Nuclear BK channels regulate gene expression via the control of nuclear calcium signaling

Nature Neuroscience

Volumn 17, Issue 8, 2014, Pages 1055-1063

  Li, Boxing ^a   Jie, Wei ^a   Huang, Lianyan ^a   Wei, Peng ^a   Li, Shuji ^a   Luo, Zhengyi ^a   Friedman, Allyson K ^b   Meredith, Andrea L ^c   Han, Ming Hu ^b   Zhu, Xin Hong ^a   Gao, Tian Ming ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SYNAPSE;

ANIMALS; CALCIUM SIGNALING; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNITS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; NUCLEAR ENVELOPE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 84905089534     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3744     Document Type: Article

References (71)

1. Wheeler, D.G. et al. CaV1 and CaV2 channels engage distinct modes of Ca2+ signaling to control CREB-dependent gene expression. Cell 149, 1112-1124 (2012
2. Jiang, D., Zhao, L.&Clapham, D.E. Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science 326, 144-147 (2009
3. Calcraft, P.J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600 (2009
4. Dong, X.P. et al. The type IV mucolipidosis-Associated protein TRPML1 is an endolysosomal iron release channel. Nature 455, 992-996 (2008
5. Wegierski, T. et al. TRPP2 channels regulate apoptosis through the Ca2+ concentration in the endoplasmic reticulum. EMBO J. 28, 490-499 (2009
6. Bootman, M.D., Fearnley, C., Smyrnias, I., MacDonald, F.&Roderick, H.L. An update on nuclear calcium signalling. J. Cell Sci. 122, 2337-2350 (2009
7. Carafoli, E., Nicotera, P.&Santella, L. Calcium signalling in the cell nucleus. Cell Calcium 22, 313-319 (1997
8. Gerasimenko, O.V., Gerasimenko, J.V., Tepikin, A.V.&Petersen, O.H. ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope. Cell 80, 439-444 (1995
9. Leite, M.F. et al. Nuclear and cytosolic calcium are regulated independently. Proc. Natl. Acad. Sci. USA 100, 2975-2980 (2003
10. Stehno-Bittel, L., Luckhoff, A.&Clapham, D.E. Calcium release from the nucleus by InsP3 receptor channels. Neuron 14, 163-167 (1995
11. Bading, H. Nuclear calcium signalling in the regulation of brain function. Nat. Rev. Neurosci. 14, 593-608 (2013
12. Zhang, S.J. et al. Nuclear calcium signaling controls expression of a large gene pool: Identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet. 5, e1000604 (2009
13. Mauceri, D., Freitag, H.E., Oliveira, A.M., Bengtson, C.P.&Bading, H. Nuclear calcium-VEGFD signaling controls maintenance of dendrite arborization necessary for memory formation. Neuron 71, 117-130 (2011
14. Limbäck-Stokin, K., Korzus, E., Nagaoka-Yasuda, R.&Mayford, M. Nuclear calcium/calmodulin regulates memory consolidation. J. Neurosci. 24, 10858-10867 (2004
15. Papadia, S., Stevenson, P., Hardingham, N.R., Bading, H.&Hardingham, G.E. Nuclear Ca2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J. Neurosci. 25, 4279-4287 (2005
16. Misonou, H. et al. Immunolocalization of the Ca2+-Activated K+ channel Slo1 in axons and nerve terminals of mammalian brain and cultured neurons. J. Comp. Neurol. 496, 289-302 (2006
17. Douglas, R.M. et al. The calcium-sensitive large-conductance potassium channel (BK/MAXI K) is present in the inner mitochondrial membrane of rat brain. Neuroscience 139, 1249-1261 (2006
18. Singh, H. et al. MitoBKCa is encoded by the Kcnma1 gene, and a splicing sequence defines its mitochondrial location. Proc. Natl. Acad. Sci. USA 110, 10836-10841 (2013
19. Gong, L.W., Gao, T.M., Huang, H., Zhuang, Z.Y.&Tong, Z. Transient forebrain ischemia induces persistent hyperactivity of large conductance Ca2+-Activated potassium channels via oxidation modulation in rat hippocampal CA1 pyramidal neurons. Eur. J. Neurosci. 15, 779-783 (2002
20. Hu, H. et al. Presynaptic Ca2+-Activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. 21, 9585-9597 (2001
21. Lee, U.S.&Cui, J. BK channel activation: Structural and functional insights. Trends Neurosci. 33, 415-423 (2010
22. Salkoff, L., Butler, A., Ferreira, G., Santi, C.&Wei, A. High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7, 921-931 (2006
23. Fricker, M., Hollinshead, M., White, N.&Vaux, D. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136, 531-544 (1997
24. Quesada, I. et al. Nuclear KATP channels trigger nuclear Ca2+ transients that modulate nuclear function. Proc. Natl. Acad. Sci. USA 99, 9544-9549 (2002
25. Wu, B., Yamaguchi, H., Lai, F.A.&Shen, J. Presenilins regulate calcium homeostasis and presynaptic function via ryanodine receptors in hippocampal neurons. Proc. Natl. Acad. Sci. USA 110, 15091-15096 (2013
26. Deisseroth, K., Mermelstein, P.G., Xia, H.&Tsien, R.W. Signaling from synapse to nucleus: The logic behind the mechanisms. Curr. Opin. Neurobiol. 13, 354-365 (2003
27. Han, M.H. et al. Role of cAMP response element-binding protein in the rat locus ceruleus: Regulation of neuronal activity and opiate withdrawal behaviors. J. Neurosci. 26, 4624-4629 (2006
28. Sheng, M., Thompson, M.A.&Greenberg, M.E. CREB: A Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427-1430 (1991
29. Bito, H., Deisseroth, K.&Tsien, R.W. CREB phosphorylation and dephosphorylation: A Ca2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203-1214 (1996
30. Xing, J., Ginty, D.D.&Greenberg, M.E. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963 (1996
31. Hardingham, G.E., Arnold, F.J.&Bading, H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4, 261-267 (2001
32. Rodrigues, M.A. et al. Nucleoplasmic calcium is required for cell proliferation. J. Biol. Chem. 282, 17061-17068 (2007
33. Lin, Y. et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204 (2008
34. Ramamoorthi, K. et al. Npas4 regulates a transcriptional program in CA3 required for contextual memory formation. Science 334, 1669-1675 (2011
35. Meredith, A.L., Thorneloe, K.S., Werner, M.E., Nelson, M.T.&Aldrich, R.W. Overactive bladder and incontinence in the absence of the BK large conductance Ca2+-Activated K+ channel. J. Biol. Chem. 279, 36746-36752 (2004
36. Meredith, A.L. et al. BK calcium-Activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat. Neurosci. 9, 1041-1049 (2006
37. Sausbier, M. et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-Activated K+ channel deficiency. Proc. Natl. Acad. Sci. USA 101, 9474-9478 (2004
38. Xu, W. et al. Cytoprotective role of Ca2+- activated K+ channels in the cardiac inner mitochondrial membrane. Science 298, 1029-1033 (2002
39. Mazzanti, M., Bustamante, J.O.&Oberleithner, H. Electrical dimension of the nuclear envelope. Physiol. Rev. 81, 1-19 (2001
40. Dick, D.A. The distribution of sodium, potassium and chloride in the nucleus and cytoplasm of Bufo bufo oocytes measured by electron microprobe analysis. J. Physiol. (Lond.) 284, 37-53 (1978
41. Garner, M.H. Na,K-ATPase in the nuclear envelope regulates Na+: K+ gradients in hepatocyte nuclei. J. Membr. Biol. 187, 97-115 (2002
42. Gifford, J.D., Galla, J.H., Luke, R.G.&Rick, R. Ion concentrations in the rat CCD: Differences between cell types and effect of alkalosis. Am. J. Physiol. 259, F778-F782 (1990
43. Rick, R. pHi determines rate of sodium transport in frog skin: Results of a new method to determine pHi. Am. J. Physiol. 266, F367-F374 (1994
44. Endo, M. Calcium-induced calcium release in skeletal muscle. Physiol. Rev. 89, 1153-1176 (2009
45. Chen, S.R., Li, X., Ebisawa, K.&Zhang, L. Functional characterization of the recombinant type 3 Ca2+ release channel (ryanodine receptor) expressed in HEK293 cells. J. Biol. Chem. 272, 24234-24246 (1997
46. ZahradníkovÁ, A.&Meszaros, L.G. Voltage change-induced gating transitions of the rabbit skeletal muscle Ca2+ release channel. J. Physiol. (Lond.) 509, 29-38 (1998
47. van Welie, I.&du Lac, S. Bidirectional control of BK channel open probability by CAMKII and PKC in medial vestibular nucleus neurons. J. Neurophysiol. 105, 1651-1659 (2011
48. Loane, D.J., Hicks, G.A., Perrino, B.A.&Marrion, N.V. Inhibition of BK channel activity by association with calcineurin in rat brain. Eur. J. Neurosci. 24, 433-441 (2006
49. Shamloo, M. et al. Npas4, a novel helix-loop-helix PAS domain protein, is regulated in response to cerebral ischemia. Eur. J. Neurosci. 24, 2705-2720 (2006).
50. Huang, L., Li, B., Li, W., Guo, H.&Zou, F. ATP-sensitive potassium channels control glioma cells proliferation by regulating ERK activity. Carcinogenesis 30, 737-744 (2009
51. Avdonin, V., Tang, X.D.&Hoshi, T. Stimulatory action of internal protons on Slo1 BK channels. Biophys. J. 84, 2969-2980 (2003
52. Tang, X.D. et al. Haem can bind to and inhibit mammalian calcium-dependent Slo1 BK channels. Nature 425, 531-535 (2003
53. Taylor, C.W. et al. IP3 receptors: Some lessons from DT40 cells. Immunol. Rev. 231, 23-44 (2009
54. Cao, X. et al. Astrocyte-derived ATP modulates depressive-like behaviors. Nat. Med. 19, 773-777 (2013
55. Woo, R.S. et al. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54, 599-610 (2007
56. Chen, Y.J. et al. ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc. Natl. Acad. Sci. USA 107, 21818-21823 (2010
57. Li, X.M. et al. Contribution of downregulation of L-type calcium currents to delayed neuronal death in rat hippocampus after global cerebral ischemia and reperfusion. J. Neurosci. 27, 5249-5259 (2007
58. Hristov, K.L., Chen, M., Kellett, W.F., Rovner, E.S.&Petkov, G.V. Large-conductance voltage- and Ca2+-Activated K+ channels regulate human detrusor smooth muscle function. Am. J. Physiol. Cell Physiol. 301, C903-C912 (2011
59. Zhuang, X., Semenova, E., Maric, D.&Craigie, R. Dephosphorylation of barrier-to-Autointegration factor by protein phosphatase 4 and its role in cell mitosis. J. Biol. Chem. 289, 1119-1127 (2014
60. Muller, F.L. et al. Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 488, 337-342 (2012
61. Cameron, P.H., Chevet, E., Pluquet, O., Thomas, D.Y.&Bergeron, J.J. Calnexin phosphorylation attenuates the release of partially misfolded alpha1-Antitrypsin to the secretory pathway. J. Biol. Chem. 284, 34570-34579 (2009
62. Obexer, P. et al. p16INK4A sensitizes human leukemia cells to FAS- and glucocorticoid-induced apoptosis via induction of BBC3/Puma and repression of MCL1 and BCL2. J. Biol. Chem. 284, 30933-30940 (2009
63. Zaru, R., Ronkina, N., Gaestel, M., Arthur, J.S.&Watts, C. The MAPK-Activated kinase Rsk controls an acute Toll-like receptor signaling response in dendritic cells and is activated through two distinct pathways. Nat. Immunol. 8, 1227-1235 (2007
64. Gehani, S.S. et al. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell 39, 886-900 (2010
65. Tai, Y. et al. TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J. Cell Sci. 121, 2301-2307 (2008
66. Muller, M., Cardenas, C., Mei, L., Cheung, K.H.&Foskett, J.K. Constitutive cAMP response element binding protein (CREB) activation by Alzheimer?s disease presenilin-driven inositol trisphosphate receptor (InsP3R) Ca2+ signaling. Proc. Natl. Acad. Sci. USA 108, 13293-13298 (2011
67. Yu, C. et al. Pharmacologic mitogen-Activated protein/extracellular signal-regulated kinase kinase/mitogen-Activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res. 62, 188-199 (2002
68. Fei, Z., Bera, T.K., Liu, X., Xiang, L.&Pastan, I. Ankrd26 gene disruption enhances adipogenesis of mouse embryonic fibroblasts. J. Biol. Chem. 286, 27761-27768 (2011
69. Wei, F., Scholer, H.R.&Atchison, M.L. Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J. Biol. Chem. 282, 21551-21560 (2007
70. Walton, P.D. et al. Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J. Cell Biol. 113, 1145-1157 (1991
71. Beliveau, F. et al. Essential role of endocytosis of the type II transmembrane serine protease TMPRSS6 in regulating its functionality. J. Biol. Chem. 286, 29035-29043 (2011