Abstract
Signaling events controlled by calcineurin promote cardiac hypertrophy, but the degree to which such pathways are required to transduce the effects of various hypertrophic stimuli remains uncertain. In particular, the administration of immunosuppressive drugs that inhibit calcineurin has inconsistent effects in blocking cardiac hypertrophy in various animal models. As an alternative approach to inhibiting calcineurin in the hearts of intact animals, transgenic mice were engineered to overexpress a human cDNA encoding the calcineurin-binding protein, myocyte-enriched calcineurin-interacting protein-1 (hMCIP1) under control of the cardiac-specific, alpha-myosin heavy chain promoter (alpha-MHC). In unstressed mice, forced expression of hMCIP1 resulted in a 5-10% decline in cardiac mass relative to wild-type littermates, but otherwise produced no apparent structural or functional abnormalities. However, cardiac-specific expression of hMCIP1 inhibited cardiac hypertrophy, reinduction of fetal gene expression, and progression to dilated cardiomyopathy that otherwise result from expression of a constitutively active form of calcineurin. Expression of the hMCIP1 transgene also inhibited hypertrophic responses to beta-adrenergic receptor stimulation or exercise training. These results demonstrate that levels of hMCIP1 producing no apparent deleterious effects in cells of the normal heart are sufficient to inhibit several forms of cardiac hypertrophy, and suggest an important role for calcineurin signaling in diverse forms of cardiac hypertrophy. The future development of measures to increase expression or activity of MCIP proteins selectively within the heart may have clinical value for prevention of heart failure.
MeSH Terms
Animals
Calcineurin Inhibitors
Cardiomyopathy, Dilated/genetics,pathology,prevention & control
DNA-Binding Proteins
Female
Gene Expression
Humans
Intracellular Signaling Peptides and Proteins
Mice
Mice, Inbred C57BL
Mice, Transgenic
Models, Genetic
Muscle Proteins/genetics,physiology
Myosin Heavy Chains/genetics
Recombinant Fusion Proteins/genetics,physiology
Chemicals
Calcineurin Inhibitors
DNA-Binding Proteins
Intracellular Signaling Peptides and Proteins
Muscle Proteins
RCAN1 protein, human
Recombinant Fusion Proteins
Myosin Heavy Chains
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Rothermel B A
Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
McKinsey T A
Vega R B
Nicol R L
Mammen P
Yang J
Antos C L
Shelton J M
Bassel-Duby R
Olson E N
Williams R S
References (31)
31 references, click to expand
-
Calcineurin plays a critical role in pressure overload-induced cardiac hypertrophy.
Circulation. 1999 Dec 14;100(24):2449-54
PMID: 10595959
-
IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1.
Nature. 1999 Aug 5;400(6744):581-5
PMID: 10448862
-
A new gene family including DSCR1 (Down Syndrome Candidate Region 1) and ZAKI-4: characterization from yeast to human and identification of DSCR1-like 2, a novel human member (DSCR1L2).
Genomics. 2000 Mar 15;64(3):252-63
PMID: 10756093
-
Reversal of cardiac hypertrophy in transgenic disease models by calcineurin inhibition.
J Mol Cell Cardiol. 2000 Apr;32(4):697-709
PMID: 10756124
-
MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type.
EMBO J. 2000 May 2;19(9):1963-73
PMID: 10790363
-
Calcineurin activity is required for the initiation of skeletal muscle differentiation.
J Cell Biol. 2000 May 1;149(3):657-66
PMID: 10791979
-
Calcineurin is activated in rat hearts with physiological left ventricular hypertrophy induced by voluntary exercise training.
Circulation. 2000 May 9;101(18):2134-7
PMID: 10801751
-
Expression profiling reveals distinct sets of genes altered during induction and regression of cardiac hypertrophy.
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6745-50
PMID: 10829065
-
Cardiac hypertrophy is not a required compensatory response to short-term pressure overload.
Circulation. 2000 Jun 20;101(24):2863-9
PMID: 10859294
-
DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways.
Hum Mol Genet. 2000 Jul 1;9(11):1681-90
PMID: 10861295
-
A conserved family of calcineurin regulators.
Genes Dev. 2000 Jul 1;14(13):1595-604
PMID: 10887154
-
Cabin 1, a negative regulator for calcineurin signaling in T lymphocytes.
Immunity. 1998 Jun;8(6):703-11
PMID: 9655484
-
A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling.
J Biol Chem. 2000 Mar 24;275(12):8719-25
PMID: 10722714
-
Calcineurin signaling and muscle remodeling.
Cell. 2000 Jun 23;101(7):689-92
PMID: 10892739
-
Calcineurin: form and function.
Physiol Rev. 2000 Oct;80(4):1483-521
PMID: 11015619
-
Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles.
Circ Res. 2000 Dec 8;87(12):E61-8
PMID: 11110780
-
Calcineurin blockade prevents cardiac mitogen-activated protein kinase activation and hypertrophy in renovascular hypertension.
J Biol Chem. 2000 Dec 29;275(52):40867-73
PMID: 11016940
-
Targeted inhibition of calcineurin attenuates cardiac hypertrophy in vivo.
Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3322-7
PMID: 11248077
-
Isolation and characterization of the mouse cardiac myosin heavy chain genes.
J Biol Chem. 1991 May 15;266(14):9180-5
PMID: 2026617
-
Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation.
Nature. 1992 Jun 25;357(6380):695-7
PMID: 1377362
-
Genomic organization, alternative splicing, and expression patterns of the DSCR1 (Down syndrome candidate region 1) gene.
Genomics. 1997 Sep 15;44(3):358-61
PMID: 9325060
-
A calcineurin-dependent transcriptional pathway for cardiac hypertrophy.
Cell. 1998 Apr 17;93(2):215-28
PMID: 9568714
-
Cain, a novel physiologic protein inhibitor of calcineurin.
J Biol Chem. 1998 Jul 17;273(29):18325-31
PMID: 9660798
-
A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type.
Genes Dev. 1998 Aug 15;12(16):2499-509
PMID: 9716403
-
Prevention of cardiac hypertrophy in mice by calcineurin inhibition.
Science. 1998 Sep 11;281(5383):1690-3
PMID: 9733519
-
AKAP79 inhibits calcineurin through a site distinct from the immunophilin-binding region.
J Biol Chem. 1998 Oct 16;273(42):27412-9
PMID: 9765270
-
Generic signals and specific outcomes: signaling through Ca2+, calcineurin, and NF-AT.
Cell. 1999 Mar 5;96(5):611-4
PMID: 10089876
-
Failure of calcineurin inhibitors to prevent pressure-overload left ventricular hypertrophy in rats.
Circ Res. 1999 Apr 2;84(6):722-8
PMID: 10189360
-
Pressure overload induces severe hypertrophy in mice treated with cyclosporine, an inhibitor of calcineurin.
Circ Res. 1999 Apr 2;84(6):729-34
PMID: 10189361
-
Cyclosporine attenuates pressure-overload hypertrophy in mice while enhancing susceptibility to decompensation and heart failure.
Circ Res. 1999 Apr 2;84(6):735-40
PMID: 10189362
-
Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway.
Nature. 1999 Aug 5;400(6744):576-81
PMID: 10448861