Region-specific deletions of RIM1 reproduce a subset of global RIM1α -/- phenotypes

Genes, Brain and Behavior

Volumn 11, Issue 2, 2012, Pages 201-213

  Haws, M E ^a,b   Kaeser, P S ^c   Jarvis, D L ^a   Sudhof T C ^c   Powell, C M ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

CA3; Cerebellum; Cre recombinase; Dentate gyrus; Kainate; Locomotor; MK 801; Preproopiomelanocortin; RIM1; Schizophrenia

Indexed keywords

CRE RECOMBINASE; DIZOCILPINE; KAINIC ACID RECEPTOR; MEMBRANE PROTEIN; PREPROOPIOMELANOCORTIN; PROOPIOMELANOCORTIN; PROTEIN RIM1; PROTEIN RIM1ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GENE DELETION; HIPPOCAMPAL CA3 REGION; HYPERACTIVITY; KNOCKOUT MOUSE; LOCOMOTION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PREPULSE INHIBITION; PRIORITY JOURNAL; PROMOTER REGION; PYRAMIDAL NERVE CELL; STARTLE REFLEX;

ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; BRAIN; CONDITIONING (PSYCHOLOGY); DIZOCILPINE MALEATE; GTP-BINDING PROTEINS; MAZE LEARNING; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; PHENOTYPE; PROMOTER REGIONS, GENETIC; ROTAROD PERFORMANCE TEST; SENSORY GATING; SOCIAL BEHAVIOR; STARTLE REACTION; SYNAPSES;

MUS;

EID: 84856362852     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2011.00755.x     Document Type: Article

References (46)

1. Akbarian, S. & Huang, H.S. (2006) Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev 52, 293-304.
2. Balthasar, N., Coppari, R., Mcminn, J., Liu, S.M., Lee, C.E., Tang, V., Kenny, C.D., Mcgovern, R.A., Chua, S.C., Jr., Elmquist, J.K. & Lowell, B.B. (2004) Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron 42, 983-991.
3. Banno, R., Zimmer, D., De Jonghe, B.C., Atienza, M., Rak, K., Yang, W. & Bence, K.K. (2010) PTP1B and SHP2 in POMC neurons reciprocally regulate energy balance in mice. J Clin Invest 120, 720-734.
4. Beasley, C.L. & Reynolds, G.P. (1997) Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 24, 349-355.
5. Benes, F.M. & Berretta, S. (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25, 1-27.
6. Blundell, J., Blaiss, C. A., Etherton, M.R., Espinosa, F., Tabuchi, K., Walz, C., Bolliger, M.F., Sudhof, T.C. & Powell, C.M. (2010a) Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J Neurosci 30, 2115-2129.
7. Blundell, J., Kaeser, P.S., Sudhof, T.C. & Powell, C.M. (2010b) RIM1α and interacting proteins involved in presynaptic plasticity mediate prepulse inhibition and additional behaviors linked to schizophrenia. J Neurosci 30, 5326-5333.
8. Calakos, N., Schoch, S., Sudhof, T.C. & Malenka, R.C. (2004) Multiple roles for the active zone protein RIM1[α] in late stages of neurotransmitter release. Neuron 42, 889-896.
9. Castillo, P.E., Schoch, S., Schmitz, F., Sudhof, T.C. & Malenka, R.C. (2002) RIM1α is required for presynaptic long-term potentiation. Nature 415, 327-330.
10. Chevaleyre, V., Heifets, B.D., Kaeser, P.S., Sudhof, T.C. & Castillo, P.E. (2007) Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α. Neuron 54, 801-812.
11. Cochran, S.M., Fujimura, M., Morris, B.J. & Pratt, J.A. (2002) Acute and delayed effects of phencyclidine upon mRNA levels of markers of glutamatergic and GABAergic neurotransmitter function in the rat brain. Synapse 46, 206-214.
12. Dymecki, S.M. (1996) Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc Natl Acad Sci U S A 93, 6191-6196.
13. Eastwood, S.L., Cotter, D. & Harrison, P.J. (2001) Cerebellar synaptic protein expression in schizophrenia. Neuroscience 105, 219-229.
14. Etherton, M.R., Blaiss, C.A., Powell, C.M. & Sudhof, T.C. (2009) Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc Natl Acad Sci U S A 106, 17998-18003.
15. Feng, J., Schroer, R., Yan, J., Song, W., Yang, C., Bockholt, A., Cook, E.H., Jr., Skinner, C., Schwartz, C.E., & Sommer, S.S. (2006) High frequency of neurexin 1beta signal peptide structural variants in patients with autism. Neurosci Lett 409, 10-13.
16. Fukushima, F., Nakao, K., Shinoe, T., Fukaya, M., Muramatsu, S., Sakimura, K., Kataoka, H., Mori, H., Watanabe, M., Manabe, T. & Mishina, M. (2009) Ablation of NMDA receptors enhances the excitability of hippocampal CA3 neurons. PLoS One 4, e3993.
17. Glantz, L.A. & Lewis, D.A. (1997) Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia. Regional and diagnostic specificity. Arch Gen Psychiatry 54, 660-669.
18. Guidotti, A., Auta, J., Davis, J.M., Di-Giorgi-Gerevini, V., Dwivedi, Y., Grayson, D.R., Impagnatiello, F., Pandey, G., Pesold, C., Sharma, R., Uzunov, D. & Costa, E. (2000) Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57, 1061-1069.
19. Hashimoto, T., Volk, D.W., Eggan, S.M., Mirnics, K., Pierri, J.N., Sun, Z., Sampson, A.R. & Lewis, D.A. (2003) Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23, 6315-6326.
20. Kaeser, P.S., Kwon, H.B., Chiu, C.Q., Deng, L., Castillo, P.E. & Sudhof, T.C. (2008) RIM1α and RIM1β are synthesized from distinct promoters of the RIM1 gene to mediate differential but overlapping synaptic functions. J Neurosci 28, 13435-13447.
21. Kim, H.G., Kishikawa, S., Higgins, A.W. et al. (2008) Disruption of neurexin 1 associated with autism spectrum disorder. Am J Hum Genet 82, 199-207.
22. Kinney, J.W., Davis, C.N., Tabarean, I., Conti, B., Bartfai, T. & Behrens, M.M. (2006) A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J Neurosci 26, 1604-1615.
23. Lagace, D.C., Whitman, M.C., Noonan, M.A., Ables, J.L., Decarolis, N.A., Arguello, A.A., Donovan, M.H., Fischer, S.J., Farnbauch, L.A., Beech, R.D., Dileone, R.J., Greer, C.A., Mandyam, C.D. & Eisch, A.J. (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci 27, 12623-12629.
24. Lewis, D.A., Hashimoto, T. & Volk, D.W. (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6, 312-324.
25. Li, Q., Clark, S., Lewis, D.V. & Wilson, W.A. (2002) NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity. J Neurosci 22, 3070-80.
26. McHugh, T., Jones, M.W., Quinn, J.J., Balthasar, N., Coppari, R., Elmquist, J.K., Lowell, B.B., Fanselow, M.S., Wilson, M.A. & Tonegawa, S. (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99.
27. Mukaetova-Ladinska, E.B., Hurt, J., Honer, W.G., Harrington, C.R. & Wischik, C.M. (2002) Loss of synaptic but not cytoskeletal proteins in the cerebellum of chronic schizophrenics. Neurosci Lett 317, 161-165.
28. Nakazawa, K., Quirk, M.C., Chitwood, R.A., Watanabe, M., Yeckel, M.F., Sun, L.D., Kato, A., Carr, C.A., Johnston, D., Wilson, M.A. & Tonegawa, S. (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211-218.
29. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
30. Powell, C.M., Schoch, S., Monteggia, L., Barrot, M., Matos, M.F., Feldmann, N., Sudhof, T.C. & Nestler, E.J. (2004) The presynaptic active zone protein RIM1α is critical for normal learning and memory. Neuron 42, 143-153.
31. Ramadori, G., Fujikawa, T., Fukuda, M., Anderson, J., Morgan, D.A., Mostoslavsky, R., Stuart, R.C., Perello, M., Vianna, C.R., Nillni, E.A., Rahmouni, K. & Coppari, R. (2010) SIRT1 deacetylase in POMC neurons is required for homeostatic defenses against diet-induced obesity. Cell Metab 12, 78-87.
32. Sawada, K., Barr, A.M., Nakamura, M., Arima, K., Young, C.E., Dwork, A.J., Falkai, P., Phillips, A.G. & Honer, W.G. (2005) Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch Gen Psychiatry 62, 263-272.
33. Schoch, S., Castillo, P.E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R.C. & Sudhof, T.C. (2002) RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415, 321-326.
34. Schoch, S., Mittelstaedt, T., Kaeser, P.S., Padgett, D., Feldmann, N., Chevaleyre, V., Castillo, P.E., Hammer, R.E., Han, W., Schmitz, F., Lin, W. & Sudhof, T.C. (2006) Redundant functions of RIM1α and RIM2alpha in Ca(2+)-triggered neurotransmitter release. Embo J 25, 5852-5863.
35. Singec, I., Knoth, R., Ditter, M., Frotscher, M. & Volk, B. (2003) Neurogranin expression by cerebellar neurons in rodents and non-human primates. J Comp Neurol 459, 278-289.
36. Smith, L. (2011) Good planning and serendipity: exploiting the Cre/Lox system in the testis. Reproduction 141, 151-161.
37. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21, 70-71.
38. Sundberg, R., Castensson, A. & Jazin, E. (2006) Statistical modeling in case-control real-time RT-PCR assays, for identification of differentially expressed genes in schizophrenia. Biostatistics 7, 130-144.
39. Tamminga, C., Hashimoto, T., Volk, D.W. & Lewis, D.A. (2004) GABA neurons in the human prefrontal cortex. Am J Psychiatry 161, 1764.
40. Tonegawa, S., Nakazawa, K. & Wilson, M.A. (2003) Genetic neuroscience of mammalian learning and memory. Philos Trans R Soc Lond B Biol Sci 358, 787-795.
41. Woo, T.U., Walsh, J.P. & Benes, F.M. (2004) Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch Gen Psychiatry 61, 649-657.
42. Xi, D., Zhang, W., Wang, H.X., Stradtman, G.G. & Gao, W.J. (2009) Dizocilpine (MK-801) induces distinct changes of N-methyl-D-aspartic acid receptor subunits in parvalbumin-containing interneurons in young adult rat prefrontal cortex. Int J Neuropsychopharmacol 12, 1395-1408.
43. Xu, Y., Jones, J.E., Kohno, D., Williams, K.W., Lee, C.E., Choi, M.J., Anderson, J.G., Heisler, L.K., Zigman, J.M., Lowell, B.B. & Elmquist, J.K. (2008) 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 60, 582-589.
44. Yang, Y. & Calakos, N. (2010) Acute in vivo genetic rescue demonstrates that phosphorylation of RIM1α serine 413 is not required for mossy fiber long-term potentiation. J Neurosci 30, 2542-2546.
45. Yu, M.C., Cho, E., Luo, C.B., Li, W.W., Shen, W.Z. & Yew, D.T. (1996) Immunohistochemical studies of GABA and parvalbumin in the developing human cerebellum. Neuroscience 70, 267-276.
46. Zhang, C., Wu, B., Beglopoulos, V., Wines-Samuelson, M., Zhang, D., Dragatsis, I., Sudhof, T.C. & Shen, J. (2009) Presenilins are essential for regulating neurotransmitter release. Nature 460, 632-636.