title: Mitochondria in cardiomyocyte Ca2+ signaling.
abstract: Ca(2+) signaling is of vital importance to cardiac cell function and plays an important role in heart failure. It is based on sarcolemmal, sarcoplasmic reticulum and mitochondrial Ca(2+) cycling. While the first two are well characterized, the latter remains unclear, controversial and technically challenging. In mammalian cardiac myocytes, Ca(2+) influx through L-type calcium channels in the sarcolemmal membrane triggers Ca(2+) release from the nearby junctional sarcoplasmic reticulum to produce Ca(2+) sparks. When this triggering is synchronized by the cardiac action potential, a global [Ca(2+)](i) transient arises from coordinated Ca(2+) release events. The ends of intermyofibrillar mitochondria are located within 20 nm of the junctional sarcoplasmic reticulum and thereby experience a high local [Ca(2+)] during the Ca(2+) release process. Both local and global Ca(2+) signals may thus influence calcium signaling in mitochondria and, reciprocally, mitochondria may contribute to the local control of calcium signaling. In addition to the intermyofibrillar mitochondria, morphologically distinct mitochondria are also located in the perinuclear and subsarcolemmal regions of the cardiomyocyte and thus experience a different local [Ca(2+)]. Here we review the literature in regard to several issues of broad interest: (1) the ultrastructural basis for mitochondrion - sarcoplasmic reticulum cross-signaling; (2) mechanisms of sarcoplasmic reticulum signaling; (3) mitochondrial calcium signaling; and (4) the possible interplay of calcium signaling between the sarcoplasmic reticulum and adjacent mitochondria. Finally, this review discusses experimental findings and mathematical models of cardiac calcium signaling between the sarcoplasmic reticulum and mitochondria, identifies weaknesses in these models, and suggests strategies and approaches for future investigations.
authors.affiliation: Medical Biotechnology Center, University of Maryland Biotechnology Institute, Baltimore, MD 21201, USA. lukyanen@umbi.umd.edu
authors.forename: Valeriy
authors.initials: V
authors.lastname: Lukyanenko
authors.forename: Aristide
authors.initials: A
authors.lastname: Chikando
authors.forename: W J
authors.initials: WJ
authors.lastname: Lederer
mesh_terms: D000818:Animals; D020013:Calcium Signaling / Q000502:physiology*; D006801:Humans; D008929:Mitochondria, Heart / Q000378:metabolism*; D008954:Models, Biological; D032383:Myocytes, Cardiac / Q000378:metabolism*; D012519:Sarcoplasmic Reticulum / Q000378:metabolism
references.citation: Am J Physiol Cell Physiol. 2000 Apr;278(4):C747-64
references.pmid: 10751324
references.citation: Cell Calcium. 2000 Nov-Dec;28(5-6):339-48
references.pmid: 11115373
references.citation: Nature. 2008 Dec 4;456(7222):605-10
references.pmid: 19052620
references.citation: Nature. 2001 Mar 29;410(6828):592-6
references.pmid: 11279498
references.citation: Cardiovasc Res. 1999 Jan;41(1):135-46
references.pmid: 10325961
references.citation: Nature. 2004 Jan 22;427(6972):360-4
references.pmid: 14737170
references.citation: Science. 1995 May 19;268(5213):1042-5
references.pmid: 7754383
references.citation: J Neurochem. 1996 Jan;66(1):403-11
references.pmid: 8522981
references.citation: Biochim Biophys Acta. 1980 Jul 8;591(2):251-65
references.pmid: 7397124
references.citation: J Mol Cell Cardiol. 2002 Aug;34(8):951-69
references.pmid: 12234765
references.citation: J Mol Cell Cardiol. 1998 Oct;30(10):1929-37
references.pmid: 9799647
references.citation: Cardiovasc Res. 1999 Apr;42(1):254-61
references.pmid: 10435018
references.citation: J Cardiovasc Electrophysiol. 2002 Jan;13(1):88-91
references.pmid: 11843491
references.citation: Physiol Rev. 1999 Jul;79(3):917-1017
references.pmid: 10390520
references.citation: Annu Rev Physiol. 2007;69:19-49
references.pmid: 17059356
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 18;104(38):14958-63
references.pmid: 17848521
references.citation: Biochemistry. 2006 Feb 28;45(8):2524-36
references.pmid: 16489745
references.citation: J Gen Physiol. 1985 Feb;85(2):291-320
references.pmid: 2580044
references.citation: Arch Biochem Biophys. 1985 Aug 1;240(2):723-33
references.pmid: 2411223
references.citation: Cell Calcium. 2001 Jul;30(1):19-27
references.pmid: 11396984
references.citation: Science. 1995 May 19;268(5213):1045-9
references.pmid: 7754384
references.citation: Prog Biophys Mol Biol. 2004 Jun-Jul;85(2-3):279-99
references.pmid: 15142748
references.citation: J Physiol. 1997 Apr 15;500 ( Pt 2):297-309
references.pmid: 9147318
references.citation: Cardiovasc Res. 1992 Mar;26(3):193-214
references.pmid: 1423412
references.citation: Physiol Rev. 2007 Jan;87(1):99-163
references.pmid: 17237344
references.citation: Arch Surg. 1985 Mar;120(3):332-8
references.pmid: 2982344
references.citation: J Theor Biol. 1979 Aug 21;79(4):491-541
references.pmid: 159983
references.citation: Biophys J. 1994 Nov;67(5):1942-56
references.pmid: 7858131
references.citation: Mol Cell Biochem. 1994 Jan 26;130(2):159-71
references.pmid: 8028595
references.citation: Br J Pharmacol. 1999 Aug;127(8):1846-50
references.pmid: 10482915
references.citation: EMBO J. 2001 Sep 3;20(17):4998-5007
references.pmid: 11532963
references.citation: Nanomedicine (Lond). 2007 Dec;2(6):831-46
references.pmid: 18095849
references.citation: J Physiol. 1998 Mar 15;507 ( Pt 3):667-77
references.pmid: 9508828
references.citation: Biophys J. 2003 Apr;84(4):2734-55
references.pmid: 12668482
references.citation: Annu Rev Physiol. 2007;69:51-67
references.pmid: 17007587
references.citation: J Physiol. 1993 Jan;460:603-21
references.pmid: 8387590
references.citation: J Mol Cell Cardiol. 1999 Nov;31(11):2063-76
references.pmid: 10591032
references.citation: Biophys J. 2002 Dec;83(6):2918-45
references.pmid: 12496068
references.citation: J Surg Res. 1986 May;40(5):495-8
references.pmid: 3736033
references.citation: Biophys J. 2004 Nov;87(5):3351-71
references.pmid: 15347581
references.citation: Cell Calcium. 1993 Mar;14(3):185-200
references.pmid: 8500135
references.citation: Circ Res. 2006 Aug 4;99(3):283-91
references.pmid: 16794184
references.citation: Proc R Soc Lond B Biol Sci. 1984 Dec 22;223(1231):223-38
references.pmid: 6151661
references.citation: Biophys Chem. 2007 Sep;129(2-3):93-110
references.pmid: 17566629
references.citation: J Cell Biol. 1988 Aug;107(2):481-95
references.pmid: 3417757
references.citation: Biophys J. 2001 Aug;81(2):785-98
references.pmid: 11463625
references.citation: Biophys J. 2008 Sep;95(5):2583-98
references.pmid: 18424491
references.citation: J Physiol. 2000 Dec 15;529 Pt 3:553-64
references.pmid: 11118489
references.citation: J Physiol. 2003 Mar 1;547(Pt 2):453-62
references.pmid: 12562922
references.citation: Mol Cell Biochem. 2008 Nov;318(1-2):147-65
references.pmid: 18629616
references.citation: J Biol Chem. 2003 May 23;278(21):19062-70
references.pmid: 12660243
references.citation: J Cell Biol. 1993 Feb;120(4):969-80
references.pmid: 8381786
references.citation: Biophys J. 2006 Jan 1;90(1):77-91
references.pmid: 16214852
references.citation: J Physiol. 2007 Aug 15;583(Pt 1):251-69
references.pmid: 17627991
references.citation: Am J Physiol. 1996 Jan;270(1 Pt 1):C148-59
references.pmid: 8772440
references.citation: J Physiol. 1999 Dec 15;521 Pt 3:575-85
references.pmid: 10601490
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18746-51
references.pmid: 19033201
references.citation: Biophys J. 1992 Aug;63(2):497-517
references.pmid: 1330031
references.citation: Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2198-202
references.pmid: 18268335
references.citation: EMBO J. 2001 Aug 1;20(15):4107-21
references.pmid: 11483514
references.citation: J Cardiovasc Pharmacol. 1993 Apr;21(4):595-9
references.pmid: 7681905
references.citation: J Cell Biol. 1968 May;37(2):345-69
references.pmid: 5656397
references.citation: Arch Mal Coeur Vaiss. 1999 Apr;92 Spec No 1:9-16
references.pmid: 10326153
references.citation: Anat Rec. 1981 Jun;200(2):139-51
references.pmid: 7270916
references.citation: Jpn Heart J. 1996 Jan;37(1):1-17
references.pmid: 8632617
references.citation: FASEB J. 1998 Nov;12(14):1507-20
references.pmid: 9806760
references.citation: Biophys J. 2000 Jul;79(1):39-50
references.pmid: 10866936
references.citation: Am J Physiol. 1999 Mar;276(3):H865-72
references.pmid: 10070069
references.citation: Biochem Biophys Res Commun. 1978 Sep 29;84(2):482-8
references.pmid: 214079
references.citation: J Biol Chem. 1999 Feb 26;274(9):5654-8
references.pmid: 10026183
references.citation: J Clin Invest. 2008 Jun;118(6):2230-45
references.pmid: 18483626
references.citation: Biochem J. 1999 Jul 15;341 ( Pt 2):233-49
references.pmid: 10393078
references.citation: Arch Biochem Biophys. 1999 Nov 15;371(2):317-25
references.pmid: 10545220
references.citation: Biochem Biophys Res Commun. 1990 Feb 28;167(1):148-53
references.pmid: 2310386
references.citation: Toxicol Appl Pharmacol. 1997 Dec;147(2):431-41
references.pmid: 9439738
references.citation: J Cell Biol. 1969 Jul;42(1):1-45
references.pmid: 4891913
references.citation: Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2380-5
references.pmid: 11854531
references.citation: Circulation. 1975 Jan;51(1):39-67
references.pmid: 122789
references.citation: Biophys J. 2006 Dec 1;91(11):4317-27
references.pmid: 16980364
references.citation: J Cell Biol. 2000 Sep 18;150(6):1283-98
references.pmid: 10995435
references.citation: J Bioenerg Biomembr. 2005 Jun;37(3):129-42
references.pmid: 16167170
references.citation: J Cell Biol. 1992 Apr;117(2):337-45
references.pmid: 1373142
references.citation: Cardiovasc Res. 2008 Jan 15;77(2):432-41
references.pmid: 18006452
references.citation: Am J Pathol. 1964 Mar;44:491-505
references.pmid: 14126668
references.citation: Biochem J. 1999 Oct 15;343 Pt 2:311-7
references.pmid: 10510294
references.citation: J Physiol. 2000 Nov 15;529 Pt 1:37-47
references.pmid: 11080249
references.citation: Adv Exp Med Biol. 1992;311:245-62
references.pmid: 1529757
references.citation: Annu Rev Pharmacol Toxicol. 2001;41:317-45
references.pmid: 11264460
references.citation: Science. 1993 Oct 29;262(5134):740-4
references.pmid: 8235594
references.citation: Biophys J. 1998 Mar;74(3):1149-68
references.pmid: 9512016
references.citation: Cardiovasc Res. 1993 Oct;27(10):1800-9
references.pmid: 8275527
references.citation: Adv Exp Med Biol. 1997;419:411-9
references.pmid: 9193683
references.citation: Biochem Pharmacol. 1970 Jan;19(1):197-207
references.pmid: 4323654
references.citation: Biophys J. 2000 Sep;79(3):1273-84
references.pmid: 10968991
references.citation: Cardiovasc Pathol. 2000 Jan-Feb;9(1):1-8
references.pmid: 10739901
references.citation: Mol Cell Biochem. 2004 Jan-Feb;256-257(1-2):331-9
references.pmid: 14977192
references.citation: Biophys J. 2007 Feb 1;92(3):1058-71
references.pmid: 17098804
references.citation: Biull Eksp Biol Med. 1982 Jul;94(7):116-8
references.pmid: 7126812
references.citation: J Biol Chem. 1977 Dec 10;252(23):8731-9
references.pmid: 925018
references.citation: Arch Biochem Biophys. 1979 Jul;195(2):460-7
references.pmid: 38751
references.citation: J Bioenerg Biomembr. 1998 Jun;30(3):207-22
references.pmid: 9733088
references.citation: Mol Cell Biochem. 2004 Jan-Feb;256-257(1-2):185-99
references.pmid: 14977180
references.citation: J Biol Chem. 2001 Jan 26;276(4):2586-99
references.pmid: 11029457
references.citation: Nature. 2003 Dec 18;426(6968):862-6
references.pmid: 14685243
references.citation: Biophys J. 2008 Sep 15;95(6):3079-99
references.pmid: 18757564
references.citation: Science. 1990 Oct 26;250(4980):565-8
references.pmid: 2173135
references.citation: Cardiovasc Res. 2003 Mar 15;57(4):897-912
references.pmid: 12650868
references.citation: J Physiol. 1992;453:591-608
references.pmid: 1464847
references.citation: Biophys J. 2006 Aug 15;91(4):1564-89
references.pmid: 16679365
references.citation: Biochim Biophys Acta. 2006 May-Jun;1757(5-6):509-17
references.pmid: 16829228
references.citation: Biophys J. 1998 Oct;75(4):2004-14
references.pmid: 9746542
references.citation: Mol Cell Biochem. 2004 Jan-Feb;256-257(1-2):107-15
references.pmid: 14977174
references.citation: J Mol Cell Cardiol. 2002 Aug;34(8):941-50
references.pmid: 12234764
references.citation: J Cell Biol. 1982 Jun;93(3):883-92
references.pmid: 6749864
references.citation: J Neurophysiol. 2002 Feb;87(2):740-9
references.pmid: 11826043
references.citation: Circ Res. 1998 Nov 2;83(9):898-907
references.pmid: 9797338
references.citation: Free Radic Res. 2004 Oct;38(10):1113-8
references.pmid: 15512800
references.citation: Am J Physiol. 1990 May;258(5 Pt 1):C755-86
references.pmid: 2185657
references.citation: Nature. 1995 Oct 5;377(6548):438-41
references.pmid: 7566122
references.citation: J Gen Physiol. 1999 Mar;113(3):469-89
references.pmid: 10051521
references.citation: Cardiovasc Res. 2007 Mar 1;73(4):631-40
references.pmid: 17157285
references.citation: J Neurochem. 2002 Feb;80(4):706-14
references.pmid: 11841577
references.citation: J Biol Chem. 2001 Aug 24;276(34):32257-63
references.pmid: 11413128
references.citation: Biophys J. 2002 Aug;83(2):587-604
references.pmid: 12124250
references.citation: J Mol Cell Cardiol. 1998 Oct;30(10):2013-23
references.pmid: 9799655
references.citation: J Bioenerg Biomembr. 1987 Aug;19(4):309-20
references.pmid: 3305491
references.citation: Front Biosci. 2002 Jul 1;7:d1697-711
references.pmid: 12086924
references.citation: J Biol Chem. 2000 May 19;275(20):15305-13
references.pmid: 10809765
references.citation: Biophys J. 1989 Aug;56(2):229-42
references.pmid: 2673420
references.citation: J Physiol. 1995 Sep 15;487 ( Pt 3):601-8
references.pmid: 8544124
references.citation: J Muscle Res Cell Motil. 2006;27(5-7):297-306
references.pmid: 16897575
references.citation: Am J Physiol. 1998 Jan;274(1):H8-17
references.pmid: 9458846
references.citation: J Biol Chem. 2001 Aug 3;276(31):29430-9
references.pmid: 11358971
references.citation: J Physiol. 1999 Jul 1;518(Pt 1):173-86
references.pmid: 10373699
references.citation: Biochim Biophys Acta. 2007 Jul;1768(7):1784-95
references.pmid: 17499575
references.citation: FEBS Lett. 1980 Mar 10;111(2):261-8
references.pmid: 6987089
references.citation: Circ Res. 2000 Aug 4;87(3):201-6
references.pmid: 10926870
references.citation: J Cell Biol. 1969 Jul;42(1):46-67
references.pmid: 5786989
references.citation: Am J Physiol Cell Physiol. 2006 Nov;291(5):C840-50
references.pmid: 16723510
references.citation: Proc R Soc Lond B Biol Sci. 1984 Dec 22;223(1231):239-54
references.pmid: 6151662
references.citation: Am J Physiol. 1994 Aug;267(2 Pt 1):C313-39
references.pmid: 8074170
references.citation: J Biol Chem. 2000 Jul 14;275(28):21566-71
references.pmid: 10781610
references.citation: J Biol Chem. 1991 Feb 25;266(6):3376-9
references.pmid: 1847371
references.citation: J Physiol. 2001 Oct 15;536(Pt 2):387-96
references.pmid: 11600674
references.citation: Physiol Rev. 1994 Jul;74(3):595-636
references.pmid: 8036248
references.citation: Pharmacol Toxicol. 1998 Nov;83(5):214-9
references.pmid: 9834970
references.citation: Physiology (Bethesda). 2008 Apr;23:84-94
references.pmid: 18400691
references.citation: Curr Opin Struct Biol. 2000 Oct;10(5):548-56
references.pmid: 11042452
references.citation: J Bioenerg Biomembr. 1994 Oct;26(5):509-17
references.pmid: 7896766
references.citation: EMBO J. 2002 May 1;21(9):2198-206
references.pmid: 11980717
references.citation: Eur J Pharmacol. 1997 Dec 11;340(2-3):295-300
references.pmid: 9537826
references.citation: Cell. 2002 Nov 1;111(3):331-42
references.pmid: 12419244
references.citation: Circ Res. 2002 Aug 23;91(4):315-22
references.pmid: 12193464
references.citation: Biophys J. 2002 Jul;83(1):59-78
references.pmid: 12080100
references.citation: Physiol Rev. 2008 Oct;88(4):1491-545
references.pmid: 18923188
references.citation: Biophys J. 2004 Jul;87(1):696-713
references.pmid: 15240503
references.citation: Cell Calcium. 2008 Jul;44(1):77-91
references.pmid: 18178248
references.citation: Am J Physiol. 1997 Aug;273(2 Pt 1):C717-33
references.pmid: 9277370
references.citation: J Biol Chem. 1998 Apr 24;273(17):10223-31
references.pmid: 9553073
references.citation: Biochim Biophys Acta. 1995 Jul 17;1241(2):139-76
references.pmid: 7640294
references.citation: Pflugers Arch. 1996 Oct;432(6):1047-54
references.pmid: 8781199
references.citation: Am J Physiol Heart Circ Physiol. 2007 Jul;293(1):H307-13
references.pmid: 17351070
references.citation: Curr Med Chem. 2003 Jun;10(11):967-81
references.pmid: 12678683
references.citation: Cell. 2003 Nov 26;115(5):629-40
references.pmid: 14651853
references.citation: J Cell Biol. 1987 May;104(5):1343-52
references.pmid: 3553210
references.citation: Mol Cell Biochem. 2004 Jan-Feb;256-257(1-2):341-58
references.pmid: 14977193
references.citation: Recent Adv Stud Cardiac Struct Metab. 1976 May 26-29;12:471-5
references.pmid: 145642
references.citation: J Bioenerg Biomembr. 2000 Feb;32(1):97-104
references.pmid: 11768767
references.citation: Annu Rev Biomed Eng. 2001;3:57-81
references.pmid: 11447057
references.citation: Ann Biomed Eng. 2002 Jun;30(6):808-27
references.pmid: 12220081
references.citation: Biophys J. 2001 Jan;80(1):103-20
references.pmid: 11159386
references.citation: Am J Physiol Cell Physiol. 2007 Jun;292(6):C2004-20
references.pmid: 17344315
references.citation: Biophys J. 2000 Jan;78(1):322-33
references.pmid: 10620296
references.citation: Biophys J. 2006 Feb 1;90(3):1107-19
references.pmid: 16284268
references.citation: Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3099-104
references.pmid: 15710901
references.citation: J Cell Biol. 2004 Feb 16;164(4):493-9
references.pmid: 14769861
references.citation: Biochem Biophys Res Commun. 1997 May 8;234(1):252-6
references.pmid: 9168998
references.citation: Biochem Biophys Res Commun. 1995 Apr 6;209(1):167-74
references.pmid: 7726831
references.citation: Science. 1993 Oct 29;262(5134):744-7
references.pmid: 8235595
references.citation: J Membr Biol. 2002 May 15;187(2):147-56
references.pmid: 12029371
references.citation: J Bioenerg Biomembr. 2004 Aug;36(4):277-81
references.pmid: 15377857
references.citation: Drug Discov Today Dis Models. 2007;4(4):207-217
references.pmid: 18650959
references.citation: Biophys J. 2005 Sep;89(3):1893-901
references.pmid: 15980179
references.citation: Chem Immunol. 2000;75:121-45
references.pmid: 10851782
references.citation: J Mol Cell Cardiol. 2000 Nov;32(11):1981-94
references.pmid: 11040103
references.citation: J Biol Chem. 2008 Nov 21;283(47):32771-80
references.pmid: 18790739
references.citation: Biochim Biophys Acta. 1996 Jun 13;1274(3):81-8
references.pmid: 8664307
references.citation: Circ Res. 2001 Sep 14;89(6):526-33
references.pmid: 11557740
references.citation: Nat Biotechnol. 2003 Mar;21(3):281-6
references.pmid: 12592411
references.citation: Cell Calcium. 2008 Jul;44(1):51-63
references.pmid: 18242694
references.citation: Ann N Y Acad Sci. 1998 Sep 16;853:341-4
references.pmid: 10603975
references.citation: J Physiol. 2008 Jul 1;586(13):3267-85
references.pmid: 18467367
references.citation: Ann N Y Acad Sci. 1998 Sep 16;853:20-30
references.pmid: 10603933
references.citation: Circulation. 2001 Mar 20;103(11):1577-84
references.pmid: 11257088
references.citation: Biophys J. 1999 Sep;77(3):1528-39
references.pmid: 10465763
references.citation: Prog Biophys Mol Biol. 2004 Jun-Jul;85(2-3):141-62
references.pmid: 15142741
references.citation: Circ Res. 2001 Jul 20;89(2):153-9
references.pmid: 11463722
references.citation: Proc Natl Acad Sci U S A. 2006 May 16;103(20):7906-10
references.pmid: 16672364
references.citation: J Biol Chem. 2000 Nov 10;275(45):35402-7
references.pmid: 10958797
references.citation: Biochim Biophys Acta. 2001 Apr 2;1504(2-3):248-61
references.pmid: 11245789
references.citation: Biochem J. 2000 Nov 15;352 Pt 1:61-70
references.pmid: 11062058
references.citation: J Bioenerg Biomembr. 2000 Feb;32(1):15-25
references.pmid: 11768758
references.citation: Am J Physiol. 1992 Aug;263(2 Pt 1):C545-50
references.pmid: 1514597
references.citation: J Membr Biol. 1995 Jul;146(2):133-44
references.pmid: 7473684
references.citation: Anticancer Drugs. 2002 Nov;13(10):1017-29
references.pmid: 12439336
references.citation: Am J Physiol. 1998 Apr;274(4):C1174-84
references.pmid: 9575814
references.citation: Biochem Biophys Res Commun. 2000 Dec 29;279(3):858-63
references.pmid: 11162440
references.citation: Biochem J. 2001 Feb 1;353(Pt 3):531-6
references.pmid: 11171049
references.citation: Cardiovasc Res. 1999 Dec;44(3):556-67
references.pmid: 10690288
references.citation: J Mol Cell Cardiol. 2001 Apr;33(4):615-24
references.pmid: 11273716
references.citation: Am J Physiol Heart Circ Physiol. 2005 Apr;288(4):H1820-8
references.pmid: 15563537
references.citation: Biochem J. 2001 Jun 1;356(Pt 2):643-57
references.pmid: 11368796
references.citation: Cell Calcium. 2003 Apr;33(4):247-56
references.pmid: 12618145
references.citation: Basic Res Cardiol. 2007 Sep;102(5):369-92
references.pmid: 17657400
references.citation: Circ Res. 2002 Oct 4;91(7):594-600
references.pmid: 12364387
references.citation: Biochem J. 1997 Sep 1;326 ( Pt 2):401-5
references.pmid: 9291111
references.citation: Circ Res. 2005 Jan 7;96(1):82-90
references.pmid: 15569829
references.citation: J Neurochem. 2002 Feb;80(3):405-15
references.pmid: 11905989
references.citation: J Physiol. 2000 Feb 15;523 Pt 1:29-44
references.pmid: 10673543
references.citation: Circ Res. 2000 Dec 8;87(12):1087-94
references.pmid: 11110764
references.citation: Biophys J. 2002 Jan;82(1 Pt 1):193-205
references.pmid: 11751308
references.citation: Biochem J. 2001 Aug 15;358(Pt 1):147-55
references.pmid: 11485562
references.citation: Nature. 2006 Oct 12;443(7112):658-62
references.pmid: 17035996
references.citation: Trends Pharmacol Sci. 1993 Nov;14(11):408-13
references.pmid: 8296399
references.citation: Biophys J. 1998 Dec;75(6):2801-10
references.pmid: 9826602
references.citation: J Mol Cell Cardiol. 1997 Sep;29(9):2441-50
references.pmid: 9299367
references.citation: Biochim Biophys Acta. 2002 Dec 2;1556(2-3):155-67
references.pmid: 12460673
references.citation: Circ Res. 1976 Mar;38(3):156-62
references.pmid: 1248063
references.citation: J Biol Chem. 1995 Nov 17;270(46):27510-5
references.pmid: 7499209
references.citation: Circ Res. 1987 Mar;60(3):327-36
references.pmid: 2953507
references.citation: Circ Res. 1991 May;68(5):1378-89
references.pmid: 2018996
references.citation: Pflugers Arch. 2001 Feb;441(5):674-7
references.pmid: 11294249
references.citation: Philos Trans A Math Phys Eng Sci. 2008 Sep 28;366(1879):3381-409
references.pmid: 18603526
references.citation: Am J Physiol. 1991 Oct;261(4 Pt 2):H1123-34
references.pmid: 1928394
references.citation: Anat Rec. 1980 May;197(1):33-48
references.pmid: 7425305
references.citation: J Clin Invest. 2005 Dec;115(12):3527-35
references.pmid: 16284648
references.citation: J Biol Chem. 2001 Jun 15;276(24):21482-8
references.pmid: 11297554
references.citation: J Biol Chem. 1996 Mar 29;271(13):7398-403
references.pmid: 8631764
references.citation: J Biol Chem. 1982 Feb 10;257(3):1540-8
references.pmid: 6460026
references.citation: Circ Res. 2002 Aug 23;91(4):276-7
references.pmid: 12193458
references.citation: Circ Res. 1996 Jan;78(1):166-71
references.pmid: 8603501
references.citation: J Physiol. 1999 Jul 15;518 ( Pt 2):433-47
references.pmid: 10381590
references.citation: Mol Cell Biochem. 2002 Sep;238(1-2):119-27
references.pmid: 12349899
references.citation: Science. 1990 Apr 20;248(4953):283
references.pmid: 2326638
references.citation: Ann N Y Acad Sci. 2005 Jun;1047:127-37
references.pmid: 16093491
references.citation: Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1484-9
references.pmid: 9465041
references.citation: Nature. 2002 Jan 10;415(6868):198-205
references.pmid: 11805843
references.citation: Cell Calcium. 2002 Feb;31(2):97-104
references.pmid: 11969250
references.citation: J Biol Chem. 2001 Jun 29;276(26):24145-52
references.pmid: 11328820
references.citation: J Bioenerg Biomembr. 2008 Jun;40(3):163-70
references.pmid: 18654841
references.citation: J Biol Chem. 2002 Sep 13;277(37):33664-9
references.pmid: 12087096
references.citation: J Physiol. 1994 Feb 1;474(3):463-71
references.pmid: 8014907
references.citation: Int J Biochem. 1993 Apr;25(4):589-96
references.pmid: 8385638
references.citation: J Physiol. 1997 Jan 1;498 ( Pt 1):31-47
references.pmid: 9023766
references.citation: J Cell Biol. 1999 Nov 15;147(4):809-22
references.pmid: 10562282
references.citation: Cell. 2008 Jul 25;134(2):279-90
references.pmid: 18662543
references.citation: Biochem J. 1996 Oct 1;319 ( Pt 1):143-8
references.pmid: 8870661
references.citation: Circ Res. 2006 Jul 21;99(2):172-82
references.pmid: 16778127
references.citation: Curr Opin Chem Biol. 2000 Dec;4(6):653-60
references.pmid: 11102870
references.citation: Circ Res. 2003 Apr 4;92(6):651-8
references.pmid: 12600875
references.citation: J Mol Med (Berl). 2000;78(1):26-35
references.pmid: 10759027
references.citation: Circ Res. 2001 Sep 28;89(7):614-22
references.pmid: 11577027
references.citation: J Physiol. 2005 Jun 15;565(Pt 3):855-72
references.pmid: 15845582
references.citation: Cell Physiol Biochem. 2002;12(5-6):269-78
references.pmid: 12438763
references.citation: Am J Physiol. 1998 Apr;274(4):C1158-73
references.pmid: 9575813
references.citation: J Physiol. 1999 Jul 15;518 ( Pt 2):577-84
references.pmid: 10381602
references.citation: Mol Cell Biochem. 2000 Jul;210(1-2):153-8
references.pmid: 10976768
references.citation: Trends Biochem Sci. 2000 Jul;25(7):319-24
references.pmid: 10871882