Reelin supplementation recovers synaptic plasticity and cognitive deficits in a mouse model for Angelman syndrome

European Journal of Neuroscience

Volumn 41, Issue 10, 2015, Pages 1372-1380

  Hethorn, Whitney R ^a,b   Ciarlone, Stephanie L ^a,b   Filonova, Irina ^a,b   Rogers, Justin T ^a,b   Aguirre, Daniela ^b   Ramirez, Raquel A ^a,b   Grieco, Joseph C ^a,b   Peters, Melinda M ^a,b   Gulick, Danielle ^a,b   Anderson, Anne E ^c   L Banko, Jessica ^a,b   Lussier, April L ^a,b   Weeber, Edwin J ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Behavior; Cannulation; Hippocampus; Ubiquitin ligase; Ventricle

Indexed keywords

REELIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN ELECTROPHYSIOLOGY; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; ELEVATED PLUS MAZE TEST; FEMALE; HAPPY PUPPET SYNDROME; HUMAN; HUMAN CELL; HUMAN TISSUE; LONG TERM POTENTIATION; MALE; MOLECULAR MECHANICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; ROTAROD TEST; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; SPATIAL MEMORY TEST; TREATMENT RESPONSE; ANGELMAN SYNDROME; ANIMAL; BRAIN CORTEX; DISEASE MODEL; DRUG EFFECTS; HEK293 CELL LINE; HIPPOCAMPUS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PSYCHOLOGY; ULTRASTRUCTURE;

ANGELMAN SYNDROME; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; INJECTIONS, INTRAVENTRICULAR; LONG-TERM POTENTIATION; MALE; MICE; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; SERINE ENDOPEPTIDASES; SPATIAL LEARNING; SPATIAL MEMORY;

EID: 84929510668     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12893     Document Type: Article

References (42)

1. Alcantara, S., Ruiz, M., D'Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C. & Soriano, E. (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci., 18, 7779-7799.
2. Arnaud, L., Ballif, B.A., Förster, E. & Cooper, J.A. (2003) Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr. Biol., 13, 9-17.
3. Chen, Y., Beffert, U., Ertunc, M., Tang, T.-S.S., Kavalali, E.T., Bezprozvanny, I. & Herz, J. (2005) Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci., 25, 8209-8216.
4. Chen, Z.Y., Jing, D., Bath, K.G., Ieraci, A., Khan, T., Siao, C.J., Herrera, D.G., Toth, M., Yang, C., McEwen, B.S., Hempstead, B.L. & Lee, F.S. (2006) Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science, 314, 140-143.
5. Daily, J.L., Nash, K., Jinwal, U., Golde, T., Rogers, J., Peters, M.M., Burdine, R.D., Dickey, C., Banko, J.L. & Weeber, E.J. (2011) Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome. PLoS One, 6, e27221.
6. D'Arcangelo, G. (2006) Reelin mouse mutants as models of cortical development disorders. Epilepsy Behav., 8, 81-90.
7. Dindot, S.V., Antalffy, B.A., Bhattacharjee, M.B. & Beaudet, A.L. (2008) The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum. Mol. Genet., 17, 111-118.
8. Filonova, I., Trotter, J.H., Banko, J.L. & Weeber, E.J. (2014) Activity-dependent changes in MAPK activation in the Angelman Syndrome mouse model. Learn. Memory, 21, 98-104.
9. Ghosh, A. & Greenberg, M.E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science, 268, 239-247.
10. Goffinet, A.M. (1982) The embryonic development of the cerebellum in normal and reeler mutant mice. Anat. Embryol., 168, 73-86.
11. Greer, P.L., Hanayama, R., Bloodgood, B.L., Mardinly, A.R., Lipton, D.M., Flavell, S.W., Kim, T.K., Griffith, E.C., Waldon, Z., Maehr, R., Ploegh, H.L., Chowdhury, S., Worley, P.F., Steen, J. & Greenberg, M.E. (2010) The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell, 140, 704-716.
12. Gustin, R.M., Bichell, T.J., Bubser, M., Daily, J., Filonova, I., Mrelashvili, D., Deutch, A.Y., Colbran, R.J., Weeber, E.J. & Haas, K.F. (2010) Tissue-specific variation of Ube3a protein expression in rodents and in a mouse model of Angelman syndrome. Neurobiol. Dis., 39, 283-291.
13. Hack, I., Bancila, M., Loulier, K., Carroll, P. & Cremer, H. (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci., 5, 939-945.
14. Heinrich, C., Nitta, N., Flubacher, A., Muller, M., Fahrner, A., Kirsch, M., Freiman, T., Suzuki, F., Depaulis, A., Frotscher, M. & Haas, C.A. (2006) Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci., 26, 4701-4713.
15. Howell, B.W., Gertler, F.B. & Cooper, J.A. (1997) Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J., 16, 121-132.
16. Jiang, Y.H., Armstrong, D., Albrecht, U., Atkins, C.M., Noebels, J.L., Eichele, G., Sweatt, J.D. & Beaudet, A.L. (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron, 21, 799-811.
17. Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., de Rouvroit, C.L. & Goffinet, A.M. (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci., 24, 514-521.
18. Jossin, Y., Gui, L. & Goffinet, A.M. (2007) Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J. Neurosci., 27, 4243-4252.
19. Kaphzan, H., Hernandez, P., Jung, J.I., Cowansage, K.K., Deinhardt, K., Chao, M.V., Abel, T. & Klann, E. (2012) Reversal of impaired hippocampal long-term potentiation and contextual fear memory deficits in Angelman syndrome model mice by ErbB inhibitors. Biol. Psychiat., 72, 182-190.
20. Koie, M., Okumura, K., Hisanaga, A., Kamei, T., Sasaki, K., Deng, M., Baba, A., Kohno, T. & Hattori, M. (2014) Cleavage within Reelin repeat 3 regulates the duration and range of the signaling activity of Reelin protein. J. Biol. Chem., 289, 12922-12930.
21. Krstic, D., Rodriguez, M. & Knuesel, I. (2012) Regulated proteolytic processing of Reelin through interplay of tissue plasminogen activator (tPA), ADAMTS-4, ADAMTS-5, and their modulators. PLoS One, 7, e47793.
22. Levenson, J.M., Roth, T.L., Lubin, F.D., Miller, C.A., Huang, I.-C., Desai, P., Malone, L.M. & Sweatt, J.D. (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J. Biol. Chem., 281, 15763-15773.
23. Miao, S., Chen, R., Ye, J., Tan, G.-H., Li, S., Zhang, J., Jiang, Y.-H. & Xiong, Z.-Q. (2013) The Angelman syndrome protein Ube3a is required for polarized dendrite morphogenesis in pyramidal neurons. J. Neurosci., 33, 327-333.
24. Nakajima, K., Mikoshiba, K., Miyata, T., Kudo, C. & Ogawa, M. (1997) Disruption of hippocampal development in vivo by CR-50 mAb against reelin. Proc. Natl. Acad. Sci. USA, 94, 8196-8201.
25. Nawaz, Z., Lonard, D.M., Smith, C.L., Lev-Lehman, E., Tsai, S.Y., Tsai, M.-J. & O'Malley, B.W. (1999) The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol. Cell. Biol., 19, 1182-1189.
26. Niu, S., Renfro, A., Quattrocchi, C.C., Sheldon, M. & D'Arcangelo, G. (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron, 41, 71-84.
27. Pesold, C., Impagnatiello, F., Pisu, M.G., Uzunov, D.P., Costa, E., Guidotti, A. & Caruncho, H.J. (1998) Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. USA, 95, 3221-3226.
28. Qiu, S., Zhao, L.F., Korwek, K.M. & Weeber, E.J. (2006) Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. J. Neurosci., 26, 12943-12955.
29. Rogers, J.T. & Weeber, E.J. (2008) Reelin and apoE actions on signal transduction, synaptic function and memory formation. Neuron Glia Biol., 4, 259-270.
30. Rogers, J.T., Rusiana, I., Trotter, J., Zhao, L., Donaldson, E., Pak, D.T., Babus, L.W., Peters, M., Banko, J.L., Chavis, P., Rebeck, G.W., Hoe, H.-S.S. & Weeber, E.J. (2011) Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density. Learn. Memory, 18, 558-564.
31. Rogers, J.T., Zhao, L., Trotter, J.H., Rusiana, I., Peters, M.M., Li, Q., Donaldson, E., Banko, J.L., Keenoy, K.E., Rebeck, G.W., Hoe, H.S., D'Arcangelo, G. & Weeber, E.J. (2013) Reelin supplementation recovers sensorimotor gating, synaptic plasticity and associative learning deficits in the heterozygous reeler mouse. J. Psychopharmacol., 27, 389-395.
32. de Rouvroit, C.L., de Bergeyck, V., Cortvrindt, C., Bar, I., Eeckhout, Y. & Goffinet, A.M. (1999) Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp. Neurol., 156, 214-217.
33. Sinagra, M., Verrier, D., Frankova, D., Korwek, K.M., Blahos, J., Weeber, E.J., Manzoni, O.J. & Chavis, P. (2005) Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro. J. Neurosci., 25, 6127-6136.
34. Steffenburg, S., Gillberg, C.L., Steffenburg, U. & Kyllerman, M. (1996) Autism in Angelman syndrome: a population-based study. Pediatr. Neurol., 14, 131-136.
35. Trotter, J., Lee, G.H., Kazdoba, T.M., Crowell, B., Domogauer, J., Mahoney, H.M., Franco, S.J., Müller, U., Weeber, E.J. & D'Arcangelo, G. (2013) Dab1 is required for synaptic plasticity and associative learning. J. Neurosci., 33, 15652-15668.
36. Trotter, J.H., Lussier, A.L., Psilos, K.E., Mahoney, H.L., Sponaugle, A.E., Hoe, H.S., Rebeck, G.W. & Weeber, E.J. (2014) Extracellular proteolysis of reelin by tissue plasminogen activator following synaptic potentiation. Neuroscience, 274, 299-307.
37. Utsunomiya-Tate, N., Kubo, K.-I., Tate, S.-I., Kainosho, M., Katayama, E., Nakajima, K. & Mikoshiba, K. (2000) Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proc. Natl. Acad. Sci. USA, 97, 9729-9734.
38. Weeber, E.J., Beffert, U., Jones, C., Christian, J.M., Forster, E., Sweatt, J.D. & Herz, J. (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem., 277, 39944-39952.
39. Weeber, E.J., Jiang, Y.H., Elgersma, Y., Varga, A.W., Carrasquillo, Y., Brown, S.E., Christian, J.M., Mirnikjoo, B., Silva, A., Beaudet, A.L. & Sweatt, J.D. (2003) Derangements of hippocampal calcium/calmodulin-dependent protein kinase II in a mouse model for Angelman mental retardation syndrome. J. Neurosci., 23, 2634-2644.
40. Williams, C.A., Beaudet, A.L., Clayton-Smith, J., Knoll, J.H., Kyllerman, M., Laan, L.A., Magenis, R.E., Moncla, A., Schinzel, A.A., Summers, J.A. & Wagstaff, J. (2006) Angelman syndrome 2005: updated consensus for diagnostic criteria. Am. J. Med. Genet. A., 140, 413-418.
41. van Woerden, G.M., Harris, K.D., Hojjati, M.R., Gustin, R.M., Qiu, S., de Avila Freire, R., Jiang, Y.H., Elgersma, Y. & Weeber, E.J. (2007) Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alphaCaMKII inhibitory phosphorylation. Nat. Neurosci., 10, 280-282.
42. Won, S.J., Kim, S.H., Xie, L., Wang, Y., Mao, X.O., Jin, K. & Greenberg, D.A. (2006) Reelin-deficient mice show impaired neurogenesis and increased stroke size. Exp. Neurol., 198, 250-259.