Mice lacking Asic3 show reduced anxiety-like behavior on the elevated plus maze and reduced aggression

Genes, Brain and Behavior

Volumn 9, Issue 6, 2010, Pages 603-614

  Wu, W L ^a,b   Lin, Y W ^c   Min, M Y ^d   Chen, C C ^b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Aggression; anxiety; ASIC3; LTP; Me5; mouse; sensory

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 3; MESSENGER RNA; UNCLASSIFIED DRUG;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; ASIC3 GENE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SENSORY DYSFUNCTION; STEREOTYPY;

AGGRESSION; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, KNOCKOUT; SENSORY RECEPTOR CELLS; SODIUM CHANNELS; TRIGEMINAL GANGLION;

MUS;

EID: 77955144561     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2010.00591.x     Document Type: Article

References (73)

1. Akopian, A.N., Chen, C.C., Ding, Y., Cesare, P. Wood, J.N. (2000) A new member of the acid-sensing ion channel family. Neuroreport 11, 2217 2222.
2. Arnold, L.M. (2008) Management of fibromyalgia and comorbid psychiatric disorders. J Clin Psychiatry 69, 14 19.
3. Arnold, L.M. (2009) Pain and the brain: chronic widespread pain. J Clin Psychiatry 70, e10.
4. Bielsky, I.F., Hu, S.B., Ren, X., Terwilliger, E.F. Young, L.J. (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47, 503 513.
5. Boria, S., Fabbri-Destro, M., Cattaneo, L., Sparaci, L., Sinigaglia, C., Santelli, E., Cossu, G. Rizzolatti, G. (2009) Intention understanding in autism. PLoS ONE 4, e5596.
6. Borsook, D., Becerra, L., Carlezon, W.A. Jr, Shaw, M., Renshaw, P., Elman, I. Levine, J. (2007) Reward-aversion circuitry in analgesia and pain: implications for psychiatric disorders. Eur J Pain 11, 7 20.
7. Brain, P.F., Smoothy, R. Benton, D. (1985) An ethological analysis of the effects of tifluadom on social encounters in male albino mice. Pharmacol Biochem Behav 23, 979 985. (Pubitemid 16178370)
8. Burnes, L.A., Kolker, S.J., Danielson, J.F., Walder, R.Y. Sluka, K.A. (2008) Enhanced muscle fatigue occurs in male but not female ASIC3-/- mice. Am J Physiol Regul Integr Comp Physiol 294, R1347 R1355.
9. Chen, C.C., England, S., Akopian, A.N. Wood, J.N. (1998) A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci U S A 95, 10240 10245.
10. Chen, C.C., Zimmer, A., Sun, W.H., Hall, J. Brownstein, M.J. (2002) A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc Natl Acad Sci U S A 99, 8992 8997.
11. Chen, C.H., Hsu, Y.T., Chen, C.C. Huang, R.C. (2009a) Acid-sensing ion channels in neurones of the rat suprachiasmatic nucleus. J Physiol 587, 1727 1737.
12. Chen, Y.J., Huang, C.W., Lin, C.S., Chang, W.H. Sun, W.H. (2009b) Expression and function of proton-sensing G-protein-coupled receptors in inflammatory pain. Mol Pain 5, 39.
13. Chiavegatto, S., Dawson, V.L., Mamounas, L.A., Koliatsos, V.E., Dawson, T.M. Nelson, R.J. (2001) Brain serotonin dysfunction accounts for aggression in male mice lacking neuronal nitric oxide synthase. Proc Natl Acad Sci U S A 98, 1277 1281.
14. Chiel, H.J. Beer, R.D. (1997) The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20, 553 557.
15. Choleris, E., Ogawa, S., Kavaliers, M., Gustafsson, J.A., Korach, K.S., Muglia, L.J. Pfaff, D.W. (2006) Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: A detailed behavioral analysis with knockout female mice. Genes Brain Behav 5, 528 539.
16. Connor, M., Naves, L.A. McCleskey, E.W. (2005) Contrasting phenotypes of putative proprioceptive and nociceptive trigeminal neurons innervating jaw muscle in rat. Mol Pain 1, 31.
17. Coryell, M.W., Ziemann, A.E., Westmoreland, P.J., Haenfler, J.M., Kurjakovic, Z., Zha, X.M., Price, M., Schnizler, M.K. Wemmie, J.A. (2007) Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatry 62, 1140 1148.
18. Coryell, M.W., Wunsch, A.M., Haenfler, J.M., Allen, J.E., McBride, J.L., Davidson, B.L. Wemmie, J.A. (2008) Restoring acid-sensing ion channel-1a in the amygdala of knock-out mice rescues fear memory but not unconditioned fear responses. J Neurosci 28, 13738 13741.
19. Coryell, M.W., Wunsch, A.M., Haenfler, J.M., Allen, J.E., Schnizler, M., Ziemann, A.E., Cook, M.N., Dunning, J.P., Price, M.P., Rainier, J.D., Liu, Z., Light, A.R., Langbehn, D.R. Wemmie, J.A. (2009) Acid-sensing ion channel-1a in the amygdala, a novel therapeutic target in depression-related behavior. J Neurosci 29, 5381 5388.
20. Crawley, J.N. (2007) Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 17, 448 459.
21. Crawley, J.N. (2008) Behavioral phenotyping strategies for mutant mice. Neuron 57, 809 818.
22. Crusio, W.E., Goldowitz, D., Holmes, A. Wolfer, D. (2009) Standards for the publication of mouse mutant studies. Genes Brain Behav 8, 1 4.
23. Cryan, J.F. Holmes, A. (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4, 775 790.
24. Dudek, S.M. Bear, M.F. (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89, 4363 4367.
25. Dwyer, J.M., Rizzo, S.J., Neal, S.J., Lin, Q., Jow, F., Arias, R.L., Rosenzweig-Lipson, S., Dunlop, J. Beyer, C.E. (2009) Acid sensing ion channel (ASIC) inhibitors exhibit anxiolytic-like activity in preclinical pharmacological models. Psychopharmacology (Berl) 203, 41 52.
26. Ettaiche, M., Deval, E., Pagnotta, S., Lazdunski, M. Lingueglia, E. (2009) Acid-sensing ion channel 3 in retinal function and survival. Invest Ophthalmol Vis Sci 50, 2417 2426.
27. Finn, D.A., Rutledge-Gorman, M.T. Crabbe, J.C. (2003) Genetic animal models of anxiety. Neurogenetics 4, 109 135.
28. Gordon, J.A. Hen, R. (2004) Genetic approaches to the study of anxiety. Annu Rev Neurosci 27, 193 222.
29. Gregoire, S. Matricon, J. (2009) Differential involvement of ASIC1a in the basolateral amygdala in fear memory and unconditioned fear responses. J Neurosci 29, 6053 6054.
30. Groen, W.B., Zwiers, M.P., van der Gaag, R.J. Buitelaar, J.K. (2008) The phenotype and neural correlates of language in autism: an integrative review. Neurosci Biobehav Rev 32, 1416 1425.
31. Harkin, A., Kelly, J.P. Leonard, B.E. (2003) A review of the relevance and validity of olfactory bulbectomy as a model of depression. Clin Neurosci Res 3, 253 262.
32. Hendricks, T.J., Fyodorov, D.V., Wegman, L.J., Lelutiu, N.B., Pehek, E.A., Yamamoto, B., Silver, J., Weeber, E.J., Sweatt, J.D. Deneris, E.S. (2003) Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 37, 233 247.
33. Hettema, J.M., An, S.S., Neale, M.C., van den Oord, E.J., Kendler, K.S. Chen, X. (2008) Lack of association between the amiloride-sensitive cation channel 2 (ACCN2) gene and anxiety spectrum disorders. Psychiatr Genet 18, 73 79.
34. Hildebrand, M.S., de Silva, M.G., Klockars, T., Rose, E., Price, M., Smith, R.J., McGuirt, W.T., Christopoulos, H., Petit, C. Dahl, H.H. (2004) Characterisation of DRASIC in the mouse inner ear. Hear Res 190, 149 160.
35. Hiler, D.J., Bhattacherjee, A., Yamazaki, S., Tei, H. Geusz, M.E. (2008) Circadian mPer1 gene expression in mesencephalic trigeminal nucleus cultures. Brain Res 1214, 84 93.
36. Hofer, S.B., Mrsic-Flogel, T.D., Bonhoeffer, T. Hubener, M. (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457, 313 317.
37. Holmes, A., Kinney, J.W., Wrenn, C.C., Li, Q., Yang, R.J., Ma, L., Vishwanath, J., Saavedra, M.C., Innerfield, C.E., Jacoby, A.S., Shine, J., Iismaa, T.P. Crawley, J.N. (2003) Galanin GAL-R1 receptor null mutant mice display increased anxiety-like behavior specific to the elevated plus-maze. Neuropsychopharmacology 28, 1031 1044.
38. Huang, C.W., Tzeng, J.N., Chen, Y.J., Tsai, W.F., Chen, C.C. Sun, W.H. (2007) Nociceptors of dorsal root ganglion express proton-sensing G-protein-coupled receptors. Mol Cell Neurosci 36, 195 210.
39. Ishii, T., Furuoka, H., Itou, T., Kitamura, N. Nishimura, M. (2005) The mesencephalic trigeminal sensory nucleus is involved in the control of feeding and exploratory behavior in mice. Brain Res 1048, 80 86.
40. Ishii, T., Furuoka, H., Kitamura, N., Muroi, Y. Nishimura, M. (2006) The mesencephalic trigeminal sensory nucleus is involved in acquisition of active exploratory behavior induced by changing from a diet of exclusively milk formula to food pellets in mice. Brain Res 1111, 153 161.
41. Jin, D., Liu, H.X., Hirai, H. et al. (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446, 41 45.
42. Kelley, A.E. (2001) Measurement of rodent stereotyped behavior. Curr Protoc Neurosci Chapter 8, Unit 8.8.
43. Krishtal, O. (2003) The ASICs: signaling molecules? Modulators? Trends Neurosci 26, 477 483.
44. Leffler, A., Monter, B. Koltzenburg, M. (2006) The role of the capsaicin receptor TRPV1 and acid-sensing ion channels (ASICS) in proton sensitivity of subpopulations of primary nociceptive neurons in rats and mice. Neuroscience 139, 699 709.
45. Lein, E.S., Hawrylycz, M.J., Ao, N. et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168 176.
46. Li, J., Xiong, K.H., Li, Y.Q., Kaneko, T. Mizuno, N. (2000) Serotonergic innervation of mesencephalic trigeminal nucleus neurons: a light and electron microscopic study in the rat. Neurosci Res 37, 127 140.
47. Lin, Y.W., Min, M.Y., Chiu, T.H. Yang, H.W. (2003) Enhancement of associative long-term potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J Neurosci 23, 4173 4181.
48. Lin, Y.W., Min, M.Y., Lin, C.C., Chen, W.N., Wu, W.L., Yu, H.M. Chen, C.C. (2008a) Identification and characterization of a subset of mouse sensory neurons that express acid-sensing ion channel 3. Neuroscience 151, 544 557.
49. Lin, Y.W., Yang, H.W., Min, M.Y. Chiu, T.H. (2008b) Inhibition of associative long-term depression by activation of beta-adrenergic receptors in rat hippocampal CA1 synapses. J Biomed Sci 15, 123 131.
50. Lingueglia, E. (2007) Acid-sensing ion channels in sensory perception. J Biol Chem 282, 17325 17329.
51. Loken, L.S., Wessberg, J., Morrison, I., McGlone, F. Olausson, H. (2009) Coding of pleasant touch by unmyelinated afferents in humans. Nat Neurosci 12, 547 548.
52. Maubaret, C., Delettre, C., Sola, S. Hamel, C.P. (2002) Identification of preferentially expressed mRNAs in retina and cochlea. DNA Cell Biol 21, 781 791.
53. McPhie-Lalmansingh, A.A., Tejada, L.D., Weaver, J.L. Rissman, E.F. (2008) Sex chromosome complement affects social interactions in mice. Horm Behav 54, 565 570.
54. Meng, Q.Y., Wang, W., Chen, X.N., Xu, T.L. Zhou, J.N. (2009) Distribution of acid-sensing ion channel 3 in the rat hypothalamus. Neuroscience 159, 1126 1134.
55. Molliver, D.C., Immke, D.C., Fierro, L., Pare, M., Rice, F.L. McCleskey, E.W. (2005) ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain 1, 35.
56. Price, M.P., McIlwrath, S.L., Xie, J., Cheng, C., Qiao, J., Tarr, D.E., Sluka, K.A., Brennan, T.J., Lewin, G.R. Welsh, M.J. (2001) The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32, 1071 1083.
57. Sakai, H., Lingueglia, E., Champigny, G., Mattei, M.G. Lazdunski, M. (1999) Cloning and functional expression of a novel degenerin-like Na+ channel gene in mammals. J Physiol 519, 323 333.
58. Saudou, F., Amara, D.A., Dierich, A., LeMeur, M., Ramboz, S., Segu, L., Buhot, M.C. Hen, R. (1994) Enhanced aggressive behavior in mice lacking 5-HT1B receptor. Science 265, 1875 1878.
59. Shih, H.T. Mok, H.K. (2000) ETHOM: Event-recording computer software for the study of animal behavior. Acta Zoologica Taiwanica 11, 47 61.
60. Sluka, K.A., Price, M.P., Breese, N.M., Stucky, C.L., Wemmie, J.A. Welsh, M.J. (2003) Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 106, 229 239.
61. Sluka, K.A., Radhakrishnan, R., Benson, C.J., Eshcol, J.O., Price, M.P., Babinski, K., Audette, K.M., Yeomans, D.C. Wilson, S.P. (2007) ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 129, 102 112.
62. Stiedl, O. Meyer, M. (2003) Cardiac dynamics in corticotropin-releasing factor receptor subtype-2 deficient mice. Neuropeptides 37, 3 16.
63. Sugiura, T., Dang, K., Lamb, K., Bielefeldt, K. Gebhart, G.F. (2005) Acid-sensing properties in rat gastric sensory neurons from normal and ulcerated stomach. J Neurosci 25, 2617 2627.
64. Turri, M.G., Datta, S.R., DeFries, J., Henderson, N.D. Flint, J. (2001) QTL analysis identifies multiple behavioral dimensions in ethological tests of anxiety in laboratory mice. Curr Biol 11, 725 734.
65. Waldmann, R. Lazdunski, M. (1998) H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 8, 418 424.
66. Wemmie, J.A., Askwith, C.C., Lamani, E., Cassell, M.D., Freeman, J.H. Jr Welsh, M.J. (2003) Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 23, 5496 5502.
67. Wemmie, J.A., Coryell, M.W., Askwith, C.C., Lamani, E., Leonard, A.S., Sigmund, C.D. Welsh, M.J. (2004) Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc Natl Acad Sci U S A 101, 3621 3626.
68. Wemmie, J.A., Price, M.P. Welsh, M.J. (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29, 578 586.
69. Wu, W.L., Wang, C.H., Huang, E.Y. Chen, C.C. (2009) Asic3(-/-) female mice with hearing deficit affects social development of pups. PLoS ONE 4, e6508.
70. Yang, H.W., Lin, Y.W., Yen, C.D. Min, M.Y. (2002) Change in bi-directional plasticity at CA1 synapses in hippocampal slices taken from 6-hydroxydopamine-treated rats: the role of endogenous norepinephrine. Eur J Neurosci 16, 1117 1128.
71. Yen, Y.T., Tu, P.H., Chen, C.J., Lin, Y.W., Hsieh, S.T. Chen, C.C. (2009) Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Mol Pain 5, 1.
72. Zhang, M., Gong, N., Lu, Y.G., Jia, N.L., Xu, T.L. Chen, L. (2008) Functional characterization of acid-sensing ion channels in cultured neurons of rat inferior colliculus. Neuroscience 154, 461 472.
73. Zimmer, A., Zimmer, A.M., Baffi, J., Usdin, T., Reynolds, K., Konig, M., Palkovits, M. Mezey, E. (1998) Hypoalgesia in mice with a targeted deletion of the tachykinin 1 gene. Proc Natl Acad Sci U S A 95, 2630 2635. This study was supported by the Institute of Biomedical Sciences, Academia Sinica (to W.-L.W and C.-C.C.), Taiwanese Mouse Clinic (NSC98-3112-B-001-020) funded by the National Research Program for Genomic Medicine of Taiwan (to C.-C.C), a postdoctoral fellowship from Academia Sinica (to Y.-W.L.) and a National Science Council grant (NSC93-2320-B-002-137) (to M.-Y.M). W.-L.W. wishes to additionally acknowledge a travel fellowship supported by the Foundation for the Advancement of Outstanding Scholarship.