Human induced pluripotent stem cell–derived cardiomyocytes as an in vitro model for coxsackievirus B3–induced myocarditis and antiviral drug screening platform
Open accessAbstract
Rationale: Viral myocarditis is a life-threatening illness that may lead to heart failure or cardiac arrhythmias. A major causative agent for viral myocarditis is the B3 strain of coxsackievirus, a positive-sense RNA enterovirus. However, human cardiac tissues are difficult to procure in sufficient enough quantities for studying the mechanisms of cardiac-specific viral infection. Objective: This study examined whether human induced pluripotent stem cell–derived cardiomyocytes (hiPSC-CMs) could be used to model the pathogenic processes of coxsackievirus-induced viral myocarditis and to screen antiviral therapeutics for efficacy. Methods and Results: hiPSC-CMs were infected with a luciferase-expressing coxsackievirus B3 strain (CVB3-Luc). Brightfield microscopy, immunofluorescence, and calcium imaging were used to characterize virally infected hiPSC-CMs for alterations in cellular morphology and calcium handling. Viral proliferation in hiPSC-CMs was quantified using bioluminescence imaging. Antiviral compounds including interferonβ1, ribavirin, pyrrolidine dithiocarbamate, and fluoxetine were tested for their capacity to abrogate CVB3-Luc proliferation in hiPSC-CMs in vitro. The ability of these compounds to reduce CVB3-Luc proliferation in hiPSC-CMs was consistent with reported drug effects in previous studies. Mechanistic analyses via gene expression profiling of hiPSC-CMs infected with CVB3-Luc revealed an activation of viral RNA and protein clearance pathways after interferonβ1 treatment. Conclusions: This study demonstrates that hiPSC-CMs express the coxsackievirus and adenovirus receptor, are susceptible to coxsackievirus infection, and can be used to predict antiviral drug efficacy. Our results suggest that the hiPSC-CM/CVB3-Luc assay is a sensitive platform that can screen novel antiviral therapeutics for their effectiveness in a high-throughput fashion.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Using patient-specific hiPSC-CMs, researchers can model various CVDs such as long QT syndrome, LV non-compaction, hypertrophic cardiomyopathy, and dilated cardiomyopathy.
“In addition, using patient-specific hiPSC-CMs, researchers are able to model various CVDs such as long QT syndrome, LV non-compaction, hypertrophic cardiomyopathy and dilated cardiomyopathy [217,423,424].”
From Cardiovascular disease models: A game changing paradigm in drug discovery and screening (2019) · cites this paper as [424]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells
Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., et al. (2007) · Science · doi:10.1126/science.1151526 · Cited by 10,310 · see citing works
Antiviral Actions of Interferons
Samuel, C. E. (2001) · Clinical Microbiology Reviews · doi:10.1128/cmr.14.4.778-809.2001 · Cited by 2,743 · see citing works
Sudden Deaths in Young Competitive Athletes
Maron, B. J., Doerer, J. J., Haas, T. S., Tierney, D. M., & Mueller, F. O. (2009) · Circulation · doi:10.1161/circulationaha.108.804617 · Cited by 2,075 · see citing works
Lian, X., Hsiao, C., Wilson, G., Zhu, K., Hazeltine, L. B., Azarin, S. M., Raval, K. K., Zhang, J., Kamp, T. J., & Palecek, S. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200250109 · Cited by 1,717 · see citing works
Claycomb, W. C., Lanson, N. A., Stallworth, B. S., Egeland, D. B., Delcarpio, J. B., Bahinski, A., & Izzo, N. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.2979 · Cited by 1,546 · see citing works
Cooper, L. T. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0800028 · Cited by 1,317 · see citing works
Tohyama, S., Hattori, F., Sano, M., Hishiki, T., Nagahata, Y., Matsuura, T., Hashimoto, H., Suzuki, T., Yamashita, H., Satoh, Y., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.09.013 · Cited by 1,045 · see citing works
Feldman, A. M., & McNamara, D. M. (2000) · New England Journal of Medicine · doi:10.1056/nejm200011093431908 · Cited by 962 · see citing works
The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen
Crotty, S., Maag, D., Arnold, J. J., Zhong, W., Lau, J. Y. N., Hong, Z., Andino, R., & Cameron, C. E. (2000) · Nature Medicine · doi:10.1038/82191 · Cited by 823 · see citing works
Structural and Functional Maturation of Cardiomyocytes Derived from Human Pluripotent Stem Cells
Lundy, S. D., Zhu, W.-Z., Regnier, M., & Laflamme, M. A. (2013) · Stem Cells and Development · doi:10.1089/scd.2012.0490 · Cited by 738 · see citing works
The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction
Cohen, C. J., Shieh, J. T. C., Pickles, R. J., Okegawa, T., Hsieh, J., & Bergelson, J. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261452898 · Cited by 702 · see citing works
Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy
Sun, N., Yazawa, M., Liu, J., Han, L., Sanchez-Freire, V., Abilez, O. J., Navarrete, E. G., Hu, S., Wang, L., Lee, A., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003552 · Cited by 696 · see citing works
Self-citationBurridge, P. W., Keller, G., Gold, J. D., & Wu, J. C. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2011.12.013 · Cited by 670 · see citing works
Self-citationBowles, N. E., Olsen, E. G. J., Richardson, P. J., & ARCHARD, L. C. (1986) · The Lancet · doi:10.1016/s0140-6736(86)91837-4 · Cited by 601 · see citing works
Badorff, C., Lee, G.-H., Lamphear, B. J., Martone, M. E., Campbell, K. P., Rhoads, R. E., & Knowlton, K. U. (1999) · Nature Medicine · doi:10.1038/6543 · Cited by 574 · see citing works
Active Myocarditis in the Spectrum of Acute Dilated Cardiomyopathies
DEC, G. W., Palacios, I. F., Fallon, J. T., Aretz, H. T., Mills, J. L., Lee, D. C.-S., & Johnson, R. A. (1985) · New England Journal of Medicine · doi:10.1056/nejm198504043121404 · Cited by 562 · see citing works
Baughman, K. L. (2006) · Circulation · doi:10.1161/circulationaha.105.589663 · Cited by 543 · see citing works
Kühl, U., Pauschinger, M., Schwimmbeck, P. L., Seeberg, B., Lober, C., Noutsias, M., Poller, W. C., & Schultheiß, H. (2003) · Circulation · doi:10.1161/01.cir.0000072766.67150.51 · Cited by 499 · see citing works
Sudden unexpected death in persons <40 years of age
Drory, Y., Turetz, Y., Hiss, Y., Lev, B. I., Fisman, E. Z., Pines, A., & Kramer, M. R. (1991) · The American Journal of Cardiology · doi:10.1016/0002-9149(91)90251-f · Cited by 422 · see citing works
Gale, M., & Katze, M. G. (1998) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(97)00165-4 · Cited by 388 · see citing works
Cardiac fatty acid uptake and transport in health and disease
Vusse, G. J. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00263-1 · Cited by 318 · see citing works
Mukherjee, A., Morosky, S. A., Delorme‐Axford, E., Dybdahl-Sissoko, N., Oberste, M. S., Wang, T., & Coyne, C. B. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1001311 · Cited by 306 · see citing works
Mitcheson, J. S. (1998) · Cardiovascular Research · doi:10.1016/s0008-6363(98)00128-x · Cited by 251 · see citing works
Drug-induced long QT and torsade de pointes: recent advances
Kannankeril, P. J., & Roden, D. M. (2006) · Current Opinion in Cardiology · doi:10.1097/hco.0b013e32801129eb · Cited by 230 · see citing works
Human Stem Cells for Modeling Heart Disease and for Drug Discovery
Matsa, E., Burridge, P. W., & Wu, J. C. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008921 · Cited by 210 · see citing works
Self-citationNoutsias, M., Fechner, H., de Jonge, H. W., Wang, X., Dekkers, D. H. W., Houtsmuller, A. B., Pauschinger, M., Bergelson, J. M., Warraich, R. S., Yacoub, M. H., et al. (2001) · Circulation · doi:10.1161/01.cir.104.3.275 · Cited by 203 · see citing works
GBF1, a Guanine Nucleotide Exchange Factor for Arf, Is Crucial for Coxsackievirus B3 RNA Replication
Lanke, K. H. W., van der Schaar, H. M., Belov, G. A., Feng, Q., Duijsings, D., Jackson, C. L., Ehrenfeld, E., & van Kuppeveld, F. J. M. (2009) · Journal of Virology · doi:10.1128/jvi.01244-09 · Cited by 179 · see citing works
Cunningham, M. W., Antone, S. M., Gulizia, J. M., McManus, B. M., Fischetti, V. A., & Gauntt, C. J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.4.1320 · Cited by 176 · see citing works
The group B coxsackieviruses and myocarditis
Kim, K., Hufnagel, G., Chapman, N. M., & Tracy, S. (2001) · Reviews in Medical Virology · doi:10.1002/rmv.326 · Cited by 174 · see citing works
Carthy, C. M., Granville, D. J., Watson, K. A., Anderson, D. R., Wilson, J. E., Yang, D., Hunt, D. W. C., & McManus, B. M. (1998) · Journal of Virology · doi:10.1128/jvi.72.9.7669-7675.1998 · Cited by 172 · see citing works
Nalbantoglu, J. N., Pari, G., Karpati, G., & Holland, P. C. (1999) · Human Gene Therapy · doi:10.1089/10430349950018409 · Cited by 169 · see citing works
Protective Role for Interferon-β in Coxsackievirus B3 Infection
Deonarain, R., Cerullo, D., Fuse, K., Liu, P. P., & Fish, E. N. (2004) · Circulation · doi:10.1161/01.cir.0000136824.73458.20 · Cited by 160 · see citing works
Coxsackie B3 virus can replicate in cultured human foetal heart cells and is inhibited by interferon
Kandolf, R., Canu, A., & Hofschneider, P. H. (1985) · Journal of Molecular and Cellular Cardiology · doi:10.1016/s0022-2828(85)80019-5 · Cited by 136 · see citing works
Coxsackievirus-adenovirus receptor (CAR) is essential for early embryonic cardiac development
Dorner, A. A., Wegmann, F., Butz, S., Wolburg‐Buchholz, K., Wolburg, H., Mack, A. F., Nasdala, I., August, B. K., Westermann, J., Rathjen, F. G., et al. (2005) · Journal of Cell Science · doi:10.1242/jcs.02476 · Cited by 128 · see citing works
Treatment of picornavirus infections
Rotbart, H. A. (2002) · Antiviral Research · doi:10.1016/s0166-3542(01)00206-6 · Cited by 110 · see citing works
Si, X., McManus, B. M., Zhang, J., Ji, Y., Cheung, C., Esfandiarei, M., Suarez, A., Morgan, A., & Luo, H. (2005) · Journal of Virology · doi:10.1128/jvi.79.13.8014-8023.2005 · Cited by 110 · see citing works
Fluoxetine is a potent inhibitor of coxsackievirus replication
Zuo, J., Quinn, K. K., Kye, S., Cooper, P., Damoiseaux, R., & Krogstad, P. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00983-12 · Cited by 104 · see citing works
Churko, J. M., Burridge, P. W., & Wu, J. C. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-511-8_7 · Cited by 95 · see citing works
Self-citationCoxsackievirus and adenovirus receptor is essential for cardiomyocyte development
Asher, D. R., Cerny, A., Weiler, S. R., Horner, J. W., Keeler, M. L., Neptune, M. A., Jones, S. N., Bronson, R. T., DePinho, R. A., & Finberg, R. W. (2005) · genesis · doi:10.1002/gene.20127 · Cited by 92 · see citing works
Fechner, H., Noutsias, M., Tschöepe, C., Hinze, K., Wang, X., Escher, F., Pauschinger, M., Dekkers, D. H. W., Vetter, R., Paul, M., et al. (2003) · Circulation · doi:10.1161/01.cir.0000050150.27478.c5 · Cited by 92 · see citing works
Cardiomyocyte apoptosis in experimental coxsackievirus B3 myocarditis.
Saraste, A., Arola, A., Vuorinen, T., Kytö, V., Kallajoki, M., Pulkki, K., Voipio-Pulkki, L., & Hyypiä, T. (2003) · Cardiovascular pathology · doi:10.1016/s1054-8807(03)00077-2 · Cited by 90 · see citing works
CVB Infection and Mechanisms of Viral Cardiomyopathy
Knowlton, K. U. (2008) · Springer eBooks · doi:10.1007/978-3-540-75546-3_15 · Cited by 82 · see citing works
Lanke, K. H. W., Krenn, B. M., Melchers, W. J. G., Seipelt, J., & van Kuppeveld, F. J. M. (2007) · Journal of General Virology · doi:10.1099/vir.0.82634-0 · Cited by 72 · see citing works
Virus-Host Coevolution in a Persistently Coxsackievirus B3-Infected Cardiomyocyte Cell Line
Pinkert, S., Klingel, K., Lindig, V., Dörner, A., Zeichhardt, H., Spiller, O. B., & Fechner, H. (2011) · Journal of Virology · doi:10.1128/jvi.00621-11 · Cited by 58 · see citing works
Lombardi, R., Bell, A., Senthil, V., Sidhu, J. S., Noseda, M., Roberts, R., & Marian, A. J. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn078 · Cited by 57 · see citing works
Kashimura, T., Kodama, M., Hotta, Y., Hosoya, J., Yoshida, K., Ozawa, T., Watanabe, R., Okura, Y., Kato, K., Hanawa, H., et al. (2004) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-003-0925-9 · Cited by 52 · see citing works
Fluoxetine-induced cardiotoxicity with response to bicarbonate therapy
Graudins, A., Vossler, C., & Wang, R. T. (1997) · The American Journal of Emergency Medicine · doi:10.1016/s0735-6757(97)90194-7 · Cited by 42 · see citing works
Patient-Specific Stem Cells and Cardiovascular Drug Discovery
Mordwinkin, N. M., Lee, A. S., & Wu, J. C. (2013) · JAMA · doi:10.1001/jama.2013.282409 · Cited by 40 · see citing works
Self-citationHeim, A., Grumbach, I. M., Pring‐Åkerblom, P., Stille‐Siegener, M., Müller, G., Kandolf, R., & Figulla, H. (1997) · Antiviral Research · doi:10.1016/s0166-3542(97)01028-0 · Cited by 34 · see citing works
Scassa, M. É., de Giusti, C. J., Questa, M., Prêtre, G., Videla-Richardson, G. A., Blüguermann, C., Romorini, L., Ferrer, M. F., Sevlever, G. E., Miriuka, S., et al. (2010) · Stem Cell Research · doi:10.1016/j.scr.2010.09.002 · Cited by 22 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [31]Kim KS Hufnagel G Chapman NM Tracy S The group b coxsackieviruses and myocarditis Reviews in Medical Virology 2001 11 355 368 11746998
Cited by
Sorted by citations
Myocarditis and inflammatory cardiomyopathy: current evidence and future directions
Tschöpe, C., Ammirati, E., Bozkurt, B., Caforio, A. L. P., Cooper, L. T., Felix, S. B., Hare, J. M., Heidecker, B., Heymans, S., Hübner, N., et al. (2021) · Nature Reviews Cardiology · doi:10.1038/s41569-020-00435-x · Cited by 1,217 · see citing works
Viral myocarditis—diagnosis, treatment options, and current controversies
Pollack, A., Kontorovich, A. R., Fuster, V., & Dec, G. W. (2015) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2015.108 · Cited by 657 · see citing works
Sharma, A., Burridge, P. W., McKeithan, W. L., Serrano, R., Shukla, P., Sayed, N., Churko, J. M., Kitani, T., Wu, H., Holmström, A., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf2584 · Cited by 404 · see citing works
Self-citationHuman iPSC-Derived Cardiomyocytes Are Susceptible to SARS-CoV-2 Infection
Sharma, A., Garcia, G., Wang, Y., Plummer, J., Morizono, K., Arumugaswami, V., & Svendsen, C. N. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2020.100052 · Cited by 318 · see citing works
Self-citationRNA–protein interaction detection in living cells
Ramanathan, M., Majzoub, K., Rao, D. S., Neela, P. H., Zarnegar, B. J., Mondal, S., Roth, J. G., Gai, H., Kovalski, J. R., Siprashvili, Z., et al. (2018) · Nature Methods · doi:10.1038/nmeth.4601 · Cited by 301 · see citing works
Self-citationDenning, C., Borgdorff, V., Crutchley, J., Firth, K. S. A., George, V., Kalra, S., Kondrashov, A., Hoang, M. D., Mosqueira, D., Patel, A., et al. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.10.014 · Cited by 293 · see citing works
Translation of Human iPSCs: From Clinical Trial in a Dish to Precision Medicine
Sayed, N., Liu, C., & Wu, J. C. (2016) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2016.01.083 · Cited by 263 · see citing works
Self-citationInduced Pluripotent Stem Cells 10 Years Later
Yoshida, Y., & Yamanaka, S. (2017) · Circulation Research · doi:10.1161/circresaha.117.311080 · Cited by 266 · see citing works
Musunuru, K., Sheikh, F., Gupta, R. M., Houser, S. R., Maher, K. O., Milan, D. J., Terzic, A., & Wu, J. C. (2018) · Circulation Genomic and Precision Medicine · doi:10.1161/hcg.0000000000000043 · Cited by 230 · see citing works
Self-citationCardiovascular disease models: A game changing paradigm in drug discovery and screening
Savoji, H., Mohammadi, M. H., Rafatian, N., Toroghi, M. K., Wang, E. Y., Zhao, Y., Korolj, A., Ahadian, S., & Radisic, M. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.09.036 · Cited by 223 · see citing works
Kitani, T., Ong, S.-G., Lam, C. K., Rhee, J.-W., Zhang, J. Z., Oikonomopoulos, A., Ma, N., Tian, L., Lee, J., Telli, M. L., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.037357 · Cited by 200 · see citing works
Self-citationInduced pluripotent stem cells: at the heart of cardiovascular precision medicine
Chen, I. Y., Matsa, E., & Wu, J. C. (2016) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2016.36 · Cited by 191 · see citing works
Self-citationRoshanbinfar, K., Vogt, L., Greber, B., Diecke, S., Boccaccini, A. R., Scheibel, T., & Engel, F. B. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201803951 · Cited by 193 · see citing works
Self-citationFeaster, T. K., Cadar, A. G., Wang, L., Williams, C. H., Chun, Y. W., Hempel, J. E., Bloodworth, N. C., Merryman, W. D., Lim, C. C., Wu, J. C., et al. (2015) · Circulation Research · doi:10.1161/circresaha.115.307580 · Cited by 178 · see citing works
Self-citationComparable calcium handling of human iPSC-derived cardiomyocytes generated by multiple laboratories
Hwang, H. S., Kryshtal, D. O., Feaster, T. K., Sánchez-Freire, V., Zhang, J., Kamp, T. J., Hong, C. C., Wu, J. C., & Knollmann, B. C. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.05.003 · Cited by 173 · see citing works
Self-citationYücel, G., Zhao, Z., El‐Battrawy, I., Lan, H., Lang, S., Li, X., Buljubasic, F., Zimmermann, W., Cyganek, L., Utikal, J. S., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-03147-4 · Cited by 163 · see citing works
Smith, A. S. T., Macadangdang, J., Leung, W., Laflamme, M., & Kim, D.-H. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.12.002 · Cited by 137 · see citing works
Use of human induced pluripotent stem cell–derived cardiomyocytes to assess drug cardiotoxicity
Sharma, A., McKeithan, W. L., Serrano, R., Kitani, T., Burridge, P. W., del Álamo, J. C., Mercola, M. A., & Wu, J. C. (2018) · Nature Protocols · doi:10.1038/s41596-018-0076-8 · Cited by 141 · see citing works
Self-citationTFRC upregulation promotes ferroptosis in CVB3 infection via nucleus recruitment of Sp1
Lu, Y., Hu, Y., Wu, Z., Li, Y., Kong, M., Kang, Z., Zuoyuan, B., & Yang, Z. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05027-w · Cited by 133 · see citing works
Mitoconfusion: Noncanonical Functioning of Dynamism Factors in Static Mitochondria of the Heart
Song, M., & Dorn, G. W. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2014.12.019 · Cited by 127 · see citing works
Autosomal Recessive Cardiomyopathy Presenting as Acute Myocarditis
Belkaya, S., Kontorovich, A., Byun, M., Mulero‐Navarro, S., Bajolle, F., Cobat, A., Josowitz, R., Itan, Y., Quint, R., Lorenzo, L., et al. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.01.043 · Cited by 132 · see citing works
Roshanbinfar, K., Mohammadi, Z., Mesgar, A. S.-M., Dehghan, M. M., Oommen, O. P., Hilborn, J. G., & Engel, F. B. (2019) · Biomaterials Science · doi:10.1039/c9bm00434c · Cited by 115 · see citing works
Sharma, A., Li, G., Rajarajan, K., Hamaguchi, R., Burridge, P. W., & Wu, S. M. (2015) · Journal of Visualized Experiments · doi:10.3791/52628 · Cited by 110 · see citing works
Self-citationRecent progress in understanding coxsackievirus replication, dissemination, and pathogenesis
Sin, J., Mangale, V., Thienphrapa, W., Gottlieb, R. A., & Feuer, R. (2015) · Virology · doi:10.1016/j.virol.2015.06.006 · Cited by 106 · see citing works
Matsa, E., Ahrens, J. H., & Wu, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00036.2015 · Cited by 105 · see citing works
Self-citationAntitumor/antiviral carbon quantum dots based on carrageenan and pullulan
Emam, H. E., & Ahmed, H. B. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.12.151 · Cited by 102 · see citing works
Ergir, E., Oliver-De La Cruz, J., Fernandes, S., Cassani, M., Niro, F., Pereira-Sousa, D., Vrbský, J., Vinarský, V., Perestrelo, A. R., Debellis, D., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-22225-w · Cited by 99 · see citing works
Native cardiac environment and its impact on engineering cardiac tissue
Schwach, V., & Passier, R. C. (2019) · Biomaterials Science · doi:10.1039/c8bm01348a · Cited by 92 · see citing works
van der Velden, J., Asselbergs, F. W., Bakkers, J., Batkai, S., Bertrand, L., Bezzina, C. R., Bot, I., Brundel, B. J. J. M., Carrier, L., Chamuleau, S. A. J., et al. (2022) · Cardiovascular Research · doi:10.1093/cvr/cvab370 · Cited by 88 · see citing works
Choi, S. W., Shin, J. S., Park, S., Jung, E., Park, Y.-G., Lee, J., Kim, S. J., Park, H., Lee, J., Park, S., et al. (2020) · Antiviral Research · doi:10.1016/j.antiviral.2020.104955 · Cited by 83 · see citing works
Cheng, Y., Hsieh, M. L., Lin, C., Chang, C. M., Huang, C.-Y., Puntney, R., Moy, A., Ting, C.-Y., Chan, D. Z. H., Nicholson, M. W., et al. (2023) · Circulation · doi:10.1161/circulationaha.122.061736 · Cited by 77 · see citing works
Human Induced Pluripotent Stem-Cell-Derived Cardiomyocytes as Models for Genetic Cardiomyopathies
Brodehl, A., Ebbinghaus, H., Deutsch, M., Gummert, J., Gärtner, A., Ratnavadivel, S., & Milting, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184381 · Cited by 58 · see citing works
Findley, A. S., Monziani, A., Richards, A. L., Rhodes, K., Ward, M. C., Kalita, C. A., Alazizi, A., Pazokitoroudi, A., Sankararaman, S., Wen, X., et al. (2021) · eLife · doi:10.7554/elife.67077 · Cited by 66 · see citing works
van Mil, A., Balk, G. M., Neef, K., Buikema, J. W., Asselbergs, F. W., Wu, S. M., Doevendans, P. A., & Sluijter, J. P. G. (2018) · Cardiovascular Research · doi:10.1093/cvr/cvy208 · Cited by 65 · see citing works
Self-citationModelling cadmium‐induced cardiotoxicity using human pluripotent stem cell‐derived cardiomyocytes
Shen, J., Wang, X., Zhou, D., Li, T., Tang, L. F. P., Gong, T., Su, J., & Liang, P. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13702 · Cited by 54 · see citing works
Self-citationZhou, R., Xu, A., Gingold, J. A., Strong, L. C., Zhao, R., & Lee, D. (2017) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2017.07.004 · Cited by 52 · see citing works
Ebert, A., Diecke, S., Chen, I. Y., & Wu, J. C. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201504395 · Cited by 52 · see citing works
Self-citationCai, C., Fang, J., Guo, P., Wang, Q., Hong, H., Moslehi, J. J., & Cheng, F. (2018) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.7b00641 · Cited by 52 · see citing works
Macrophages enhance contractile force in iPSC-derived human engineered cardiac tissue
Lock, R. I., Graney, P. L., Tavakol, D. N., Nash, T. R., Kim, Y., Sanchez, E., Morsink, M. A. J., Ning, D., Chen, C., Fleischer, S., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114302 · Cited by 48 · see citing works
Burridge, P. W., Diecke, S., Matsa, E., Sharma, A., Wu, H., & Wu, J. C. (2015) · Methods in molecular biology · doi:10.1007/7651_2015_196 · Cited by 47 · see citing works
Self-citationStem Cells in Cardiovascular Medicine: Historical Overview and Future Prospects
Samak, M., & Hinkel, R. (2019) · Cells · doi:10.3390/cells8121530 · Cited by 45 · see citing works
Strauss, D. G., & Blinova, K. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.10.009 · Cited by 42 · see citing works
Sharma, A., Zhang, Y., Buikema, J. W., Serpooshan, V., Chirikian, O., Kosaric, N., Churko, J. M., Dzilic, E., Shieh, A., Burridge, P. W., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-24954-3 · Cited by 41 · see citing works
Self-citationBakr, R. O., Amer, R. I., Attia, D. A., Abdelhafez, M. M., Al‐Mokaddem, A. K., El‐Gendy, A. E. G., El-Fishawy, A. M., Fayed, M. A. A., & Gad, S. S. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111225 · Cited by 41 · see citing works
Tang, X., Wang, Z., Hu, S., & Zhou, B. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14071313 · Cited by 40 · see citing works
Differentiation and Contractile Analysis of GFP‐Sarcomere Reporter hiPSC‐Cardiomyocytes
Sharma, A., Toepfer, C. N., Schmid, M., Garfinkel, A. C., & Seidman, C. E. (2018) · Current Protocols in Human Genetics · doi:10.1002/cphg.53 · Cited by 38 · see citing works
Self-citationBozzi, A., Sayed, N., Matsa, E., Sass, G., Neofytou, E. A., Clemons, K. V., Corrêa‐Oliveira, R., Stevens, D. A., & Wu, J. C. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.04.017 · Cited by 37 · see citing works
Self-citationMozneb, M., Jenkins, A., Sances, S., Pohlman, S., Workman, M. J., West, D., Ondatje, B. N., El‐Ghazawi, K., Woodbury, A., Garcia, V. J., et al. (2024) · Lab on a Chip · doi:10.1039/d3lc00745f · Cited by 36 · see citing works
Self-citationLam, C. K., & Wu, J. C. (2021) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.314695 · Cited by 37 · see citing works
Self-citationDavis, J. A., Chouman, A., Creech, J., da Rocha, A. M., Ponce‐Balbuena, D., Jiménez‐Vázquez, E. N., Nichols, R., Lozhkin, A. P., Madamanchi, N. R., Campbell, K. F., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.134368 · Cited by 36 · see citing works
Innate and adaptive immunity in acute myocarditis
Golino, M., Harding, D., Buono, M. G. D., Fanti, S., MOHIDDIN, S. A., Toldo, S. A., Smyth, J. W., Sanna, T., Marelli‐Berg, F. M., & Abbate, A. (2024) · International Journal of Cardiology · doi:10.1016/j.ijcard.2024.131901 · Cited by 38 · see citing works
Eissa, M., Hashim, Y. Z. H.-Y., El‐Kersh, D. M., Azziz, S. S. S. A., Salleh, H. M., Isa, M., & Warif, N. M. A. (2020) · Processes · doi:10.3390/pr8020202 · Cited by 35 · see citing works
Hwang, H., Liu, R., Maxwell, J. T., Yang, J., & Xu, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-73801-x · Cited by 35 · see citing works
Luteolin inhibits CVB3 replication through inhibiting inflammation
Wu, S., Wang, H., Guo, T., & Li, Y. (2019) · Journal of Asian Natural Products Research · doi:10.1080/10286020.2019.1642329 · Cited by 34 · see citing works
Self-citationMogharbel, A. T., Abu‐Melha, S., Hameed, A. M., Attar, R. M. S., Alrefaei, A. F., Almahri, A., & El‐Metwaly, N. M. (2022) · Arabian Journal of Chemistry · doi:10.1016/j.arabjc.2022.104419 · Cited by 34 · see citing works
Sattler, K., El‐Battrawy, I., Cyganek, L., Lang, S., Lan, H., Li, X., Zhao, Z., Utikal, J. S., Wieland, T., Borggrefe, M. M., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-93958-3 · Cited by 31 · see citing works
Hamed, A. A., Saad, G. R., Abdelhamid, I. A., Elwahy, A. H. M., Abdel‐Aziz, M. M., & Elsabee, M. Z. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.03.199 · Cited by 31 · see citing works
Oxymatrine provides protection against Coxsackievirus B3-induced myocarditis in BALB/c mice
Jiang, Y., Zhu, Y., Mu, Q., Luo, H., Zhi, Y., & Shen, X. (2017) · Antiviral Research · doi:10.1016/j.antiviral.2017.01.013 · Cited by 31 · see citing works
Trevisan, M., Sinigaglia, A., Desole, G., Berto, A., Pacenti, M., Palù, G., & Barzon, L. (2015) · Viruses · doi:10.3390/v7072800 · Cited by 28 · see citing works
A new era of disease modeling and drug discovery using induced pluripotent stem cells
Suh, W. (2016) · Archives of Pharmacal Research · doi:10.1007/s12272-016-0871-0 · Cited by 29 · see citing works
Sharma, A., Mücke, M. B., & Seidman, C. E. (2018) · Current Protocols in Molecular Biology · doi:10.1002/cpmb.58 · Cited by 27 · see citing works
Self-citationCHIR99021 Promotes hiPSC‐Derived Cardiomyocyte Proliferation in Engineered 3D Microtissues
Hesselbarth, R., Esser, T. U., Roshanbinfar, K., Schrüfer, S., Schubert, D. W., & Engel, F. B. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202100926 · Cited by 26 · see citing works
Zhu, K., Bao, X., Wang, Y., Lu, T., & Zhang, L. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113970 · Cited by 26 · see citing works
Biodegradable suture development-based albumin composites for tissue engineering applications
Naser, M. A., Sayed, A. M., Abdelmoez, W., El-Wakad, M. T., & Abdo, M. S. E. (2024) · Scientific Reports · doi:10.1038/s41598-024-58194-5 · Cited by 25 · see citing works
Adenovirus targets transcriptional and posttranslational mechanisms to limit gap junction function
Calhoun, P. J., Phan, A. V., Taylor, J. D., James, C. C., Padget, R. L., Zeitz, M. J., & Smyth, J. W. (2020) · The FASEB Journal · doi:10.1096/fj.202000667r · Cited by 25 · see citing works
Harnessing the Induction of Cardiomyocyte Proliferation for Cardiac Regenerative Medicine
Sharma, A., Zhang, Y., & Wu, S. M. (2015) · Current Treatment Options in Cardiovascular Medicine · doi:10.1007/s11936-015-0404-z · Cited by 25 · see citing works
Self-citationLara, L. D. S., de Andrade-Lima, L. C., Calvet, C. M., Borsoi, J., Duque, T. L. A., Henriques‐Pons, A., Pereira, M. C. D. S., & Pereira, L. V. (2018) · Microbes and Infection · doi:10.1016/j.micinf.2018.03.002 · Cited by 25 · see citing works
Deciphering pathogenicity of variants of uncertain significance with CRISPR-edited iPSCs
Guo, H., Liu, L., Nishiga, M., Cong, L., & Wu, J. C. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.08.009 · Cited by 27 · see citing works
Self-citationCardiac regeneration: Options for repairing the injured heart
Wang, J., An, M., Haubner, B. J., & Penninger, J. M. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.981982 · Cited by 24 · see citing works
Knowlton, K. U. (2019) · Circulation · doi:10.1161/circulationaha.119.040037 · Cited by 23 · see citing works
Modeling Inherited Arrhythmia Disorders Using Induced Pluripotent Stem Cell-Derived Cardiomyocytes
Bezzerides, V. J., Zhang, D., & Pu, W. T. (2016) · Circulation Journal · doi:10.1253/circj.cj-16-1113 · Cited by 23 · see citing works
Luo, Y., Zhang, M., Chen, Y., Chen, Y., & Zhu, D. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.720099 · Cited by 22 · see citing works
Inhaled Atorvastatin Nanoparticles for Lung Cancer
Tulbah, A. S. (2022) · Current Drug Delivery · doi:10.2174/1567201819666220426091500 · Cited by 22 · see citing works
Wong, C., Lam, T.-H., Liao, S.-Y., Lau, Y., Tse, H., & So, B. Y. F. (2023) · Biomedicines · doi:10.3390/biomedicines11010107 · Cited by 21 · see citing works
Newehy, A. S. E., Gheda, S. F., Ismail, M. M., Aldisi, D. A., Abulmeaty, M. M. A., & Elshobary, M. E. (2025) · Pharmaceutics · doi:10.3390/pharmaceutics17070826 · Cited by 20 · see citing works
Fonoudi, H., Ansari, H., Abbasalizadeh, S., Blue, G. M., Aghdami, N., Winlaw, D. S., Harvey, R. P., Bosman, A., & Baharvand, H. (2016) · Journal of Visualized Experiments · doi:10.3791/54276 · Cited by 20 · see citing works
Atmanli, A., & Domian, I. J. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.11.010 · Cited by 19 · see citing works
Yamasaki, Y., Matsuura, K., Sasaki, D., & Shimizu, T. (2021) · Regenerative Therapy · doi:10.1016/j.reth.2021.03.007 · Cited by 19 · see citing works
Knowlton, K. U. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.02.008 · Cited by 19 · see citing works
Lack in Treatment Options for Virus-Induced Inflammatory Cardiomyopathy
Linthout, S. V., Tschöpe, C., & Schultheiß, H. (2014) · Circulation Research · doi:10.1161/circresaha.114.304951 · Cited by 18 · see citing works
White, M. C., Pang, L., & Yang, X. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.05.025 · Cited by 17 · see citing works
Kalra, R. S., Dhanjal, J. K., Das, M., Singh, B., & Naithani, R. (2021) · Cells · doi:10.3390/cells10102558 · Cited by 17 · see citing works
Bekhite, M. M., & Schulze, P. C. (2021) · Cells · doi:10.3390/cells10123483 · Cited by 17 · see citing works
Osama, S., El-Sherei, M. M., Al-Mahdy, D. A., Bishr, M. M., Salama, O., & Raafat, M. M. (2023) · AMB Express · doi:10.1186/s13568-023-01602-2 · Cited by 17 · see citing works
Cardiomyopathy: pathogenesis and therapeutic interventions
Huang, S., Li, J., Li, Q., Wang, Q., Zhou, X., Chen, J., Chen, X., Bellou, A., Zhuang, J., & Lei, L. (2024) · MedComm · doi:10.1002/mco2.772 · Cited by 17 · see citing works
Shereef, H. A., Shaban, S. Y., Moemen, Y. S., El‐Khouly, M. E., & El‐Nahas, A. M. (2022) · Applied Organometallic Chemistry · doi:10.1002/aoc.6583 · Cited by 16 · see citing works
Modeling Cardiac SARS-CoV-2 Infection with Human Pluripotent Stem Cells
Rockwood, S. J., Arzt, M., & Sharma, A. (2022) · Current Cardiology Reports · doi:10.1007/s11886-022-01813-2 · Cited by 15 · see citing works
Self-citationPeischard, S., Ho, H. T., Piccini, I., Strutz‐Seebohm, N., Röpke, A., Liashkovich, I., Gosain, H., Rieger, B., Klingel, K., Eggers, B., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-72966-9 · Cited by 15 · see citing works
Pluripotent Stem Cell-Derived Hepatocyte-like Cells: A Tool to Study Infectious Disease
Schwartz, R. E., Bram, Y., & Frankel, A. S. (2016) · Current Pathobiology Reports · doi:10.1007/s40139-016-0113-7 · Cited by 15 · see citing works
Hepatitis C virus-induced innate immune responses in human iPS cell-derived hepatocyte-like cells
Sakurai, F., Kunito, T., Takayama, K., Hashimoto, R., Tachibana, M., Sakamoto, N., Wakita, T., & Mizuguchi, H. (2017) · Virus Research · doi:10.1016/j.virusres.2017.09.004 · Cited by 15 · see citing works
Pinheiro, E. A., Magdy, T., & Burridge, P. W. (2020) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-020-09962-x · Cited by 15 · see citing works
Self-citationGheraissa, N., Chemsa, A. E., Cherrada, N., Erol, E., Elsharkawy, E. R., Amara, D. G., Zeghoud, S., Rebiai, A., Messaoudi, M., SAWICKA, B. H., et al. (2023) · Molecules · doi:10.3390/molecules28083580 · Cited by 14 · see citing works
Mohamed, H. R. H., Elberry, Y. A., Magdy, H., Ismail, M., Michael, M., Eltayeb, N., & Safwat, G. (2025) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-025-03962-x · Cited by 13 · see citing works
Kraft, L., Sauter, M., Seebohm, G., & Klingel, K. (2021) · Viruses · doi:10.3390/v13091835 · Cited by 13 · see citing works
Rossler, K. J., de Lange, W. J., Mann, M. W., Aballo, T. J., Melby, J. A., Zhang, J., Kim, G., Bayne, E. F., Zhu, Y., Farrell, E. T., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.172168 · Cited by 12 · see citing works
Kamal, N. H., Saber, F. R., Salama, A., Abouhussein, D. M. N., Ismail, S., El-Hefnawy, H. M., & Meselhy, M. R. (2024) · Future Journal of Pharmaceutical Sciences · doi:10.1186/s43094-024-00678-2 · Cited by 12 · see citing works
Povsic, T. J., Scott, R. C., Mahaffey, K. W., Blaustein, R. O., Edelberg, J. M., Lefkowitz, M. P., Solomon, S. D., Fox, J. C., Healy, K. E., Khakoo, A. Y., et al. (2017) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-017-6739-9 · Cited by 12 · see citing works
Self-citationInvestigating pediatric disorders with induced pluripotent stem cells
Durbin, M. D., Cadar, A. G., Chun, Y. W., & Hong, C. C. (2018) · Pediatric Research · doi:10.1038/s41390-018-0064-2 · Cited by 11 · see citing works
Mohsen, E. M. A., Saeed, A. A. M., & Yahia, A.-R. A. B. (2024) · Results in Chemistry · doi:10.1016/j.rechem.2024.101535 · Cited by 10 · see citing works
Bioengineering and Stem Cell Technology in the Treatment of Congenital Heart Disease
Bosman, A., Edel, M. J., Blue, G. M., Dilley, R. J., Harvey, R. P., & Winlaw, D. S. (2015) · Journal of Clinical Medicine · doi:10.3390/jcm4040768 · Cited by 10 · see citing works
- Authors
- Sharma, A., Marceau, C., Hamaguchi, R., Burridge, P. W., Rajarajan, K., Churko, J. M., Wu, H., Sallam, K. I., Matsa, E., Sturzu, A. C., Che, Y., Ebert, A., Diecke, S., Liang, P., Red-Horse, K., Carette, J. E., Wu, S. M., & Wu, J. C.
- Affiliations
- Institute for Stem Cell Biology and Regenerative Medicine (IN)
- From the Department of Medicine, Division of Cardiology (A.S., R.H., P.W.B., K.R., J.M.C., H.W., K.I.S., E.M., A.C.S., Y.C., A.E., S.D., P.L., S.M.W., J.C.W.), Institute for Stem Cell Biology and Regenerative Medicine (A.S., R.H., P.W.B., K.R., J.M.C., H.W., K.I.S., E.M., A.C.S., Y.C., A.E., S.D., P.L., S.M.W., J.C.W.), Stanford Cardiovascular Institute (A.S., R.H., P.W.B., K.R., J.M.C., H.W., K.I.S., E.M., A.C.S., Y.C., A.E., S.D., P.L., K.R.-H., S.M.W., J.C.W.), Department of Biology (A.S., R.H.,...
- ORCID
- Venue
- Circulation Research
- Published
- 2014-08-29
- Volume
- 115
- Issue
- 6
- Pages
- 556-566
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC4149868
- OpenAlex
- W1998190377
- Cited by
- 148
- References
- 50
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 14 · 2023: 8 · 2022: 17 · 2021: 19 · 2020: 14 · 2019: 8 · 2018: 16 · 2017: 12 · 2016: 12 · 2015: 18 · 2014: 2
- FWCI
- 10.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- National Institutes of Health (DP2OD004411, NS069375)
- National Heart, Lung, and Blood Institute (U01HL099776, T32HL007208, R01HL113006)
- National Institute of Allergy and Infectious Diseases (DP2AI104557, T32AI007328)
- National Institute of Neurological Disorders and Stroke (NS069375, P30NS069375)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- coxsackievirus B3, viral myocarditis, human induced pluripotent stem cell-derived cardiomyocytes, antiviral drug screening, interferon-beta, ribavirin, pyrrolidine dithiocarbamate, fluoxetine, coxsackievirus and adenovirus receptor, calcium handling, viral RNA clearance, high-throughput screening, in vitro disease model
- MeSH terms
- Antiviral Agents, Calcium, Cells, Cultured, Drug Evaluation, Preclinical, Enterovirus Infections, Humans, Models, Cardiovascular, Myocarditis, RNA, Viral, Treatment Outcome, Enterovirus B, Human, Myocytes, Cardiac, Pluripotent Stem Cells, Cell Proliferation, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review