Circadian clock regulates the shape and content of dendritic spines in mouse barrel cortex
Autoři:
Malgorzata Jasinska aff001; Ewa Jasek-Gajda aff001; Olga Woznicka aff002; Grzegorz J. Lis aff001; Elzbieta Pyza aff002; Jan A. Litwin aff001
Působiště autorů:
Department of Histology, Jagiellonian University Medical College, Krakow, Poland
aff001; Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University, Krakow, Poland
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225394
Souhrn
Circadian rhythmicity affects neuronal activity induced changes in the density of synaptic contacts and dendritic spines, the most common location of synapses, in mouse somatosensory cortex. In the present study we analyzed morphology of single- and double-synapse spines under light/dark (12:12) and constant darkness conditions. Using serial electron micrographs we examined the shape of spines (stubby, thin, mushroom) and their content (smooth endoplasmic reticulum, spine apparatus), because these features are related to the maturation and stabilization of spines. We observed significant diurnal and circadian changes in the shape of spines that are differentially regulated: single-synapse spines remain under circadian clock regulation, while changes of double-synapse spines are driven by light. The thin and mushroom single-synapse spines, regardless of their content, are more stable comparing with the stubby single-synapse spines that show the greatest diversity. All types of double-synapse spines demonstrate a similar level of stability. In light/dark regime, formation of new mushroom single-synapse spines occurs, while under constant darkness new stubby single-synapse spines are formed. There are no shape preferences for new double-synapse spines. Diurnal and circadian alterations also concern spine content: both light exposure and the clock influence translocation of smooth endoplasmic reticulum from dendritic shaft to the spine. The increasing number of mushroom single-synapse spines and the presence of only those mushroom double-synapse spines that contain spine apparatus in the light phase indicates that the exposure to light, a stress factor for nocturnal animals, promotes enlargement and maturation of spines to increase synaptic strength and to enhance the effectiveness of neurotransmission.
Klíčová slova:
Chronobiology – Synapses – Biological locomotion – Neck – Circadian rhythms – Endoplasmic reticulum – Neuronal dendrites – Somatosensory cortex
Zdroje
1. Holtmaat AJGD Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron. 2005;45: 279–291. doi: 10.1016/j.neuron.2005.01.003 15664179
2. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol. 2007;17: 381–386. doi: 10.1016/j.conb.2007.04.009 17498943
3. Deller T, Bas Orth C, Del Turco D, Vlachos A, Burbach GJ, Drakew A, et al. A role for synaptopodin and the spine apparatus in hippocampal synaptic plasticity. Ann Anat. 2007;189: 5–16. doi: 10.1016/j.aanat.2006.06.013 17319604
4. Holbro N, Grunditz A, Oertner TG. Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proc Natl Acad Sci. 2009;106: 15055–15060. doi: 10.1073/pnas.0905110106 19706463
5. Parajuli LK, Tanaka S, Okabe S. Insights into age-old questions of new dendritic spines: From form to function. Brain Res Bull. 2017;129: 3–11. doi: 10.1016/j.brainresbull.2016.07.014 27491624
6. Ziv NE, Smith SJ. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron. 1996;17: 91–102. doi: 10.1016/S0896-6273(00)80283-4 8755481
7. Fiala JC, Feinberg M, Popov V, Harris KM. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci. 1998;18: 8900–11. doi: 10.1523/JNEUROSCI.18-21-08900.1998 9786995
8. Harris K. Structure and plasticity of dendritic spines. Curr Opin Neurobiol. 1999;9: 343–348. doi: 10.1016/S0959-4388(99)80050-6 10395574
9. Harris K, Kater SB. Dendritic Spines: Cellular Specializations Imparting Both Stability and Flexibility to Synaptic Function. Annu Rev Neurosci. 1994;17: 341–371. doi: 10.1146/annurev.ne.17.030194.002013 8210179
10. van der Zee EA. Synapses, spines and kinases in mammalian learning and memory, and the impact of aging. Neurosci Biobehav Rev. 2015;50: 77–85. doi: 10.1016/j.neubiorev.2014.06.012 24998408
11. Kwon H-B, Sabatini BL. Glutamate induces de novo growth of functional spines in developing cortex. Nature. 2011;474: 100–104. doi: 10.1038/nature09986 21552280
12. Sorra KE, Harris KM. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus. 2000;10: 501–511. doi: 10.1002/1098-1063(2000)10:5<501::AID-HIPO1>3.0.CO;2-T 11075821
13. Dumitriu D, Hao J, Hara Y, Kaufmann J, Janssen WGM, Lou W, et al. Selective Changes in Thin Spine Density and Morphology in Monkey Prefrontal Cortex Correlate with Aging-Related Cognitive Impairment. J Neurosci. 2010;30: 7507–7515. doi: 10.1523/JNEUROSCI.6410-09.2010 20519525
14. Matsuzaki M, Ellis-Davies GCR, Nemoto T, Miyashita Y, Iino M, Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci. 2001;4: 1086–1092. doi: 10.1038/nn736 11687814
15. Bourne JN, Harris KM. Balancing Structure and Funcion at Hippocampal Dendritic Spines. Annu Rev Neurosci. 2008;31: 47–67. doi: 10.1146/annurev.neuro.31.060407.125646 18284372
16. Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci. 2000;3: 887–894. doi: 10.1038/78791 10966619
17. Attardo A, Fitzgerald JE, Schnitzer MJ. Impermanence of dendritic spines in live adult CA1 hippocampus. Nature. 2015;523: 592–596. doi: 10.1038/nature14467 26098371
18. Yadav A, Gao YZ, Rodriguez A, Dickstein DL, Susan L, Luebke JI, et al. Morphologic Evidence for Spatially Clustered Spines in Apical Dendrites of Monkey Neocortical Pyramidal Cells. J Comp Neurol. 2012;520: 2888–2902. doi: 10.1002/cne.23070 22315181
19. Lu J, Zuo Y. Clustered structural and functional plasticity of dendritic spines. Brain Res Bull. 2017;129:18–22. doi: 10.1016/j.brainresbull.2016.09.008 27637453
20. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003;26: 360–368. doi: 10.1016/S0166-2236(03)00162-0 12850432
21. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature. 2004;429: 761–766. doi: 10.1038/nature02617 15190253
22. González-Tapia D, Martínez-Torres NI, Hernández-González M, Guevara MA, González-Burgos I. Plastic changes to dendritic spines on layer V pyramidal neurons are involved in the rectifying role of the prefrontal cortex during the fast period of motor learning. Behav Brain Res. 2016;298: 261–267. doi: 10.1016/j.bbr.2015.11.013 26589803
23. Gray EG. Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature. 1959;183: 1592–1593. doi: 10.1038/1831592a0 13666826
24. Deller T, Korte M, Chabanis S, Drakew A, Schwegler H, Stefani GG, et al. Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc Natl Acad Sci U S A. 2003;100: 10494–10499. doi: 10.1073/pnas.1832384100 12928494
25. Fifkova E, Markham JA, Delay RJ. Calcium in the spine apparatus of dendritic spines in the dentate molecular layer. Brain Res. 1983;266: 163–168. doi: 10.1016/0006-8993(83)91322-7 6189559
26. Vlachos A, Korkotian E, Schonfeld E, Copanaki E, Deller T, Segal M. Synaptopodin regulates plasticity of dendritic spines in hippocampal neurons. J Neurosci. 2009;29: 1017–1033. doi: 10.1523/JNEUROSCI.5528-08.2009 19176811
27. Korkotian E, Segal M. Synaptopodin regulates release of calcium from stores in dendritic spines of cultured hippocampal neurons. J Physiol. 2011;589: 5987–5995. doi: 10.1113/jphysiol.2011.217315 22025667
28. Okubo-Suzuki R, Okada D, Sekiguchi M, Inokuchi K. Synaptopodin maintains the neural activity-dependent enlargement of dendritic spines in hippocampal neurons. Mol Cell Neurosci. 2008;38: 266–276. doi: 10.1016/j.mcn.2008.03.001 18424168
29. Wang L, Dumoulin A, Renner M, Triller A, Specht CG. The role of synaptopodin in membrane protein diffusion in the dendritic spine neck. PLoS One. 2016;11: e0148310. doi: 10.1371/journal.pone.0148310 26840625
30. Jedlicka P, Deller T. Understanding the role of synaptopodin and the spine apparatus in Hebbian synaptic plasticity–New perspectives and the need for computational modeling. Neurobiol Learn Mem. 2017;138: 21–30. doi: 10.1016/j.nlm.2016.07.023 27470091
31. Pierce JP, van Leyen K, McCarthy JB. Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat Neurosci. 2000;3: 311–313. doi: 10.1038/73868 10725917
32. Pierce JP, Mayer T, McCarthy JB. Evidence for a satellite secretory pathway in neuronal dendritic spines. Curr Biol. 2001;11: 351–355. doi: 10.1016/s0960-9822(01)00077-x 11267872
33. Ostroff LE, Cain CK, Bedont J, Monfils MH, LeDoux JE. Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proc Natl Acad Sci. 2010;107: 9418–9423. doi: 10.1073/pnas.0913384107 20439732
34. Chirillo MA, Waters MS, Lindsey LF, Bourne JN, Harris KM. Local resources of polyribosomes and SER promote synapse enlargement and spine clustering after long-term potentiation in adult rat hippocampus. Sci Rep.; 2019;9: 3861. doi: 10.1038/s41598-019-40520-x 30846859
35. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci. 2006;9: 1117–1124. doi: 10.1038/nn1747 16892056
36. Spacek J, Harris KM. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J Neurosci. 1997;17: 190–203. doi: 10.1523/JNEUROSCI.17-01-00190.1997 8987748
37. Havekes R, Park AJ, Tudor JC, Luczak VG, Hansen RT, Ferri SL, et al. Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1. Elife. 2016;5: 1–22. doi: 10.7554/elife.13424 27549340
38. de Vivo L, Bellesi M, Marshall W, Bushong EA, Ellisman MH, Tononi G, et al. Ultrastructural Evidence for Synaptic Scaling Across the Wake/ sleep Cycle. Science 2017;355: 507–510. doi: 10.1126/science.aah5982 28154076
39. Frank MG, Cantera R. Sleep, clocks, and synaptic plasticity. Trends Neurosci. 2014;37: 491–501. doi: 10.1016/j.tins.2014.06.005 25087980
40. Ikeda M, Hojo Y, Komatsuzaki Y, Okamoto M, Kato A, Takeda T, et al. Hippocampal spine changes across the sleep-wake cycle: corticosterone and kinases. J Endocrinol. 2015;226: M13–M27. doi: 10.1530/JOE-15-0078 26034071
41. Jasinska M, Grzegorczyk A, Woznicka O, Jasek E, Kossut M, Barbacka-Surowiak G, et al. Circadian rhythmicity of synapses in mouse somatosensory cortex. Eur J Neurosci. 2015;42: 2585–2594. doi: 10.1111/ejn.13045 26274013
42. Jasinska M, Siucinska E, Cybulska-Klosowicz A, Pyza E, Furness DN, Kossut M, et al. Rapid, Learning-Induced Inhibitory Synaptogenesis in Murine Barrel Field. J Neurosci. 2010;30: 1176–1184. doi: 10.1523/JNEUROSCI.2970-09.2010 20089926
43. Knott GW, Quairiaux C, Genoud C, Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 2002;34: 265–273. doi: 10.1016/S0896-6273(02)00663-3 11970868
44. Harris KM, Jensen FE, Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci. 1992;12: 2685–2705. doi: 10.1523/JNEUROSCI.12-07-02685.1992 1613552
45. Jasinska M, Siucinska E, Jasek E, Litwin JA, Pyza E, Kossut M. Effect of associative learning on memory spine formation in mouse barrel cortex. Neural Plast. 2016; 2016:9828517. doi: 10.1155/2016/9828517 26819780
46. Perez-Cruz C, Simon M, Flügge G, Fuchs E, Czéh B. Diurnal rhythm and stress regulate dendritic architecture and spine density of pyramidal neurons in the rat infralimbic cortex. Behav Brain Res. 2009;205: 406–413. doi: 10.1016/j.bbr.2009.07.021 19643147
47. Ikeno T, Weil ZM, Nelson RJ. Photoperiod affects the diurnal rhythm of hippocampal neuronal morphology of siberian hamsters. Chronobiol Int. 2013;30: 1089–1100. doi: 10.3109/07420528.2013.800090 23879697
48. Matus A. Actin-Based Plasticity in Dendritic Spines. Science. 2000;754: 754–759. doi: 10.1126/science.290.5492.754
49. Hotulainen P, Hoogenraad CC. Actin in dendritic spines: Connecting dynamics to function. J Cell Biol. 2010;189: 619–629. doi: 10.1083/jcb.201003008 20457765
50. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010;33: 121–129. doi: 10.1016/j.tins.2010.01.001 20138375
51. Bellot A, Guivernau B, Tajes M, Bosch-Morató M, Valls-Comamala V, Muñoz FJ. The structure and function of actin cytoskeleton in mature glutamatergic dendritic spines. Brain Res. 2014;1573: 1–16. doi: 10.1016/j.brainres.2014.05.024 24854120
52. Geinisman Y, Disterhoft JF, Gundersen HJG, Mcechron MD, Persina IS, Power JM, et al. Remodeling of hippocampal synapses after hippocampus-dependent associative learning. J Comp Neurol. 2000;417: 49–59. doi: 10.1002/(SICI)1096-9861(20000131)417:1<49::AID-CNE4>3.0.CO;2–3 10660887
53. Jasińska M, Siucińska E, Głazewski S, Pyza E, Kossut M. Characterization and plasticity of the double synapse spines in the barrel cortex of the mouse. Acta Neurobiol Exp (Wars). 2006;66: 99–104.
54. Micheva KD, Beaulieu C. An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. Proc Natl Acad Sci U S A. 1995;92: 11834–11838. doi: 10.1073/pnas.92.25.11834 8524859
55. Dehay C, Douglas RJ, Martin KA, Nelson C. Excitation by geniculocortical synapses is not 'vetoed' at the level of dendritic spines in cat visual cortex. J Physiol. 1991;440: 723–734. doi: 10.1113/jphysiol.1991.sp018732 1804984
56. Chiu CQ, Lur G, Morse TM, Carnevale NT, Ellis-Davies GC, Higley MJ. Compartmentalization of GABAergic inhibition by dendritic spines. Science. 2013;340: 759–762. doi: 10.1126/science.1234274 23661763
57. Woolsey T, Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970;17: 205–242. doi: 10.1016/0006-8993(70)90079-X 4904874
58. Foster R, Hankins M. Non-rod, non-cone photoreception in the vertebrates. Prog Retin Eye Res. 2002;21: 507–527. doi: 10.1016/S1350-9462(02)00036-8 12433375
59. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau K-W, et al. Central Projections of Melanopsin-Expressing Retinal Ganglion Cells in the Mouse. J Comp Neurol. 2006;497: 326–349. doi: 10.1002/cne.20970 16736474
60. Vandewalle G, Balteau E, Phillips C, Degueldre C, Moreau V, Sterpenich V, et al. Daytime Light Exposure Dynamically Enhances Brain Responses. Curr Biol. 2006;16: 1616–1621. doi: 10.1016/j.cub.2006.06.031 16920622
61. Gooley JJ, Lu J, Fischer D, Saper CB. A broad role for melanopsin in nonvisual photoreception. J Neurosci. 2003;23: 7093–106. doi: 10.1523/JNEUROSCI.23-18-07093.2003 12904470
62. Chellappa SL, Steiner R, Blattner P, Oelhafen P, Götz T, Cajochen C. Non-visual effects of light on melatonin, alertness and cognitive performance: Can blue-enriched light keep us alert? PLoS One. 2011;6. doi: 10.1371/journal.pone.0016429 21298068
63. Hasegawa S, Sakuragi S, Tominaga-Yoshino K, Ogura A. Dendritic spine dynamics leading to spine elimination after repeated inductions of LTD. Sci Rep. 2015;5: 1–6. doi: 10.1038/srep07707 25573377
64. Harris M., Structure development, and plasticity of dendritic spines. Curr Opin Neurobiol. 1999; 9:343–348. doi: 10.1016/S0959-4388(99)80050-6 10395574
65. Liston C, Cichon JM, Jeanneteau F, Jia Z, Chao M V, Gan WB. Circadian glucocorticoid oscillations promote learning- dependent synapse formation and maintenance. Nat Neurosci. 2013;16: 698–705. doi: 10.1038/nn.3387 23624512
66. Dickmeis T. Glucocorticoids and the circadian clock. J Endocrinol. 2009;200: 3–22. doi: 10.1677/JOE-08-0415 18971218
67. Chrousos GP. Stress and disorders of the stress system. Nat Rev Endocrinol. 2009;5: 374–381. doi: 10.1038/nrendo.2009.106 19488073
68. Nader N, Chrousos GP, Kino T. Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol Metab.; 2010;21: 277–286. doi: 10.1016/j.tem.2009.12.011 20106676
69. Buijs RM, van Eden CG, Goncharuk VD, Kalsbeek A. The biological clock tunes the organs of the body: Timing by hormones and the autonomic nervous system. J Endocrinol. 2003;177: 17–26. doi: 10.1677/joe.0.1770017 12697033
70. Liu S, Cai Y, Sothern RB, Guan Y, Chan P. Chronobiological analysis of circadian patterns in transcription of seven key clock genes in six peripheral tissues in mice. Chronobiol Int. 2007;24: 793–820. doi: 10.1080/07420520701672556 17994338
71. Koch CE, Leinweber B, Drengberg BC, Blaum C, Oster H. Interaction between circadian rhythms and stress. Neurobiol Stress.; 2016;6: 57–67. doi: 10.1016/j.ynstr.2016.09.001 28229109
72. Oster H, Damerow S, Kiessling S, Jakubcakova V, Abraham D, Tian J, et al. The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab. 2006;4: 163–173. doi: 10.1016/j.cmet.2006.07.002 16890544
73. Cheifetz P. The daily rhythm of the secretion of corticotrophin and corticosterone in rats and mice. J Endocrinol. 1971;49: xi–xii.
74. Chung S, Son GH, Kim K. Circadian rhythm of adrenal glucocorticoid: its regulation and clinical implications. Biochim Biophys Acta—Mol Basis Dis. 2011;1812: 581–591. doi: 10.1016/j.bbadis.2011.02.003
75. Liston C, Gan WB. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci U S A. 2011;108: 16074–16079. doi: 10.1073/pnas.1110444108 21911374
76. Vlachos A, Korkotian E, Schonfeld E, Copanaki E, Deller T, Segal M. Synaptopodin Regulates Plasticity of Dendritic Spines in Hippocampal Neurons. J Neurosci. 2009;29: 1017–1033. doi: 10.1523/JNEUROSCI.5528-08.2009 19176811
77. Korkotian E, Frotscher M, Segal M. Synaptopodin Regulates Spine Plasticity: Mediation by Calcium Stores. J Neurosci. 2014;34: 11641–11651. doi: 10.1523/JNEUROSCI.0381-14.2014 25164660
Článok vyšiel v časopise
PLOS One
2019 Číslo 11
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF