Behavioral analysis of Ste20 kinase SPAK knockout mice

Behavioural Brain Research

Volumn 208, Issue 2, 2010, Pages 377-382

  Geng, Yang ^a   Byun, Nellie ^b   Delpire, Eric ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Dorsal root ganglion; K Cl cotransporter; Na K 2Cl cotransporters; Spinal cord

Indexed keywords

PROTEIN KINASE; STE20 RELATED PROLINE ALANINE RICH KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIORAL SCIENCE; BODY EQUILIBRIUM; CENTRAL NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; HOT PLATE TEST; ION TRANSPORT; KNOCKOUT MOUSE; LIGHT DARK CYCLE; LOCOMOTION; MICROARRAY ANALYSIS; MOUSE; NEUROTRANSMISSION; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRIORITY JOURNAL; PROPRIOCEPTION; TAIL FLICK TEST; WILD TYPE;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BEHAVIOR, ANIMAL; EXPLORATORY BEHAVIOR; FUNCTIONAL LATERALITY; HINDLIMB SUSPENSION; HYPERALGESIA; MICE; MICE, KNOCKOUT; MUSCLE STRENGTH; PAIN MEASUREMENT; PAIN THRESHOLD; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; PSYCHOMOTOR PERFORMANCE; STARTLE REACTION; STATISTICS, NONPARAMETRIC; SWIMMING;

EID: 77249135749     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.12.005     Document Type: Article

References (48)

1. Alvarez-Leefmans F.J., Gamiño S.M., Giraldez F., and Nogueron I. Intracellular chloride regulation in amphibian dorsal root ganglion neurons studied with ion-selective microelectrodes. J Physiol (Lond) 406 (1988) 225-246
2. - cotransporter in HeLa cells. Proc Natl Acad Sci U S A 103 (2006) 10883-10888
3. Coull J.A., Boudreau D., Bachand K., Prescott S.A., Nault F., Sik A., et al. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424 (2003) 938-942
4. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9 (1985) 37-44
5. Dan I., Watanabe N.M., and Kusumi A. The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11 (2001) 220-230
6. Delpire E. The mammalian family of sterile20p-like protein kinases. Pflügers Arch Eur J Physiol 458 (2009) 953-967
7. Delpire E., Days E., Mi D., Lewis M., Kim K., Lidnsley C., et al. Small molecule screen identifies inhibitors of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci U S A 106 (2009) 5383-5388
8. Delpire E., and Gagnon K.B. Genome-wide analysis of SPAK/OSR1 binding motifs. Physiol Genomics 28 (2007) 223-231
9. Delpire E., and Gagnon K.B. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J 409 (2008) 321-331
10. Denton J., Nehrke K., Yin X., Morrison R., and Strange K. GCK-3, a newly identified Ste20 kinase, binds to and regulates the activity of a cell cycle-dependent ClC anion channel. J Gen Physiol 125 (2005) 113-125
11. Dowd B.F., and Forbush B. PASK (proline-alanine-rich STE20-related kinase), a regulatory kinase of the Na-K-Cl cotransporter (NKCC1). J Biol Chem 278 (2003) 27347-27353
12. Gagnon K.B., England R., and Delpire E. Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol Cell Biol 26 (2006) 689-698
13. Gagnon K.B., England R., and Delpire E. A single binding motif is required for SPAK activation of the Na-K-2Cl cotransporter. Cell Physiol Biochem 20 (2007) 131-142
14. Gagnon K.B., England R., and Delpire E. Volume sensitivity of cation-chloride cotransporters is modulated by the interaction of two kinases: SPAK and WNK4. Am J Physiol Cell Physiol 290 (2006) C134-C142
15. - cotransporters. Am J Physiol Renal Physiol 292 (2007) F1197-F1207
16. Geng Y., Hoke A., and Delpire E. The Ste20 kinases SPAK and OSR1 regulate NKCC1 function in sensory neurons. J Biol Chem 284 (2009) 14020-14028
17. Granados-Soto V., Arguelles C.F., and Alvarez-Leefmans F.J. Peripheral and central antinociceptive action of Na-K-2Clcotransporter blockers on formalin-induced nociception in rats. Pain 114 (2005) 231-238
18. Heyser C.J. Assessment of developmental milestones in rodents. Curr Protoc Neurosci Chaper 8 (2004) Unit 8.18
19. Irwin S. Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse. Psychopharmacologia 13 (1968) 222-257
20. Jolivalt C.G., Lee C.A., Ramos K.M., and Calcutt N.A. Allodynia and hyperalgesia in diabetic rats are mediated by GABA and depletion of spinal potassium-chloride co-transporters. Pain 140 (2008) 48-57
21. Karl T., Pabst R., and von Horsten S. Behavioral phenotyping of mice in pharmacological and toxicological research. Exp Toxicol Pathol 55 (2003) 69-83
22. Laird J.M., Garcia-Nicas E., Delpire E.J., and Cervero F. Presynaptic inhibition and spinal pain processing in mice: a possible role of the NKCC1 cation-chloride co-transporter in hyperalgesia. Neurosci Lett 361 (2004) 200-203
23. Mantyh P.W., and Hunt S.P. Setting the tone: superficial dorsal horn projection neurons regulate pain sensitivity. Trends Neurosci 27 (2004) 582-584
24. Miao N., Fung B., Sanchez R., Lydon J., Barker D., and Pang K. Isolation and expression of PASK, a serine/threonine kinase during rat embryonic development, with special emphasis on the pancreas. J Histochem Cytochem 48 (2000) 1391-1400
25. Miletic G., and Miletic V. Loose ligation of the sciatic nerve is associated with TrkB receptor-dependent decreases in KCC2 protein levels in the ipsilateral spinal dorsal horn. Pain 137 (2008) 532-539
26. Morales-Aza B.M., Chillingworth N.L., Payne J.A., and Donaldson L.F. Inflammation alters cation chloride cotransporter expression in sensory neurons. Neurobiol Dis 17 (2004) 62-69
27. Moriguchi T., Urushiyama S., Hisamoto N., Iemura S.I., Uchida S., Natsume T., et al. WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related kinases, SPAK and OSR1. J Biol Chem 280 (2006) 42685-42693
28. Nomura H., Sakai A., Nagano M., Umino M., and Suzuki H. Expression changes of cation chloride cotransporters in the rat spinal cord following intraplantar formalin. Neurosci Res 56 (2006) 435-440
29. Pellis S.M., Pellis V.C., Chen Y.C., Barzci S., and Teitelbaum P. Recovery from axial apraxia in the lateral hypothalamic labyrinthectomized rat reveals three elements of contact-righting: cephalocaudal dominance, axial rotation, and distal limb action. Behav Brain Res 35 (1989) 241-251
30. Petit-Demouliere B., Chenu F., and Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology (Berl) 177 (2005) 245-255
31. Piechotta K., Garbarini N.J., England R., and Delpire E. Characterization of the interaction of the stress kinase SPAK with the Na+-K+-2Cl- cotransporter in the nervous system: evidence for a scaffolding role of the kinase. J Biol Chem 278 (2003) 52848-52856
32. Piechotta K., Lu J., and Delpire E. Cation-chloride cotransporters interact with the stress-related kinases SPAK and OSR1. J Biol Chem 277 (2002) 50812-50819
33. Pieraut S., Matha V., Sar C., Hubert T., Méchaly I., Hilaire C., et al. NKCC1 phosphorylation stimulates neurite growth of injured adult sensory neurons. J Neurosci 27 (2007) 6751-6759
34. Pitcher M.H., Price T.J., Entrena J.M., and Cervero F. Spinal NKCC1 blockade inhibits TRPV1-dependent referred allodynia. Mol Pain 3 (2007) 17
35. Ponce-Coria J., San-Cristobal P., Kahle K.T., Vazquez N., Pacheco-Alvarez D., de Los Heros P., et al. Regulation of NKCC2 by a chloride-sensing mechanism involving the WNK3 and SPAK kinases. Proc Natl Acad Sci U S A 105 (2008) 8458-8463
36. Porsolt R.D., Bertin A., and Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229 (1977) 327-336
37. - cotransporter by the WNK-regulated kinases SPAK and OSR1. J Cell Sci 121 (2008) 675-684
38. - cotransporters required for normal blood pressure homeostasis. Proc Natl Acad Sci U S A 102 (2005) 16777-16782
39. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397 (1999) 251-255
40. Steiner H., Bonner T.I., Zimmer A.M., Kitai S.T., and Zimmer A. Altered gene expression in striatal projection neurons in CB1 cannabinoid receptor knockout mice. Proc Natl Acad Sci U S A 96 (1999) 5786-5790
41. A-receptor mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20 (2000) 7531-7538
42. Tornberg J., Voikar V., Savilahti H., Rauvala H., and Airaksinen M.S. Behavioural phenotypes of hypomorphic KCC2-deficient mice. Eur J Neurosci 21 (2005) 1327-1337
43. Van Laer L., Pfister M., Thys S., Vrijens K., Mueller M., Umans L., et al. Mice lacking Dfna5 show a diverging number of cochlear fourth row outer hair cells. Neurobiol Dis 19 (2005) 386-399
44. Villa F., Goebel J., Rafiqi F.H., Deak M., Thastrup J., Alessi D.R., et al. Structural insights into the recognition of substrates and activators by the OSR1 kinase. EMBO Rep 8 (2007) 839-845
45. Vitari A.C., Thastrup J., Rafiqi F.H., Deak M., Morrice N.A., Karlsson H.K., et al. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 397 (2006) 223-231
46. Vlainic J., and Pericic D. Effects of acute and repeated zolpidem treatment on pentylenetetrazole-induced seizure threshold and on locomotor activity: comparison with diazepam. Neuropharmacology 56 (2009) 1124-1130
47. Zhang W., Liu L.-Y., and Xu T.-L. Reduced potassium-chloride co-transporter expression in spinal cord dorsal horn neurons contributes to inflammatory pain hypersensitivity in rats. Neuroscience 152 (2008) 502-510
48. Zhu L., Lovinger D., and Delpire E. Cortical neurons lacking KCC2 expression show impaired regulation of intracellular chloride. J Neurophysiol 93 (2005) 1557-1568