Protein kinase CK2 contributes to diminished small conductance Ca 2+-activated K+ channel activity of hypothalamic pre-sympathetic neurons in hypertension

Journal of Neurochemistry

Volumn 130, Issue 5, 2014, Pages 657-667

  Pachuau, Judith ^a   Li, De Pei ^b   Chen, Shao Rui ^a   Lee, Hae Ahm ^a   Pan, Hui Lin ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

autonomic control; hypertension; hypothalamus; potassium channels; sympathetic nervous system; synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; APAMIN; CALCIUM ION; CALMODULIN; CASEIN KINASE II; GLUTAMIC ACID; MESSENGER RNA; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; GLUTAMATE RELEASE; HYPERTENSION; MALE; MEDIUM AFTER HYPERPOLARIZATION POTENTIAL; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROSECRETION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; POTASSIUM CURRENT; PRE SYMPATHETIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; SYMPATHETIC NERVE CELL; VASOMOTOR REFLEX; WHOLE CELL PATCH CLAMP; WISTAR KYOTO RAT;

AUTONOMIC CONTROL; HYPERTENSION; HYPOTHALAMUS; POTASSIUM CHANNELS; SYMPATHETIC NERVOUS SYSTEM; SYNAPTIC PLASTICITY;

ANIMALS; BLOTTING, WESTERN; CALMODULIN; CASEIN KINASE II; HYPERTENSION; MALE; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS; RATS, INBRED SHR; RATS, INBRED WKY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYMPATHETIC NERVOUS SYSTEM;

EID: 84906342430     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12758     Document Type: Article

References (41)

1. Adelman J. P., Maylie J., and, Sah P., (2012) Small-conductance Ca2+-activated K+ channels: form and function. Annu. Rev. Physiol. 74, 245-269.
2. Allen A. M., (2002) Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 39, 275-280.
3. Anderson E. A., Sinkey C. A., Lawton W. J., and, Mark A. L., (1989) Elevated sympathetic nerve activity in borderline hypertensive humans. Evidence from direct intraneural recordings. Hypertension 14, 177-183.
4. Arrigoni G., Marin O., Pagano M. A., Settimo L., Paolin B., Meggio F., and, Pinna L. A., (2004) Phosphorylation of calmodulin fragments by protein kinase CK2. Mechanistic aspects and structural consequences. Biochemistry 43, 12788-12798.
5. Bildl W., Strassmaier T., Thurm H., et al,. (2004) Protein kinase CK2 is coassembled with small conductance Ca(2+)-activated K+ channels and regulates channel gating. Neuron 43, 847-858.
6. Chen Q. H., and, Toney G. M., (2009) Excitability of paraventricular nucleus neurones that project to the rostral ventrolateral medulla is regulated by small-conductance Ca2+-activated K+ channels. J. Physiol. 587, 4235-4247.
7. Chen Q. H., Andrade M. A., Calderon A. S., and, Toney G. M., (2010) Hypertension induced by angiotensin II and a high salt diet involves reduced SK current and increased excitability of RVLM projecting PVN neurons. J. Neurophysiol. 104, 2329-2337.
8. Ehlers M. D., Zhang S., Bernhadt J. P., and, Huganir R. L., (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755.
9. Eilam R., Malach R., and, Segal M., (1994) Selective elimination of hypothalamic neurons by grafted hypertension-inducing neural tissue. J. Neurosci. 14, 4891-4902.
10. Faber E. S., Delaney A. J., and, Sah P., (2005) SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat. Neurosci. 8, 635-641.
11. Faust M., and, Montenarh M., (2000) Subcellular localization of protein kinase CK2. A key to its function? Cell Tissue Res. 301, 329-340.
12. Greenwood J. P., Stoker J. B., and, Mary D. A., (1999) Single-unit sympathetic discharge: quantitative assessment in human hypertensive disease. Circulation 100, 1305-1310.
13. Gui L., LaGrange L. P., Larson R. A., Gu M., Zhu J., and, Chen Q. H., (2012) Role of small conductance calcium-activated potassium channels expressed in PVN in regulating sympathetic nerve activity and arterial blood pressure in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R301-R310.
14. Kannan H., Hayashida Y., and, Yamashita H., (1989) Increase in sympathetic outflow by paraventricular nucleus stimulation in awake rats. Am. J. Physiol. 256, R1325-R1330.
15. Keen J. E., Khawaled R., Farrens D. L., Neelands T., Rivard A., Bond C. T., Janowsky A., Fakler B., Adelman J. P., and, Maylie J., (1999) Domains responsible for constitutive and Ca(2+)-dependent interactions between calmodulin and small conductance Ca(2+)-activated potassium channels. J. Neurosci. 19, 8830-8838.
16. Kohler M., Hirschberg B., Bond C. T., Kinzie J. M., Marrion N. V., Maylie J., and, Adelman J. P., (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273, 1709-1714.
17. Li D. P., and, Pan H. L., (2006) Plasticity of GABAergic control of hypothalamic presympathetic neurons in hypertension. Am. J. Physiol. Heart Circ. Physiol. 290, H1110-H1119.
18. Li D. P., and, Pan H. L., (2007a) Role of gamma-aminobutyric acid (GABA)A and GABAB receptors in paraventricular nucleus in control of sympathetic vasomotor tone in hypertension. J. Pharmacol. Exp. Ther. 320, 615-626.
19. Li D. P., and, Pan H. L., (2007b) Glutamatergic inputs in the hypothalamic paraventricular nucleus maintain sympathetic vasomotor tone in hypertension. Hypertension 49, 916-925.
20. Li D. P., and, Pan H. L., (2010) Increased group I metabotropic glutamate receptor activity in paraventricular nucleus supports elevated sympathetic vasomotor tone in hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R552-R561.
21. Li D. P., Chen S. R., and, Pan H. L., (2002) Nitric oxide inhibits spinally projecting paraventricular neurons through potentiation of presynaptic GABA release. J. Neurophysiol. 88, 2664-2674.
22. Li D. P., Chen S. R., and, Pan H. L., (2003) Angiotensin II stimulates spinally projecting paraventricular neurons through presynaptic disinhibition. J. Neurosci. 23, 5041-5049.
23. Li D. P., Yang Q., Pan H. M., and, Pan H. L., (2008) Pre- and postsynaptic plasticity underlying augmented glutamatergic inputs to hypothalamic presympathetic neurons in spontaneously hypertensive rats. J. Physiol. 586, 1637-1647.
24. Lieberman D. N., and, Mody I., (1999) Casein kinase-II regulates NMDA channel function in hippocampal neurons. Nat. Neurosci. 2, 125-132.
25. Maciaszek J. L., Soh H., Walikonis R. S., Tzingounis A. V., and, Lykotrafitis G., (2012) Topography of native SK channels revealed by force nanoscopy in living neurons. J. Neurosci. 32, 11435-11440.
26. Meggio F., and, Pinna L. A., (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17, 349-368.
27. Ngo-Anh T. J., Bloodgood B. L., Lin M., Sabatini B. L., Maylie J., and, Adelman J. P., (2005) SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8, 642-649.
28. Obermair G. J., Kaufmann W. A., Knaus H. G., and, Flucher B. E., (2003) The small conductance Ca2+-activated K+ channel SK3 is localized in nerve terminals of excitatory synapses of cultured mouse hippocampal neurons. Eur. J. Neurosci. 17, 721-731.
29. Pyner S., and, Coote J. H., (2000) Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 100, 549-556.
30. Sah P., (1996) Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 19, 150-154.
31. Sah P., and, Faber E. S., (2002) Channels underlying neuronal calcium-activated potassium currents. Prog. Neurobiol. 66, 345-353.
32. Sailer C. A., Hu H., Kaufmann W. A., Trieb M., Schwarzer C., Storm J. F., and, Knaus H. G., (2002) Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. J. Neurosci. 22, 9698-9707.
33. Schumacher M. A., Rivard A. F., Bachinger H. P., and, Adelman J. P., (2001) Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin. Nature 410, 1120-1124.
34. Spergel D. J., (2007) Calcium and small-conductance calcium-activated potassium channels in gonadotropin-releasing hormone neurons before, during, and after puberty. Endocrinology 148, 2383-2390.
35. Stocker M., and, Pedarzani P., (2000) Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol. Cell. Neurosci. 15, 476-493.
36. Stocker M., Krause M., and, Pedarzani P., (1999) An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc. Natl Acad. Sci. USA 96, 4662-4667.
37. Storm J. F., (1989) An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J. Physiol. 409, 171-190.
38. Swanson L. W., and, Sawchenko P. E., (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev. Neurosci. 6, 269-324.
39. Xia X. M., Fakler B., Rivard A., et al,. (1998) Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395, 503-507.
40. Ye Z. Y., Li D. P., Li L., and, Pan H. L., (2011) Protein kinase CK2 increases glutamatergic input in the hypothalamus and sympathetic vasomotor tone in hypertension. J. Neurosci. 31, 8271-8279.
41. Ye Z. Y., Li D. P., Byun H. S., Li L., and, Pan H. L., (2012) NKCC1 upregulation disrupts chloride homeostasis in the hypothalamus and increases neuronal activity-sympathetic drive in hypertension. J. Neurosci. 32, 8560-8568.