Role of polysialylated neural cell adhesion molecule in rapid eye movement sleep regulation in rats

European Journal of Neuroscience

Volumn 30, Issue 11, 2009, Pages 2190-2204

  Black, Michelle A ^a   Deurveilher, Samüel ^a   Seki, Tatsunori ^b   Marsh, Daniel R ^a   Rutishauser, Urs ^c   Rafuse, Victor F ^a   Semba, Kazue ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Circadian rhythms; REM sleep; Sleep deprivation; Sleep homeostasis; Synaptic plasticity

Indexed keywords

NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID; SIALIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; DORSAL RAPHE NUCLEUS; HYPOTHALAMUS; IMMUNOREACTIVITY; LOCUS CERULEUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; SLOW BRAIN WAVE; WESTERN BLOTTING;

ANIMALS; BRAIN; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; GENE EXPRESSION REGULATION; GLYCOSIDE HYDROLASES; HYPOTHALAMUS; INJECTIONS, INTRAVENTRICULAR; MALE; NEURAL CELL ADHESION MOLECULE L1; RATS; RATS, WISTAR; SIALIC ACIDS; SLEEP DEPRIVATION; SLEEP, REM; STATISTICS, NONPARAMETRIC; TIME FACTORS; WAKEFULNESS;

EID: 71249125798     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.07000.x     Document Type: Article

References (70)

1. Acheson, A., Sunshine, J.L. Rutishauser, U. (1991) NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol., 114, 143 153.
2. Basheer, R., Brown, R., Ramesh, V., Begum, S. McCarley, R.W. (2005) Sleep deprivation-induced protein changes in basal forebrain: implications for synaptic plasticity. J. Neurosci. Res., 82, 650 658.
3. Becker, C.G., Artola, A., Gerardy-Schahn, R., Becker, T., Welzl, H. Schachner, M. (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. J. Neurosci. Res., 45, 143 152. (Pubitemid 26257315)
4. Becquet, D., Girardet, C., Guillaumond, F., Francois-Bellan, A.M. Bosler, O. (2008) Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment. Glia, 56, 294 305.
5. Boissard, R., Fort, P., Gervasoni, D., Barbagli, B. Luppi, P.H. (2003) Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur. J. Neurosci., 18, 1627 1639.
6. Bonfanti, L. (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol., 80, 129 164.
7. Bonfanti, L. Theodosis, D.T. (2009) Polysialic acid and activity-dependent synapse remodeling. Cell Adh. Migr., 3, 43 50.
8. Bonfanti, L., Olive, S., Poulain, D.A. Theodosis, D.T. (1992) Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience, 49, 419 436.
9. Borbely, A.A. (1982) A two process model of sleep regulation. Hum. Neurobiol., 1, 195 204.
10. Burgess, A., Wainwright, S.R., Shihabuddin, L.S., Rutishauser, U., Seki, T. Aubert, I. (2008) Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev. Neurobiol., 68, 1580 1590.
11. Citri, A. Malenka, R. (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology, 33, 18 41.
12. Crown, E.D., Ye, Z., Johnson, K.M., Xu, G.-Y., McAdoo, D.J., Westlund, K.N. Hulsebosch, C.E. (2005) Upregulation of the phosphorylated form of CREB in spinothalamic tract cells following spinal cord injury: relation to central neuropathic pain. Neurosci. Lett., 384, 139 144.
13. Dalva, M.B., McClelland, A.C. Kayser, M.S. (2007) Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci., 8, 206 220.
14. Daniloff, J.K., Levi, G., Grumet, M., Rieger, F. Edelman, G.M. (1986) Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair. J. Cell Biol., 103, 929 945.
15. Deboer, T., Vansteensel, M.J., Detari, L. Meijer, J.H. (2003) Sleep states alter activity of suprachiasmatic nucleus neurons. Nat. Neurosci., 6, 1086 1090.
16. Dijk, D.J. Czeisler, C.A. (1995) Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J. Neurosci., 15, 3526 3538.
17. Doyle, E., Nolan, P.M., Bell, R. Regan, C.M. (1992) Hippocampal NCAM180 transiently increases sialylation during the acquisition and consolidation of a passive avoidance response in the adult rat. J. Neurosci. Res., 31, 513 523.
18. Endo, T., Roth, C., Landolt, H.P., Werth, E., Aeschbach, D., Achermann, P. Borbély, A.A. (1998) Selective REM sleep deprivation in humans: effects on sleep and sleep EEG. Am. J. Physiol., 274, R1186 R1194.
19. Glass, J.D., Shen, H., Fedorkova, L., Chen, L., Tomasiewicz, H. Watanabe, M. (2000) Polysialylated neural cell adhesion molecule modulates photic signaling in the mouse suprachiasmatic nucleus. Neurosci. Lett., 280, 207 210.
20. Glass, J.D., Watanabe, M., Fedorkova, L., Shen, H., Ungers, G. Rutishauser, U. (2003) Dynamic regulation of polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroscience, 117, 203 211. (Pubitemid 36246517)
21. Grivel, J., Cvetkovic, V., Bayer, L., Machard, D., Tobler, I., Muhlethaler, M. Serafin, M. (2005) The wake-promoting hypocretin/orexin neurons change their response to noradrenaline after sleep deprivation. J. Neurosci., 25, 4127 4130.
22. Gvilia, I., Turner, A., McGinty, D. Szymusiak, R. (2006a) Preoptic area neurons and the homeostatic regulation of rapid eye movement sleep. J. Neurosci., 26, 3037 3044.
23. Gvilia, I., Xu, F., McGinty, D. Szymusiak, R. (2006b) Homeostatic regulation of sleep: a role for preoptic area neurons. J. Neurosci., 26, 9426 9433.
24. Horvath, T.L. Gao, X.B. (2005) Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab., 1, 279 286.
25. Hou, X.E. Dahlstrom, A. (2000) Synaptic vesicle proteins and neuronal plasticity in adrenergic neurons. Neurochem. Res., 25, 1275 1300.
26. Hoyk, Z., Parducz, A. Theodosis, D.T. (2001) The highly sialylated isoform of the neural cell adhesion molecule is required for estradiol-induced morphological synaptic plasticity in the adult arcuate nucleus. Eur. J. Neurosci., 13, 649 656.
27. Huber, R., Tononi, G. Cirelli, C. (2007) Exploratory behavior, cortical BDNF expression, and sleep homeostasis. Sleep, 30, 129 139.
28. Johnson, C.P., Fujimoto, I., Rutishauser, U. Leckband, D.E. (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem., 280, 137 145.
29. Kalinchuk, A.V., McCarley, R.W., Stenberg, D., Porkka-Heiskanen, T. Basheer, R. (2008) The role of cholinergic basal forebrain neurons in adenosine-mediated homeostatic control of sleep: lessons from 192 IgG-saporin lesions. Neuroscience, 157, 238 253.
30. Kalsbeek, A., Kreier, F., Fliers, E., Sauerwein, H.P., Romijn, J.A. Buijs, R.M. (2007) Circadian control of metabolism by the suprachiasmatic nuclei. Endocrinology, 148, 5635 5639.
31. Kaur, S., Junek, A., Black, M.A. Semba, K. (2008) Effects of ibotenate and 192IgG-saporin lesions of the nucleus basalis magnocellularis/substantia innominata on spontaneous sleep and wake states and on recovery sleep after sleep deprivation in rats. J. Neurosci., 28, 491 504.
32. Lopez-Fernandez, M.A., Montaron, M.F., Varea, E., Rougon, G., Venero, C., Abrous, D.N. Sandi, C. (2007) Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. J. Neurosci., 27, 4552 4561.
33. Lu, J., Sherman, D., Devor, M. Saper, C.B. (2006) A putative flip-flop switch for control of REM sleep. Nature, 441, 589 594.
34. Luppi, P.H., Gervasoni, D., Verret, L., Goutagny, R., Peyron, C., Salvert, D., Leger, L. Fort, P. (2006) Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J. Physiol. Paris, 100, 271 283.
35. McCarley, R.W. (2007) Neurobiology of REM and NREM sleep. Sleep Med., 8, 302 330.
36. McCarley, R.W. Massaquoi, S.G. (1986) A limit cycle mathematical model of the REM sleep oscillator system. Am. J. Physiol., 251, R1011 R1029.
37. Mendelson, W.B., Bergmann, B.M. Tung, A. (2003) Baseline and post-deprivation recovery sleep in SCN-lesioned rats. Brain Res., 980, 185 190.
38. Mistlberger, R.E. (2005) Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res. Brain Res. Rev., 49, 429 454.
39. Mistlberger, R.E., Bergmann, B.M., Waldenar, W. Rechtschaffen, A. (1983) Recovery sleep following sleep deprivation in intact and suprachiasmatic nuclei-lesioned rats. Sleep, 6, 217 233.
40. Mistlberger, R.E., Belcourt, J. Antle, M.C. (2002) Circadian clock resetting by sleep deprivation without exercise in Syrian hamsters: dark pulses revisited. J. Biol. Rhythms, 17, 227 237.
41. Modirrousta, M., Mainville, L. Jones, B.E. (2007) Dynamic changes in GABAA receptors on basal forebrain cholinergic neurons following sleep deprivation and recovery. BMC Neurosci., 8, 15.
42. Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G. Kiss, J.Z. (2000) Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus. Proc. Natl Acad. Sci. USA, 97, 4315 4320.
43. Nacher, J., Pham, K., Gil-Fernandez, V. McEwen, B.S. (2004) Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience, 126, 503 509.
44. Parducz, A., Perez, J. Garcia-Segura, L.M. (1993) Estradiol induces plasticity of gabaergic synapses in the hypothalamus. Neuroscience, 53, 395 401.
45. Paxinos, G. Watson, W. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
46. Petridis, A.K., El-Maarouf, A. Rutishauser, U. (2004) Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev. Dyn., 230, 675 684.
47. Pham, K., Nacher, J., Hof, P.R. McEwen, B.S. (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci., 17, 879 886.
48. Pinto, S., Roseberry, A., Liu, H., Diano, S., Shanabrough, M., Cai, X., Friedman, J. Horvath, T. (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science, 304, 110 115.
49. Prosser, R.A., Rutishauser, U., Ungers, G., Fedorkova, L. Glass, J.D. (2003) Intrinsic role of polysialylated neural cell adhesion molecule in photic phase resetting of the mammalian circadian clock. J. Neurosci., 23, 652 658.
50. Rao, Y., Liu, Z.W., Borok, E., Rabenstein, R.L., Shanabrough, M., Lu, M., Picciotto, M.R., Horvath, T.L. Gao, X.B. (2007) Prolonged wakefulness induces experience-dependent synaptic plasticity in mouse hypocretin/orexin neurons. J. Clin. Invest., 117, 4022 4033.
51. Rougon, G., Dubois, C., Buckley, N., Magnani, J.L. Zollinger, W. (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol., 103, 2429 2437.
52. Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci., 9, 26 35.
53. Rutishauser, U. Landmesser, L. (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci., 19, 422 427.
54. Sakurai, T. (2007) The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat. Rev. Neurosci., 8, 171 181.
55. Sandi, C., Merino, J.J., Cordero, M.I., Touyarot, K. Venero, C. (2001) Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience, 102, 329 339.
56. Saper, C.B., Scammell, T.E. Lu, J. (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature, 437, 1257 1263. (Pubitemid 41568665)
57. Sapin, E., Lapray, D., Bérod, A., Goutagny, R., Léger, L., Ravassard, P., Clément, O., Hanriot, L., Fort, P. Luppi, P.H. (2009) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE, 4, e4272.
58. Seki, T. Arai, Y. (1991) Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol. (Berl.), 184, 395 401.
59. Seki, T. Rutishauser, U. (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J. Neurosci., 18, 3757 3766.
60. Shen, H., Watanabe, M., Tomasiewicz, H. Glass, J.D. (2001) Genetic deletions of NCAM and PSA impair circadian function in the mouse. Physiol. Behav., 73, 185 193.
61. Suntsova, N., Szymusiak, R., Alam, M.N., Guzman-Marin, R. McGinty, D. (2002) Sleep-waking discharge patterns of median preoptic nucleus neurons in rats. J. Physiol., 543, 665 677.
62. Swanson, L.W. (2002) Brain Architecture: Understanding the Basic Plan. Oxford University Press, New York.
63. Ter Horst, J.P., Loscher, J.S., Pickering, M., Regan, C.M. Murphy, K.J. (2008) Learning associated regulation of polysialylated neural cell adhesion molecule expression in the rat prefrontal cortex is region-, cell type- and paradigm-specific. Eur. J. Neurosci., 28, 419 427.
64. Theodosis, D.T., Rougon, G. Poulain, D.A. (1991) Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamo-neurohypophysial system. Proc. Natl Acad. Sci. USA, 88, 5494 5498.
65. Theodosis, D., Bonfanti, L., Olive, S., Rougon, G. Poulain, D. (1994) Adhesion molecules and structural plasticity of the adult hypothalamo- neurohypophysial system. Psychoneuroendocrinology, 19, 455 462.
66. Theodosis, D.T., Bonhomme, R., Vitiello, S., Rougon, G. Poulain, D.A. (1999) Cell surface expression of polysialic acid on NCAM is a prerequisite for activity-dependent morphological neuronal and glial plasticity. J. Neurosci., 19, 10228 10236.
67. Tobler, I. Borbely, A.A. (1990) The effect of 3-h and 6-h sleep deprivation on sleep and EEG spectra of the rat. Behav. Brain Res., 36, 73 78. (Pubitemid 20026606)
68. Uschakov, A., Gong, H., McGinty, D. Szymusiak, R. (2007) Efferent projections from the median preoptic nucleus to sleep- and arousal-regulatory nuclei in the rat brain. Neuroscience, 150, 104 120.
69. Vyazovskiy, V.V., Achermann, P. Tobler, I. (2007) Sleep homeostasis in the rat in the light and dark period. Brain Res. Bull., 74, 37 44.
70. Wurts, S.W. Edgar, D.M. (2000) Circadian and homeostatic control of rapid eye movement (REM) sleep: promotion of REM tendency by the suprachiasmatic nucleus. J. Neurosci., 20, 4300 4310.