Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1

eLife

Volumn 5, Issue AUGUST, 2016, Pages

  Havekes, Robbert ^a,b   Park, Alan J ^a,g   Tudor, Jennifer C ^a   Luczak, Vincent G ^a   Hansen, Rolf T ^a   Ferri, Sarah L ^a   Bruinenberg, Vibeke M ^b   Poplawski, Shane G ^a   Day, Jonathan P ^c   Aton, Sara J ^d   Radwańska, Kasia ^e   Meerlo, Peter ^b   Houslay, Miles D ^f   Baillie, George S ^c   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF MICHIGAN   (United States)

^e NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^f KING'S COLLEGE LONDON   (United Kingdom)

^g NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; CYCLIC AMP; CYCLIC AMP PHOSPHODIESTERASE; GREEN FLUORESCENT PROTEIN; LIM KINASE; ACTIN DEPOLYMERIZING FACTOR; PDE4A PROTEIN, MOUSE; PHOSPHODIESTERASE IV;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC SPINE; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; LONG TERM MEMORY; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; SLEEP DEPRIVATION; WESTERN BLOTTING; ANIMAL; COMPLICATION; CYTOLOGY; MEMORY DISORDER; METABOLISM; NERVE CELL; PHYSIOLOGY;

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; DENDRITIC SPINES; MEMORY DISORDERS; MICE; NEURONS; SLEEP DEPRIVATION;

EID: 84983616629     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13424.001     Document Type: Article

References (68)

1. Abel T, Havekes R, Saletin JM, Walker MP. 2013. Sleep, plasticity and memory from molecules to whole-brain networks. Current Biology 23:R774–788. doi: 10.1016/j.cub.2013.07.025
2. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, Lefkowitz RJ, Houslay MD. 2003. beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. PNAS 100:940–945. doi: 10.1073/pnas.262787199
3. Bamburg JR. 1999. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annual Review of Cell and Developmental Biology 15:185–230. doi: 10.1146/annurev.cellbio.15.1.185
4. Bolger GB, Peden AH, Steele MR, MacKenzie C, McEwan DG, Wallace DA, Huston E, Baillie GS, Houslay MD. 2003. Attenuation of the activity of the cAMP-specific phosphodiesterase PDE4A5 by interaction with the immunophilin XAP2. Journal of Biological Chemistry 278:33351–33363. doi: 10.1074/jbc.M303269200
5. Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y. 2014. Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82:444–459. doi: 10.1016/j.neuron.2014.03.021
6. Briz V, Zhu G, Wang Y, Liu Y, Avetisyan M, Bi X, Baudry M. 2015. Activity-dependent rapid local RhoA synthesis is required for hippocampal synaptic plasticity. Journal of Neuroscience 35:2269–2282. doi: 10.1523/JNEUROSCI.2302-14.2015
7. Bryant PA, Trinder J, Curtis N. 2004. Sick and tired: Does sleep have a vital role in the immune system? Nature Reviews Immunology 4:457–467. doi: 10.1038/nri1369
8. Caroni P, Donato F, Muller D. 2012. Structural plasticity upon learning: regulation and functions. Nature Reviews Neuroscience 13:478–490. doi: 10.1038/nrn3258
9. Chen LY, Rex CS, Casale MS, Gall CM, Lynch G. 2007. Changes in synaptic morphology accompany actin signaling during LTP. Journal of Neuroscience 27:5363–5372. doi: 10.1523/JNEUROSCI.0164-07.2007
10. Davis RC, Marsden IT, Maloney MT, Minamide LS, Podlisny M, Selkoe DJ, Bamburg JR. 2011. Amyloid beta dimers/trimers potently induce cofilin-actin rods that are inhibited by maintaining cofilin-phosphorylation. Molecular Neurodegeneration 6:10. doi: 10.1186/1750-1326-6-10
11. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie TW, Helmchen F, Denk W, Brecht M, Osten P. 2004. Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. PNAS 101:18206–18211. doi: 10.1073/pnas.0407976101
12. Fedulov V, Rex CS, Simmons DA, Palmer L, Gall CM, Lynch G. 2007. Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. Journal of Neuroscience 27:8031–8039. doi: 10.1523/JNEUROSCI.2003-07.2007
13. Florian C, Vecsey CG, Halassa MM, Haydon PG, Abel T. 2011. Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. Journal of Neuroscience 31:6956–6962. doi: 10.1523/JNEUROSCI.5761-10.2011
14. González-Burgos I, Alejandre-Gómez M, Cervantes M. 2005. Spine-type densities of hippocampal CA1 neurons vary in proestrus and estrus rats. Neuroscience Letters 379:52–54. doi: 10.1016/j.neulet.2004.12.043
15. Graves LA, Heller EA, Pack AI, Abel T. 2003. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learning & Memory 10:168–176. doi: 10.1101/lm.48803
16. Gurniak CB, Perlas E, Witke W. 2005. The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Developmental Biology 278:231–241. doi: 10.1016/j.ydbio.2004.11.010
17. Hagewoud R, Whitcomb SN, Heeringa AN, Havekes R, Koolhaas JM, Meerlo P. 2010a. A time for learning and a time for sleep: the effect of sleep deprivation on contextual fear conditioning at different times of the day. Sleep 33:1315–1322.
18. Hagewoud R, Havekes R, Novati A, Keijser JN, Van der Zee EA, Meerlo P. 2010b. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. Journal of Sleep Research 19:280–288. doi: 10.1111/j.1365-2869.2009.00799.x
19. Hagewoud R, Havekes R, Tiba PA, Novati A, Hogenelst K, Weinreder P, Van der Zee EA, Meerlo P. 2010c. Coping with sleep deprivation: shifts in regional brain activity and learning strategy. Sleep 33:1465–1473.
20. Harrison Y, Horne JA. 2000. Sleep loss and temporal memory. The Quarterly Journal of Experimental Psychology Section A 53:271–279. doi: 10.1080/713755870
21. Havekes R, Bruinenberg VM, Tudor JC, Ferri SL, Baumann A, Meerlo P, Abel T. 2014. Transiently increasing cAMP levels selectively in hippocampal excitatory neurons during sleep deprivation prevents memory deficits caused by sleep loss. Journal of Neuroscience 34:15715–15721. doi: 10.1523/JNEUROSCI.2403-14.2014
22. Havekes R, Canton DA, Park AJ, Huang T, Nie T, Day JP, Guercio LA, Grimes Q, Luczak V, Gelman IH, Baillie GS, Scott JD, Abel T. 2012b. Gravin orchestrates protein kinase A and b2-adrenergic receptor signaling critical for synaptic plasticity and memory. Journal of Neuroscience 32:18137–18149. doi: 10.1523/JNEUROSCI.3612-12.2012
23. Havekes R, Vecsey CG, Abel T. 2012a. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cellular Signalling 24:1251–1260. doi: 10.1016/j.cellsig.2012.02.010
24. Houslay MD. 2010. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends in Biochemical Sciences 35:91–100. doi: 10.1016/j.tibs.2009.09.007
25. Isiegas C, McDonough C, Huang T, Havekes R, Fabian S, Wu LJ, Xu H, Zhao MG, Kim JI, Lee YS, Lee HR, Ko HG, Lee N, Choi SL, Lee JS, Son H, Zhuo M, Kaang BK, Abel T. 2008. A novel conditional genetic system reveals that increasing neuronal cAMP enhances Memorymemory and Retrievalretrieval. Journal of Neuroscience 28: 6220–6230. doi: 10.1523/JNEUROSCI.2935-07.2008
26. Konakahara S, Ohashi K, Mizuno K, Itoh K, Tsuji T. 2004. CD29 integrin- and LIMK1/cofilin-mediated actin reorganization regulates the migration of haematopoietic progenitor cells underneath bone marrow stromal cells. Genes to Cells 9:345–358. doi: 10.1111/j.1356-9597.2004.00726.x
27. Lamprecht R, LeDoux J. 2004. Structural plasticity and memory. Nature Reviews Neuroscience 5:45–54. doi: 10.1038/nrn1301
28. Leuner B, Falduto J, Shors TJ. 2003. Associative memory formation increases the observation of dendritic spines in the hippocampus. Journal of Neuroscience 23:659–665.
29. Lynch MA. 2004. Long-term potentiation and memory. Physiological Reviews 84:87–136. doi: 10.1152/physrev.00014.2003
30. Maret S, Faraguna U, Nelson AB, Cirelli C, Tononi G. 2011. Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nature Neuroscience 14:1418–1420. doi: 10.1038/nn.2934
31. Mayford M, Siegelbaum SA, Kandel ER. 2012. Synapses and memory storage. Cold Spring Harbor Perspectives in Biology 4. doi: 10.1101/cshperspect.a005751
32. McCahill A, McSorley T, Huston E, Hill EV, Lynch MJ, Gall I, Keryer G, Lygren B, Tasken K, van Heeke G, Houslay MD. 2005. In resting COS1 cells a dominant negative approach shows that specific, anchored PDE4 cAMP phosphodiesterase isoforms gate the activation, by basal cyclic AMP production, of AKAP-tethered protein kinase A type II located in the centrosomal region. Cellular Signalling 17:1158–1173. doi: 10.1016/j.cellsig.2005.04.003
33. McLaughlin KJ, Baran SE, Wright RL, Conrad CD. 2005. Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction: possible involvement of CA1 neurons. Neuroscience 135:1045–1054. doi: 10.1016/j.neuroscience.2005.06.083
34. McPhee I, Cochran S, Houslay MD. 2001. The novel long PDE4A10 cyclic AMP phosphodiesterase shows a pattern of expression within brain that is distinct from the long PDE4A5 and short PDE4A1 isoforms. Cellular Signalling 13:911–918. doi: 10.1016/S0898-6568(01)00217-0
35. Meberg PJ, Ono S, Minamide LS, Takahashi M, Bamburg JR. 1998. Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motility and the Cytoskeleton 39:172–190. doi: 10.1002/(SICI)1097-0169(1998)39:2<172::AID-CM8>3.0.CO;2-8
36. Meerlo P, de Bruin EA, Strijkstra AM, Daan S. 2001. A social conflict increases EEG slow-wave activity during subsequent sleep. Physiology & Behavior 73:331–335. doi: 10.1016/S0031-9384(01)00451-6
37. Morrell MJ, McRobbie DW, Quest RA, Cummin AR, Ghiassi R, Corfield DR. 2003. Changes in brain morphology associated with obstructive sleep apnea. Sleep Medicine 4:451–454. doi: 10.1016/S1389-9457(03)00159-X
38. Nadella KS, Saji M, Jacob NK, Pavel E, Ringel MD, Kirschner LS. 2009. Regulation of actin function by protein kinase A-mediated phosphorylation of Limk1. EMBO Reports 10:599–605. doi: 10.1038/embor.2009.58
39. Neves G, Cooke SF, Bliss TV. 2008. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nature Reviews Neuroscience 9:65–75. doi: 10.1038/nrn2303
40. Novati A, Hulshof HJ, Koolhaas JM, Lucassen PJ, Meerlo P. 2011. Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience 190:145–155. doi: 10.1016/j.neuroscience.2011.06.027
41. Oe Y, Tominaga-Yoshino K, Hasegawa S, Ogura A. 2013. Dendritic spine dynamics in synaptogenesis after repeated LTP inductions: dependence on pre-existing spine density. Scientific Reports 3:1957. doi: 10.1038/srep01957
42. Oliveira AM, Hawk JD, Abel T, Havekes R. 2010. Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learning & Memory 17:155–160. doi: 10.1101/lm.1625310
43. Pavlides C, Winson J. 1989. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journal of Neuroscience 9:2907–2918.
44. Pontrello CG, Sun MY, Lin A, Fiacco TA, DeFea KA, Ethell IM. 2012. Cofilin under control of b-arrestin-2 in NMDA-dependent dendritic spine plasticity, long-term depression (LTD), and learning. PNAS 109:E442–E451. doi: 10.1073/pnas.1118803109
45. Popow-Woźniak A, Mazur AJ, Mannherz HG, Malicka-Błaszkiewicz M, Nowak D. 2012. Cofilin overexpression affects actin cytoskeleton organization and migration of human colon adenocarcinoma cells. Histochemistry and Cell Biology 138:725–736. doi: 10.1007/s00418-012-0988-2
46. Prince TM, Wimmer M, Choi J, Havekes R, Aton S, Abel T. 2014. Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory. Neurobiology of Learning and Memory 109:122–130. doi: 10.1016/j.nlm.2013.11.021
47. Rex CS, Gavin CF, Rubio MD, Kramar EA, Chen LY, Jia Y, Huganir RL, Muzyczka N, Gall CM, Miller CA, Lynch G, Rumbaugh G. 2010. Myosin IIb regulates actin dynamics during synaptic plasticity and memory formation. Neuron 67:603–617. doi: 10.1016/j.neuron.2010.07.016
48. Riemann D, Voderholzer U, Spiegelhalder K, Hornyak M, Buysse DJ, Nissen C, Hennig J, Perlis ML, van Elst LT, Feige B. 2007. Chronic insomnia and MRI-measured hippocampal volumes: a pilot study. Sleep 30:955–958.
49. Rust MB. 2015. ADF/cofilin: a crucial regulator of synapse physiology and behavior. Cellular and Molecular Life Sciences 72:3521–3529. doi: 10.1007/s00018-015-1941-z
50. Sah P, Westbrook RF, Lüthi A. 2008. Fear conditioning and long-term potentiation in the amygdala: what really is the connection? Annals of the New York Academy of Sciences 1129:88–95. doi: 10.1196/annals.1417.020
51. Sarmiere PD, Bamburg JR. 2004. Regulation of the neuronal actin cytoskeleton by ADF/cofilin. Journal of Neurobiology 58:103–117. doi: 10.1002/neu.10267
52. Seabold GK, Daunais JB, Rau A, Grant KA, Alvarez VA. 2010. DiOLISTIC labeling of neurons from rodent and non-human primate brain slices. Journal of Visualized Experiments 41:2081. doi: 10.3791/2081
53. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. 2007. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. Journal of Neuroscience 27:2866–2875. doi: 10.1523/JNEUROSCI.4970-06.2007
54. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, Ethell IM. 2009. Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. Journal of Neuroscience 29:8129–8142. doi: 10.1523/JNEUROSCI.4681-08.2009
55. Shors TJ, Chua C, Falduto J. 2001. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. Journal of Neuroscience 21:6292–6297.
56. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–823. doi: 10.1016/j.cell.2011.02.018
57. Tononi G, Cirelli C. 2006. Sleep function and synaptic homeostasis. Sleep Medicine Reviews 10:49–62. doi: 10.1016/j.smrv.2005.05.002
58. Tononi G, Cirelli C. 2014. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81:12–34. doi: 10.1016/j.neuron.2013.12.025
59. Tretter V, Revilla-Sanchez R, Houston C, Terunuma M, Havekes R, Florian C, Jurd R, Vithlani M, Michels G, Couve A, Sieghart W, Brandon N, Abel T, Smart TG, Moss SJ. 2009. Deficits in spatial memory correlate with modified {gamma}-aminobutyric acid type A receptor tyrosine phosphorylation in the hippocampus. PNAS 106: 20039–20044. doi: 10.1073/pnas.0908840106
60. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M, Huang T, Brown KM, Li XY, Descalzi G, Kim SS, Chen T, Shang YZ, Zhuo M, Houslay MD, Abel T. 2009. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461:1122–1125. doi: 10.1038/nature08488
61. Vecsey CG, Wimmer ME, Havekes R, Park AJ, Perron IJ, Meerlo P, Abel T. 2013. Daily acclimation handling does not affect hippocampal long-term potentiation or cause chronic sleep deprivation in mice. Sleep 36:601–607. doi: 10.5665/sleep.2556
62. Vogel-Ciernia A, Matheos DP, Barrett RM, Kramár EA, Azzawi S, Chen Y, Magnan CN, Zeller M, Sylvain A, Haettig J, Jia Y, Tran A, Dang R, Post RJ, Chabrier M, Babayan AH, Wu JI, Crabtree GR, Baldi P, Baram TZ, et al. 2013. The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory. Nature Neuroscience 16:552–561. doi: 10.1038/nn.3359
63. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G. 2008. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscience 11:200–208. doi: 10.1038/nn2035
64. Whitney P, Hinson JM. 2010. Measurement of cognition in studies of sleep deprivation. Progress in Brain Research 185:37–48. doi: 10.1016/B978-0-444-53702-7.00003-8
65. Yang G, Gan WB. 2012. Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex. Developmental Neurobiology 72:1391–1398. doi: 10.1002/dneu.20996
66. Yang G, Lai CS, Cichon J, Ma L, Li W, Gan WB. 2014. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344:1173–1178. doi: 10.1126/science.1249098
67. Zhao R, Du L, Huang Y, Wu Y, Gunst SJ, Du L HY. 2008. Actin depolymerization factor/cofilin activation regulates actin polymerization and tension development in canine tracheal smooth muscle. Journal of Biological Chemistry 283:36522–36531. doi: 10.1074/jbc.M805294200
68. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749–757. doi: 10.1016/j.neuron.2004.11.011