Microdomain organization and frequency-dependence of CREB-dependent transcriptional signaling in heart cells.
Voltage-gated Ca(v)1.2 calcium channels couple membrane depolarization to cAMP response-element-binding protein (CREB)-dependent transcriptional activation. To investigate the spatial and temporal organization of CREB-dependent transcriptional nuclear microdomains, we combined perforated patch-clamp technique and FRET microscopy for monitoring CREB and CREB-binding protein interaction in the nuclei of live cells. The experimental approach to the quantitative assessment of CREB-dependent transcriptional signaling evoked by cAMP- and Ca(v)1.2-dependent mechanisms was devised in COS1 cells expressing recombinant Ca(v)1.2 calcium channels. Using continuous 2-dimensional wavelet transform and time series analyses, we found that nuclear CREB-dependent transcriptional signaling is organized differentially in spatially and temporally separated microdomains of 4 distinct types. In rat neonatal cardiomyocytes, CREB-dependent transcription is mediated by the cAMP-initiated CaMKII-sensitive and Ca(v)1.2-initiated CaMKII-insensitive mechanisms. The latter microdomains show a tendency to exhibit periodic behavior correlated with spontaneous contraction of myocytes suggestive of frequency-dependent CREB-dependent transcriptional regulation in the heart.
National Institute on Aging, National Institutes of Health, Baltimore, Maryland, USA.
Evgeny
E
Kobrinsky
Son Q
SQ
Duong
Anna
A
Sheydina
Nikolai M
NM
Soldatov
D000818:Animals; D000831:Animals, Newborn; D019556:COS Cells; D002478:Cells, Cultured; D002522:Chlorocebus aethiops; D017362:Cyclic AMP Response Element-Binding Protein / Q000235:genetics / Q000378:metabolism*; D004594:Electrophysiology; D008962:Models, Theoretical; D032383:Myocytes, Cardiac / Q000378:metabolism; D051381:Rats; D011916:Rats, Inbred F344; D015398:Signal Transduction / Q000235:genetics / Q000502:physiology; D014158:Transcription, Genetic / Q000235:genetics
D017362:Cyclic AMP Response Element-Binding Protein
Cardiovasc Drugs Ther. 2008 Feb;22(1):3-17
18205034
Mol Cell Biol. 1996 Feb;16(2):694-703
8552098
Cell. 2007 Jul 13;130(1):77-88
17632057
Nature. 2008 Nov 27;456(7221):516-9
18971928
Neuron. 2002 Apr 11;34(2):221-33
11970864
Nature. 1989 Feb 23;337(6209):749-52
2521922
J Cell Biol. 2008 Dec 1;183(5):849-63
19047462
Science. 2004 Oct 22;306(5696):704-8
15499023
J Biol Chem. 2000 Jan 7;275(1):585-98
10617655
Science. 2001 Oct 12;294(5541):333-9
11598293
Arterioscler Thromb Vasc Biol. 2006 Mar;26(3):449-55
16293792
J Biol Chem. 2003 Feb 14;278(7):5021-8
12473653
Nature. 1998 Apr 30;392(6679):933-6
9582075
Circ Res. 2003 Oct 31;93(9):e87
14592996
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10936-41
11535812
Cell Signal. 1998 May;10(5):349-54
9692678
Nature. 1997 Apr 24;386(6627):855-8
9126747
Cardiovasc Res. 2008 Apr 1;78(1):98-107
18218685
Blood. 2002 Jul 15;100(2):467-73
12091337
Cold Spring Harb Symp Quant Biol. 2007;72:421-9
18419300
Proc Natl Acad Sci U S A. 1973 Mar;70(3):641-5
4197624
Nat Rev Genet. 2009 Jul;10(7):457-66
19506577
Stem Cells. 2008 Aug;26(8):1961-72
18483424
Biophys J. 2005 May;88(5):3625-34
15722423
Circulation. 1998 Dec 8;98(23):2545-52
9843461
J Cell Biol. 1995 Apr;129(2):287-98
7536746
Circ Res. 1994 Jun;74(6):1034-41
8187273
Circ Res. 2008 Sep 26;103(7):681-3
18818410
J Biomed Opt. 2006 Nov-Dec;11(6):060504
17212522
Circulation. 1990 Apr;81(4):1401-8
2156639
Proc Natl Acad Sci U S A. 2008 Jun 10;105(23):8154-9
18535142
Nature. 1993 Oct 28;365(6449):855-9
8413673
Annu Rev Physiol. 2008;70:23-49
17988210
Science. 1991 Jun 7;252(5011):1427-30
1646483
Biochim Biophys Acta. 2005 Dec 30;1754(1-2):191-9
16213199
PLoS One. 2009 May 18;4(5):e5587
19492014
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4459-64
15753290
Science. 2009 Apr 10;324(5924):242-6
19359585
Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):2859-64
18287024
Sci Signal. 2009 Jul 28;2(81):pe47
19638614
Nat Cell Biol. 2000 Aug;2(8):507-14
10934471
Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9225-30
12089338
Mol Cell Neurosci. 1995 Apr;6(2):168-83
7551568
J Physiol. 2006 Jan 15;570(Pt 2):209-18
16284076
Nature. 2008 Sep 25;455(7212):485-90
18818649
Heart Rhythm. 2009 Apr;6(4):564-70
19324320
Biophys J. 2007 Oct 15;93(8):2900-10
17586569
J Neurochem. 2003 Apr;85(1):170-9
12641739
J Cell Sci. 1992 Nov;103 ( Pt 3):857-62
1478975
Annu Rev Neurosci. 2008;31:563-90
18558867
FEBS Lett. 2009 Dec 17;583(24):3979-83
19925790
Circulation. 2003 Jun 10;107(22):2844-9
12756152
FEBS Lett. 2008 Jun 18;582(14):1960-70
18442480
Biochim Biophys Acta. 2009 Jun;1793(6):1096-104
19250948
J Mol Biol. 2010 Jan 8;395(1):1-10
19852969
Biophys J. 2008 Feb 15;94(4):1203-15
17921221