Complex, multimodal behavioral profile of the Homer1 knockout mouse

Genes, Brain and Behavior

Volumn 6, Issue 2, 2007, Pages 141-154

  Jaubert, P J ^a   Golub, M S ^a   Lo, Y Y ^a   Germann, S L ^a   Dehoff, M H ^c   Worley, P F ^c   Kang, S H ^c   Schwarz, M K ^b   Seeburg, P H ^b   Berman, R F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Behavior; Homer1; Knockout; Learning; Social interaction

Indexed keywords

GLUTAMATE RECEPTOR 5; HOMER1 PROTEIN; N METHYL DEXTRO ASPARTIC ACID; PROTEIN; UNCLASSIFIED DRUG;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BEHAVIORAL SCIENCE; BRAIN DEVELOPMENT; COMPARATIVE STUDY; CONTROLLED STUDY; EMOTION; GENE; GROWTH RETARDATION; HOMER1 GENE; KNOCKOUT MOUSE; LEARNING; LEARNING DISORDER; MALE; MEMORY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSORY DYSFUNCTION; SENSORY EVALUATION; SOCIAL INTERACTION; SOCIAL STATUS; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BODY SIZE; CARRIER PROTEINS; FOOD PREFERENCES; HETEROZYGOTE; HIPPOCAMPUS; IMITATIVE BEHAVIOR; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR SKILLS; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; ROTAROD PERFORMANCE TEST; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

MUS;

EID: 33847262514     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2006.00240.x     Document Type: Article

References (72)

1. Abe, H., Misaka, T., Tateyama, M. & Kubo, Y. (2003) Effects of coexpression with Homer isoforms on the function of metabotropic glutamate receptor 1alpha. Mol Cell Neurosci 23, 157-168.
2. Ageta, H., Kato, A., Fukazawa, Y., Inokuchi, K. & Sugiyama, H. (2001) Effects of proteasome inhibitors on the synaptic localization of Vesl-1S/Homer-1a proteins. Brain Res Mol Brain Res 97, 186-189.
3. Aiba, A., Kano, M., Chen, C., Stanton, M.E., Fox, G.D., Herrup, K., Zwingman, T.A. & Tonegawa, S. (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79, 377-388.
4. Ango, F., Pin, J.P., Tu, J.C., Xiao, B., Worley, P.F., Bockaert, J. & Fagni, L. (2000) Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation. J Neurosci 20, 8710-8716.
5. Ango, F., Robbe, D., Tu, J.C., Xiao, B., Worley, P.F., Pin, J.P., Bockaert, J. & Fagni, L. (2002) Homer-dependent cell surface expression of metabotropic glutamate receptor type 5 in neurons. Mol Cell Neurosci 20, 323-329.
6. Anwyl, R. (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29, 83-120.
7. Bellugi, U., Adolphs, R., Cassady, C. & Chiles, M. (1999) Towards the neural basis for hypersociability in a genetic syndrome. Neuroreport 10, 1653-1657.
8. Beneken, J., Tu, J.C., Xiao, B., Nuriya, M., Yuan, J.P., Worley, P.F. & Leahy, D.J. (2000) Structure of the Homer EVH1 domain-peptide complex reveals a new twist in polyproline recognition. Neuron 26, 143-154.
9. Berke, J.D., Paletzki, R.F., Aronson, G.J., Hyman, S.E. & Gerfen, C.R. (1998) A complex program of striatal gene expression induced by dopaminergic stimulation. J Neurosci 18, 5301-5310.
10. Bottai, D., Guzowski, J.F., Schwarz, M.K., Kang, S.H., Xiao, B., Lanahan, A., Worley, P.F. & Seeburg, P.H. (2002) Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J Neurosci 22, 167-175.
11. Bozon, B., Davis, S. & Laroche, S. (2002) Regulated transcription of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12, 570-577.
12. Brakeman, P.R., Lanahan, A.A., O'Brien, R., Roche, K., Barnes, C.A., Huganir, R.L. & Worley, P.F. (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
13. Bult, A. & Lynch, C.B. (1997) Nesting and fitness: lifetime reproductive success in house mice bidirectionally selected for thermoregulatory nest-building behavior. Behav Genet 27, 231-240.
14. Bunsey, M. & Eichenbaum, H. (1995) Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus-stimulus association. Hippocampus 5, 546-556.
15. Burguiere, E., Arleo, A., Hojjati, M., Elgersma, Y., De Zeeuw, C.I., Berthoz, A. & Rondi-Reig, L. (2005) Spatial navigation impairment in mice lacking cerebellar LTD: a motor adaptation deficit? Nat Neurosci 8, 1292-1294.
16. Calamandrei, G., Venerosi, A., Branchi, I., Chiarotti, F., Verdina, A., Bucci, F. & Alleva, E. (1999) Effects of prenatal AZT on mouse neurobehavioral development and passive avoidance learning. Neurotoxicol Teratol 21, 29-40.
17. Ciruela, F., Soloviev, M.M. & McIlhinney, R.A. (1999) Co-expression of metabotropic glutamate receptor type 1alpha with homer-1a/Vesl-1S increases the cell surface expression of the receptor. Biochem J 341, 795-803.
18. Ciruela, F., Soloviev, M.M., Chan, W.Y. & McIlhinney, R.A. (2000) Homer-1c/Vesl-1L modulates the cell surface targeting of metabotropic glutamate receptor type 1alpha: evidence for an anchoring function. Mol Cell Neurosci 15, 36-50.
19. Crawley, J.N. (1996) Unusual behavioral phenotypes of inbred mouse strains. Trends Neurosci 19, 181-182; discussion 188-189.
20. Dulawa, S.C. & Geyer, M.A. (2000) Effects of strain and serotonergic agents on prepulse inhibition and habituation in mice. Neuropharmacology 39, 2170-2179.
21. Feng, W., Tu, J., Yang, T., Vernon, P.S., Allen, P.D., Worley, P.F. & Pessah, I.N. (2002) Homer regulates gain of ryanodine receptor type 1 channel complex. J Biol Chem 277, 44722-44730.
22. File, S.E. (2001) Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125, 151-157.
23. Foa, L., Rajan, I., Haas, K., Wu, G.Y., Brakeman, P., Worley, P. & Cline, H. (2001) The scaffold protein, Homer1b/c, regulates axon pathfinding in the central nervous system in vivo. Nat Neurosci 4, 499-506.
24. Francke, U. (1999) Williams-Beuren syndrome: genes and mechanisms. Hum Mol Genet 8, 1947-1954.
25. French, P.J., O'Connor, V., Jones, M.W., Davis, S., Errington, M.L., Voss, K., Truchet, B., Wotjak, C., Stean, T., Doyere, V., Maroun, M., Laroche, S. & Bliss, T.V. (2001) Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo. Eur J Neurosci 13, 968-976.
26. Gerlai, R. (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci 19, 177-181.
27. Gerlai, R. (2001) Gene targeting: technical confounds and potential solutions in behavioral brain research. Behav Brain Res 125, 13-21.
28. Golub, M.S., Germann, S.L., Han, B. & Keen, C.L. (2000) Lifelong feeding of a high aluminum diet to mice. Toxicology 150, 107-117.
29. Golub, M.S., Germann, S.L. & Lloyd, K.C. (2004) Behavioral characteristics of a nervous system-specific erbB4 knock-out mouse. Behav Brain Res 153, 159-170.
30. Graham, F.K. (1975) The more or less startling effects of weak prestimuli. Psychophysiology 12, 238-248.
31. Grant, E.C. & Mackintosh, J.H. (1963) A comparison of the social postures of some common laboratory rodents. Behavior 21, 246-259.
32. Hennou, S., Kato, A., Schneider, E.M., Lundstrom, K., Gahwiler, B.H., Inokuchi, K., Gerber, U. & Ehrengruber, M.U. (2003) Homer-1a/Vesl-1S enhances hippocampal synaptic transmission. Eur J Neurosci 18, 811-819.
33. Holinger, D.P., Bellugi, U., Mills, D.L., Korenberg, J.R., Reiss, A.L., Sherman, G.F. & Galaburda, A.M. (2005) Relative sparing of primary auditory cortex in Williams syndrome. Brain Res 1037, 35-42.
34. Huber, K.M., Roder, J.C. & Bear, M.F. (2001) Chemical induction of mGluR5- and protein synthesis - dependent long-term depression in hippocampal area CA1. J Neurophysiol 86, 321-325.
35. Ison, J.R. & Allen, P.D. (2003) Low-frequency tone pips elicit exaggerated startle reflexes in C57BL/6J mice with hearing loss. J Assoc Res Otolaryngol 4, 495-504.
36. Kammermeier, P.J., Xiao, B., Tu, J.C., Worley, P.F. & Ikeda, S.R. (2000) Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J Neurosci 20, 7238-7245.
37. Kato, A., Ozawa, F., Saitoh, Y., Hirai, K. & Inokuchi, K. (1997) vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis. FEBS Lett 412, 183-189.
38. Kato, A., Ozawa, F., Saitoh, Y., Fukazawa, Y., Sugiyama, H. & Inokuchi, K. (1998) Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. J Biol Chem 273, 23969-23975.
39. Klugmann, M., Wymond Symes, C., Leichtlein, C.B., Klaussner, B.K., Dunning, J., Fong, D., Young, D. & During, M.J. (2005) AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28, 347-360.
40. Lamberty, Y. & Gower, A.J. (1991) Simplifying environmental cues in a Morris-type water maze improves place learning in old NMRI mice. Behav Neural Biol 56, 89-100.
41. Lanahan, A. & Worley, P. (1998) Immediate-early genes and synaptic function. Neurobiol Learn Mem 70, 37-43.
42. Lister, R.G. (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 92, 180-185.
43. Lominac, K.D., Oleson, E.B., Pava, M., Klugmann, M., Schwarz, M.K., Seeburg, P.H., During, M.J., Worley, P.F., Kalivas, P.W. & Szumlinski, K.K. (2005) Distinct roles for different homer1 isoforms in behaviors and associated prefrontal cortex function. J Neurosci 25, 11586-11594.
44. Mikkelsen, J.D., Larsen, P.J., Mick, G., Vrang, N., Ebling, F.J., Maywood, E.S., Hastings, M.H. & Moller, M. (1995) Gating of retinal inputs through the suprachiasmatic nucleus: role of excitatory neurotransmission. Neurochem Int 27, 263-272.
45. Minami, I., Kengaku, M., Smitt, P.S., Shigemoto, R. & Hirano, T. (2003) Long-term potentiation of mGluR1 activity by depolarization-induced Homer1a in mouse cerebellar Purkinje neurons. Eur J Neurosci 17, 1023-1032.
46. Moser, V.C. (2000) The functional observational battery in adult and developing rats. Neurotoxicology 21, 989-996.
47. Nielsen, H.S., Georg, B., Hannibal, J. & Fahrenkrug, J. (2002) Homer-1 mRNA in the rat suprachiasmatic nucleus is regulated differentially by the retinohypothalamic tract transmitters pituitary adenylate cyclase activating polypeptide and glutamate at time points where light phase-shifts the endogenous rhythm. Brain Res Mol Brain Res 105, 79-85.
48. Okabe, S., Urushido, T., Konno, D., Okado, H. & Sobue, K. (2001) Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J Neurosci 21, 9561-9571.
49. Park, H.T., Kang, E.K. & Bae, K.W. (1997) Light regulates Homer mRNA expression in the rat suprachiasmatic nucleus. Brain Res Mol Brain Res 52, 318-322.
50. Potschka, H., Krupp, E., Ebert, U., Gumbel, C., Leichtlein, C., Lorch, B., Pickert, A., Kramps, S., Young, K., Grune, U., Keller, A., Welschof, M., Vogt, G., Xiao, B., Worley, P.F., Loscher, W. & Hiemisch, H. (2002) Kindling-induced overexpression of Homer 1A and its functional implications for epileptogenesis. Eur J Neurosci 16, 2157-2165.
51. Roche, K.W., Tu, J.C., Petralia, R.S., Xiao, B., Wenthold, R.J. & Worley, P.F. (1999) Homer 1b regulates the trafficking of group I metabotropic glutamate receptors. J Biol Chem 274, 25953-25957.
52. Routtenberg, A. (2002) Targeting the 'species gene ensemble'. Hippocampus 12, 105-108.
53. Sala, C., Piech, V., Wilson, N.R., Passafaro, M., Liu, G. & Sheng, M. (2001) Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31, 115-130.
54. Sala, C., Futai, K., Yamamoto, K., Worley, P.F., Hayashi, Y. & Sheng, M. (2003) Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a. J Neurosci 23, 6327-6337.
55. Sandona, D., Tibaldo, E. & Volpe, P. (2000) Evidence for the presence of two Homer 1 transcripts in skeletal and cardiac muscles. Biochem Biophys Res Commun 279, 348-353.
56. Shigemoto, R., Abe, T., Nomura, S., Nakanishi, S. & Hirano, T. (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12, 1245-1255.
57. Shin, D.M., Dehoff, M., Luo, X., Kang, S.H., Tu, J., Nayak, S.K., Ross, E.M., Worley, P.F. & Muallem, S. (2003) Homer 2 tunes G protein-coupled receptors stimulus intensity by regulating RGS proteins and PLCbeta GAP activities. J Cell Biol 162, 293-303.
58. Shiraishi, Y., Mizutani, A., Mikoshiba, K. & Furuichi, T. (2003a) Coincidence in dendritic clustering and synaptic targeting of homer proteins and NMDA receptor complex proteins NR2B and PSD95 during development of cultured hippocampal neurons. Mol Cell Neurosci 22, 188-201.
59. Shiraishi, Y., Mizutani, A., Yuasa, S., Mikoshiba, K. & Furuichi, T. (2003b) Glutamate-induced declustering of post-synaptic adaptor protein Cupidin (Homer 2/vesl-2) in cultured cerebellar granule cells. J Neurochem 87, 364-376.
60. Sills, R.C., Valentine, W.M., Moser, V., Graham, D.G. & Morgan, D.L. (2000) Characterization of carbon disulfide neurotoxicity in C57BL6 mice: behavioral, morphologic, and molecular effects. Toxicol Pathol 28, 142-148.
61. Sun, J., Tadokoro, S., Imanaka, T., Murakami, S.D., Nakamura, M., Kashiwada, K., Ko, J., Nishida, W. & Sobue, K. (1998) Isolation of PSD-Zip45, a novel Homer/vesl family protein containing leucine zipper motifs, from rat brain. FEBS Lett 437, 304-308.
62. Szumlinski, K.K., Dehoff, M.H., Kang, S.H., Frys, K.A., Lominac, K.D., Klugmann, M., Rohrer, J., Griffin, W., Toda, S., Champtiaux, N.P., Berry, T., Tu, J.C., Shealy, S.E., During, M.J., Middaugh, L.D., Worley, P.F. & Kalivas, P.W. (2004) Homer proteins regulate sensitivity to cocaine. Neuron 43, 401-413.
63. Szumlinski, K.K., Lominac, K.D., Kleschen, M.J., Oleson, E.B., Dehoff, M.H., Schwartz, M.K., Seeberg, P.H., Worley, P.F. & Kalivas, P.W. (2005) Behavioral and neurochemical phenotyping of Homer1 mutant mice: possible relevance to schizophrenia. Genes Brain Behav 4, 273-288.
64. Tu, J.C., Xiao, B., Yuan, J.P., Lanahan, A.A., Leoffert, K., Li, M., Linden, D.J. & Worley, P.F. (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21, 717-726.
65. Tu, J.C., Xiao, B., Naisbitt, S., Yuan, J.P., Petralia, R.S., Brakeman, P., Doan, A., Aakalu, V.K., Lanahan, A.A., Sheng, M. & Worley, P.F. (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23, 583-592.
66. Westhoff, J.H., Hwang, S.Y., Scott Duncan, R., Ozawa, F., Volpe, P., Inokuchi, K. & Koulen, P. (2003) Vesl/Homer proteins regulate ryanodine receptor type 2 function and intracellular calcium signaling. Cell Calcium 34, 261-269.
67. Wolfer, D.P., Crusio, W.E. & Lipp, H.P. (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25, 336-340.
68. Wrenn, C.C., Harris, A.P., Saavedra, M.C. & Crawley, J.N. (2003) Social transmission of food preference in mice: methodology and application to galanin-overexpressing transgenic mice. Behav Neurosci 117, 21-31.
69. Wu, J., Rush, A., Rowan, M.J. & Anwyl, R. (2001) NMDA receptor- and metabotropic glutamate receptor-dependent synaptic plasticity induced by high frequency stimulation in the rat dentate gyrus in vitro. J Physiol 533, 745-755.
70. Xiao, B., Tu, J.C., Petralia, R.S., Yuan, J.P., Doan, A., Breder, C.D., Ruggiero, A., Lanahan, A.A., Wenthold, R.J. & Worley, P.F. (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707-716.
71. Xiao, B., Tu, J.C. & Worley, P.F. (2000) Homer: a link between neural activity and glutamate receptor function. Curr Opin Neurobiol 10, 370-374.
72. Yuan, J.P., Kiselyov, K., Shin, D.M., Chen, J., Shcheynikov, N., Kang, S.H., Dehoff, M.H., Schwarz, M.K., Seeburg, P.H., Muallem, S. & Worley, P.F. (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114, 777-789.