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Tamoxifen treatment ameliorates contractile dysfunction of Duchenne muscular dystrophy stem cell-derived cardiomyocytes on bioengineered substrates

  • Gatheridge, M. A. et al. Identifying non–Duchenne muscular dystrophy–positive and false negative results in prior Duchenne muscular dystrophy newborn screening programs: a review. JAMA Neurol. 73, 111 (2016).

    PubMed 

    Google Scholar 

  • Rahimov, F. & Kunkel, L. M. Cellular and molecular mechanisms underlying muscular dystrophy. J. Cell Biol. 201, 499–510 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bladen, C. L. et al. The TREAT-NMD DMD global database: analysis of more than 7,000 Duchenne muscular dystrophy mutations. Hum. Mutat. 36, 395–402 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gao, Q. Q. & McNally, E. M. The dystrophin complex: structure, function, and implications for therapy. Compr. Physiol. 5, 1223–1239 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Deconinck, N. & Dan, B. Pathophysiology of Duchenne muscular dystrophy: current hypotheses. Pediatr. Neurol. 36, 1–7 (2007).

    PubMed 

    Google Scholar 

  • Spurney, C. F. Cardiomyopathy of Duchenne muscular dystrophy: current understanding and future directions. Muscle Nerve 44, 8–19 (2011).

    PubMed 

    Google Scholar 

  • D’Amario, D. et al. A current approach to heart failure in Duchenne muscular dystrophy. Heart 103, 1770–1779 (2017).

    PubMed 

    Google Scholar 

  • Mourkioti, F. et al. Role of telomere dysfunction in cardiac failure in Duchenne muscular dystrophy. Nat. Cell Biol. 15, 895–904 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chang, A. C. Y. et al. Telomere shortening and metabolic compromise underlie dystrophic cardiomyopathy. Proc. Natl Acad. Sci. USA 113, 13120–13125 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kamdar, F. & Garry, D. J. Dystrophin-deficient cardiomyopathy. J. Am. Coll. Cardiol. 67, 2533–2546 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Adorisio, R. et al. Duchenne dilated cardiomyopathy: cardiac management from prevention to advanced cardiovascular therapies. J. Clin. Med. 9, 3186 (2020).

    CAS 
    PubMed Central 

    Google Scholar 

  • Khairallah, R. J. et al. Microtubules underlie dysfunction in Duchenne muscular dystrophy. Sci. Signal. 5, ra56 (2012).

    PubMed 

    Google Scholar 

  • Birnkrant, D. J. et al. Diagnosis and management of Duchenne muscular dystrophy, part 2: respiratory, cardiac, bone health, and orthopaedic management. Lancet Neurol. 17, 347–361 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheeran, D. et al. Predictors of death in adults with Duchenne muscular dystrophy-associated cardiomyopathy. J. Am. Heart Assoc. 6, e006340 (2021).

    Google Scholar 

  • McNally, E. M. et al. Contemporary cardiac issues in Duchenne muscular dystrophy. Circulation 131, 1590–1598 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Spurney, C. et al. Cooperative international neuromuscular research group Duchenne natural history study demonstrates insufficient diagnosis and treatment of cardiomyopathy in Duchenne muscular dystrophy. Muscle Nerve 50, 250–256 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gayi, E. et al. Repurposing the selective oestrogen receptor modulator tamoxifen for the treatment of Duchenne muscular dystrophy. Chimia 72, 238–240 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Dorchies, O. M. et al. The anticancer drug Tamoxifen counteracts the pathology in a mouse model of Duchenne muscular dystrophy. Am. J. Pathol. 182, 485–504 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Arnott, J., Martinkovich, S., Planey, S. L. & Shah, D. Selective estrogen receptor modulators: tissue specificity and clinical utility. Clin. Interv. Aging 1437, https://doi.org/10.2147/CIA.S66690 (2014).

  • Mahmoodzadeh, S. et al. Estrogen receptor alpha up‐regulation and redistribution in human heart failure. FASEB J. 20, 926–934 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Kallen, A. N. & Pal, L. Cardiovascular disease and ovarian function. Curr. Opin. Obstet. Gynecol. 23, 258–267 (2011).

    PubMed 

    Google Scholar 

  • Yang, X.-P. & Reckelhoff, J. F. Estrogen, hormonal replacement therapy and cardiovascular disease. Curr. Opin. Nephrol. Hypertens. 20, 133–138 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Koot, R. W., Amelink, G. J., Blankenstein, M. A. & Bär, P. R. Tamoxifen and oestrogen both protect the rat muscle against physiological damage. J. Steroid Biochem. Mol. Biol. 40, 689–IN10 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • Custódio, JoséB. A., Dinis, T. C. P., Almeida, L. M. & Madeira, V. M. C. Tamoxifen and hydroxytamoxifen as intramembraneous inhibitors of lipid peroxidation. Evidence for peroxyl radical scavenging activity. Biochem. Pharmacol. 47, 1989–1998 (1994).

    PubMed 

    Google Scholar 

  • Dodds, M. L., Kargacin, M. E. & Kargacin, G. J. Effects of anti-oestrogens and β-estradiol on calcium uptake by cardiac sarcoplasmic reticulum. Br. J. Pharmacol. 132, 1374–1382 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Patel, B. M. & Desai, V. J. Beneficial role of tamoxifen in experimentally induced cardiac hypertrophy. Pharmacol. Rep. 66, 264–272 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Nagy, S. et al. Tamoxifen in Duchenne muscular dystrophy (TAMDMD): study protocol for a multicenter, randomized, placebo-controlled, double-blind phase 3 trial. Trials 20, 637 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chang, A. C. Y. et al. Telomere shortening is a hallmark of genetic cardiomyopathies. Proc. Natl Acad. Sci. USA 115, 9276–9281 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, J. Z. et al. A human iPSC double-reporter system enables purification of cardiac lineage subpopulations with distinct function and drug response profiles. Cell Stem Cell 24, 802–811.e5 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wu, H. et al. Modelling diastolic dysfunction in induced pluripotent stem cell-derived cardiomyocytes from hypertrophic cardiomyopathy patients. Eur. Heart J. 40, 3685–3695 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chang, A. C. Y. et al. Increased tissue stiffness triggers contractile dysfunction and telomere shortening in dystrophic cardiomyocytes. Stem Cell Rep. 16, 1–13 (2021).

    Google Scholar 

  • Yang, X., Pabon, L. & Murry, C. E. Engineering adolescence: maturation of human pluripotent stem cell–derived cardiomyocytes. Circ. Res. 114, 511–523 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Knöll, R., Buyandelger, B. & Lab, M. The sarcomeric Z-disc and Z-discopathies. J. Biomed. Biotechnol. 2011, 1–12 (2011).

  • Louch, W. E. Methods in cardiomyocyte isolation, culture, and gene transfer. J. Mol. Cell. Cardiol. 51, 288–298 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • da Rocha, A. M. et al. hiPSC-CM monolayer maturation state determines drug responsiveness in high throughput pro-arrhythmia screen. Sci. Rep. 7, 13834 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Madl, C. M., Flaig, I. A., Holbrook, C. A., Wang, Y. X. & Blau, H. M. Biophysical matrix cues from the regenerating niche direct muscle stem cell fate in engineered microenvironments. Biomaterials 275, 120973 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Paik, D. T., Chandy, M. & Wu, J. C. Patient and disease-specific induced pluripotent stem cells for discovery of personalized cardiovascular drugs and therapeutics. Pharmacol. Rev. 72, 320–342 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ribeiro, A. J. S. et al. Contractility of single cardiomyocytes differentiated from pluripotent stem cells depends on physiological shape and substrate stiffness. Proc. Natl Acad. Sci. USA 112, 12705–12710 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schroer, A., Pardon, G., Castillo, E., Blair, C. & Pruitt, B. Engineering hiPSC cardiomyocyte in vitro model systems for functional and structural assessment. Prog. Biophys. Mol. Biol. 144, 3–15 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Huebsch, N. et al. Automated video-based analysis of contractility and calcium flux in human-induced pluripotent stem cell-derived cardiomyocytes cultured over different spatial scales. Tissue Eng. Part C. Methods 21, 467–479 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mathur, A. et al. Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep. 5, 8883 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sakamoto, T. et al. A critical role for estrogen-related receptor signaling in cardiac maturation. Circ. Res. 126, 1685–1702 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Guan, X. et al. Dystrophin-deficient cardiomyocytes derived from human urine: new biologic reagents for drug discovery. Stem Cell Res. 12, 467–480 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Pioner, J. M. et al. Absence of full-length dystrophin impairs normal maturation and contraction of cardiomyocytes derived from human-induced pluripotent stem cells. Cardiovasc. Res. 116, 368–382 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Dick, E. et al. Two new protocols to enhance the production and isolation of human induced pluripotent stem cell lines. Stem Cell Res. 6, 158–167 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Dick, E. et al. Exon skipping and gene transfer restore dystrophin expression in human induced pluripotent stem cells-cardiomyocytes harboring DMD mutations. Stem Cells Dev. 22, 2714–2724 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kaspar, R. W. et al. Analysis of dystrophin deletion mutations predicts age of cardiomyopathy onset in Becker muscular dystrophy. Circ. Cardiovasc. Genet. 2, 544–551 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Austin, R. C., Howard, P. L., D’Souza, V. N., Klamut, H. J. & Ray, P. N. Cloning and characterization of alternatively spliced isoforms of Dp71. Hum. Mol. Genet. 4, 1475–1483 (1995).

    CAS 
    PubMed 

    Google Scholar 

  • Jelinkova, S. et al. DMD pluripotent stem cell derived cardiac cells recapitulate in vitro human cardiac pathophysiology. Front. Bioeng. Biotechnol. 8, 535 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Barresi, R. & Campbell, K. P. Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199–207 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Kamdar, F. et al. Stem cell-derived cardiomyocytes and beta-adrenergic receptor blockade in Duchenne muscular dystrophy cardiomyopathy. J. Am. Coll. Cardiol. 75, 1159–1174 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Ropero, A. B. et al. Heart estrogen receptor alpha: distinct membrane and nuclear distribution patterns and regulation by estrogen. J. Mol. Cell. Cardiol. 41, 496–510 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Lizotte, E., Grandy, S. A., Tremblay, A., Allen, B. G. & Fiset, C. Expression, distribution and regulation of sex steroid hormone receptors in mouse heart. Cell. Physiol. Biochem. 23, 075–086 (2009).

    CAS 

    Google Scholar 

  • Yaşar, P., Ayaz, G., User, S. D., Güpür, G. & Muyan, M. Molecular mechanism of estrogen–estrogen receptor signaling. Reprod. Med. Biol. 16, 4–20 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Jonsson, M. K. B., Wang, Q.-D. & Becker, B. Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes. ASSAY Drug Dev. Technol. 9, 589–599 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lemoine, M. D. et al. Human induced pluripotent stem cell–derived engineered heart tissue as a sensitive test system for QT prolongation and arrhythmic triggers. Circ. Arrhythm. Electrophysiol. 11, e006035 (2018).

  • Navarrete, E. G. et al. Screening drug-induced arrhythmia using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 128, S3–S13 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Weiss, J. N., Garfinkel, A., Karagueuzian, H. S., Chen, P.-S. & Qu, Z. Early afterdepolarizations and cardiac arrhythmias. Heart Rhythm 7, 1891–1899 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Prosser, B. L., Ward, C. W. & Lederer, W. J. X-ROS signaling: rapid mechano-chemo transduction in heart. Science 333, 1440–1445 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Bostick, B., Yue, Y. & Duan, D. Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle Nerve 42, 600–603 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sacco, A. et al. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059–1071 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jordan, V. C. Tamoxifen: a most unlikely pioneering medicine. Nat. Rev. Drug Discov. 2, 205–213 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • Cui, J., Shen, Y. & Li, R. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol. Med. 19, 197–209 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Grumbach, M. M. & Auchus, R. J. Estrogen: consequences and implications of human mutations in synthesis and action. J. Clin. Endocrinol. Metab. 84, 4677–4694 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • Yao, J., Deng, K., Huang, J., Zeng, R. & Zuo, J. Progress in the understanding of the mechanism of tamoxifen resistance in breast cancer. Front. Pharmacol. 11, 592912 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brzozowski, A. M. et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389, 753–758 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Shiau, A. K. et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95, 927–937 (1998).

    CAS 
    PubMed 

    Google Scholar 

  • Meyer, M. R., Haas, E., Prossnitz, E. R. & Barton, M. Non-genomic regulation of vascular cell function and growth by estrogen. Mol. Cell. Endocrinol. 308, 9–16 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Filardo, E. J., Quinn, J. A., Frackelton, A. R. & Bland, K. I. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16, 70–84 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Jiang, C. et al. Effect of 17β‐oestradiol on contraction, Ca2+ current and intracellular free Ca2+ in guinea‐pig isolated cardiac myocytes. Br. J. Pharmacol. 106, 739–745 (1992).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nordenskjöld, B. et al. Coronary heart disease mortality after 5 years of adjuvant tamoxifen therapy: results from a randomized trial. JNCI J. Natl Cancer Inst. 97, 1609–1610 (2005).

    PubMed 

    Google Scholar 

  • Gylling, H. et al. Tamoxifen and toremifene lower serum cholesterol by inhibition of delta 8-cholesterol conversion to lathosterol in women with breast cancer. J. Clin. Oncol. 13, 2900–2905 (1995).

    CAS 
    PubMed 

    Google Scholar 

  • Holleran, A. L., Lindenthal, B., Aldaghlas, T. A. & Kelleher, J. K. Effect of tamoxifen on cholesterol synthesis in HepG2 cells and cultured rat hepatocytes. Metabolism 47, 1504–1513 (1998).

    CAS 
    PubMed 

    Google Scholar 

  • Medina, P. de. et al. Tamoxifen is a potent inhibitor of cholesterol esterification and prevents the formation of foam cells. J. Pharmacol. Exp. Ther. 308, 1165–1173 (2004).

    PubMed 

    Google Scholar 

  • Love, R. R. et al. Effects of tamoxifen on cardiovascular risk factors in postmenopausal women. Ann. Intern. Med. 115, 860 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • Lian, X. et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl Acad. Sci. USA 109, E1848–E1857 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Burridge, P. W. et al. Chemically defined generation of human cardiomyocytes. Nat. Methods 11, 855–860 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tohyama, S. et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 12, 127–137 (2013).

    CAS 

    Google Scholar 

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