Behavioural and functional characterization of Kν10.1 (Eag1) knockout mice

Human Molecular Genetics

Volumn 22, Issue 11, 2013, Pages 2247-2262

  Ufartes, Roser ^a   Schneider, Tomasz ^b   Mortensen, Lena Sünke ^a   Romero, Camino de Juan ^c   Hentrich, Klaus ^d   Knoetgen, Hendrik ^e   Beilinson, Vadim ^f   Moebius, Wiebke ^a   Tarabykin, Victor ^g   Alves, Frauke ^a,h   Pardo, Luis A ^a   Rawlins, J Nicholas P ^b   Stuehmer, Walter ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^d GE Healthcare Life Sciences   (United Kingdom)

^e ROCHE DIAGNOSTICS GMBH   (Germany)

^f BAYER CROPSCIENCE   (United States)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^h UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; ANTIDEPRESSANT AGENT; APOMORPHINE; HALOPERIDOL; POTASSIUM CHANNEL KV10.1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BRAIN CORTEX; CATALEPSY; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO DEVELOPMENT; EXON; FUNCTIONAL STATUS; GENE DELETION; GENOTYPE; HIPPOCAMPUS; HYPERACTIVITY; IMMUNOHISTOCHEMISTRY; LEARNING; MEMORY; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PURKINJE CELL; REAL TIME POLYMERASE CHAIN REACTION; SENSITIZATION; SENSOR; SENSORIMOTOR FUNCTION; SOCIAL BEHAVIOR; WITHDRAWAL SYNDROME;

ACTION POTENTIALS; AMPHETAMINE; ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; BRAIN; CATALEPSY; CEREBELLUM; GENE KNOCKOUT TECHNIQUES; GENE ORDER; GENE TARGETING; GENOTYPE; HALOPERIDOL; MICE; MICE, KNOCKOUT; PHENOTYPE; POTASSIUM CHANNELS, VOLTAGE-GATED;

EID: 84877905311     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt076     Document Type: Article

References (62)

1. Warmke, J., Drysdale, R. and Ganetzky, B. (1991) A distinct potassium channel polypeptide encoded by the Drosophila eag locus. Science (New York, N.Y.), 252, 1560-1562.
2. Warmke, J.W. and Ganetzky, B. (1994) A family of potassium channel genes related to eag in Drosophila and mammals. Proc. Natl. Acad. Sci. USA, 91, 3438-3442.
3. Bruggemann, A., Pardo, L.A., Stuhmer, W. and Pongs, O. (1993) Ether-a-go-go encodes a voltage-gated channel permeable to K+ and Ca2+ and modulated by cAMP. Nature, 365, 445-448.
4. Kaplan, W.D. and Trout, W.E. 3rd. (1969) The behavior of four neurological mutants of Drosophila. Genetics, 61, 399-409.
5. Pearson, G., Robinson, F., Beers, GT., Xu, B.E., Karandikar, M., Berman, K. and Cobb, M.H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev., 22, 153-183.
6. Sutton, K.G., McRory, J.E., Guthrie, H., Murphy, T.H. and Snutch, T.P. (1999) P/Q-type calcium channels mediate the activity-dependent feedback of syntaxin-1A. Nature, 401, 800-804.
7. Hegle, A.P., Marble, D.D. and Wilson, G.F. (2006) A voltage-driven switch for ion-independent signaling by ether-a-go-go K+ channels. Proc. Natl. Acad. Sci. USA, 103, 2886-2891.
8. Ludwig, J., Weseloh, R., Karschin, C., Liu, Q., Netzer, R., Engeland, B., Stansfeld, C. and Pongs, O. (2000) Cloning and functional expression of rat eag2, a new member of the ether-a-go-go family of potassium channels and comparison of its distribution with that of eag1. Mol. Cell. Neurosci., 16, 59-70.
9. Schonherr, R., Gessner, G., Lober, K. and Heinemann, S.H. (2002) Functional distinction of human EAG1 and EAG2 potassium channels. FEBS Lett., 514, 204-208.
10. Ziechner, U., Schonherr, R., Born, A.K., Gavrilova-Ruch, O., Glaser, R.W., Malesevic, M., Kullertz, G. and Heinemann, S.H. (2006) Inhibition of human ether a go-go potassium channels by Ca2+/calmodulin binding to the cytosolic N- and C-termini. FEBS J., 273, 1074-1086.
11. Goncalves, J.T. and Stuhmer, W. (2008) Calmodulin interaction with hEAG1 visualized by FRET microscopy. PLoS One, 5, e10873.
12. Ludwig, J., Terlau, H., Wunder, F., Bruggemann, A., Pardo, L.A., Marquardt, A., Stuhmer, W. and Pongs, O. (1994) Functional expression of a rat homologue of the voltage gated either a go-go potassium channel reveals differences in selectivity and activation kinetics between the Drosophila channel and its mammalian counterpart. EMBO J., 13, 4451-4458.
13. Occhiodoro, T., Bernheim, L., Liu, J.H., Bijlenga, P., Sinnreich, M., Bader, C.R. and Fischer-Lougheed, J. (1998) Cloning of a human ether-a-go-go potassium channel expressed in myoblasts at the onset of fusion. FEBS Lett., 434, 177-182.
14. Ju, M. and Wray, D. (2002) Molecular identification and characterisation of the human eag2 potassium channel. FEBS Lett., 524, 204-210.
15. Pardo, L.A., del Camino, D., Sanchez, A., Alves, F., Bruggemann, A., Beckh, S. and Stuhmer, W. (1999) Oncogenic potential of EAG K(+) channels. EMBO J., 18, 5540-5547.
16. Hemmerlein, B., Weseloh, R.M., Mello de Queiroz, F., Knotgen, H., Sanchez, A., Rubio, M.E., Martin, S., Schliephacke, T., Jenke, M., Heinz Joachim, R. et al. (2006) Overexpression of Eag1 potassium channels in clinical tumours. Mol. Cancer, 5, 41.
17. Agarwal, J.R., Griesinger, F., Stuhmer, W. and Pardo, L.A. (2010) The potassium channel Ether a go-go is a novel prognostic factor with functional relevance in acute myeloid leukemia. Mol. Cancer, 9, 18.
18. Asher, V., Khan, R., Warren, A., Shaw, R., Schalkwyk, G.V., Bali, A. and Sowter, H.M. (2010) The Eag potassium channel as a new prognostic marker in ovarian cancer. Diagn. Pathol., 5, 78.
19. Mello de Queiroz, F., Suarez-Kurtz, G., Stuhmer, W. and Pardo, L.A. (2006) Ether a go-go potassium channel expression in soft tissue sarcoma patients. Mol. Cancer, 5, 42.
20. Ding, X.W., Luo, H.S., Jin, X., Yan, J.J. and Ai, Y.W. (2007) Aberrant expression of Eag1 potassium channels in gastric cancer patients and cell lines. Med. Oncol., 24, 345-350.
21. Ding, X.W., Wang, X.G., Luo, H.S., Tan, S.Y., Gao, S., Luo, B. and Jiang, H. (2008) Expression and prognostic roles of Eag1 in resected esophageal squamous cell carcinomas. Dig. Dis. Sci., 53, 2039-2044.
22. Wadhwa, S., Wadhwa, P., Dinda, A.K. and Gupta, N.P. (2009) Differential expression of potassium ion channels in human renal cell carcinoma. Int. Urol. Nephrol., 41, 251-257.
23. Rodriguez-Rasgado, J.A., Acuna-Macias, I. and Camacho, J. (2012) Eag1 channels as potential cancer biomarkers. Sensors (Basel, Switzerland), 12, 5986-5995.
24. Pardo, L.A. and Suhmer, W. (2008) Eag1 as a cancer target. Expert Opin. Ther. Targets, 12, 837-843.
25. Saganich, M.J., Machado, E. and Rudy, B. (2001) Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain. J. Neurosci., 21, 4609-4624.
26. Martin, S., Lino de Oliveira, C., Mello de Queiroz, F., Pardo, L.A., Stuhmer, W. and Del Bel, E. (2008) Eag1 potassium channel immunohistochemistry in the CNS of adult rat and selected regions of human brain. Neuroscience, 155, 833-844.
27. Gomez-Varela, D., Kohl, T., Schmidt, M., Rubio, M.E., Kawabe, H., Nehring, R.B., Schafer, S., Stuhmer, W. and Pardo, L.A. (2010) Characterization of Eag1 channel lateral mobility in rat hippocampal cultures by single-particle-tracking with quantum dots. PLoS One, 5, e8858.
28. Saganich, M.J., Vega-Saenz de Miera, E., Nadal, M.S., Baker, H., Coetzee, W.A. and Rudy, B. (1999) Cloning of components of a novel subthreshold-activating K(+) channel with a unique pattern of expression in the cerebral cortex. J. Neurosci., 19, 10789-10802.
29. Gurling, H.M., Kalsi, G., Brynjolfson, J., Sigmundsson, T., Sherrington, R., Mankoo, B.S., Read, T., Murphy, P., Blaveri, E., McQuillin, A. et al. (2001) Genomewide genetic linkage analysis confirms the presence of susceptibility loci for schizophrenia, on chromosomes 1q32.2, 5q33.2, and 8p21-22 and provides support for linkage to schizophrenia, on chromosomes 11q23.3-24 and 20q12.1-11.23. Am. J. Hum. Genet., 68, 661-673.
30. Dreixler, J.C., Bian, J., Cao, Y., Roberts, M.T., Roizen, J.D. and Houamed, K.M. (2000) Block of rat brain recombinant SK channels by tricyclic antidepressants and related compounds. Eur. J. Pharmacol., 401, 1-7.
31. Terstappen, G.C., Pula, G., Carignani, C., Chen, M.X. and Roncarati, R. (2001) Pharmacological characterisation of the human small conductance calcium-activated potassium channel hSK3 reveals sensitivity to tricyclic antidepressants and antipsychotic phenothiazines. Neuropharmacology, 40, 772-783.
32. Gavrilova-Ruch, O., Schonherr, K., Gessner, G., Schonherr, R., Klapperstuck, T., Wohlrab, W. and Heinemann, S.H. (2002) Effects of imipramine on ion channels and proliferation of IGR1 melanoma cells. J. Membr. Biol., 188, 137-149.
33. Garcia-Ferreiro, R.E., Kerschensteiner, D., Major, F., Monje, F., Stuhmer, W. and Pardo, L.A. (2004) Mechanism of block of hEag1 K+ channels by imipramine and astemizole. J. Gen. Physiol., 124, 301-317.
34. Hille, B. (2001) Ion Channels of Excitable Membranes. Sunderland, MA, Sinauer Associates.
35. Llinas, R. and Sugimori, M. (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol., 305, 171-195.
36. Ganetzky, B. and Wu, C.F. (1983) Neurogenetic analysis of potassium currents in Drosophila: synergistic effects on neuromuscular transmission in double mutants. J. Neurogenet., 1, 17-28.
37. Stengel, R., Rivera-Milla, E., Sahoo, N., Ebert, C., Bollig, F., Heinemann, S.H., Schonherr, R. and Englert, C. (2012) Kcnh1 voltage-gated potassium channels are essential for early zebrafish development. J. Biol. Chem., 287, 35565-35575.
38. Frank, P.G. and Lisanti, M.P. (2006) Zebrafish as a novel model system to study the function of caveolae and caveolin-1 in organismal biology. Am. J. Pathol., 169, 1910-1912.
39. Kalivas, P.W., Sorg, B.A. and Hooks, M.S. (1993) The pharmacology and neural circuitry of sensitization to psychostimulants. Behav. Pharmacol., 4, 315-334.
40. Nestler, E.J. (2001) Molecular neurobiology of addiction. Am. J. Addict., 10, 201-217.
41. Barr, A.M., Markou, A. and Phillips, A.G. (2002) A 'crash' course on psychostimulant withdrawal as a model of depression. Trends Pharmacol. Sci., 23, 475-482.
42. Swerdlow, N.R. and Geyer, M.A. (1993) Clozapine and haloperidol in an animal model of sensorimotor gating deficits in schizophrenia. Pharmacol. Biochem. Behav., 44, 741-744.
43. Russig, H., Murphy, C.A. and Feldon, J. (2005) Behavioural consequences of withdrawal from three different administration schedules of amphetamine. Behav. Brain Res., 165, 26-35.
44. Klemm, W.R. (1989) Drug effects on active immobility responses: what they tell us about neurotransmitter systems and motor functions. Prog. Neurobiol., 32, 403-422.
45. Joy, C.B., Adams, C.E. and Lawrie, S.M. (2006) Haloperidol versus placebo for schizophrenia. Cochrane Database Syst. Rev., 9, CD003082.
46. Gao, K., Kemp, D.E., Ganocy, S.J., Gajwani, P., Xia, G. and Calabrese, J.R. (2008) Antipsychotic-induced extrapyramidal side effects in bipolar disorder and schizophrenia: a systematic review. J. Clin. Psychopharmacol., 28, 203-209.
47. Qian, Y., Hitzemann, B. and Hitzemann, R. (1992) D1 and D2 dopamine receptor distribution in the neuroleptic nonresponsive and neuroleptic responsive lines of mice, a quantitative receptor autoradiographic study. J. Pharmacol. Exp. Ther., 261, 341-348.
48. Kanes, S.J., Hitzemann, B.A. and Hitzemann, R.J. (1993) On the relationship between D2 receptor density and neuroleptic-induced catalepsy among eight inbred strains of mice. J. Pharmacol. Exp. Ther., 267, 538-547.
49. Ferreira, N.R., Mitkovski, M., Stuhmer, W., Pardo, L.A. and Del Bel, E.A. (2012) Ether-a-go-go 1 (Eag1) potassium channel expression in dopaminergic neurons of basal ganglia is modulated by 6-hydroxydopamine lesion. Neurotox. Res., 21, 317-333.
50. Downie, B.R., Sanchez, A., Knotgen, H., Contreras-Jurado, C., Gymnopoulos, M., Weber, C., Stuhmer, W. and Pardo, L.A. (2008) Eag1 expression interferes with hypoxia homeostasis and induces angiogenesis in tumors. J. Biol. Chem., 283, 36234-36240.
51. Gomez-Varela, D., Zwick-Wallasch, E., Knotgen, H., Sanchez, A., Hettmann, T., Ossipov, D., Weseloh, R., Contreras-Jurado, C., Rothe, M., Stuhmer, W. et al. (2007) Monoclonal antibody blockade of the human Eag1 potassium channel function exerts antitumor activity. Cancer Res., 67, 7343-7349.
52. Pardo, L.A. and Stuhmer, W. (2008) Eag1: an emerging oncological target. Cancer Res., 68, 1611-1613.
53. Bock, P. (1979) Improved Nissl method to stain formaldehyde or glutaraldehyde-fixed material. Acta Neuropathol., 46, 243-244.
54. Rogers, D.C., Peters, J., Martin, J.E., Ball, S., Nicholson, S.J., Witherden, A.S., Hafezparast, M., Latcham, J., Robinson, T.L., Quilter, C.A. et al. (2001) SHIRPA, a protocol for behavioral assessment: validation for longitudinal study of neurological dysfunction in mice. Neurosci. Lett., 306, 89-92.
55. Jones, BJ, R.D. (1968) A rotarod suitable for quantitative measurements of motor incoordination in naive mice. Naunyn Schmiedebergs Arch. Exp. Pathol. Pharmakol., 259, 211.
56. Nadler, J.J., Moy, S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N.B., Barbaro, R.P., Piven, J., Magnuson, T.R. and Crawley, J.N. (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav., 3, 303-314.
57. Lister, R.G. (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl), 92, 180-185.
58. Blumstein, L.K. and Crawley, J.N. (1983) Further characterization of a simple, automated exploratory model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav., 18, 37-40.
59. Burns, L.H., Annett, L., Kelley, A.E., Everitt, B.J. and Robbins, T.W. (1996) Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: implication for limbic-striatal interactions. Behav. Neurosci., 110, 60-73.
60. Reisel, D., Bannerman, D.M., Schmitt, W.B., Deacon, R.M., Flint, J., Borchardt, T., Seeburg, P.H. and Rawlins, J.N. (2002) Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci., 5, 868-873.
61. Stiedl, O., Misane, I., Spiess, J. and Ogren, S.O. (2000) Involvement of the 5-HT1A receptors in classical fear conditioning in C57BL/6J mice. J. Neurosci., 20, 8515-8527.
62. Geyer, M.A., McIlwain, K.L. and Paylor, R. (2002) Mouse genetic models for prepulse inhibition: an early review. Mol. Psychiatry, 7, 1039-1053.