MSK1 regulates environmental enrichment-induced hippocampal plasticity and cognitive enhancement

Learning and Memory

Volumn 19, Issue 11, 2012, Pages 550-560

  Karelina, Kate ^a   Hansen, Katelin F ^a   Choi, Yun Sik ^b   DeVries, A Courtney ^a   Arthur, J Simon C ^c   Obrietan, Karl ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Catholic University of Daegu   (South Korea)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN STRESSACTIVATED KINASE 1; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; COGNITION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; ENVIRONMENTAL ENRICHMENT; HIPPOCAMPUS; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; BLOTTING, WESTERN; CELL PROLIFERATION; COGNITION; ENVIRONMENT; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; HOUSING, ANIMAL; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL STEM CELLS; NEUROGENESIS; NEURONAL PLASTICITY; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA;

EID: 84868664564     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.025775.112     Document Type: Article

References (70)

1. Agrigoroaei S, Lachman ME. 2011. Cognitive functioning in midlife and old age: Combined effects of psychosocial and behavioral factors. J Gerontol B Psychol Sci Soc Sci 66: i130-i140.
2. Alonso M, Medina JH, Pozzo-Miller L. 2004. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem 11: 172-178. (Pubitemid 38456599)
3. Arthur JSC, Cohen P. 2000. MSK1 is required for CREB phosphorylation in response to mitogens in mouse embryonic stem cells. FEBS Lett 482: 44-48.
4. Arthur JSC, Fong AL, Dwyer JM, Davare M, Reese E, Obrietan K, Impey S. 2004. Mitogen- and stress-activated protein kinase 1 mediates cAMP response element-binding protein phosphorylation and activation by neurotrophins. J Neurosci 24: 4324-4332. (Pubitemid 38608143)
5. Barker GRI, Warburton EC. 2011. When is the hippocampus involved in recognition memory? J Neurosci 31: 10721-10731.
6. Bianchi M, Fone K, Azmi N, Heidbreder C, Hagan J, Marsden C. 2006. Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. Eur J Neurosci 24: 2894-2902. (Pubitemid 44813840)
7. Bolshakov V, Carboni L, Cobb M, Siegelbaum S, Belardetti F. 2000. Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapses. Nat Neurosci 3: 1107-1112.
8. Broadbent NJ, Gaskin S, Squire LR, Clark RE. 2010. Object recognition memory and the rodent hippocampus. Learn Mem 17: 5-11.
9. Bruel-Jungerman E, Laroche S, Rampon C. 2005. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21: 513-521. (Pubitemid 40204254)
10. Choi YS, Cho HY, Hoyt KR, Naegele JR, Obrietan K. 2008. IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus. Glia 56: 791-800.
11. Chwang WB, Arthur JS, Schumacher A, Sweatt JD. 2007. The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 27: 12732-12742. (Pubitemid 350127810)
12. Cotman CW, Berchtold NC. 2002. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25: 295-301. (Pubitemid 34667010)
13. Cruz-Orive LM. 1999. Precision of Cavalieri sections and slices with local errors. J Microsc 193: 182-198. (Pubitemid 29145154)
14. Davis S, Vanhoutte P, Pagès C, Caboche J, Laroche S. 2000. The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20: 4563-4572. (Pubitemid 30396622)
15. Deak M, Clifton AD, Lucocq JM, Alessi DR. 1998. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J 17: 4426-4441. (Pubitemid 28362632)
16. Deng W, Saxe MD, Gallina IS, Gage FH. 2009. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29: 13532-13542.
17. Dijkhuizen PA, Ghosh A. 2005. BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J Neurobiol 62: 278-288. (Pubitemid 40096402)
18. English JD, Sweatt JD. 1997. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272: 19103-19106. (Pubitemid 27337694)
19. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM. 2011. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci 108: 3017-3022.
20. Faherty CJ, Kerley D, Smeyne RJ. 2003. A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Dev Brain Res 141: 55-61. (Pubitemid 36315692)
21. Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME. 1997. CREB: A major mediator of neuronal neurotrophin responses. Neuron 19: 1031-1047. (Pubitemid 27512364)
22. Fonseca R, Nägerl UV, Morris RGM, Bonhoeffer T. 2004. Competing for memory: Hippocampal LTP under regimes of reduced protein synthesis. Neuron 44: 1011-1020. (Pubitemid 39643096)
23. Goldin M, Segal M. 2003. Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons. Eur J Neurosci 17: 2529-2539. (Pubitemid 36819278)
24. Hansen KF, Sakamoto K, Wayman GA, Impey S, Obrietan K. 2010. Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One 5: e15497. doi: 10.1371/journal.pone.0015497.
25. Hauge C, Frodin M. 2006. RSK and MSK in MAP kinase signaling. J Cell Sci 119: 3021-3023. (Pubitemid 44322115)
26. Horch HW, Katz LC. 2002. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 5: 1177-1184. (Pubitemid 35247177)
27. Hsieh J, Gage FH. 2005. Chromatin remodeling in neural development and plasticity. Curr Opin Cell Biol 17: 664-671. (Pubitemid 41540418)
28. Ibi D, Takuma K, Koike H, Mizoguchi H, Tsuritani K, Kuwahara Y, Kamei H, Nagai T, Yoneda Y, Nabeshima T. 2008. Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J Neurochem 105: 921-932. (Pubitemid 351562741)
29. Ickes BR, PhamTM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC. 2000. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164: 45-52. (Pubitemid 30490721)
30. Jeltsch H, Bertrand F, Lazarus C, Cassel JC. 2001. Cognitive performances and locomotor activity following dentate granule cell damage in rats: Role of lesionextent andtype ofmemory tested.Neurobiol LearnMem76:81-105. (Pubitemid 32566150)
31. Kamata Y, Shiraga H, Tai A, Kawamoto Y, Gohda E. 2007. Induction of neurite outgrowth in PC12 cells by the medium-chain fatty acid octanoic acid. Neuroscience 146: 1073-1081. (Pubitemid 46694153)
32. Kano Y, Nohno T, Shimada K, Nakagiri S, Hiragami F, Kawamura K, Motoda H, Numata K, Murai H, Koike Y. 2007. Osmotic shock-induced neurite extension via activation of p38 mitogen-activated protein kinase and CREB. Brain Res 1154: 1-7. (Pubitemid 46856332)
33. Kaplan DR, Miller FD. 2000. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10: 381-391. (Pubitemid 30389307)
34. Kelly Á, Laroche S, Davis S. 2003. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23: 5354-5360. (Pubitemid 36793264)
35. Kempermann G, Gage F. 2002. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16: 129-136. (Pubitemid 35463603)
36. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495. (Pubitemid 27164074)
37. Kempermann G, Brandon EP, Gage FH. 1998. Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol 8: 939-944.
38. Komitova M, Eriksson PS. 2004. Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369: 24-27. (Pubitemid 39369496)
39. Kumar V, Zhang MX, Swank MW, Kunz J, Wu GY. 2005. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25: 11288-11299. (Pubitemid 43083703)
40. Leranth C, Hajszan T. 2007. Extrinsic afferent systems to the dentate gyrus. Prog Brain Res 163: 63-799.
41. Levenson JM, Sweatt JD. 2005. Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6: 108-118. (Pubitemid 40188945)
42. Lindecke A, Korte M, Zagrebelsky M, Horejschi V, Elvers M, Widera D, Prüllage M, Pfeiffer J, Kaltschmidt B, Kaltschmidt C. 2006. Long-term depression activates transcription of immediate early transcription factor genes: Involvement of serum response factor/Elk-1. Eur J Neurosci 24: 555-563. (Pubitemid 44100347)
43. Martin E, Betuing S, Pagès C, Cambon K, Auregan G, Deglon N, Roze E, Caboche J. 2011. Mitogen- and stress-activated protein kinase 1-induced neuroprotection in Huntington's disease: Role on chromatin remodeling at the PGC-1-alpha promoter. Hum Mol Genet 20: 2422-2434.
44. Merz K, Herold S, Lie DC. 2011. CREB in adult neurogenesis - master and partner in the development of adult born neurons? Eur J Neuro 33: 1078-1086.
45. Muroi Y, Ishii T, Teramoto K, Hori M, Nishimura M. 2004. Calcineurin contributes to the enhancing effect of adenosine on nerve growth factor-induced neurite outgrowth via the decreased duration of p38 mitogen-activated protein kinase phosphorylation. J Pharmacol Sci 95: 124-131. (Pubitemid 38856054)
46. Nägerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T. 2004. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44: 759-767. (Pubitemid 39575630)
47. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. 1999. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39: 569-578. (Pubitemid 29260777)
48. Paxinos G,Watson C. 2007. The rat brain in stereotaxic coordinates: Hard cover edition. Academic Press, Waltham, MA.
49. Rasband WS. 1997-2012. ImageJ. U.S. National Institutes of Health, Bethesda, MD. http://imagej.nih.gov/ij/.
50. Roozendaal B, Castello NA, Vedana G, Barsegyan A, McGaugh JL. 2008. Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory. Neurobiol Learn Mem 90: 576-579.
51. Scholzen T, Gerdes J. 2000. The Ki-67 protein: From the known and the unknown. J Cell Physiol 182: 311-322. (Pubitemid 30054364)
52. Shieh PB, Ghosh A. 1999. Molecular mechanisms underlying activitydependent regulation of BDNF expression. J Neurobiol 41: 127-134. (Pubitemid 29467612)
53. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372-375.
54. Silva-Gomez AB, Rojas D, Juarez I, Flores G. 2003. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983: 128-136. (Pubitemid 36957950)
55. Sindreu CB, Scheiner ZS, Storm DR. 2007. Ca2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53: 79-89. (Pubitemid 44969491)
56. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, Hazzalin CA, Mahadevan LC, Arthur JSC. 2003. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J 22: 2788-2797. (Pubitemid 36712374)
57. Su C, Underwood W, Rybalchenko N, Singh M. 2011. ERK1/2 and ERK5 have distinct roles in the regulation of brain-derived neurotrophic factor expression. J Neurosci Res 89: 1542-1550.
58. Sugiura H, Tanaka H, Yasuda S, Takemiya T, Yamagata K. 2009. Transducing neuronal activity into dendritic spine morphology: New roles for p38 MAP kinase and N-cadherin. Neuroscientist 15: 90-104.
59. Sunyer B, Patil S, Hoger H, Lubec G. 2007. Barnes maze, a useful task to assess spatial reference memory in the mice. Nat Protoc 390: 10-38.
60. Thomas GM, Huganir RL. 2004. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5: 173-183. (Pubitemid 38252474)
61. Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, Mahadevan LC. 1999. The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J 18: 4779-4793. (Pubitemid 29415531)
62. Vaillant AR, Zanassi P, Walsh GS, Aumont A, Alonso A, Miller FD. 2002. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 34: 985-998. (Pubitemid 34722287)
63. van Praag H, Kempermann G, Gage FH. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191-198.
64. Wiggin GR, Soloaga A, Foster JM, Murray-Tait V, Cohen P, Arthur JSC. 2002. MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol Cell Biol 22: 2871-2881. (Pubitemid 34263007)
65. Wu J, Rowan MJ, Anwyl R. 2006. Long-term potentiation is mediated by multiple kinase cascades involving CaMKII or either PKA or p42/44 MAPK in the adult rat dentate gyrus in vitro. J Neurophysiol 95: 3519-3527. (Pubitemid 43846161)
66. Yilmaz-Rastoder E, Miyamae T, Braun AE, Thiels E. 2010. LTP- and LTD-inducing stimulations cause opposite changes in arc/arg3.1 mRNA level in hippocampal area CA1 in vivo. Hippocampus 21: 1290-1301.
67. Zagrebelsky M, Holz A, Dechant G, Barde YA, Bonhoeffer T, Korte M. 2005. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J Neurosci 25: 9989-9999. (Pubitemid 41528037)
68. Zhang W, Liu HT. 2002. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12: 9-18. (Pubitemid 135708299)
69. Zhang X, Sullivan JA, Moskal JR, Stanton PK. 2008. A NMDA receptor glycine site partial agonist, GLYX-13, simultaneously enhances LTP and reduces LTD at Schaffer collateral-CA1 synapses in hippocampus. Neuropharmacology 55: 1238-1250.
70. Zhen X, Du W, Romano AG, Friedman E, Harvey JA. 2001. The p38 mitogen-activated protein kinase is involved in associative learning in rabbits. J Neurosci 21: 5513-5519. (Pubitemid 32692149)