Sex-dependent up-regulation of two splicing factors, Psf and Srp20, during hippocampal memory formation

Learning and Memory

Volumn 14, Issue 10, 2007, Pages 693-702

  Antunes Martins, Ana ^a,c   Mizuno, Keiko ^a   Irvine, Elaine E ^a   Lepicard, Eve M ^a,d   Giese, K Peter ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE (CALCIUM,CALMODULIN); CALCIUM CALMODULIN DEPENDENT KINASE KINASE; CALCIUM-CALMODULIN-DEPENDENT KINASE KINASE; MESSENGER RNA; NERVE PROTEIN; PROTEIN SERINE THREONINE KINASE; PTB ASSOCIATED SPLICING FACTOR; PTB-ASSOCIATED SPLICING FACTOR; RNA BINDING PROTEIN; SFRS3 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PSF GENE; SEX DIFFERENCE; SRP20 GENE; UPREGULATION; ALTERNATIVE RNA SPLICING; ANIMAL; AVOIDANCE BEHAVIOR; BIOSYNTHESIS; COMPARATIVE STUDY; CONDITIONED REFLEX; FEAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MAZE TEST; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; SEXUAL MATURATION;

ALTERNATIVE SPLICING; ANIMALS; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; FEAR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICE; NERVE TISSUE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; RNA-BINDING PROTEINS; SEX CHARACTERISTICS; SEXUAL MATURATION;

EID: 35448969301     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.640307     Document Type: Article

References (69)

1. Aguilar-Valles, A., Sanchez, E., deGortari, P., Balderas, I., Ramirez-Amaya, V., Bermudez-Rattoni, F., and Joseph-Bravo, P. 2005. Analysis of the stress response in rats trained in the water-maze: Differential expression of corticotropin-releasing hormone, CRH-R1, glucocorticoid receptors and brain-derived neurotrophic factor in limbic regions. Neuroendocrinology 82: 306-319.
2. Angelo, M., Plattner, F., Irvine, E.E., and Giese, K.P. 2003. Improved reversal learning and altered fear conditioning in transgenic mice with regionally restricted p25 expression. Eur. J. Neurosci. 18: 423-431.
3. Balschun, D., Wolfer, D.P., Gass, P., Mantamadiotis, T., Welzl, H., Schutz, G., Frey, J.U., and Lipp, H.P. 2003. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J. Neurosci. 23: 6304-6314.
4. Beffert, U., Weeber, E.J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J.D., Li, W.P., Adelmann, G., Frotscher, M., Hammer, R.E., et al. 2005. Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47: 567-579.
5. Bladen, C.L., Udayakumar, D., Takeda, Y., and Dynan, W.S. 2005. Identification of the polypyrimidine tract binding protein-associated splicing factor.p54(nrb) complex as a candidate DNA double-strand break rejoining factor. J. Biol. Chem. 280: 5205-5210.
6. 2+/calmodulin kinase kinase α-deficient mice. Mol. Cell. Biol. 26: 9105-9115.
7. Bottai, D., Guzowski, J.F., Schwarz, M.K., Kang, S.H., Xiao, B., Lanahan, A., Worley, P.F., and Seeburg, P.H. 2002. Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J. Neurosci. 22: 167-175.
8. Brightwell, J.J., Gallagher, M., and Colombo, P.J. 2004. Hippocampal CREB1 but not CREB2 is decreased in aged rats with spatial memory impairments. Neurobiol. Learn. Mem. 81: 19-26.
9. Bustin, S.A. 2000. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25: 169-193.
10. Cavallaro, S., D'Agata, V., Manickam, P., Dufour, F., and Alkon, D.L. 2002. Memory-specific temporal profiles of gene expression in the hippocampus. Proc. Natl. Acad. Sci. 99: 16279-16284.
11. Chanas-Sacre, G., Mazy-Servais, C., Wattiez, R., Pirard, S., Rogister, B., Patton, J.G., Belachew, S., Malgrange, B., Moonen, G., and Leprince, P. 1999. Identification of PSF, the polypyrimidine tract-binding protein-associated splicing factor, as a developmentally regulated neuronal protein. J. Neurosci. Res. 57: 62-73.
12. Chow, F.A., Anderson, K.A., Noeldner, P.K., and Means, A.R. 2005. The autonomous activity of calcium/calmodulin-dependent protein kinase IV is required for its role in transcription. J. Biol. Chem. 280: 20530-20538.
13. 2+/calmodulin- dependent protein kinase cascades in transcriptional regulation. J. Biol. Chem. 276: 2975-2978.
14. Frye, C.A. 1995. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 57: 5-14.
15. Galiana-Arnoux, D., Lejeune, F., Gesnel, M.C., Stevenin, J., Breathnach, R., and Gatto-Konczak, F. 2003. The CD44 alternative v9 exon contains a splicing enhancer responsive to the SR proteins 9G8, ASF/SF2, and SRp20. J. Biol. Chem. 278: 32943-32953.
16. Gartler, S.M. and Riggs, A.D. 1983. Mammalian X-chromosome inactivation. Annu. Rev. Genet. 17: 155-190.
17. Grant, S.G. and Chapman, V.M. 1988. Mechanisms of X-chromosome regulation. Annu. Rev. Genet. 22: 199-233.
18. Guzowski, J.F., Lyford, G.L., Stevenson, G.D., Houston, F.P., McGaugh, J.L., Worley, P.F., and Barnes, C.A. 2000. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 20: 3993-4001.
19. Guzowski, J.F., Setlow, B., Wagner, E.K., and McGaugh, J.L. 2001. Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21: 5089-5098.
20. Hall, J., Thomas, K.L., and Everitt, B.J. 2000. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 3: 533-535.
21. Hebda-Bauer, E.K., Watson, S.J., and Akil, H. 2005. Cognitive performance is highly sensitive to prior experience in mice with a learning and memory deficit: Failure leads to more failure. Learn. Mem. 12: 461-471.
22. Huang, Y. and Steitz, J.A. 2001. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7: 899-905.
23. Jonasson, Z. 2005. Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data. Neurosci. Biobehav. Rev. 28: 811-825.
24. Jumaa, H. and Nielsen, P.J. 1997. The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16: 5077-5085.
25. Koshibu, K. and Levitt, P. 2005. Sex differences in expression of transforming growth factor-α and epidermal growth factor receptor mRNA in Waved-1 and C57Bl6 mice. Neuroscience 134: 877-887.
26. Kudo, K., Qiao, C.X., Kanba, S., and Arita, J. 2004. A selective increase in phosphorylation of cyclic AMP response element-binding protein in hippocampal CA1 region of male, but not female, rats following contextual fear and passive avoidance conditioning. Brain Res. 1024: 233-243.
27. Lee, C.J. and Irizarry, K. 2003. Alternative splicing in the nervous system: An emerging source of diversity and regulation. Biol. Psychiatry 54: 771-776.
28. Lee, S.J., Campomanes, C.R., Sikat, P.T., Greenfield, A.T., Allen, P.B., and McEwen, B.S. 2004. Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 124: 549-560.
29. Lee, J.A., Xing, Y., Nguyen, D., Xie, J., Lee, C.J., and Black, D.L. 2007. Depolarization and CaM kinase IV modulate NMDA receptor splicing through two essential RNA elements. PLoS Biol. 5: e40, doi: 10.1371/journal.pbio.0050040.
30. Leil, T.A., Ossadtchi, A., Cortes, J.S., Leahy, R.M., and Smith, D.J. 2002. Finding new candidate genes for learning and memory. J. Neurosci. Res. 68: 127-137.
31. Leil, T.A., Ossadtchi, A., Nichols, T.E., Leahy, R.M., and Smith, D.J. 2003. Genes regulated by learning in the hippocampus. J. Neurosci. Res. 71: 763-768.
32. Lepicard, E.M., Mizuno, K., Antunes-Martins, A., von Hertzen, L.S., and Giese, K.P. 2006. An endogenous inhibitor of calcium/calmodulin-dependent kinase II is up-regulated during consolidation of fear memory. Eur. J. Neurosci. 23: 3063-3070.
33. Liu, H.H., Payne, H.R., Wang, B., and Brady, S.T. 2006. Gender differences in response of hippocampus to chronic glucocorticoid stress: Role of glutamate receptors. J. Neurosci. Res. 83: 775-786.
34. Lou, H., Neugebauer, K.M., Gagel, R.F., and Berget, S.M. 1998. Regulation of alternative polyadenylation by U1 snRNPs and SRp20. Mol. Cell. Biol. 18: 4977-4985.
35. Maguire, E.A., Burgess, N., and O'Keefe, J. 1999. Human spatial navigation: Cognitive maps, sexual dimorphism, and neural substrates. Curr. Opin. Neurobiol. 9: 171-177.
36. Mathur, M., Tucker, P.W., and Samuels, H.H. 2001. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell. Biol. 21: 2298-2311.
37. Matsuyama, S., Namgung, U., and Routtenberg, A. 1997. Long-term potentiation persistence greater in C57BL/6 than DBA/2 mice: Predicted on basis of protein kinase C levels and learning performance. Brain Res. 763: 127-130.
38. Mizuno, K. and Giese, K.P. 2005. Hippocampus-dependent memory formation: Do memory type-specific mechanisms exist? J. Pharmacol. Sci. 98: 191-197.
39. 2+/calmodulin kinase kinase α is dispensable for brain development but is required for distinct memories in male, though not in female, mice. Mol. Cell. Biol. 26: 9094-9104.
40. Mizuno, K., Antunes-Martins, A., Ris, L., Peters, M., Godaux, E., and Giese, K.P. 2007. Calcium/calmodulin kinase kinase β has a male-specific role in memory formation. Neuroscience 145: 393-402.
41. Morris, R.G. 2006. Elements of a neurobiological theory of hippocampal function: The role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci. 23: 2829-2846.
42. Nijholt, I., Farchi, N., Kye, M., Sklan, E.H., Shoham, S., Verbeure, B., Owen, D., Hochner, B., Spiess, J., Soreq, H., et al. 2004. Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation. Mol. Psychiatry 9: 174-183.
43. O'Connor, V., Genin, A., Davis, S., Karishma, K.K., Doyere, V., De Zeeuw, C.I., Sanger, G., Hunt, S.P., Richter-Levin, G., Mallet, J., et al. 2004. Differential amplification of intron-containing transcripts reveals long term potentiation-associated up-regulation of specific Pde10A phosphodiesterase splice variants. J. Biol. Chem. 279: 15841-15849.
44. Oh, M.M., Kuo, A.G., Wu, W.W., Sametsky, E.A., and Disterhoft, J.F. 2003. Watermaze learning enhances excitability of CA1 pyramidal neurons. J. Neurophysiol. 90: 2171-2179.
45. Omoto, Y., Lathe, R., Warner, M., and Gustafsson, J.A. 2005. Early onset of puberty and early ovarian failure in CYP7B1 knockout mice. Proc. Natl. Acad. Sci. 102: 2814-2819.
46. Patton, J.G., Porro, E.B., Galceran, J., Tempst, P., and Nadal-Ginard, B. 1993. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes & Dev. 7: 393-406.
47. Paxinos, G. and Franklin, K.B.J. 2001. The mouse brain in stereotaxic coordinates. Academic Press, San Diego.
48. Perrot-Sinal, T.S., Kostenuik, M.A., Ossenkopp, K.P., and Kavaliers, M. 1996. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav. Neurosci. 110: 1309-1320.
49. 2+/calmodulin kinase kinase β affects the formation of some, but not all, types of hippocampus-dependent long-term memory. J. Neurosci. 23: 9752-9760.
50. Phillips, R.G. and LeDoux, J.E. 1994. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn. Mem. 1: 34-44.
51. Plath, N., Ohana, O., Dammermann, B., Errington, M.L., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., et al. 2006. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
52. Rattiner, L.M., Davis, M., and Ressler, K.J. 2004. Differential regulation of brain-derived neurotrophic factor transcripts during the consolidation of fear learning. Learn. Mem. 11: 727-731.
53. Roof, R.L. and Stein, D.G. 1999. Gender differences in Morris water maze performance depend on task parameters. Physiol. Behav. 68: 81-86.
54. Sandstrom, N.J., Kaufman, J., and Huettel, S.A. 1998. Males and females use different distal cues in a virtual environment navigation task. Brain Res. Cogn. Brain Res. 6: 351-360.
55. Sanford, J.R., Ellis, J., and Caceres, J.F. 2005. Multiple roles of arginine/serine-rich splicing factors in RNA processing. Biochem. Soc. Trans. 33: 443-446.
56. Sawai, T., Bernier, F., Fukushima, T., Hashimoto, T., Ogura, H., and Nishizawa, Y. 2002. Estrogen induces a rapid increase of calcium-calmodulin- dependent protein kinase II activity in the hippocampus. Brain Res. 950: 308-311.
57. Scharfman, H.E. and MacLusky, N.J. 2005. Similarities between actions of estrogen and BDNF in the hippocampus: Coincidence or clue? Trends Neurosci. 28: 79-85.
58. Shav-Tal, Y. and Zipori, D. 2002. PSF and p54(nrb)/NonO-multifunctional nuclear proteins. FEBS Lett. 531: 109-114.
59. Shors, T.J., Beylin, A.V., Wood, G.E., and Gould, E. 2000. The modulation of Pavlovian memory. Behav. Brain Res. 110: 39-52.
60. Silva, A.J. and Giese, K.P. 1994. Plastic genes are in! Curr. Opin. Neurobiol. 4: 413-420.
61. 2+/calmodulin-dependent protein kinase (CaMK). J. Biol. Chem. 278: 18597-18605.
62. Ule, J. and Darnell, R.B. 2006. RNA binding proteins and the regulation of neuronal synaptic plasticity. Curr. Opin. Neurobiol. 16: 102-110.
63. Urban, R.J. and Bodenburg, Y. 2002. PTB-associated splicing factor regulates growth factor-stimulated gene expression in mammalian cells. Am. J. Physiol. Endocrinol. Metab. 283: E794-E798, doi: 10.1152/ajpendo.00174.2002.
64. Vaynman, S., Ying, Z., and Gomez-Pinilla, F. 2004. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci. 20: 2580-2590.
65. von Hertzen, L.S. and Giese, K.P. 2005. Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J. Neurosci. 25: 1935-1942.
66. Westenbroek, C., Den Boer, J.A., and Ter Horst, G.J. 2003. Gender-specific effects of social housing on chronic stress-induced limbic Fos expression. Neuroscience 121: 189-199.
67. Xie, J., Jan, C., Stoilov, P., Park, J., and Black, D.L. 2005. A consensus CaMK IV-responsive RNA sequence mediates regulation of alternative exons in neurons. RNA 11: 1825-1834.
68. Yu, Q., Guo, J., and Zhou, J. 2004. A minimal length between τ exon 10 and 11 is required for correct splicing of exon 10. J. Neurochem. 90: 164-172.
69. Zhang, Z. and Carmichael, G.G. 2001. The fate of dsRNA in the nucleus: A p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 106: 465-475.