Synthetic microRNA-mediated downregulation of Nogo-A in transgenic rats reveals its role as regulator of synaptic plasticity and cognitive function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 16, 2013, Pages 6583-6588

  Tews, Björn ^a,b   Schönig, Kai ^b   Arzt, Michael E ^a   Clementi, Stefano ^b   Rioult Pedotti, Mengia Seraina ^c,d   Zemmar, Ajmal ^a   Berger, Stefan M ^b   Schneider, Miriam ^b   Enkel, Thomas ^b   Weinmann, Oliver ^a   Kasper, Hansjörg ^a   Schwab, Martin E ^a   Bartsch, Dusan ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; PROTEIN NOGO A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HIPPOCAMPUS; IN VIVO STUDY; INTRON; LONG TERM POTENTIATION; MALE; MOTOR CORTEX; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OLIGODENDROGLIA; PERSEVERATION; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOSOCIAL WITHDRAWAL; RAT; RNA INTERFERENCE; SCHIZOPHRENIA; TRANSGENIC RAT; UPREGULATION;

ANIMALS; COGNITION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; LONG-TERM POTENTIATION; MICRORNAS; MYELIN PROTEINS; NEURONAL PLASTICITY; RATS; RATS, TRANSGENIC; RNA INTERFERENCE; SYNAPSES; TRANSGENES;

RATTUS;

EID: 84876231872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217665110     Document Type: Article

References (61)

1. Glaser S, Anastassiadis K, Stewart AF (2005) Current issues in mouse genome engineering. Nat Genet 37(11):1187-1193.
2. Tong C, et al. (2012) Rapid and cost-effective gene targeting in rat embryonic stem cells by TALENs. J Genet Genomics 39(6):275-280.
3. Hemann MT, et al. (2003) An epi-allelic series of p53 hypomorphs created by stable RNAi produces distinct tumor phenotypes in vivo. Nat Genet 33(3):396-400.
4. Volpicelli-Daley LA, Li Y, Zhang CJ, Kahn RA (2005) Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol Biol Cell 16(10):4495-4508.
5. Aitman TJ, et al. (2008) Progress and prospects in rat genetics: A community view. Nat Genet 40(5):516-522.
6. Wang D, et al. (2009) Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PLoS One 4(10):e7486.
7. Buehr M, et al. (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135(7):1287-1298.
8. Grant E, Mackintosh H (1963) A comparison of the social postures of some common laboratory rodents. Behaviour 21(3/4):246-259.
9. Kotnik K, et al. (2009) Inducible transgenic rat model for diabetes mellitus based on shRNA-mediated gene knockdown. PLoS One 4(4):e5124.
10. Wienholds E, Plasterk RH (2005) MicroRNA function in animal development. FEBS Lett 579(26):5911-5922.
11. Berger SM, et al. (2010) Quantitative analysis of conditional gene inactivation using rationally designed, tetracycline-controlled miRNAs. Nucleic Acids Res 38(17):e168.
12. Karagiannis TC, El-Osta A (2005) RNA interference and potential therapeutic applications of short interfering RNAs. Cancer Gene Ther 12(10):787-795.
13. Kunath T, et al. (2003) Transgenic RNA interference in ES cell-derived embryos recapitulates a genetic null phenotype. Nat Biotechnol 21(5):559-561.
14. Xia XG, Zhou H, Samper E, Melov S, Xu Z (2006) Pol II-expressed shRNA knocks down Sod2 gene expression and causes phenotypes of the gene knockout in mice. PLoS Genet 2(1):e10.
15. Willi R, et al. (2010) Constitutive genetic deletion of the growth regulator Nogo-A induces schizophrenia-related endophenotypes. J Neurosci 30(2):556-567.
16. Brinster RL, Allen JM, Behringer RR, Gelinas RE, Palmiter RD (1988) Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci USA 85(3):836-840.
17. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108(2):193-199.
18. Schönig K, Bujard H (2003) Generating conditional mouse mutants via tetracycline-controlled gene expression. Methods Mol Biol 209:69-104.
19. Grimm D, et al. (2006) Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441(7092):537-541.
20. Huber AB, Weinmann O, Brösamle C, Oertle T, Schwab ME (2002) Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 22(9):3553-3567.
21. Rioult-Pedotti MS, Friedman D, Donoghue JP (2000) Learning-induced LTP in neo-cortex. Science 290(5491):533-536.
22. Hess G, Aizenman CD, Donoghue JP (1996) Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neuro-physiol 75(5):1765-1778.
23. Schwab ME (2010) Functions of Nogo proteins and their receptors in the nervous system. Nat Rev Neurosci 11(12):799-811.
24. Willi R, Schwab ME (2013) Nogo and Nogo receptor: Relevance to schizophrenia? Neurobiol Dis, 10.1016/j.nbd.2013.01.011.
25. Cozzi J, Fraichard A, Thiam K (2008) Use of genetically modified rat models for translational medicine. Drug Discov Today 13(11-12):488-494.
26. Gill TJ, 3rd, Smith GJ, Wissler RW, Kunz HW (1989) The rat as an experimental animal. Science 245(4915):269-276.
27. Herold MJ, van den Brandt J, Seibler J, Reichardt HM (2008) Inducible and reversible gene silencing by stable integration of an shRNA-encoding lentivirus in transgenic rats. Proc Natl Acad Sci USA 105(47):18507-18512.
28. Hakamata Y, et al. (2001) Green fluorescent protein-transgenic rat: A tool for organ transplantation research. Biochem Biophys Res Commun 286(4):779-785.
29. Michalkiewicz M, et al. (2007) Efficient transgenic rat production by a lentiviral vector. Am J Physiol Heart Circ Physiol 293(1):H881-H894.
30. Weber T, Schönig K, Tews B, Bartsch D (2011) Inducible gene manipulations in brain serotonergic neurons of transgenic rats. PLoS One 6(11):e28283.
31. Geyer MA, Moghaddam B (2002) Animal models relevant to schizophrenia disorders. Neuropsychopharmacology: The Fifth Generation of Progress, eds Davis KL, Charney DS, Coyle JT, Nemeroff C (Lippincott Williams & Wilkins, Philadelphia), pp 689-701.
32. File SE, Hyde JR (1978) Can social interaction be used to measure anxiety? Br J Pharmacol 62(1):19-24.
33. Willi R, Aloy EM, Yee BK, Feldon J, Schwab ME (2009) Behavioral characterization of mice lacking the neurite outgrowth inhibitor Nogo-A. Genes Brain Behav 8(2):181-192.
34. American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders (American Psychiatric Association, Washington, DC), 4th Ed.
35. Kellendonk C, Simpson EH, Kandel ER (2009) Modeling cognitive endophenotypes of schizophrenia in mice. Trends Neurosci 32(6):347-358.
36. Drew MR, et al. (2007) Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci 27(29):7731-7739.
37. Ward RD, Simpson EH, Kandel ER, Balsam PD (2011) Modeling motivational deficits in mouse models of schizophrenia: Behavior analysis as a guide for neuroscience. Behav Processes 87(1):149-156.
38. Ho BC, Nopoulos P, Flaum M, Arndt S, Andreasen NC (1998) Two-year outcome in first-episode schizophrenia: Predictive value of symptoms for quality of life. Am J Psychiatry 155(9):1196-1201.
39. Silbersweig DA, et al. (1995) A functional neuroanatomy of hallucinations in schizophrenia. Nature 378(6553):176-179.
40. Dierks T, et al. (1999) Activation of Heschl's gyrus during auditory hallucinations. Neuron 22(3):615-621.
41. Delekate A, Zagrebelsky M, Kramer S, Schwab ME, Korte M (2011) NogoA restricts synaptic plasticity in the adult hippocampus on a fast time scale. Proc Natl Acad Sci USA 108(6):2569-2574.
42. Aloy EM, et al. (2006) Synaptic destabilization by neuronal Nogo-A. Brain Cell Biol 35(2-3):137-156.
43. Petrinovic MM, et al. (2013) Neuronal Nogo-A negatively regulates dendritic morphology and synaptic transmission in the cerebellum. Proc Natl Acad Sci USA 110(3):1083-1088.
44. Abel T, Martin KC, Bartsch D, Kandel ER (1998) Memory suppressor genes: Inhibitory constraints on the storage of long-term memory. Science 279(5349):338-341.
45. Bartsch D, et al. (1995) Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell 83(6):979-992.
46. Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108(5):689-703.
47. Malleret G, et al. (2001) Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104(5):675-686.
48. Chen A, et al. (2003) Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron 39(4):655-669.
49. Abel T, et al. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88(5):615-626.
50. Gerlai R, Henderson JT, Roder JC, Jia Z (1998) Multiple behavioral anomalies in GluR2 mutant mice exhibiting enhanced LTP. Behav Brain Res 95(1):37-45.
51. Kaksonen M, et al. (2002) Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol Cell Neurosci 21(1):158-172.
52. Kim MH, et al. (2009) Enhanced NMDA receptor-mediated synaptic transmission, enhanced long-term potentiation, and impaired learning and memory in mice lacking IRSp53. J Neurosci 29(5):1586-1595.
53. Rutten K, et al. (2008) Enhanced long-term potentiation and impaired learning in phosphodiesterase 4D-knockout (PDE4D) mice. Eur J Neurosci 28(3):625-632.
54. Uetani N, et al. (2000) Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice. EMBO J 19(12):2775-2785.
55. Kim JE, Li S, GrandPré T, Qiu D, Strittmatter SM (2003) Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 38(2):187-199.
56. Simonen M, et al. (2003) Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38(2):201-211.
57. Zheng B, et al. (2003) Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38(2):213-224.
58. Dimou L, et al. (2006) Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J Neurosci 26(21):5591-5603.
59. Miller BH, Wahlestedt C (2010) MicroRNA dysregulation in psychiatric disease. Brain Res 1338:89-99.
60. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007) Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8(5):355-367.
61. Buckingham SD, Esmaeili B, Wood M, Sattelle DB (2004) RNA interference: From model organisms towards therapy for neural and neuromuscular disorders. Hum Mol Genet 13(Spec No 2):R275-R288.