Loss of Enigma Homolog Protein Results in Dilated Cardiomyopathy
Open accessAbstract
Rationale: The Z-line, alternatively termed the Z-band or Z-disc, is a highly ordered structure at the border between 2 sarcomeres. Enigma subfamily proteins (Enigma, Enigma homolog protein, and Cypher) of the PDZ-LIM domain protein family are Z-line proteins. Among the Enigma subfamily, Cypher has been demonstrated to play a pivotal role in the structure and function of striated muscle, whereas the role of Enigma homolog protein (ENH) in muscle remains largely unknown. Objective: We studied the role of Enigma homolog protein in the heart using global and cardiac-specific ENH knockout mouse models. Methods and Results: We identified new exons and splice isoforms for ENH in the mouse heart. Impaired cardiac contraction and dilated cardiomyopathy were observed in ENH null mice. Mice with cardiac specific ENH deletion developed a similar dilated cardiomyopathy. Like Cypher, ENH interacted with Calsarcin-1, another Z-line protein. Moreover, biochemical studies showed that ENH, Cypher short isoform and Calsarcin-1 are within the same protein complex at the Z-line. Cypher short isoform and Calsarcin-1 proteins are specifically downregulated in ENH null hearts. Conclusions: We have identified an ENH-CypherS-Calsarcin protein complex at the Z-line. Ablation of ENH leads to destabilization of this protein complex and dilated cardiomyopathy.
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ENH is a family of PDZ-LIM domain proteins that localize to Z-disk and serve as scaffolds for signaling complexes.
“ENH is a family of PDZ-LIM domain proteins that localize to Z-disk and serve as scaffolds for signaling complexes (65).”
From Distinct hypertrophic cardiomyopathy genotypes result in convergent sarcomeric proteoform profiles revealed by top-down proteomics (2020) · cites this paper as [65]
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“Disturbance of the mechanical link between the Z-disc and the sarcolemma and/or cytoskeletal proteins has been shown to cause DCM [3,16].”
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“Modifications to PDLIM5 result in either HCM or DCM depending on the pathway taken during mutation [112].”
BackgroundAn Overview of the Cytoskeleton-Associated Role of PDLIM5
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“The plasmids were generated in the PXJ40 vector as previously described (29).”
MethodSelf-citationMyofibril diameter is set by a finely tuned mechanism of protein oligomerization in Drosophila
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Overview of the Muscle Cytoskeleton
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Selective deletion of long but not short Cypher isoforms leads to late-onset dilated cardiomyopathy
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Self-citationReimann, L., Wiese, H., Leber, Y., Schwäble, A. N., Fricke, A. L., Rohland, A., Knapp, B. L., Peikert, C. D., Drepper, F., van der Ven, P. F. M., et al. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m116.065425 · Cited by 40 · see citing works
“Further PKC anchoring proteins at the Z-disc are LDB3, also called cypher or ZASP (74, 75, 76), and enigma homologue protein ENH (PDLIM5) (77), which together with calsarcin-1 (MYOZ2) form a complex with an important role in linking Z-discs to the extracellular matrix via the multi-adaptor protein FLNc (78).”
BackgroundLiao, K. A., González‐Morales, N., & Schöck, F. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006400 · Cited by 36 · see citing works
Understanding the molecular basis of cardiomyopathy
Bang, M., Bogomolovas, J., & Chen, J. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00562.2021 · Cited by 36 · see citing works
Self-citationRBPMS regulates cardiomyocyte contraction and cardiac function through RNA alternative splicing
Gan, P., Wang, Z., Bezprozvannaya, S., McAnally, J., Tan, W. H., Li, H. Z., Bassel‐Duby, R., Liu, N., & Olson, E. N. (2023) · Cardiovascular Research · doi:10.1093/cvr/cvad166 · Cited by 33 · see citing works
The Role of Leucine-Rich Repeat Containing Protein 10 (LRRC10) in Dilated Cardiomyopathy
Brody, M. J., & Lee, Y. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00337 · Cited by 34 · see citing works
“…OH, USA, 2Department of Cell and Regenerative Biology, University of Wisconsin-Madison, Madison, WI, USA Leucine-rich repeat containing protein 10 (LRRC10) is a cardiomyocyte-specific member of the Leucine-rich repeat containing (LRRC) protein superfamily with critical roles in cardiac function…”
BackgroundWang, D., Fang, J., Lv, J., Pan, Z., Yin, X., Cheng, H., & Guo, X. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14607 · Cited by 33 · see citing works
Self-citationHuang, J., Cai, C., Zheng, T., Wu, X., Wang, D., Zhang, K., Xu, B., Yan, R., Gong, H., Zhang, J., et al. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.314172 · Cited by 33 · see citing works
Self-citationThe Application of Decellularized Adipose Tissue Promotes Wound Healing
Xia, Z., Guo, X. P., Yu, N., Zeng, A., Si, L., Long, F., Zhang, W., Wang, X., Zhu, L., & Liu, Z. (2020) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-020-00286-0 · Cited by 33 · see citing works
Baandrup, J. D., Markvardsen, L. H., Peters, C. D., Schou, U. K., Jensen, J. L., Magnusson, N. E., Orntoft, T. F., Kruhøffer, M., & Simonsen, U. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015859 · Cited by 33 · see citing works
“FHL is contained in a complex within the cardiomyocyte sacromere and mice lacking FHL displayed a blunted hypertrophic response suggesting FHL1 to mediates hypertrophic biomechanical stress responses in the myocardium [25], while the Enigma protein family are Z-line proteins at the border between two sarcomers [26].”
RBM 20 and RBM 24 cooperatively promote the expression of short enh splice variants
Ito, J., Iijima, M., Yoshimoto, N., Niimi, T., Kuroda, S., & Maturana, A. D. (2016) · FEBS Letters · doi:10.1002/1873-3468.12251 · Cited by 32 · see citing works
Stargazing microRNA maps a new miR-21 star for cardiac hypertrophy
Indolfi, C., & Curcio, A. (2014) · Journal of Clinical Investigation · doi:10.1172/jci75801 · Cited by 31 · see citing works
LRRC10 is required to maintain cardiac function in response to pressure overload
Brody, M. J., Feng, L., Grimes, A. C., Hacker, T. A., Olson, T. M., Kamp, T. J., Balijepalli, R. C., & Lee, Y.-S. (2015) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00717.2014 · Cited by 30 · see citing works
Xu, J., Tao, B., Guo, X., Zhou, S., Li, Y., Zhang, Y., Zhou, Z., Cheng, H., Zhang, X. Z., & Ke, Y. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601696 · Cited by 30 · see citing works
“The plasmids were generated in the pXJ40 vector as previously described (37).”
MethodSelf-citationWei, T.-C., Lin, H.-Y., Lu, C.-C., Chen, C.-M., & You, L.-R. (2011) · Gene Expression Patterns · doi:10.1016/j.gep.2011.05.001 · Cited by 28 · see citing works
Novel insights into sarcomere regulatory systems control of cardiac thin filament activation
Solı́s, C., & Solaro, R. J. (2021) · The Journal of General Physiology · doi:10.1085/jgp.202012777 · Cited by 29 · see citing works
Hou, Y., Crossman, D. J., Rajagopal, V., Baddeley, D., Jayasinghe, I., & Soeller, C. (2014) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2014.07.003 · Cited by 27 · see citing works
Prevalence and spectrum of LRRC10 mutations associated with idiopathic dilated cardiomyopathy
Qu, X., Yuan, F., Li, R., Xu, L., JING, W.-F., Liu, H., Xu, Y., Zhang, M., Liu, X., Fang, W., et al. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3843 · Cited by 27 · see citing works
“Genetic deletion of several Z-disc and costameric proteins has been reported to cause DCM in mice, including Cypher (38), muscle LIM protein (39), enigma homologue protein (40), integrin-linked kinase (41) and vinculin (42).”
Wei, X., Zhang, Y., Yu, S., Li, S., Jiang, W. G., Zhu, Y., Xu, Y., Yang, C., Tian, G., Mi, J., et al. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.03.159 · Cited by 27 · see citing works
The unexpected versatility of ALP/Enigma family proteins
Fisher, L. A. B., & Schöck, F. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.963608 · Cited by 26 · see citing works
“as well as the ALP subfamily in which the proteins only possess one LIM domain (Cheng et al., 2011; reviewed in Zheng et al., 2009). These proteins could represent the “blocking” isoforms in the Drosophila Z-disc diameter model which would function to end Z-disc growth at the specified diameter. Interestingly, in mous…”
BackgroundMethodResultInfluentialKonze, S. A., Werneburg, S., Oberbeck, A., Olmer, R., Kempf, H., Jara-Avaca, M., Pich, A., Zweigerdt, R., & Buettner, F. F. R. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00534 · Cited by 24 · see citing works
Urban, A. E., Quick, E. O., Miller, K. P., Krcmery, J., & Simon, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164042 · Cited by 24 · see citing works
Rasooly, D., Giambartolomei, C., Peloso, G. M., Dashti, H., Ferolito, B. R., Golden, D. J., Horimoto, A. R. V. R., Pietzner, M., Farber‐Eger, E. H., Wells, Q. S., et al. (2025) · Nature Cardiovascular Research · doi:10.1038/s44161-025-00609-1 · Cited by 22 · see citing works
“In support of this, global and cardiac-specific ablation of PDLIM5 gene in mice resulted in dilated cardiomyopathy phenotype, all of which indicate that agonism of PDLIM5 is the MoA for an HFrEF therapy 34 .”
He, H., Yin, H., Yu, X., Zhang, Y., Ma, M., Li, D., & Zhu, Q. C. (2021) · Animals · doi:10.3390/ani11041016 · Cited by 21 · see citing works
“As one among them, PDLIM5 is linked to a number of medical problems, including mental illnesses [7] and heart diseases [8], and its expression has caused concern with the progression of gastric cancer [9], lung cancer [10], and breast cancer [11].”
BackgroundLoss of the Cytoskeletal Protein Pdlim7 Predisposes Mice to Heart Defects and Hemostatic Dysfunction
Krcmery, J., Gupta, R., Sadleir, R. W., Ahrens, M. J., Misener, S., Kamide, C., Fitchev, P., Losordo, D. W., Crawford, S. E., & Simon, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080809 · Cited by 21 · see citing works
“However, other PDZLIM proteins have been reported to function in the maintenance of muscle contractility [4,5,8,55], thus it is plausible that Pdlim7 could also function in smooth muscle contraction, and thereby influence blood flow.”
InfluentialZasp regulates integrin activation
Bouaouina, M., Jani, K., Long, J. Y., Czerniecki, S., Morse, E. M., Ellis, S. J., Tanentzapf, G., Schöck, F., & Calderwood, D. (2012) · Journal of Cell Science · doi:10.1242/jcs.103291 · Cited by 21 · see citing works
“…through the costamere, which is consistent with recent data showing that long isoforms of Zasp/Cypher are present in the non-filament fraction of heart tissue together with b1D integrin, whereas the short isoform lacking LIM domains was present only in the filament fraction (Cheng et al., 2010).”
Comparative proteomic analysis reveals heart toxicity induced by chronic arsenic exposure in rats
Huang, Q., Xi, G., Alamdar, A., Zhang, J., & Shen, H. (2017) · Environmental Pollution · doi:10.1016/j.envpol.2017.05.077 · Cited by 21 · see citing works
Hu, X., Dong, J., Geng, P., Sun, Y., Du, W., Zhao, X., Wang, Q., Liu, C., Wang, X., Liu, Y., et al. (2023) · Translational Stroke Research · doi:10.1007/s12975-023-01158-0 · Cited by 20 · see citing works
“Pdlim 5 -/- mice were from Professor Hongqiang Cheng’s lab, and they were generated by targeting the third exon of the murine Enh gene [21].”
Self-citationClark, K. A., & Kadrmas, J. L. (2013) · Cytoskeleton · doi:10.1002/cm.21106 · Cited by 19 · see citing works
“…of the Zasp/Cypher/ALP family of PDZ and LIM domain proteins colocalize with a-actinin in muscle and make critical contributions to myofibrillogenesis and muscle structural integrity [Pashmforoush et al., 2001; Zhou et al., 2001; Jani and Schock, 2007; Han and Beckerle, 2009; Cheng et al., 2010].”
BackgroundCypher and Enigma Homolog Protein Are Essential for Cardiac Development and Embryonic Survival
Mu, Y., Jing, R., Peter, A. K., Lange, S., Lin, L., Zhang, J., Ouyang, K., Fang, X., Veevers, J., Zhou, X., et al. (2015) · Journal of the American Heart Association · doi:10.1161/jaha.115.001950 · Cited by 19 · see citing works
“Although there are no cardiomyopathies yet associated with ENH mutations in humans, we previously reported that global loss of ENH in mice (ENH / ) is associated with dilated cardiomyopathy and disorganization of cardiac Z-lines.(21) Furthermore, ENH forms a protein complex with Cypher short isoform (CypherS) and Cals…”
BackgroundMethodInfluentialSelf-citationTargeting of miR-432 to myozenin1 to regulate myoblast proliferation and differentiation
Ren, R. M., Liu, H., Zhao, S. H., & Cao, J. H. (2016) · Genetics and Molecular Research · doi:10.4238/gmr15049313 · Cited by 19 · see citing works
The insect perspective on Z-disc structure and biology
Schöck, F., & González‐Morales, N. (2022) · Journal of Cell Science · doi:10.1242/jcs.260179 · Cited by 19 · see citing works
“Although Zasp oligomerization has been described in Drosophila, mice with mutations in their two Zasp homologs, Zasp and Enigma (also known as PDLIM3 and PDLIM7), also have smaller sarcomeres than normal, suggesting that a similar oligomerization mechanism occurs in vertebrates (Cheng et al., 2010; Zhou et al., 2001).”
BackgroundCooley, N., Ouyang, K., McMullen, J. R., Kiriazis, H., Sheikh, F., Wei, W., Mu, Y., Du, X., Chen, J., & Woodcock, E. A. (2012) · Circulation Heart Failure · doi:10.1161/circheartfailure.112.972158 · Cited by 18 · see citing works
Self-citationA High-Throughput Screening Platform Targeting PDLIM5 for Pulmonary Hypertension
Cheng, H., Chen, T., Tor, M., Park, D., Zhou, Q., Huang, J. B., Khatib, N., Rong, L., & Zhou, G. (2016) · SLAS DISCOVERY · doi:10.1177/1087057115625924 · Cited by 18 · see citing works
“PDLIM5 can interact with α-actinin, protein kinase C, protein kinase D, and ID2, a DNA transcription inhibitor, and has been implicated in heart disease and mental disorders.(10) We have shown that in PASMC, suppression of PDLIM5 induces TGF-β3, TβR1, TGF-β activity, Smad2, and phosphorylated Smad2/3 as well as nuclea…”
BackgroundSelf-citationGonzález‐Morales, N., Marsh, T. W., Katzemich, A. R., Marescal, O., Xiao, Y. S., & Schöck, F. (2019) · Genetics · doi:10.1534/genetics.119.302217 · Cited by 17 · see citing works
Splicing transitions of the anchoring protein ENH during striated muscle development
Ito, J., Hashimoto, T., Nakamura, S., Aita, Y., Yamazaki, T., Schlegel, W., Takimoto, K., & Maturana, A. D. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.03.142 · Cited by 16 · see citing works
Ito, J., Iijima, M., Yoshimoto, N., Niimi, T., Kuroda, S., & Maturana, A. D. (2015) · Cellular Signalling · doi:10.1016/j.cellsig.2015.09.007 · Cited by 15 · see citing works
“The LIM domains of ENH1 bind to various signaling proteins: Protein Kinase C (PKC) isozymes [7,8], the Protein Kinase D 1 (PKD1) [9], Id2 [10], Calsarcin-1 [11] and, the 5′ Adenosine Monophosphate-activated Protein Kinase (AMPK) [5].”
BackgroundInsulin and Insulin-Like Growth Factor 1 Signaling Preserves Sarcomere Integrity in the Adult Heart
Riehle, C., Weatherford, E. T., McCarty, N. S., Seei, A., Jaishy, B. P., Manivel, R., Galuppo, P., Allamargot, C., Hameed, T., Boudreau, R. L., et al. (2022) · Molecular and Cellular Biology · doi:10.1128/mcb.00163-22 · Cited by 14 · see citing works
“PDLIM5 also interacts with the cytoskeletal protein a-actinin (36), and deletion of PDLIM5 results in DCM (37).”
BackgroundInfluentialThe novel roles of four and a half LIM proteins 1 and 2 in the cardiovascular system.
Chu, P., & Chen, J. (2011) · PubMed · Cited by 14 · see citing works
Self-citationscCompass: An Integrated Multi‐Species scRNA‐seq Database for AI‐Ready
Wang, P., Liu, W., Wang, J., Liu, Y., Li, P., Xu, P., Cui, W., Zhang, R., Long, Q., Hu, Z., et al. (2025) · Advanced Science · doi:10.1002/advs.202500870 · Cited by 17 · see citing works
Self-citationVerdonschot, J. A. J., Robinson, E. L., James, K. N., Mohamed, M. W., Claes, G. R. F., Casas, K. A., Vanhoutte, E. K., Hazebroek, M. R., Kringlen, G., Pasierb, M. M., et al. (2019) · Molecular Genetics & Genomic Medicine · doi:10.1002/mgg3.1049 · Cited by 12 · see citing works
“Subsequent research showed that PDLIM5 undergoes even more extensive splicing and that there are multiple isoforms in the mouse, and 23 transcripts in the human; although only 14 are shown to be protein coding (Cheng et al., 2010; GTEx Consortium, 2013).”
BackgroundInfluentialSantos, W. S., Montoni, F., Eichler, R. A. D. S., Arcos, S. S. S., Andreotti, D. Z., Kisaki, C. Y., Evangelista, K. B., Calacina, H. M., Lima, I. F., Soares, M. A. M., et al. (2022) · Journal of Proteomics · doi:10.1016/j.jprot.2022.104530 · Cited by 12 · see citing works
Copy number variants in Ebstein anomaly
Giannakou, A., Sicko, R. J., Zhang, W., Romitti, P. A., Browne, M. L., Caggana, M., Brody, L. C., Jelliffe‐Pawlowski, L. L., Shaw, G. M., Kay, D. M., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188168 · Cited by 12 · see citing works
Enigma homolog 1 promotes myogenic gene expression and differentiation of C2C12 cells
Ito, J., Takita, M., Takimoto, K., & Maturana, A. D. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.05.016 · Cited by 11 · see citing works
Ντάλλα, Ι., Weng, L.-C. C., Cartwright, J., Hall, A. W., Sveinbjörnsson, G., Tucker, N. R., Choi, S. H., Chaffin, M. D., Roselli, C., Barnes, M. R., et al. (2020) · Apollo (University of Cambridge) · doi:10.17863/cam.53684 · Cited by 11 · see citing works
Wang, Q., Wang, M., Sun, Y., Hu, X., Geng, P., Shu, H., Wang, X., Wang, H., Zhang, J., Cheng, H., et al. (2022) · Acta Pharmacologica Sinica · doi:10.1038/s41401-022-00974-8 · Cited by 11 · see citing works
“Pdlim5mice: Pdlim5 mice were a gift from Professor Hong-qiang Cheng’s lab and were generated by targeting the third exon of the murine ENH gene [25].”
MethodSelf-citationExtracellular vesicles in cardiomyopathies: A narrative review
Rizzuto, A. S., Faggiano, A., Macchi, C., Carugo, S., Perrino, C., & Ruscica, M. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e23765 · Cited by 10 · see citing works
“Cardiomyocyte-specific PDLIM5 knockout mice develop cardiomyopathy, suggesting PDLIM5 to play a major role in cardiac muscle structure and function [46].”
BackgroundSun, B., & Kekenes-Huskey, P. M. (2023) · Quarterly Reviews of Biophysics · doi:10.1017/s003358352300001x · Cited by 9 · see citing works
Ng, Y., Blazev, R., McNamara, J. W., Dutt, M., Molendijk, J., Porrello, E. R., Elliott, D. A., & Parker, B. L. (2024) · Journal of Proteome Research · doi:10.1021/acs.jproteome.3c00716 · Cited by 9 · see citing works
MicroRNA-21-containing microvesicles from tubular epithelial cells promote cardiomyocyte hypertrophy
Di, J., Yang, M., Zhou, H., Li, M., & Zhao, J. (2021) · Renal Failure · doi:10.1080/0886022x.2021.1891098 · Cited by 8 · see citing works
“myocardial contractile dysfunction and dilated cardiomyopathy [20].”
Leveraging Extracellular Non-coding RNAs to Diagnose and Treat Heart Diseases
Zhao, Z., Guo, N., Chen, W., & Zh, W. (2022) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-022-10252-x · Cited by 8 · see citing works
Unraveling Enigma in the Z-Disks
Wang, X., & Su, H. (2010) · Circulation Research · doi:10.1161/circresaha.110.225615 · Cited by 8 · see citing works
Deletion of Enigma Homologue from the Z-disc slows tension development kinetics in mouse myocardium
Gregorich, Z. R., Patel, J. R., Cai, W., Lin, Z., Heurer, R., Fitzsimons, D. P., Moss, R. L., & Ge, Y. (2019) · Journal of General Physiology · doi:10.1085/jgp.201812214 · Cited by 6 · see citing works
“Genotypes were determined from toe clips by PCR with the following primer sets: P1 (5′-GCA GGA AGC ACA CCC AGT AT-3′) versus P2 (5′-TGG TCT CCA ACA TTT CAC CA-3′) to probe for the wildtype allele, and Frtneo (5′-AAT GGG CTG ACC GCT TCC TCGT-3′) versus P4 (5′-TCG GAT GGA TGC TCT CTT CT-3′) to probe for the knockout all…”
BackgroundMethodResultInfluentialWu, C., & Arora, P. K. (2014) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.114.000805 · Cited by 5 · see citing works
scCompass: An integrated cross-species scRNA-seq database for AI-readyPreprint
Wang, P., Liu, W., Wang, J., Liu, Y., Li, P., Xu, P., Cui, W., Zhang, R., Long, Q., Hu, Z., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.12.623138 · Cited by 5 · see citing works
Self-citationExpression of PDLIM5 Spliceosomes and Regulatory Functions on Myogenesis in Pigs
Fu, Y., Li, S., Nie, J., Yan, D., Zhang, B., Hao, X., & Zhang, H. (2024) · Cells · doi:10.3390/cells13080720 · Cited by 4 · see citing works
Cypher/ZASP drives cardiomyocyte maturation via actin-mediated MRTFA-SRF signalling
Lyu, J., Pan, Z., Li, R., Yu, H., Zhang, Y., Wang, D., Yin, X., He, Y., Zhao, L., Chen, S., et al. (2024) · Theranostics · doi:10.7150/thno.98734 · Cited by 5 · see citing works
“Interestingly, ENH (another PDZ-LIM protein) mutant and Cypher-ENH double mutant CMs have reduced sarcomere diameters [46, 47], indicating that ENH may also play a role in mediating CM maturation.”
BackgroundSelf-citationYu, J., Wen-Zhao, Y. A. N., Zhang, X., Zheng, B., Pan, W., Yang, Z., ZHANG, H., Nie, Z.-Y., Ma, Y., Bai, Y., et al. (2023) · 老年心脏病学杂志：英文版 · doi:10.26599/1671-5411.2023.06.002 · Cited by 4 · see citing works
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Mechanisms of Stress-Induced Cardiac Hypertrophy
Frey, N., Olson, E. N., & Hill, J. A. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-381510-1.00035-1 · Cited by 2 · see citing works
Rbpms2 prevents major cardiac defects in cardiomyocyte-specific Rbpms-deficient mice
Shan, L., Dieterich, C., Britto‐Borges, T., Günther, S., Kreher, S., Eibach, Y., Kuenne, C. T., Schneider, A., & Braun, T. W. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.06.013 · Cited by 2 · see citing works
Protein kinase D is essential for embryonic survival through functionally redundant subtypes
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Self-citationHund, T. J. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.717963301.793465201
RNA splicing to cytoskeleton: A new path to cardiomyocyte ploidy and division?
Liu, S., & Martin, J. F. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.04.002
Circulation Research Thematic Synopsis
Editors, T. (2012) · Circulation Research · doi:10.1161/res.0b013e31826396e8
Circulation Research Thematic Synopsis
Editors, T. (2012) · Circulation Research · doi:10.1161/circresaha.112.275891
- Authors
- Cheng, H., Kimura, K., Peter, A. K., Cui, L., Ouyang, K., Shen, T., Liu, Y., Gu, Y., Dalton, N. D., Evans, S. M., Knowlton, K. U., Peterson, K. L., & Chen, J.
- Affiliations
- University of California San Diego (US)
- From the Department of Medicine, University of California–San Diego, La Jolla, Calif.
- ORCID
- Venue
- Circulation Research
- Published
- 2010-08-06
- Volume
- 107
- Issue
- 3
- Pages
- 348-356
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC3684396
- OpenAlex
- W2004101138
- Cited by
- 106
- References
- 45
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 5 · 2022: 8 · 2021: 6 · 2020: 8 · 2019: 6 · 2018: 1 · 2017: 6 · 2016: 9 · 2015: 9 · 2014: 6 · 2013: 8 · 2012: 11
- FWCI
- 6.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (1r01hl106968-01)
- National Heart, Lung, and Blood Institute (R01-HL106968, P01HL046345, R01HL066100, T32HL007444)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiomyopathy and Myosin Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- dilated cardiomyopathy, Z-line, Cypher, sarcomere, cardiac contraction, protein complexes, cardiac-specific knockout mice, striated muscle
- MeSH terms
- Animals, Cardiomyopathy, Dilated, Carrier Proteins, Exons, Microfilament Proteins, Muscle Proteins, Myocardial Contraction, Plasmids, Systole, Polymerase Chain Reaction, Alternative Splicing, Mice, Knockout, Homeodomain Proteins, Protein Isoforms, Adaptor Proteins, Signal Transducing, Mice, LIM Domain Proteins
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