Behavioural and EEG effects of chronic rapamycin treatment in a mouse model of Tuberous Sclerosis Complex

Neuropharmacology

Volumn 67, Issue , 2013, Pages 1-7

  Cambiaghi, Marco ^a   Cursi, Marco ^a   Magri, Laura ^a,b   Castoldi, Valerio ^a   Comi, Giancarlo ^a,c   Minicucci, Fabio ^a   Galli, Rossella ^a,b   Leocani, Letizia ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b Neural Stem Cell Biology Unit   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Behaviour; EEG; Rapamycin; Spectral analysis; Tuberous Sclerosis Complex

Indexed keywords

RAPAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CONTROL; BODY WEIGHT; BRAIN FUNCTION; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG EFFECT; ELECTROENCEPHALOGRAPHY; FORCED SWIMMING TEST; MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; TUBEROUS SCLEROSIS; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; MAZE LEARNING; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; SIROLIMUS; TREATMENT OUTCOME; TUBEROUS SCLEROSIS; TUMOR SUPPRESSOR PROTEINS;

EID: 84873325835     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.11.003     Document Type: Article

References (60)

1. S. Aydin-Abidin, M. Yildirim, I. Abidin, and A. Cansu Chronic application of topiramate and carbamazepine differentially affects the EEG and penicillin-induced epileptiform activity in rats Neurol. Res. 34 3 Apr 2012 246 251
2. R.J. Barry, A.R. Clarke, M. Hajos, R. McCarthy, M. Selikowitz, and J.M. Bruggemann Acute atomoxetine effects on the EEG of children with attention-deficit/hyperactivity disorder Neuropharmacology 57 7-8 2009 Dec 702 707
3. C.R. Baumann, E. Kilic, B. Petit, E. Werth, D.M. Hermann, M. Tafti, and C.L. Bassetti Sleep EEG changes after middle cerebral artery infarcts in mice: different effects of striatal and cortical lesions Sleep 29 2006 1339 1344
4. J.J. Bissler, F.X. McCormack, L.R. Young, J.M. Elwing, G. Chuck, J.M. Leonard, V.J. Schmithorst, T. Laor, A.S. Brody, and J. Bean Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis N. Engl. J. Med. 358 2008 140 151
5. S.G. Buckman, S.R. Hodgson, R.S. Hofford, and S. Eitan Increased elevated plus maze open-arm time in mice during spontaneous morphine withdrawal Behav. Brain Res. 197 2009 454 456
6. M. Cambiaghi, M. Cursi, E. Monzani, F. Benfenati, G. Comi, F. Minicucci, F. Valtorta, and L. Leocani Temporal evolution of neurophysiological and behavioral features of synapsin I/II/III triple knock-out mice Epilepsy Res. 2012
7. V. Castagne, P. Moser, S. Roux, and R.D. Porsolt Rodent models of depression: forced swim and tail suspension behavioural despair tests in rats and mice Curr. Protoc. Neurosci. 2011 (Chapter 8), Unit 8 10A.
8. C. Cleary, J.A. Linde, K.M. Hiscock, I. Hadas, R.H. Belmaker, G. Agam, S. Flaisher-Grinberg, and H. Einat Antidepressive-like effects of rapamycin in animal models: implications for mTOR inhibition as a new target for treatment of affective disorders Brain Res. Bull. 76 2008 469 473
9. D. Colas, R. Cespuglio, and N. Sarda Sleep wake profile and EEG spectral power in young or old senescence accelerated mice Neurobiol. Aging 26 2 2005 Feb 265 273
10. P.B. Crino, K.L. Nathanson, and E.P. Henske The tuberous sclerosis complex N. Engl. J. Med. 355 2006 1345 1356
11. R. Crupi, M. Cambiaghi, L. Spatz, R. Hen, M. Thorn, E. Friedman, G. Vita, and F. Battaglia Reduced adult neurogenesis and altered emotional behaviors in autoimmune-prone B-cell activating factor transgenic mice 15 Biol. Psychiatry 67 6 2010 558 566
12. P. Curatolo, R. Bombardieri, and S. Jozwiak Tuberous sclerosis Lancet 372 2008 657 668
13. D.M. Davies, P.J. de Vries, S.R. Johnson, D.L. McCartney, J.A. Cox, A.L. Serra, P.C. Watson, C.J. Howe, T. Doyle, K. Pointon, J.J. Cross, A.E. Tattersfield, J.C. Kingswood, and J.R. Sampson Sirolimus therapy for angiomyolipoma in tuberous sclerosis and sporadic lymphangioleiomyomatosis: a phase 2 trial 15 Clin. Cancer Res. 17 12 2011 4071 4081
14. P. de Vries, A. Humphrey, D. McCartney, P. Prather, P. Bolton, and A. Hunt Consensus clinical guidelines for the assessment of cognitive and behavioural problems in tuberous sclerosis Eur. Child. Adolesc. Psychiatry 14 2005 183 190
15. F.J. DiMario Jr. Brain abnormalities in tuberous sclerosis complex J. Child. Neurol. 19 2004 650 657
16. D. Ehninger, and A.J. Silva Rapamycin for treating tuberous sclerosis and autism spectrum disorders Trends Mol. Med. 172 2011 78 87
17. D. Ehninger, and A.J. Silva Increased levels of anxiety-related behaviours in a Tsc2 dominant negative transgenic mouse model of tuberous sclerosis Behav. Genet. 413 2011 357 363
18. D. Ehninger, S. Han, C. Shilyansky, Y. Zhou, W. Li, D.J. Kwiatkowski, V. Ramesh, and A.J. Silva Reversal of learning deficits in a Tsc2+/- mouse model of Tuberous sclerosis Nat. Med. 14 2008 843 848
19. D. Ehninger From genes to cognition in tuberous sclerosis: implications for mTOR inhibitor-based treatment approaches Neuropharmacology 2012 May 22
20. M. Fedor, R.F. Berman, J.P. Muizelaar, and B.G. Lyeth Hippocampal dysfunction after lateral fluid percussion injury J. Neurotrauma 27 2010 1605 1615
21. D.N. Franz, J. Leonard, C. Tudor, G. Chuck, M. Care, G. Sethuraman, A. Dinopoulos, G. Thomas, and K.R. Crone Rapamycin causes regression of astrocytomas in tuberous sclerosis complex Ann. Neurol. 59 2006 490 498
22. S.M. Goorden, G.M. van Woerden, L. van der Weerd, J.P. Cheadle, and Y. Elgersma Cognitive deficits in Tsc1+/- mice in the absence of cerebral lesions and seizures Ann. Neurol. 62 2007 648 655
23. C. Graversen, S.S. Olesen, A.E. Olesen, K. Steimle, D. Farina, O.H. Wilder-Smith, S.A. Bouwense, H. van Goor, and A.M. Drewes The analgesic effect of pregabalin in patients with chronic pain is reflected by changes in pharmaco-EEG spectral indices Br. J. Clin. Pharmacol. 73 3 2012 Mar 363 372
24. J. Jaworski, and M. Sheng The growing role of mTOR in neuronal development and plasticity Mol. Neurobiol. 34 2006 205 219
25. C. Joinson, F.J. O'Callaghan, J.P. Osborne, C. Martyn, T. Harris, and P.F. Bolton Learning disability and epilepsy in an epidemiological sample of individuals with tuberous sclerosis complex Psychol. Med. 33 2003 335 344
26. D.H. Kim, D.D. Sarbassov, S.M. Ali, J.E. King, R.R. Latek, H. Erdjument-Bromage, P. Tempst, and D.M. Sabatini mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery Cell 110 2002 163 175
27. W.R. Klemm Are there EEG correlates of mental states in animals? Neuropsychobiology 26 1992 151 165
28. W. Klimesch EEG-alpha rhythms and memory processes Int. J. Psychophysiol. 26 1997 319 340 (IQ)
29. W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis Brain Res. Cogn. Brain Res. Rev. 29 2-3 1999 169 195
30. F. Krijzer, P. Koopman, and B. Olivier Classification of psychotropic drugs based on pharmaco-electrocorticographic studies in vigilance-controlled rats Neuropsychobiology 28 3 1993 122 137
31. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2012 274 293
32. L. Leocani, T. Locatelli, V. Martinelli, M. Rovaris, M. Falautano, M. Filippi, G. Magnani, and G. Comi Electroencephalographic coherence analysis in multiple sclerosis: correlation with clinical, neuropsychological, and MRI findings J. Neurol. Neurosurg. Psychiatr. 69 2 2000 Aug 192 198
33. L. Leocani, J.J. Gonzalez-Rosa, and G. Comi Neurophysiological correlates of cognitive disturbances in multiple sclerosis Neurol. Sci. 31 Suppl. 2 Nov 2010 S249 S253
34. H. van Lier, W.H. Drinkenburg, Y.J. van Eeten, and A.M. Coenen Effects of diazepam and zolpidem on EEG beta frequencies are behaviour-specific in rats Neuropharmacology 47 2004 163 174
35. R. Loewith, E. Jacinto, S. Wullschleger, A. Lorberg, J.L. Crespo, D. Bonenfant, W. Oppliger, P. Jenoe, and M.N. Hall Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control Mol. Cell. 10 2002 457 468
36. L. Magri, M. Cambiaghi, M. Cominelli, C. Alfaro-Cervello, M. Cursi, M. Pala, A. Bulfone, J.M. Garcia-Verdugo, L. Leocani, and F. Minicucci Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions Cell Stem Cell 9 2011 447 462
37. P. Major, S. Rakowski, M.V. Simon, M.L. Cheng, E. Eskandar, J. Baron, B.A. Leeman, M.P. Frosch, and E.A. Thiele Are cortical tubers epileptogenic? Evidence from electrocorticography Epilepsia 50 2009 147 154
38. C.M. McCormick, C. Smith, and I.Z. Mathews Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats Behav. Brain Res. 187 2008 228 238
39. L. Meikle, D.M. Talos, H. Onda, K. Pollizzi, A. Rotenberg, M. Sahin, F.E. Jensen, and D.J. Kwiatkowski A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival J. Neurosci. 27 2007 5546 5558
40. L. Meikle, K. Pollizzi, A. Egnor, I. Kramvis, H. Lane, M. Sahin, and D.J. Kwiatkowski Response of a neuronal model of tuberous sclerosis to mammalian target of rapamycin mTOR inhibitors: effects on mTORC1 and Akt signaling lead to improved survival and function J. Neurosci. 28 2008 5422 5432
41. V. Mosienko, B. Bert, D. Beis, S. Matthes, H. Fink, M. Bader, and N. Alenina Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin Transl. Psychiatry 29 2012 May 2
42. D.A. Muzykewicz, P. Newberry, N. Danforth, E.F. Halpern, and E.A. Thiele Psychiatric comorbid conditions in a clinic population of 241 patients with tuberous sclerosis complex Epilepsy Behav. 114 2007 506 513
43. N. Narboux-Nême, C. Sagné, S. Doly, S.L. Diaz, C.B. Martin, G. Angenard, M.P. Martres, B. Giros, M. Hamon, L. Lanfumey, P. Gaspar, and R. Mongeau Severe serotonin depletion after conditional deletion of the vesicular monoamine transporter 2 gene in serotonin neurons: neural and behavioral consequences Neuropsychopharmacology 36 12 2011 Nov 2538 2550
44. T. Páleníček, M. Fujáková, M. Brunovský, J. Horáček, I. Gorman, M. Balíková , L. Rambousek, K. Syslová, P. Kačer, P. Zach, V. Bubeníková-Valešová, F. Tylš, A. Kubešová, J. Puskarčíková, and C. Höschl Behavioral, neurochemical and pharmaco-EEG profiles of the psychedelic drug 4-bromo-2,5-dimethoxyphenethylamine (2C-B) in rats Psychopharmacology (Berl) 2012 Jul 29
45. R. Parmentier, H. Ohtsu, Z. Djebbara-Hannas, J.L. Valatx, T. Watanabe, and J.S. Lin Anatomical, physiological, and pharmacological characteristics of histidine decarboxylase knock-out mice: evidence for the role of brain histamine in behavioral and sleep-wake control J. Neurosci. 22 17 2002 Sep 1 7695 7711
46. R.D. Porsolt, A. Bertin, and M. Jalfre Behavioral despair in mice: a primary screening test for antidepressants Arch. Int. Pharmacodyn. Ther. 229 1977 327 336
47. B.P. Poschel, P.M. Ho, and F.W. Ninteman Arousal deficit shown in aged rat's quantitative EEG and ameliorative action of pramiracetam compared to piracetam Experientia 41 11 1985 Nov 15 1433 1435
48. D.M. Sabatini, H. Erdjument-Bromage, M. Lui, P. Tempst, and S.H. Snyder RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs Cell 78 1994 35 43
49. M. Salinsky, D. Spencer, B. Oken, and D. Storzbach Effects of oxcarbazepine and phenytoin on the EEG and cognition in healthy volunteers Epilepsy Behav. 5 2004 894 902
50. K.V. Savelieva, S. Zhao, V.M. Pogorelov, I. Rajan, Q. Yang, E. Cullinan, and T.H. Lanthorn Genetic disruption of both tryptophan hydroxylase genes dramatically reduces serotonin and affects behavior in models sensitive to antidepressants PLoS One 3 10 2008
51. S.F. Tavazoie, V.A. Alvarez, D.A. Ridenour, D.J. Kwiatkowski, and B.L. Sabatini Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2 Nat. Neurosci. 8 2005 1727 1734
52. E.J. Uhlmann, M. Wong, R.L. Baldwin, M.L. Bajenaru, H. Onda, D.J. Kwiatkowski, K. Yamada, and D.H. Gutmann Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures Ann. Neurol. 52 2002 285 296
53. P.J. de Vries, and C.J. Howe The tuberous sclerosis complex proteins-a GRIPP on cognition and neurodevelopment Trends Mol. Med. 13 2007 319 326
54. P.J. de Vries, and P.A. Prather The tuberous sclerosis complex N. Engl. J. Med. 356 1 2007 Jan 4 92
55. P.J. de Vries, J. Gardiner, and P.F. Bolton Neuropsychological attention deficits in tuberous sclerosis complex TSC Am. J. Med. Genet. A 149A 2009 387 395
56. S.W. Way, J. McKenna 3rd, U. Mietzsch, R.M. Reith, H.C. Wu, and M.J. Gambello Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse Hum. Mol. Genet. 18 2009 1252 1265
57. S.M. Weiss, G. Wadsworth, A. Fletcher, and C.T. Dourish Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety Neurosci. Biobehav. Rev. 23 1998 265 271
58. P.D. Welch The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms IEEE Trans. Audio Electroacoustics AU-15 1967 70 73
59. L.H. Zeng, L. Xu, D.H. Gutmann, and M. Wong Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex Ann. Neurol. 63 2008 444 453
60. R. Zoncu, A. Efeyan, and D.M. Sabatini mTOR: from growth signal integration to cancer, diabetes and ageing Nat. Rev. Mol. Cell. Biol. 12 2011 21 35