, Janson AA, Platenburg GJ, Sipkens JA, et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 2011, 364(16):1513-1522. 10.1056/NEJMoa1011367, 21428760.
14. Biddie Simon C, John S, Sabo Pete J, Thurman Robert E, Johnson Thomas A, Schiltz RL, Miranda Tina B, Sung M-H, Trump S, Lightman Stafford L, et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol Cell 2011, 43(1):145-155. 10.1016/j.molcel.2011.06.016, 3138120, 21726817.
15. Williams JH, Schray RC, Patterson CA, Ayitey SO, Tallent MK, Lutz GJ. Oligonucleotide-mediated survival of motor neuron protein expression in CNS improves phenotype in a mouse model of spinal muscular atrophy. J Neurosci 2009, 29(24):7633-7638. 10.1523/JNEUROSCI.0950-09.2009, 19535574.
16. Burghes AH, McGovern VL. Antisense oligonucleotides and spinal muscular atrophy: skipping along. Genes Dev 2010, 24(15):1574-1579. 10.1101/gad.1961710, 2912553, 20679391.
17. Nlend Nlend R, Meyer K, Schumperli D. Repair of pre-mRNA splicing: prospects for a therapy for spinal muscular atrophy. RNA Biol 2010, 7(4):430-440. 10.4161/rna.7.4.12206, 3070909, 20523126.
18. Pitts MW, Todorovic C, Blank T, Takahashi LK. The central nucleus of the amygdala and corticotropin-releasing factor: insights into contextual fear memory. J Neurosci 2009, 29(22):7379-7388. 10.1523/JNEUROSCI.0740-09.2009, 2771694, 19494159.
19. Pitts MW, Takahashi LK. The central amygdala nucleus via corticotropin-releasing factor is necessary for time-limited consolidation processing but not storage of contextual fear memory. Neurobiol Learn Mem 2011, 95(1):86-91. 10.1016/j.nlm.2010.11.006, 3022075, 21093597.
20. Ma L, Wang D-D, Zhang T-Y, Yu H, Wang Y, Huang S-H, Lee FS, Chen Z-Y. Region-specific involvement of BDNF secretion and synthesis in conditioned taste aversion memory formation. J Neurosci 2011, 31(6):2079-2090. 10.1523/JNEUROSCI.5348-10.2011, 3044502, 21307245.
21. Smith RA, Miller TM, Yamanaka K, Monia BP, Condon TP, Hung G, Lobsiger CS, Ward CM, McAlonis-Downes M, Wei H, et al. Antisense oligonucleotide therapy for neurodegenerative disease. J Clin Invest 2006, 116(8):2290-2296. 10.1172/JCI25424, 1518790, 16878173.
22. Kamei Y, Xu L, Heinzel T, Torchia J, Kurokawa R, Gloss B, Lin SC, Heyman RA, Rose DW, Glass CK, et al. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 1996, 85(3):403-414. 10.1016/S0092-8674(00)81118-6, 8616895.
23. Kalkhoven E, Valentine JE, Heery DM, Parker MG. Isoforms of steroid receptor co-activator 1 differ in their ability to potentiate transcription by the oestrogen receptor. EMBO J 1998, 17(1):232-243. 10.1093/emboj/17.1.232, 1170374, 9427757.
24. Meijer OC, Kalkhoven E, van der Laan S, Steenbergen PJ, Houtman SH, Dijkmans TF, Pearce D, de Kloet ER. Steroid receptor coactivator-1 splice variants differentially affect corticosteroid receptor signaling. Endocrinology 2005, 146(3):1438-1448.
25. Tetel MJ, Auger AP, Charlier TD. Who's in charge? Nuclear receptor coactivator and corepressor function in brain and behavior. Front Neuroendocrinol 2009, 30(3):328-342. 10.1016/j.yfrne.2009.04.008, 2720417, 19401208.
26. Meijer OC, Steenbergen PJ, De Kloet ER. Differential expression and regional distribution of steroid receptor coactivators SRC-1 and SRC-2 in brain and pituitary. Endocrinology 2000, 141(6):2192-2199. 10.1210/en.141.6.2192, 10830308.
27. van der Laan S, Lachize SB, Vreugdenhil E, de Kloet ER, Meijer OC. Nuclear receptor coregulators differentially modulate induction and glucocorticoid receptor-mediated repression of the corticotropin-releasing hormone gene. Endocrinology 2008, 149(2):725-732.
28. Tynan RJ, Naicker S, Hinwood M, Nalivaiko E, Buller KM, Pow DV, Day TA, Walker FR. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav Immun 2010, 24(7):1058-1068. 10.1016/j.bbi.2010.02.001, 20153418.
29. Herber DL, Maloney JL, Roth LM, Freeman MJ, Morgan D, Gordon MN. Diverse microglial responses after intrahippocampal administration of lipopolysaccharide. Glia 2006, 53(4):382-391. 10.1002/glia.20272, 16288481.
30. Apostolakis EM, Ramamurphy M, Zhou D, Oñate S, O'Malley BW. Acute disruption of select steroid receptor coactivators prevents reproductive behavior in rats and unmasks genetic adaptation in knockout mice. Mol Endocrinol 2002, 16(7):1511-1523. 10.1210/me.16.7.1511, 12089347.
31. Winkler J, Stessl M, Amartey J, Noe CR. Off-target effects related to the phosphorothioate modification of nucleic acids. Chem Med Chem 2010, 5(8):1344-1352.
32. Jeanneteau FD, Lambert WM, Ismaili N, Bath KG, Lee FS, Garabedian MJ, Chao MV. BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus. Proc Natl Acad Sci 2012, 109(4):1305-1310. 10.1073/pnas.1114122109, 3268297, 22232675.
33. Chiasson BJ, Armstrong JN, Hooper ML, Murphy PR, Robertson HA. The application of antisense oligonucleotide technology to the brain: some pitfalls. Cell Mol Neurobiol 1994, 14(5):507-521. 10.1007/BF02088834, 7621510.
34. Okun E, Lathia JD, Mattson MP. Adhesion- and migration-related side effects of phosphothioated CpG oligodeoxynucleotides. Cell Adh Migr 2009, 3(3):272-274. 10.4161/cam.3.3.8692, 2712808, 19458479.
35. Robbins M, Judge A, Liang L, McClintock K, Yaworski E, MacLachlan I. 2'-O-methyl-modified RNAs act as TLR7 antagonists. Mol Ther 2007, 15(9):1663-1669. 10.1038/sj.mt.6300240, 17579574.
36. Juliano RL, Ming X, Nakagawa O. Cellular uptake and intracellular trafficking of antisense and siRNA oligonucleotides. Bioconjug Chem 2012, 23(2):147-157. 10.1021/bc200377d, 21992697.
37. Heemskerk H, de Winter C, van Kuik P, Heuvelmans N, Sabatelli P, Rimessi P, Braghetta P, van Ommen GJ, de Kimpe S, Ferlini A, et al. Preclinical PK and PD studies on 2'-O-methyl-phosphorothioate RNA antisense oligonucleotides in the mdx mouse model. Mol Ther 2010, 18(6):1210-1217. 10.1038/mt.2010.72, 2889733, 20407428.
38. Akhtar S, Juliano RL. Cellular uptake and intracellular fate of antisense oligonucleotides. Trends Cell Biol 1992, 2(5):139-144. 10.1016/0962-8924(92)90100-2, 14731968.
39. Alam MR, Ming X, Dixit V, Fisher M, Chen X, Juliano RL. The biological effect of an antisense oligonucleotide depends on its route of endocytosis and trafficking. Oligonucleotides 2010, 20(2):103-109. 10.1089/oli.2009.0211, 2883474, 20038250.
40. Koller E, Vincent TM, Chappell A, De S, Manoharan M, Bennett CF. Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes. Nucleic Acids Res 2011, 39(11):4795-4807. 10.1093/nar/gkr089, 3113586, 21345934.
41. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 2010, 285(23):17442-17452. 10.1074/jbc.M110.107821, 2878508, 20353945.
42. Manoharan M, Johnson LK, McGee DPC, Guinosso CJ, Ramasamy K, Springer RH, Bennett CF, Ecker DJ, Vickers T, Cowsert L, et al. Chemical modifications to improve uptake and bioavailability of antisense oligonucleotides. Ann N Y Acad Sci 1992, 660(1):306-309. 10.1111/j.1749-6632.1992.tb21095.x, 1364095.
43. Aartsma-Rus A, Kaman WE, Bremmer-Bout M, Janson AA, den Dunnen JT, van Ommen GJ, van Deutekom JC. Comparative analysis of antisense oligonucleotide analogs for targeted DMD exon 46 skipping in muscle cells. Gene Ther 2004, 11(18):1391-1398. 10.1038/sj.gt.3302313, 15229633.
44. Kolber BJ, Roberts MS, Howell MP, Wozniak DF, Sands MS, Muglia LJ. Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proc Natl Acad Sci USA 2008, 105(33):12004-12009. 10.1073/pnas.0803216105, 2575312, 18695245.
45. Lachize S, Apostolakis EM, van der Laan S, Tijssen AM, Xu J, de Kloet ER, Meijer OC. Steroid receptor coactivator-1 is necessary for regulation of corticotropin-releasing hormone by chronic stress and glucocorticoids. Proc Natl Acad Sci USA 2009, 106(19):8038-8042. 10.1073/pnas.0812062106, 2683087, 19416907.
46. Bushong EA, Martone ME, Jones YZ, Ellisman MH. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 2002, 22(1):183-192.
47. Takeichi T, Takarada-Iemata M, Hashida K, Sudo H, Okuda T, Kokame K, Hatano T, Takanashi M, Funabe S, Hattori N, et al. The effect of Ndrg2 expression on astroglial activation. Neurochem Int 2011, 59(1):21-27. 10.1016/j.neuint.2011.03.019, 21672576.
48. Aartsma-Rus A, Janson AAM, Kaman WE, Bremmer-Bout M, den Dunnen JT, Baas F, van Ommen G-JB, van Deutekom JCT. Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet 2003, 12(8):907-914. 10.1093/hmg/ddg100, 12668614.
49. Aartsma-Rus A, Janson AAM, Kaman WE, Bremmer-Bout M, van Ommen G-JB, den Dunnen JT, van Deutekom JCT. Antisense-induced multiexon skipping for duchenne muscular dystrophy makes more sense. Am J Hum Genet 2004, 74(1):83-92. 10.1086/381039, 1181915, 14681829.
50. Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates 2001, USA: Academic Press, Elsevier.
51. Sioud M, Furset G, Cekaite L. Suppression of immunostimulatory siRNA-driven innate immune activation by 2'-modified RNAs. Biochem Biophys Res Commun 2007, 361(1):122-126. 10.1016/j.bbrc.2007.06.177, 17658482.
52. Hamm S, Latz E, Hangel D, Müller T, Yu P, Golenbock D, Sparwasser T, Wagner H, Bauer S. Alternating 2'-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology 2010, 215(7):559-569. 10.1016/j.imbio.2009.09.003, 19854535.
53. Datson NA, Meijer L, Steenbergen PJ, Morsink MC, van der Laan S, Meijer OC, de Kloet ER. Expression profiling in laser-microdissected hippocampal subregions in rat brain reveals large subregion-specific differences in expression. Eur J Neurosci 2004, 20(10):2541-2554. 10.1111/j.1460-9568.2004.03738.x, 15548198.
54. Erickson HS, Albert PS, Gillespie JW, Rodriguez-Canales J, Marston Linehan W, Pinto PA, Chuaqui RF, Emmert-Buck MR. Quantitative RT-PCR gene expression analysis of laser microdissected tissue samples. Nat Protoc 2009, 4(6):902-922. 10.1038/nprot.2009.61, 2760821, 19478806.
55. Datson NA, Morsink MC, Steenbergen PJ, Aubert Y, Schlumbohm C, Fuchs E, de Kloet ER. A molecular blueprint of gene expression in hippocampal subregions CA1, CA3, and DG is conserved in the brain of the common marmoset. Hippocampus 2009, 19(8):739-752. 10.1002/hipo.20555, 19156849.
56. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45. 10.1093/nar/29.9.e45, 55695, 11328886.