Synaptic plasticity and learning in animal models of tuberous sclerosis complex

Neural Plasticity

Volumn 2012, Issue , 2012, Pages

  Kirschstein, Timo ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TARGET OF RAPAMYCIN KINASE;

BEHAVIOR CHANGE; COGNITIVE DEFECT; FREQUENCY MODULATION; GENE MUTATION; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; REVIEW; SYNAPTIC TRANSMISSION; TUBEROUS SCLEROSIS; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; RAT; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; LEARNING; MICE; NEURONAL PLASTICITY; RATS; SYNAPSES; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS;

EID: 84864913319     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2012/279834     Document Type: Review

References (72)

1. Crino P. B., Nathanson K. L., Henske E. P., Medical progress: the tuberous sclerosis complex The New England Journal of Medicine 2006 355 13 1345 1356
2. Curatolo P., Bombardieri R., Jozwiak S., Tuberous sclerosis The Lancet 2008 372 9639 657 668
3. Huttenlocher P. R., Wollmann R. L., Cellular neuropathology of tuberous sclerosis Annals of the New York Academy of Sciences 1991 615 140 148
4. Mizuguchi M., Takashima S., Neuropathology of tuberous sclerosis Brain and Development 2001 23 7 508 515 (Pubitemid 32999117)
5. Bolton P. F., Park R. J., Higgins J. N. P., Griffiths P. D., Pickles A., Neuro-epileptic determinants of autism spectrum disorDers in tuberous sclerosis complex Brain 2002 125 6 1247 1255 (Pubitemid 34587134)
6. Joinson C., O'Callaghan F. J., Osborne J. P., Martyn C., Harris T., Bolton P. F., Learning disability and epilepsy in an epidemiological sample of individuals with tuberous sclerosis complex Psychological Medicine 2003 33 2 335 344 (Pubitemid 36221465)
7. Prather P., De Vries P. J., Behavioral and cognitive aspects of tuberous sclerosis complex Journal of Child Neurology 2004 19 9 666 674 (Pubitemid 39530075)
8. De Vries P., Humphrey A., McCartney D., Prather P., Bolton P., Hunt A., Assel M., Chugani D., Creighton L., Elias C., Franz D., Hubbeling A., King B., Mastbaum C., Medcalf J., MulDer J., Ridler K., Rothberg B., Santosh P., Whittemore V., Consensus clinical guidelines for the assessment of cognitive and behavioural problems in Tuberous Sclerosis European Child and Adolescent Psychiatry 2005 14 4 183 190
9. Winterkorn E. B., Pulsifer M. B., Thiele E. A., Cognitive prognosis of patients with tuberous sclerosis complex Neurology 2007 68 1 62 64 (Pubitemid 46058555)
10. Manning B. D., Cantley L. C., Rheb fills a GAP between TSC and TOR Trends in Biochemical Sciences 2003 28 11 573 576 (Pubitemid 38352801)
11. Tee A. R., Manning B. D., Roux P. P., Cantley L. C., Blenis J., Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb Current Biology 2003 13 15 1259 1268 (Pubitemid 36953298)
12. Jozwiak J., Hamartin and tuberin: working together for tumour suppression International Journal of Cancer 2006 118 1 1 5 (Pubitemid 41681573)
13. Tavazoie S. F., Alvarez V. A., RiDenour D. A., Kwiatkowski D. J., Sabatini B. L., Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2 Nature Neuroscience 2005 8 12 1727 1734 (Pubitemid 41683201)
14. Jaworski J., Sheng M., The growing role of mTOR in neuronal Development and plasticity Molecular Neurobiology 2006 34 3 205 219
15. De Vries P. J., Howe C. J., The tuberous sclerosis complex proteins-a GRIPP on cognition and neuroDevelopment Trends in Molecular Medicine 2007 13 8 319 326 (Pubitemid 47126986)
16. Richter J. D., Klann E., Making synaptic plasticity and memory last: mechanisms of translational regulation Genes and Development 2009 23 1 1 11
17. Bliss T. V. P., Lomo T., Long lasting potentiation of synaptic transmission in the Dentate area of the anaesthetized rabbit following stimulation of the perforant path Journal of Physiology 1973 232 2 331 356
18. Bliss T. V. P., Collingridge G. L., A synaptic model of memory: long-term potentiation in the hippocampus Nature 1993 361 6407 31 39 (Pubitemid 23020772)
19. Kandel E. R., The molecular biology of memory storage: a dialogue between genes and synapses Science 2001 294 5544 1030 1038 (Pubitemid 33041851)
20. Collingridge G. L., Peineau S., Howland J. G., Wang Y. T., Long-term depression in the CNS Nature Reviews Neuroscience 2010 11 7 459 473
21. Palmer M. J., Irving A. J., Seabrook G. R., Jane D. E., Collingridge G. L., The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus Neuropharmacology 1997 36 11-12 1517 1532 (Pubitemid 28085911)
22. Oliet S. H. R., Malenka R. C., Nicoll R. A., Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells Neuron 1997 18 6 969 982 (Pubitemid 27274615)
23. Huber K. M., Kayser M. S., Bear M. F., Role for rapid Dendritic protein synthesis in hippocampal mGluR- depenDent long-term depression Science 2000 288 5469 1254 1256 (Pubitemid 30367205)
24. Huber K. M., RoDer J. C., Bear M. F., Chemical induction of mGluR5- and protein synthesis-depenDent long-term depression in hippocampal area CA1 Journal of Neurophysiology 2001 86 1 321 325 (Pubitemid 32623237)
25. SnyDer E. M., Philpot B. D., Huber K. M., Dong X., Fallon J. R., Bear M. F., Internalization of ionotropic glutamate receptors in response to mGluR activation Nature Neuroscience 2001 4 11 1079 1085 (Pubitemid 34116552)
26. Waltereit R., Welzl H., Dichgans J., Lipp H. P., Schmidt W. J., Weller M., Enhanced episodic-like memory and kindling epilepsy in a rat model of tuberous sclerosis Journal of Neurochemistry 2006 96 2 407 413
27. Von Der Brelie C., Waltereit R., Zhang L., Beck H., Kirschstein T., Impaired synaptic plasticity in a rat model of tuberous sclerosis European Journal of Neuroscience 2006 23 3 686 692
28. Waltereit R., Japs B., SchneiDer M., De Vries P. J., Bartsch D., Epilepsy and Tsc2 haploinsufficiency lead to autistic-like social deficit behaviors in rats Behavior Genetics 2011 41 3 364 372
29. Ehninger D., Han S., Shilyansky C., Zhou Y., Li W., Kwiatkowski D. J., Ramesh V., Silva A. J., Reversal of learning Deficits in a Tsc2 +/- mouse model of tuberous sclerosis Nature Medicine 2008 14 8 843 848
30. Auerbach B. D., Osterweil E. K., Bear M. F., Mutations causing syndromic autism define an axis of synaptic pathophysiology Nature 2011 480 7375 63 68
31. Chévere-Torres I., Kaphzan H., Bhattacharya A., Kang A., Maki J. M., Gambello M. J., Arbiser J. L., Santini E., Klann E., Metabotropic glutamate receptor-depenDent long-term depression is impaired due to elevated ERK signaling in the RG mouse model of tuberous sclerosis complex Neurobiology of Disease 2012 45 3 1101 1110
32. Ehninger D., Silva A. J., Increased levels of anxiety-related behaviors in a Tsc2 dominant negative transgenic mouse model of tuberous sclerosis Behavior Genetics 2011 41 3 357 363
33. Chévere-Torres I., Maki J. M., Santini E., Klann E., Impaired social interactions and motor learning skills in tuberous sclerosis complex model mice expressing a dominant/negative form of tuberin Neurobiology of Disease 2012 45 1 156 164
34. Zeng L. H., Ouyang Y., Gazit V., Cirrito J. R., Jansen L. A., Ess K. C., Yamada K. A., Wozniak D. F., Holtzman D. M., Gutmann D. H., Wong M., Abnormal glutamate homeostasis and impaired synaptic plasticity and learning in a mouse model of tuberous sclerosis complex Neurobiology of Disease 2007 28 2 184 196 (Pubitemid 47615457)
35. Bateup H. S., Takasaki K. T., Saulnier J. L., Denefrio C. L., Sabatini B. L., Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excitatory synaptic function Journal of Neuroscience 2011 31 24 8862 8869
36. GoorDen S. M. I., Van WoerDen G. M., Van Der Weerd L., Cheadle J. P., Elgersma Y., Cognitive Deficits in Tsc1 +/- mice in the absence of cerebral lesions and seizures Annals of Neurology 2007 62 6 648 655
37. Eker R., Mossige J., Vincents Johannessen J., Aars H., Hereditary renal aDenomas and aDenocarcinomas in rats Diagnostic Histopathology 1981 4 1 99 110 (Pubitemid 11191589)
38. Yeung R. S., Katsetos C. D., Klein-Szanto A., Subependymal astrocytic hamartomas in the Eker rat model of tuberous sclerosis American Journal of Pathology 1997 151 5 1477 1486 (Pubitemid 27479778)
39. Mizuguchi M., Takashima S., Yamanouchi H., Nakazato Y., Mitani H., Hino O., Novel cerebral lesions in the Eker rat model of tuberous sclerosis: cortical tuber and anaplastic ganglioglioma Journal of Neuropathology and Experimental Neurology 2000 59 3 188 196 (Pubitemid 30143877)
40. Takahashi D. K., Dinday M. T., Barbaro N. M., Baraban S. C., Abnormal cortical cells and astrocytomas in the Eker rat model of tuberous sclerosis complex Epilepsia 2004 45 12 1525 1530 (Pubitemid 39648277)
41. Wenzel H. J., Patel L. S., Robbins C. A., Emmi A., Yeung R. S., Schwartzkroin P. A., Morphology of cerebral lesions in the Eker rat model of tuberous sclerosis Acta Neuropathologica 2004 108 2 97 108 (Pubitemid 39136294)
42. Chan J. A., Zhang H., Roberts P. S., Jozwiak S., Wieslawa G., Lewin-Kowalik J., Kotulska K., Kwiatkowski D. J., Pathogenesis of tuberous sclerosis subependymal giant cell astrocytomas: biallelic inactivation of Tsc1 or Tsc2 leads to mTOR activation Journal of Neuropathology and Experimental Neurology 2004 63 12 1236 1242 (Pubitemid 39603395)
43. Crino P. B., Molecular pathogenesis of tuber formation in tuberous sclerosis complex Journal of Child Neurology 2004 19 9 716 725 (Pubitemid 39530082)
44. Stoica L., Zhu P. J., Huang W., Zhou H., Kozma S. C., Costa-Mattioli M., Selective pharmacogenetic inhibition of mammalian target of Rapamycin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage Proceedings of the National Academy of Sciences of the United States of America 2011 108 9 3791 3796
45. Way S. W., Mckenna J. III, Mietzsch U., Reith R. M., Wu H. C. J., Gambello M. J., Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse Human Molecular Genetics 2009 18 7 1252 1265
46. Tang S. J., Reis G., Kang H., Gingras A. C., Sonenberg N., Schuman E. M., A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus Proceedings of the National Academy of Sciences of the United States of America 2002 99 1 467 472 (Pubitemid 34060384)
47. Frey U., Krug M., Reymann K. G., Matthies H., Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro Brain Research 1988 452 1-2 57 65
48. Huang Y. Y., Kandel E. R., Recruitment of long-lasting and protein kinase A-depenDent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization Learning Memory 1994 1 1 74 82 (Pubitemid 2113963)
49. Lee H. K., Barbarosie M., Kameyama K., Bear M. F., Huganir R. L., Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity Nature 2000 405 6789 955 959 (Pubitemid 30435052)
50. Lisman J., Schulman H., Cline H., The molecular basis of CaMKII function in synaptic and behavioural memory Nature Reviews Neuroscience 2002 3 3 175 190 (Pubitemid 135706588)
51. Uhlmann E. J., Wong M., Baldwin R. L., Bajenaru M. L., Onda H., Kwiatkowski D. J., Yamada K., Gutmann D. H., Astrocyte-specific Tsc1 conditional knockout mice exhibit abnormal neuronal organization and seizures Annals of Neurology 2002 52 3 285 296 (Pubitemid 35001494)
52. Ess K. C., Uhlmann E. J., Li W., Li H., Declue J. E., Crino P. B., Gutmann D. H., Expression profiling in tuberous sclerosis complex (TSC) knockout mouse astrocytes to characterize human TSC brain pathology Glia 2004 46 1 28 40 (Pubitemid 38461721)
53. Kurtz A., Zimmer A., Schnutgen F., Bruning G., Spener F., Muller T., The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell Development Development 1994 120 9 2637 2649 (Pubitemid 24268837)
54. Hartfuss E., Galli R., Heins N., Gtz M., Characterization of CNS precursor subtypes and radial glia Developmental Biology 2001 229 1 15 30 (Pubitemid 32061711)
55. Meikle L., Talos D. M., Onda H., Pollizzi K., Rotenberg A., Sahin M., Jensen F. E., Kwiatkowski D. J., A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival Journal of Neuroscience 2007 27 21 5546 5558 (Pubitemid 350021088)
56. Ronesi J. A., Huber K. M., Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation Journal of Neuroscience 2008 28 2 543 547
57. Waung M. W., Pfeiffer B. E., Nosyreva E. D., Ronesi J. A., Huber K. M., Rapid Translation of Arc/Arg3.1 Selectively Mediates mGluR-depenDent LTD through Persistent Increases in AMPAR Endocytosis Rate Neuron 2008 59 1 84 97 (Pubitemid 351905854)
58. Hou L., Klann E., Activation of the phosphoinositide 3-kinase-Akt- mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-depenDent long-term depression Journal of Neuroscience 2004 24 28 6352 6361 (Pubitemid 38944226)
59. Banko J. L., Hou L., Klann E., NMDA receptor activation results in PKA- and ERK-depenDent Mnk1 activation and increased eIF4E phosphorylation in hippocampal area CA1 Journal of Neurochemistry 2004 91 2 462 470 (Pubitemid 39363445)
60. Gallagher S. M., Daly C. A., Bear M. F., Huber K. M., Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-depenDent long-term depression in hippocampal area CA1 Journal of Neuroscience 2004 24 20 4859 4864 (Pubitemid 38668210)
61. Kwiatkowski D. J., Zhang H., Bandura J. L., Heiberger K. M., Glogauer M., el-Hashemite N., Onda H., A mouse model of Tsc1 reveals sex-depenDent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells Human Molecular Genetics 2002 11 5 525 534 (Pubitemid 34257489)
62. Kelleher R. J. III, Bear M. F., The autistic neuron: troubled translation? Cell 2008 135 3 401 406
63. Govindarajan B., Brat D. J., Csete M., Martin W. D., Murad E., Litani K., Cohen C., Cerimele F., Nunnelley M., Lefkove B., Yamamoto T., Lee C., Arbiser J. L., Transgenic expression of dominant negative tuberin through a strong constitutive promoter results in a tissue-specific tuberous sclerosis phenotype in the skin and brain Journal of Biological Chemistry 2005 280 7 5870 5874 (Pubitemid 40280069)
64. Pasumarthi K. B. S., Nakajima H., Nakajima H. O., Jing S., Field L. J., Enhanced cardiomyocyte DNA synthesis during myocardial hypertrophy in mice expressing a modified Tsc2 transgene Circulation Research 2000 86 10 1069 1077 (Pubitemid 30367866)
65. Steele R. J., Morris R. G. M., delay-depenDent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5 Hippocampus 1999 9 2 118 136 (Pubitemid 29196956)
66. Reid I. C., Stewart C. A., Seizures, memory and synaptic plasticity Seizure 1997 6 5 351 359 (Pubitemid 27483439)
67. Beck H., Goussakov I. V., Lie A., Helmstaedter C., Elger C. E., Synaptic plasticity in the human Dentate gyrus Journal of Neuroscience 2000 20 18 7080 7086
68. Kirschstein T., Bauer M., Mller L., Rschenschmidt C., Reitze M., Becker A. J., Schoch S., Beck H., Loss of metabotropic glutamate receptor-depenDent long-term depression via downregulation of mGluR5 after status epilepticus Journal of Neuroscience 2007 27 29 7696 7704 (Pubitemid 47093822)
69. Sgobio C., Ghiglieri V., Costa C., Bagetta V., Siliquini S., Barone I., Di Filippo M., Gardoni F., Gundelfinger E. D., Di Luca M., Picconi B., Calabresi P., Hippocampal synaptic plasticity, memory, and epilepsy: effects of long-term valproic acid treatment Biological Psychiatry 2010 67 6 567 574
70. Wong M., Ess K. C., Uhlmann E. J., Jansen L. A., Li W., Crino P. B., Mennerick S., Yamada K. A., Gutmann D. H., Impaired glial glutamate transport in a mouse tuberous sclerosis epilepsy model Annals of Neurology 2003 54 2 251 256 (Pubitemid 36909626)
71. Ménard C., Quirion R., Successful cognitive aging in rats: a role for mGluR5 glutamate receptors, homer 1 proteins and downstream signaling pathways PLoS ONE 2012 7 1
72. Radwanska K., Medvedev N. I., Pereira G. S., Engmann O., Thiede N., Moraes M. F. D., Villers A., Irvine E. E., Maunganidze N. S., Pyza E. M., Ris L., Szymaska M., Lipiski M., Kaczmarek L., Stewart M. G., Giese K. P., Mechanism for long-term memory formation when synaptic strengthening is impaired Proceedings of the National Academy of Sciences of the United States of America 2011 108 45 18471 18475