Kinases SPAK and OSR1 are upregulated by estradiol and activate NKCC1 in the developing hypothalamus

Journal of Neuroscience

Volumn 32, Issue 2, 2012, Pages 593-598

  Nugent, Bridget M ^a   Valenzuela, Carla V ^d   Simons, Timothy J ^c   Mccarthy, Margaret M ^a,b  

^a Program in Neuroscience   (United States)

^b SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANTISENSE OLIGONUCLEOTIDE; CALCIUM; CYCLOHEXIMIDE; DACTINOMYCIN; ESTRADIOL; ESTRADIOL BENZOATE; OXIDATIVE STRESS RESPONSIVE KINASE 1; PROTEIN KINASE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SPS1 RELATED PROLINE ALANINE RICH KINASE; STE20 RELATED KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO; FEMALE; GENE SILENCING; HYPOTHALAMUS; IMAGING; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; ESTRADIOL; FEMALE; GAMMA-AMINOBUTYRIC ACID; HYPOTHALAMUS; MALE; PHOSPHORYLATION; PREGNANCY; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RATS; SEX CHARACTERISTICS; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; UP-REGULATION;

EID: 84855673929     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5415-11.2012     Document Type: Article

References (40)

1. Amateau SK, McCarthy MM (2002) A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J Neurosci 22:8586-8596
2. Barbin G, Pollard H, Gaïarsa J, Ben-Ari Y (1993) Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons. Neurosci Lett 152:150-154
3. Barker JL, Behar T, Li YX, Liu QY, Ma W, Maric D, Maric I, Schaffner AE, Serafini R, Smith SV, Somogyi R, Vautrin JY, Wen XL, Xian H (1998) GABAergic cells and signals in CNS development. Perspect Dev Neurobiol 5:305-322
4. Beato M, Herrlich P, Schütz G (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83:851-857
5. Belhage B, Hansen GH, Elster L, Schousboe A (1998) Effects of gammaaminobutyric acid (GABA) on synaptogenesis and synaptic function. Perspect Dev Neurobiol 5:235-246
6. Ben-Ari Y (2002) Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 3:728-739
7. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303-325
8. Blankenship A G, Feller M B (2010) Mechanismsunderlyingspontaneouspatterned activity in developing neural circuits. Nat Rev Neurosci 11:18-29
9. Bolteus AJ, Bordey A (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24:7623-7631
10. Briggs SW, Galanopoulou AS (2011) Altered GABA signaling in early life epilepsies. Neural Plast. Advance online publication. Retrieved July 25, 2011. doi:10.1155/2011/527605.
11. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: An excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519
12. Choi HJ, Lee CJ, Schroeder A, Kim YS, Jung SH, Kim JS, Kim do Y, Son EJ, Han HC, Hong SK, Colwell CS, Kim YI (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28:5450-5459
13. Cruzalegui FH, Bading H (2000) Calcium-regulated protein kinase cascades and their transcription factor targets. Cell Mol Life Sci 57:402-410
14. Geng Y, Hoke A, Delpire E (2009) The ste20 kinases SPAK and OSR1 regulate NKCC1 function in sensory neurons. J Biol Chem 284:14020-14028
15. Greer PL, Greenberg ME (2008) From synapse to nucleus: calciumdependent gene transcription in control of synapse development and function. Neuron 59:846-860
16. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, Bigelow LB, Weinberger DR, Kleinman JE (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31:11088-11095
17. Lee H, Chen CX, Liu YJ, Aizenman E, Kandler K (2005) KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci 21:2593-2599
18. Liu X, Wang Q, Haydar TF, Bordey A (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAPexpressing progenitors. Nat Neurosci 8:1179-1187
19. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298
20. Luk K, Sadikot A (2001) GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: an in vivo study with stereology. Neuroscience 104:93-103
21. Maric D, Liu QY, Maric I, Chaudry S, Chang YH, Smith SV, Sieghart W, Fritschy JM, Barker JL (2001) GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABAA Autoreceptor/Cl {-} channels. J Neurosci 21:2343-2360
22. McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14:677-683
23. McCarthy MM, Auger AP, Mong JA, Sickel MJ, Davis A M (2000) Antisense oligonucleotides as a tool in developmental neuroendocrinology. Methods 22:239-248
24. McEwen BS (1991) Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol Sci 12:141-147
25. Mitchell CK, Redburn DA (1996) GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina. Brain Res Dev Brain Res 95:63-71
26. Nuñez JL, McCarthy MM (2007) Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus. Dev Neurobiol 67:1879-1890
27. Obata K (1997) Excitatory and trophic action of GABA and related substances in newborn mice and organotypic cerebellar culture. Dev Neurosci 19:117-119
28. 2+ elevating to depressing. J Neurosci 15:5065-5077
29. Perrot-Sinal TS, Davis AM, Gregerson KA, Kao JP, McCarthy MM (2001) Estradiol enhances excitatory gammabutyric acid-mediated calcium signaling in neonatal hypothalamic neurons. Endocrinology 142:2238-2243
30. Perrot-Sinal TS, Sinal CJ, Reader JC, Speert DB, McCarthy MM (2007) Sex differences in the chloride cotransporters, NKCC1 and KCC2, in the developing hypothalamus. J Neuroendocrinol 19:302-308
31. Piechotta K, Lu J, Delpire E (2002) Cation chloride cotransporters interact with the stress-related kinases Ste20-related proline-alanine-rich kinase (SPAK) and oxidative stress response 1 (OSR1). J Biol Chem 277:50812-50819
32. Pizzarelli R, Cherubini E (2011) Alterations of GABAergic signaling in autism spectrum disorders. Neural Plast. Advance online publication. Retrieved July 25, 2011. doi:10.1155/2011/527605.
33. Plotkin MD, Snyder EY, Hebert SC, Delpire E (1997) Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: A possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 33:781-795
34. Rheims S, Holmgren CD, Chazal G, Mulder J, Harkany T, Zilberter T, Zilberter Y (2009) GABA action in immature neocortical neurons directly depends on the availability of ketone bodies. J Neurochem 110:1330-1338
35. Sauer JF, Bartos M (2010) Recruitment of early postnatal parvalbuminpositive hippocampal interneurons by GABAergic excitation. J Neurosci 30:110-115
36. Sernagor E, Chabrol F, Bony G, Cancedda L (2010) GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: general rules and differences in diverse systems. Front Cell Neurosci 4:11.
37. Tamari M, Daigo Y, Nakamura Y (1999) Isolation and characterization of a novel serine threonine kinase gene on chromosome 3p22-21.3. J Hum Genet 44:116-120
38. Vitari AC, Deak M, Morrice NA, Alessi DR (2005) The WNK1 and WNK4 protein kinases that are mutated in Gordon's hypertension syndrome phosphorylate and activate SPAK and OSR1 protein kinases. Biochem J 391:17-24
39. Waddell J, Kim J, Alger BE, McCarthy MM (2011) The depolarizing action of GABA in cultured hippocampal neurons is not due to the absence of ketone bodies. PloS One 6:e23020.
40. Wang DD, Kriegstein AR (2008) GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci 28:5547-5558.