Influence of genetic background on ex vivo and in vivo cardiac function in several commonly used inbred mouse strains
Open accessAbstract
Inbred mouse strains play a critical role in biomedical research. Genetic homogeneity within inbred strains and their general amenability to genetic manipulation have made them an ideal resource for dissecting the physiological function(s) of individual genes. However, the inbreeding that makes inbred mice so useful also results in genetic divergence between them. This genetic divergence is often unaccounted for but may be a confounding factor when comparing studies that have utilized distinct inbred strains. Here, we compared the cardiac function of C57BL/6J mice to seven other commonly used inbred mouse strains: FVB/NJ, DBA/2J, C3H/HeJ, BALB/cJ, 129X1/SvJ, C57BL/10SnJ, and 129S1/SvImJ. The assays used to compare cardiac function were the ex vivo isolated Langendorff heart preparation and in vivo real-time hemodynamic analysis using conductance micromanometry. We report significant strain-dependent differences in cardiac function between C57BL/6J and other commonly used inbred strains. C57BL/6J maintained better cardiac function than most inbred strains after ex vivo ischemia, particularly compared with 129S1/SvImJ, 129X1/SvJ, and C57BL/10SnJ strains. However, during in vivo acute hypoxia 129X1/SvJ and 129S1/SvImJ maintained relatively normal cardiac function, whereas C57BL/6J animals showed dramatic cardiac decompensation. Additionally, C3H/HeJ showed rapid and marked cardiac decompensation in response to esmolol infusion compared with effects of other strains. These findings demonstrate the complex effects of genetic divergence between inbred strains on cardiac function. These results may help inform analysis of gene ablation or transgenic studies and further demonstrate specific quantitative traits that could be useful in discovery of genetic modifiers relevant to cardiac health and disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Various cardiac functions, parameters, properties, and responses to stress vary depending on mouse strains.
“various cardiac functions, parameters, properties, and response to stress vary depending on the mouse strains (Barnabei, Palpant, & Metzger, 2010; Hoit, et al., 2002; Howden, et al., 2008; A. P. Shah, et al., 2010; Stull, et al., 2006; van den Borne, et al., 2009).”
From Small and large animal models in cardiac contraction research: advantages and disadvantages (2014) · cites this paper as Barnabei, et al., 2010
Cites
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187 · see citing works
Heart Disease and Stroke Statistics—2010 Update: A Report From the American Heart Association
WRITING GROUP MEMBERS, Lloyd-Jones, D., Adams, R. J., Brown, T. M., Carnethon, M., Dai, S., De Simone, G., Ferguson, T. B., Ford, E., Furie, K., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.192667 · Cited by 5,700 · see citing works
Executive Summary: Heart Disease and Stroke Statistics—2010 Update
WRITING GROUP MEMBERS, Lloyd‐Jones, D. M., Adams, R. J., Brown, T. M., Carnethon, M. R., Dai, S., SIMONE, G. D., Ferguson, T. B., Ford, E. S., Furie, K. L., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.192666 · Cited by 1,358 · see citing works
Untersuchungen am überlebenden Säugethierherzen
Langendorff, O. (1895) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf01812150 · Cited by 1,329 · see citing works
The Molecular Basis of Muscular Dystrophy in the <i>mdx</i> Mouse: a Point Mutation
Sicinski, P., Geng, Y., Ryder-Cook, A. S., Barnard, E. A., Darlison, M. G., & Barnard, P. J. (1989) · Science · doi:10.1126/science.2662404 · Cited by 1,086 · see citing works
Genealogies of mouse inbred strains
Beck, J. A., Lloyd, S. E., Hafezparast, M., Lennon-Pierce, M., Eppig, J. T., Festing, M. F. W., & Fisher, E. (2000) · Nature Genetics · doi:10.1038/71641 · Cited by 825 · see citing works
Pacher, P., Nagayama, T., Mukhopadhyay, P., Bátkai, S., & Kass, D. A. (2008) · Nature Protocols · doi:10.1038/nprot.2008.138 · Cited by 734 · see citing works
FVB/N: an inbred mouse strain preferable for transgenic analyses.
Taketo, M. M., Schroeder, A. C., Mobraaten, L. E., Gunning, K. B., Hanten, G. R., Fox, R. R., Roderick, T. H., Stewart, C. L., Lilly, F., & Hansen, C. T. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.6.2065 · Cited by 598 · see citing works
Isolated heart perfusion according to Langendorff—Still viable in the new millennium
Skrzypiec‐Spring, M., Grotthus, B., Szeląg, A., & Schulz, R. (2006) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2006.05.006 · Cited by 356 · see citing works
Bittner, R. E., Anderson, L. V. B., Burkhardt, E., Bashir, R., Vafiadaki, E., Ivanova, S., Raffelsberger, T., Maerk, I., Höger, H., Jung, M., et al. (1999) · Nature Genetics · doi:10.1038/13770 · Cited by 219 · see citing works
Latent TGF-β–binding protein 4 modifies muscular dystrophy in mice
Heydemann, A., Ceco, E., Lim, J. E., Hadhazy, M., Ryder, P. V., Moran, J. L., Beier, D. R., Palmer, A. A., & McNally, E. M. (2009) · Journal of Clinical Investigation · doi:10.1172/jci39845 · Cited by 212 · see citing works
Ho, M. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh212 · Cited by 201 · see citing works
Merin, R. G., Bernard, J.-M., Doursout, M., Cohen, M., & Chelly, J. E. (1991) · Anesthesiology · doi:10.1097/00000542-199103000-00027 · Cited by 162 · see citing works
Naturally Occurring Variability in Anesthetic Potency Among Inbred Mouse Strains
Sonner, J. M., Gong, D., & Eger, E. I. (2000) · Anesthesia & Analgesia · doi:10.1097/00000539-200009000-00042 · Cited by 144 · see citing works
To knockout in 129 or in C57BL/6: that is the question
Seong, E., Saunders, T. L., Stewart, C. L., & Burmeister, M. (2003) · Trends in Genetics · doi:10.1016/j.tig.2003.12.006 · Cited by 141 · see citing works
Localization of the mdx mutation within the mouse dystrophin gene
Ryder‐Cook, A. S., Sicinski, P., Thomas, K., Davies, K. E., Worton, R. G., Barnard, E. A., Darlison, M. G., & Barnard, P. J. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03165.x · Cited by 139 · see citing works
Prabhakar, R., Boivin, G. P., Grupp, I. L., Hoit, B. D., Arteaga, G. M., Solaro, R. J., & Wieczorek, D. F. (2001) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2001.1445 · Cited by 134 · see citing works
Townsend, D., Blankinship, M. J., Allen, J. M., Gregorevic, P., Chamberlain, J. S., & Metzger, J. M. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300144 · Cited by 133 · see citing works
Self-citationAlpha-skeletal actin is associated with increased contractility in the mouse heart.
Hewett, T. E., Grupp, I. L., Grupp, G., & Robbins, J. M. (1994) · Circulation Research · doi:10.1161/01.res.74.4.740 · Cited by 127 · see citing works
Emergent Dilated Cardiomyopathy Caused by Targeted Repair of Dystrophic Skeletal Muscle
Townsend, D., Yasuda, S., Li, S., Chamberlain, J. S., & Metzger, J. M. (2008) · Molecular Therapy · doi:10.1038/mt.2008.52 · Cited by 118 · see citing works
Self-citationPractical Methods in Cardiovascular Research
Dhein, S., Mohr, F. W., & Delmar, M. (2005) · Springer eBooks · doi:10.1007/b137833 · Cited by 117 · see citing works
Naturally occurring variation in cardiovascular traits among inbred mouse strains
Hoit, B. D., Kiatchoosakun, S., Restivo, J., Kirkpatrick, D., Olszens, K., Shao, H., Pao, Y.-H., & Nadeau, J. H. (2002) · Genomics · doi:10.1006/geno.2002.6754 · Cited by 110 · see citing works
Naturally Occurring Variability in Anesthetic Potency Among Inbred Mouse Strains
Sonner, J. M., Gong, D., & Eger, E. I. (2000) · Anesthesia & Analgesia · doi:10.1213/00000539-200009000-00042 · Cited by 105 · see citing works
Gender modulates cardiac phenotype development in genetically modified mice
Du, X. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.03.027 · Cited by 104 · see citing works
Histidine button engineered into cardiac troponin I protects the ischemic and failing heart
Day, S. M., Westfall, M. V., Fomicheva, E. V., Hoyer, K., Yasuda, S., Cross, N. C. L., D’Alecy, L. G., Ingwall, J. S., & Metzger, J. M. (2006) · Nature Medicine · doi:10.1038/nm1346 · Cited by 100 · see citing works
Self-citationGenetic background influences muscular dystrophy
Heydemann, A., Huber, J. M., Demonbreun, A. R., Hadhazy, M., & McNally, E. M. (2005) · Neuromuscular Disorders · doi:10.1016/j.nmd.2005.05.004 · Cited by 92 · see citing works
Cardiac and coronary function in the Langendorff‐perfused mouse heart model
Reichelt, M. E., Willems, L., Hack, B., Peart, J. N., & Headrick, J. P. (2008) · Experimental Physiology · doi:10.1113/expphysiol.2008.043554 · Cited by 88 · see citing works
Saha, D. C., Saha, A. C., Malik, G., Astiz, M. E., & Rackow, E. C. (2007) · PubMed · Cited by 85 · see citing works
Michele, D. E., Gomez, C. A., Hong, K. E., Westfall, M. V., & Metzger, J. M. (2002) · Circulation Research · doi:10.1161/01.res.0000027530.58419.82 · Cited by 68 · see citing works
Self-citationHalogenated anaesthetics and cardiac protection in cardiac and non-cardiac anaesthesia
Landoni, G., Bignami, E., Fochi, O., & Zangrillo, A. (2009) · Annals of Cardiac Anaesthesia · doi:10.4103/0971-9784.45006 · Cited by 65 · see citing works
Gros, D. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.02.010 · Cited by 65 · see citing works
Genetic Modifier Loci Affecting Survival and Cardiac Function in Murine Dilated Cardiomyopathy
Suzuki, M., Carlson, K. M., Marchuk, D. A., & Rockman, H. A. (2002) · Circulation · doi:10.1161/01.cir.0000014926.32463.89 · Cited by 58 · see citing works
QTL associated with blood pressure, heart rate, and heart weight in CBA/CaJ and BALB/cJ mice
Sugiyama, F., Churchill, G. A., Li, R., Libby, L. J. M., Carver, T., Yagami, K., John, S. W. M., & Paigen, B. J. (2002) · Physiological Genomics · doi:10.1152/physiolgenomics.00002.2002 · Cited by 53 · see citing works
Genetic background affects function and intracellular calcium regulation of mouse hearts
Shah, A. P., Siedlecka, U., Gandhi, A., Navaratnarajah, M., Al‐Saud, S. A., Yacoub, M. H., & Terracciano, C. M. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq111 · Cited by 49 · see citing works
Skolleborg, K. C., Grønbech, J. E., Grong, K., Abyholm, F. E., & LEKVEN, J. (1990) · Laboratory Animals · doi:10.1258/002367790780866100 · Cited by 46 · see citing works
Direct Comparative Effects of Isoflurane and Desflurane in Isolated Guinea Pig Hearts
Boban, M., Stowe, D. F., Buljubasíc, N., Kampine, J. P., & Bosniak, Z. J. (1992) · Anesthesiology · doi:10.1097/00000542-199205000-00016 · Cited by 45 · see citing works
Mogil, J. S., Smith, S. B., O'Reilly, M. K., & Plourde, G. (2005) · Anesthesiology · doi:10.1097/00000542-200510000-00013 · Cited by 43 · see citing works
Systolic Blood Pressure in Eight Inbred Strains of Mice
Schlager, G. (1966) · Nature · doi:10.1038/212519a0 · Cited by 41 · see citing works
Sossey‐Alaoui, K., Kitamura, E., Head, K. L., & Cowell, J. K. (2002) · Genomics · doi:10.1006/geno.2002.6792 · Cited by 40 · see citing works
Strain-Dependent Variation in Vascular Responses to Nitric Oxide in the Isolated Murine Heart
Bendall, J. K., Heymes, C., Wright, T. J. F., Wheatcroft, S. B., Grieve, D., Shah, A. M., & Cave, A. C. (2002) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2002.2083 · Cited by 39 · see citing works
Waldeyer, C., Fabritz, L., Fortmueller, L., Gerß, J., Damke, D., Blana, A., Laakmann, S., Kreienkamp, N., Volkery, D., BREITHARDT, G. E., et al. (2009) · Basic Research in Cardiology · doi:10.1007/s00395-009-0019-1 · Cited by 35 · see citing works
Utility of a C57BL/6 ES line versus 129 ES lines for Targeted Mutations in Mice
Ware, C. B., Siverts, L., Nelson, A. M., Morton, J., & Ladiges, W. (2003) · Transgenic Research · doi:10.1023/b:trag.0000005246.35812.c8 · Cited by 34 · see citing works
Cardiac activity in the mouse: Strain differences.
Blizard, D. A., & Welty, R. (1971) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0031655 · Cited by 33 · see citing works
Pharmacological responses to pentobarbital in different strains of mice.
Nabeshima, T., & Ho, I. K. (1981) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)32397-9 · Cited by 32 · see citing works
Transgenic Studies of Cardiac Adrenergic Receptor Regulation
Eckhart, A. D., & Koch, W. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29294-6 · Cited by 31 · see citing works
Beta-adrenergic receptors in heart failure.
Insel, P. A., & Hammond, H. K. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116867 · Cited by 26 · see citing works
Murine strain differences in contractile function are temperature- and frequency-dependent
Stull, L. B., Hiranandani, N., Kelley, M. A., Leppo, M. K., Marbán, E., & Janssen, P. M. L. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-005-0020-y · Cited by 24 · see citing works
Differences in DBA/1J and DBA/2J reveal lipid QTL genes
Stylianou, I. M., Langley, S. R., Walsh, K., Chen, Y., Revenu, C., & Paigen, B. J. (2008) · Journal of Lipid Research · doi:10.1194/jlr.m800244-jlr200 · Cited by 24 · see citing works
Induction and Analysis of Cardiac Hypertrophy in Transgenic Animal Models
Barbosa, M. E., Alenina, N. V., & Bäder, M. (2005) · Humana Press eBooks · doi:10.1385/1-59259-879-x:339 · Cited by 24 · see citing works
Genetically engineered mice as a model for studying cardiac arrhythmias
Tamargo, J. L. (2006) · Frontiers in bioscience · doi:10.2741/2046 · Cited by 22 · see citing works
Calcium regulatory proteins and their alteration by transgenic approaches
DILLMANN, W. H. (1999) · The American Journal of Cardiology · doi:10.1016/s0002-9149(99)00268-4 · Cited by 22 · see citing works
Knockin Animal Models of Inherited Arrhythmogenic Diseases: What Have We Learned From Them?
Nilles, K. M., & London, B. (2007) · Journal of Cardiovascular Electrophysiology · doi:10.1111/j.1540-8167.2007.00884.x · Cited by 17 · see citing works
Ferrier, G. R., & Guyette, C. M. (1991) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199102000-00008 · Cited by 16 · see citing works
Palpant, N. J., D’Alecy, L. G., & Metzger, J. M. (2009) · The FASEB Journal · doi:10.1096/fj.08-121996 · Cited by 16 · see citing works
Self-citationPalpant, N. J., Szatkowski, M. L., Wang, W., Townsend, D., Bedada, F. B., Koch, L. G., Britton, S. L., & Metzger, J. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006117 · Cited by 16 · see citing works
Self-citationMixed Effects Models for Quantitative Trait Loci Mapping With Inbred Strains
Bauman, L., Sinsheimer, J., Sobel, E., & Lange, K. (2008) · Genetics · doi:10.1534/genetics.108.091058 · Cited by 15 · see citing works
Doorenbos, C., Tsaih, S., Sheehan, S., Ishimori, N., Navis, G. J., Churchill, G. A., DiPetrillo, K., & Korstanje, R. (2008) · Genetics · doi:10.1534/genetics.107.085142 · Cited by 15 · see citing works
Ultrasonographic monitoring of a spontaneous abortion in an owl monkey (Aotus nancymaae).
Schuler, A. M., Parks, V. L., Abee, C. R., & Scammell, J. G. (2007) · PubMed · Cited by 14 · see citing works
Blizard, D. A., Lionikas, A., Vandenbergh, D. J., Vasilopoulos, T., Gerhard, G. S., Griffith, J. W., Klein, L. C., Stout, J. T., Mack, H. A., Lakoski, J. M., et al. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.00035.2008 · Cited by 11 · see citing works
β-Adrenergic Receptors in Heart Failure
Engelhardt, S. H. (2005) · Heart Failure Clinics · doi:10.1016/j.hfc.2005.04.005 · Cited by 11 · see citing works
Dalal, P. G., Corner, A., Chin, C., Wood, C., & Razavi, R. (2008) · Journal of Clinical Anesthesia · doi:10.1016/j.jclinane.2007.08.004 · Cited by 10 · see citing works
SPECIFIC INHIBITION OF Ca2+-ATPase ACTIVITY BY VOLATILE ANESTHETICS
Roszczyńska, G., & Kosk‐Kosicka, D. (1992) · Anesthesiology · doi:10.1097/00000542-199209001-00775 · Cited by 3 · see citing works
Duke, P. C., Morton, M., Ong, B. Y., & Hill, K. (1991) · Anesthesiology · doi:10.1097/00000542-199109001-00567 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cell Biology of Ischemia/Reperfusion Injury
Kalogeris, T. J., Baines, C. P., Krenz, M., & Korthuis, R. J. (2012) · International review of cytology · doi:10.1016/b978-0-12-394309-5.00006-7 · Cited by 2,207 · see citing works
Kalogeris, T. J., Baines, C. P., Krenz, M., & Korthuis, R. J. (2016) · Comprehensive physiology · doi:10.1002/cphy.c160006 · Cited by 841 · see citing works
Small and large animal models in cardiac contraction research: advantages and disadvantages
Milani-Nejad, N., & Janssen, P. M. L. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.10.007 · Cited by 484 · see citing works
Taegtmeyer, H., Young, M. E., Lopaschuk, G. D., Abel, E. D., Brunengraber, H., Darley-Usmar, V. M., Rosiers, C. D., Gerszten, R. E., Glatz, J. F. C., Griffin, J. L., et al. (2016) · Circulation Research · doi:10.1161/res.0000000000000097 · Cited by 283 · see citing works
Ronchi, J. A., Figueira, T. R., Ravagnani, F. G., Oliveira, H. C. F., Vercesi, A. E., & Castilho, R. F. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.049 · Cited by 283 · see citing works
Lecour, S., Bøtker, H. E., Condorelli, G., Davidson, S. M., David Garcia-dorado, A., Engel, F. B., Ferdinandy, P., Heusch, G., Madonna, R., Ovize, M., et al. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu225 · Cited by 163 · see citing works
Kalogeris, T. J., Baines, C. P., Krenz, M., & Korthuis, R. J. (2017) · Comprehensive physiology · doi:10.1002/j.2040-4603.2017.tb00741.x · Cited by 115 · see citing works
Davis, J., Maillet, M., Miano, J. M., & Molkentin, J. D. (2012) · Circulation Research · doi:10.1161/circresaha.111.262717 · Cited by 113 · see citing works
Chen, B., Guo, A., Zhang, C., Chen, R., Zhu, Y., Jiang, H., Kutschke, W. J., Zimmerman, K., Weiss, R. M., Zingman, L. V., et al. (2013) · Cardiovascular Research · doi:10.1093/cvr/cvt180 · Cited by 102 · see citing works
Martindale, J. J., & Metzger, J. M. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.12.008 · Cited by 69 · see citing works
Self-citationDour, C. L., Chatzifrangkeskou, M., Macquart, C., Magiera, M. M., Peccate, C., Jouve, C., Virtanen, L., Heliö, T. M., Aalto‐Setälä, K., Crasto, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-35639-x · Cited by 66 · see citing works
Lemckert, F. A., Bournazos, A., Eckert, D. M., Kenzler, M., Hawkes, J. M., Butler, T. L., Ceely, B., North, K. N., Winlaw, D. S., Egan, J. R., et al. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw017 · Cited by 54 · see citing works
Pravastatin therapy during preeclampsia prevents long-term adverse health effects in mice
Garrett, N., Pombo, J., Umpierrez, M., Clark, J., Simmons, M., & Girardi, G. (2018) · JCI Insight · doi:10.1172/jci.insight.120147 · Cited by 52 · see citing works
Zhang, H., & Faber, J. E. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.07.020 · Cited by 51 · see citing works
Luitel, H., Sydykov, A. S., Schymura, Y., Mamazhakypov, A., Janssen, W., Pradhan, K., Wietelmann, A., Kosanovic, D., Dahal, B. K., Weißmann, N., et al. (2017) · Physiological Reports · doi:10.14814/phy2.13146 · Cited by 50 · see citing works
Forte, E., Panahi, M., Baxan, N., Ng, F. S., Boyle, J. J., Branca, J. A., Bedard, O., Hasham, M. G., Benson, L., Harding, S. E., et al. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15937 · Cited by 49 · see citing works
Revisiting Cardiac Biology in the Era of Single Cell and Spatial Omics
Palmer, J. A., Rosenthal, N. A., Teichmann, S. A., & Litviňuková, M. (2024) · Circulation Research · doi:10.1161/circresaha.124.323672 · Cited by 48 · see citing works
Comprehensive Echocardiographic Assessment of the Right Ventricle in Murine Models
Kohut, A. R., Patel, N. H., & Singh, H. (2016) · Journal of Cardiovascular Ultrasound · doi:10.4250/jcu.2016.24.3.229 · Cited by 48 · see citing works
Wang, Y., Pinto, J. R., Solis, R. S., Dweck, D., Liang, J., Diaz-Perez, Z., Ge, Y., Walker, J. W., & Potter, J. D. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.294306 · Cited by 41 · see citing works
Egemnazarov, B., Schmidt, A. G., Crnković, S., Sydykov, A. S., Nagy, B. M., Kovács, G., Weißmann, N., Olschewski, H., Olschewski, A., Kwapiszewska, G., et al. (2015) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2015.02.014 · Cited by 40 · see citing works
Mylk3null C57BL/6N mice develop cardiomyopathy, whereasNntnull C57BL/6J mice do not
Williams, J. L., Paudyal, A., Awad, S., Nicholson, J., Grzesik, D., Botta, J. A., Meimaridou, E., Maharaj, A. V., Stewart, M. E., Tinker, A., et al. (2020) · Life Science Alliance · doi:10.26508/lsa.201900593 · Cited by 40 · see citing works
Moreth, K., Fischer, R., Fuchs, H., Gailus‐Durner, V., Wurst, W., Katus, H. A., Bekeredjian, R., & de Angelis, M. H. (2014) · Journal of Comparative Physiology B · doi:10.1007/s00360-014-0830-3 · Cited by 38 · see citing works
Genetically modified mouse models to help fight COVID-19
Gurumurthy, C. B., Quadros, R. M., Richardson, G. P., Poluektova, L. Y., Mansour, S. L., & Ohtsuka, M. (2020) · Nature Protocols · doi:10.1038/s41596-020-00403-2 · Cited by 38 · see citing works
Ruiz, M., Gélinas, R., Vaillant, F., Lauzier, B., & Rosiers, C. D. (2015) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2015.06.026 · Cited by 31 · see citing works
Mastrototaro, G., Liang, X., Li, X., Carullo, P., Piroddi, N., Tesi, C., Gu, Y., Dalton, N. D., Peterson, K. L., Poggesi, C., et al. (2015) · Cardiovascular Research · doi:10.1093/cvr/cvv156 · Cited by 29 · see citing works
Non-invasive assessment of HFpEF in mouse models: current gaps and future directions
Villalba‐Orero, M., García‐Pavía, P., & Lara‐Pezzi, E. (2022) · BMC Medicine · doi:10.1186/s12916-022-02546-3 · Cited by 29 · see citing works
Myeloperoxidase is a critical mediator of anthracycline-induced cardiomyopathy
Nettersheim, F. S., Schlüter, J. D., Kreuzberg, W., Mehrkens, D., Grimm, S., Nemade, H., Braumann, S., Hof, A., Guthoff, H., Peters, V. B. M., et al. (2023) · Basic Research in Cardiology · doi:10.1007/s00395-023-01006-0 · Cited by 29 · see citing works
Mitochondrial dysfunction in human immunodeficiency virus‐1 transgenic mouse cardiac myocytes
Cheung, J. Y., Gordon, J., Wang, J., Song, J., Zhang, X.-Q., Jaña, F., Shanmughapriya, S., Rajan, S., Tomar, D., Tahrir, F. G., et al. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27232 · Cited by 26 · see citing works
Mouse strain differences in metabolic fluxes and function of ex vivo working hearts
Vaillant, F., Lauzier, B., Poirier, I., Gélinas, R., Rivard, M.-È., Frayne, I. R., Thorin, É., & Rosiers, C. D. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00465.2013 · Cited by 24 · see citing works
Functional resilience of C57BL/6J mouse heart to dietary fat overload
Tadinada, S. M., Weatherford, E. T., Collins, G. V., Bhardwaj, G., Cochran, J. D., Kutschke, W. J., Zimmerman, K., Bosko, A., O'Neill, B. T., Weiss, R. M., et al. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00419.2021 · Cited by 24 · see citing works
Vignier, N., Mougenot, N., Bonne, G., & Muchir, A. (2019) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2019.100664 · Cited by 23 · see citing works
Persistent, comorbid pain and anxiety can be uncoupled in a mouse model
Liu, Y., Liu, Y., Yu, J. M., & Zhang, Y. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.07.004 · Cited by 23 · see citing works
Kaakinen, M., Reichelt, M. E., Ma, Z., Ferguson, C., Martel, N., Porrello, E. R., Hudson, J. E., Thomas, W. G., Parton, R. G., & Headrick, J. P. (2017) · Basic Research in Cardiology · doi:10.1007/s00395-017-0613-6 · Cited by 21 · see citing works
Critical Ischemia Time, Perfusion, and Drainage Function of Vascularized Lymph Nodes
Yang, C., Ho, O. A., Cheng, M., & Hsiao, H. (2018) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000004673 · Cited by 21 · see citing works
The heart of cardiac reprogramming: The cardiac fibroblasts
Ricketts, S. N., & Li, Q. (2022) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2022.08.004 · Cited by 20 · see citing works
Veith, C., Neghabian, D., Luitel, H., Wilhelm, J., Egemnazarov, B., Muntanjohl, C., Fischer, J.-H., Dahal, B. K., SCHERMULY, R. T., Ghofrani, H. A., et al. (2020) · Basic Research in Cardiology · doi:10.1007/s00395-019-0767-5 · Cited by 19 · see citing works
Pritchard, T. J., Kawase, Y., Haghighi, K., Anjak, A., Cai, W., Jiang, M., Nicolaou, P. A., Pylar, G., Karakikes, I., Rapti, K., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080717 · Cited by 19 · see citing works
Sharp, C. N., Doll, M. A., Dupre, T. V., Beverly, L. J., & Siskind, L. J. (2018) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00463.2018 · Cited by 19 · see citing works
Commonly used mouse strains have distinct vascular properties
Steppan, J., Jandu, S., Wang, H., Kang, S., Savage, W. J., Narayanan, R., Nandakumar, K., & Santhanam, L. (2020) · Hypertension Research · doi:10.1038/s41440-020-0467-4 · Cited by 19 · see citing works
Genetic background influences expression and function of the cation channel TRPM4 in the mouse heart
Medert, R., Pironet, A., Bacmeister, L., Segin, S., Londoño, J. E. C., Vennekens, R., & Freichel, M. (2020) · Basic Research in Cardiology · doi:10.1007/s00395-020-00831-x · Cited by 19 · see citing works
Li, Y., Kubo, H., Yu, D., Yang, Y., Johnson, J. P., Eaton, D., Berretta, R. M., Foster, M., McKinsey, T. A., Yu, J., et al. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00594.2022 · Cited by 18 · see citing works
McGee, A. M., & Baines, C. P. (2012) · Biochemical Journal · doi:10.1042/bj20111881 · Cited by 17 · see citing works
Townsend, D., Daly, M., Chamberlain, J. S., & Metzger, J. M. (2011) · Molecular Therapy · doi:10.1038/mt.2011.120 · Cited by 17 · see citing works
Self-citationTankersley, C. G., Georgakopoulos, D., Tang, W., Abston, E. D., Bierman, A. M., & Sborz, N. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfs273 · Cited by 17 · see citing works
Chowdhury, S. A. K., Warren, C. M., Simon, J. N., Ryba, D. M., Batra, A., Varga, P., Kranias, E. G., Tardiff, J. C., Solaro, R. J., & Wolska, B. M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00107 · Cited by 17 · see citing works
Han, M., Evsikov, A. V., Zhang, L., Lastra-Vicente, R., & Linask, K. K. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.03.039 · Cited by 17 · see citing works
Smiley-Walters, S. A., Farrell, T. M., & Gibbs, H. L. (2018) · Toxicon · doi:10.1016/j.toxicon.2018.01.022 · Cited by 16 · see citing works
Gazarov, E. A., Zequeira, S., Senetra, A. S., Howard, J. C., Sharma, A., McCurdy, C. R., Lewis, J. M., Bizon, J. L., & Setlow, B. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1227220 · Cited by 15 · see citing works
Alam, F., Gaspari, T. A., Kemp‐Harper, B. K., Low, E., Aw, A., Ferens, D. M., Spizzo, I., Jefferis, A., Praveen, P., Widdop, R. E., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114370 · Cited by 15 · see citing works
Measuring Pressure Volume Loops in the Mouse
Townsend, D. (2016) · Journal of Visualized Experiments · doi:10.3791/53810 · Cited by 15 · see citing works
Gene and stress history interplay in emergence of PTSD-like features
Chakraborty, N., Meyerhoff, J. L., Gautam, A., Muhie, S. Y., Jibitu, M., de Lima, T. C. M., Hammamieh, R., & Jett, M. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.05.038 · Cited by 13 · see citing works
Huby, A.-C., Turdi, S., James, J., Towbin, J. A., & Purevjav, E. (2015) · Clinical Science · doi:10.1042/cs20150624 · Cited by 12 · see citing works
Vaillant, F., Lauzier, B., Ruiz, M., Shi, Y., Lachance, D., Rivard, M.-È., Bolduc, V., Thorin, É., Tardif, J., & Rosiers, C. D. (2016) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00789.2015 · Cited by 12 · see citing works
Nixon, B. R., Williams, A. F., Glennon, M. S., de Feria, A. E., Sebag, S. C., Baldwin, H. S., & Becker, J. R. (2017) · JCI Insight · doi:10.1172/jci.insight.90656 · Cited by 13 · see citing works
Recent advances and future prospects in direct cardiac reprogramming
Xie, Y., Handel, B. V., Li, Q., & Ardehali, R. (2023) · Nature Cardiovascular Research · doi:10.1038/s44161-023-00377-w · Cited by 12 · see citing works
Király, G., Egu, J. C., Hargitai, Z., Kovács, I., Fábián, I., Kalmár, J., & Szemán-Nagy, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189756 · Cited by 10 · see citing works
Marton, J., Albert, D., Wiltshire, S. A., Park, R., Bergen, A. A. B., Qureshi, S. T., Malo, D., Burelle, Y., & Vidal, S. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138222 · Cited by 10 · see citing works
Sex differences in porcine left ventricular myocardial remodeling due to right ventricular pacing
Kiczak, L., Tomaszek, A., Pasławska, U., Bania, J., Noszczyk-Nowak, A., Skrzypczak, P., Pasławski, R., Zacharski, M., Janiszewski, A., Kuropka, P., et al. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0048-4 · Cited by 9 · see citing works
Wang, J., Song, J., Gao, E., Zhang, X.-Q., Gu, T., Yu, D., Koch, W. J., Feldman, A. M., & Cheung, J. Y. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00861.2013 · Cited by 9 · see citing works
Animal Models of Myocardial Disease
Breckenridge, R. A. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-415894-8.00007-5 · Cited by 8 · see citing works
de Groot, N. E., van den Hoogenhof, M. M. G., Najafi, A., van der Made, I., van der Velden, J., Beqqali, A., Pinto, Y. M., & Creemers, E. E. (2020) · Scientific Reports · doi:10.1038/s41598-020-64667-0 · Cited by 7 · see citing works
Pluteanu, F., Boknı́k, P., Heinick, A., König, C., Müller, F. U., Weidlich, A., & Kirchhefer, U. (2022) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00539.2021 · Cited by 7 · see citing works
Models to Investigate Cardiac Metabolism
Schwarzer, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802394-5.00008-x · Cited by 6 · see citing works
Deckx, S., Carai, P., Bateman, J. F., Heymans, S. R. B., & Papageorgiou, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139199 · Cited by 6 · see citing works
Comparative Study of Transcriptome in the Hearts Isolated from Mice, Rats, and Humans
Okada, D., Okamoto, Y., Io, T., Oka, M., Kobayashi, D., Ito, S., Yamada, R., Ishii, K., & Ono, K. (2022) · Biomolecules · doi:10.3390/biom12060859 · Cited by 6 · see citing works
Therapeutic potential of thymosin β4 in myocardial infarct and heart failure.
Stark, C., Taimen, P., Tarkia, M., Pärkkä, J., Saraste, A., Alastalo, T., Savunen, T., & Koskenvuo, J. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06695.x · Cited by 5 · see citing works
Karbassi, E., Monte, E., Chapski, D. J., Lopez, R., Rosa‐Garrido, M., Kim, J., Wisniewski, N., Rau, C. D., Wang, J., Weiss, J. N., et al. (2016) · Physiological Genomics · doi:10.1152/physiolgenomics.00035.2016 · Cited by 5 · see citing works
Steijns, F., Renard, M., Vanhomwegen, M., Vermassen, P., Desloovere, J., Raedt, R., Larsen, L. E., Tóth, M. I., Backer, J. F. A. D., & Sips, P. Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197024 · Cited by 4 · see citing works
Pediatric viral myocarditis: mechanisms, experimental models, and research gaps
Ling, I., Alburquerque, R. A., & Steed, A. L. (2026) · Pediatric Research · doi:10.1038/s41390-026-04845-4 · Cited by 3 · see citing works
Introduction to ischemia–reperfusion injury
Ahmed, N. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-818023-5.00001-7 · Cited by 3 · see citing works
Wang, C., Chakraborty, A., Somanader, D. V. N., Nguyen, M., Chen, W., Widdop, R. E., & Samuel, C. S. (2023) · Fibrosis · doi:10.35534/fibrosis.2023.10006 · Cited by 2 · see citing works
Methamphetamine conditioned place preference in adolescent mice: Interaction between sex and strain
Severino, L. N., Toussaint, A. B., Langa, R. M., McKenna, G., Bodziony, I., & Burghardt, N. S. (2026) · Journal of Psychopharmacology · doi:10.1177/02698811261420102 · Cited by 2 · see citing works
Blain, A. M., Greally, E., Laval, S. H., Blamire, A. M., MacGowan, G. A., & Straub, V. W. (2014) · Neuromuscular Disorders · doi:10.1016/j.nmd.2014.09.013 · Cited by 2 · see citing works
Cardiac Response to β-Adrenergic Stimulation Determined by Pressure-Volume Loop Analysis
Medert, R., Bacmeister, L., Segin, S., Freichel, M., & Londoño, J. E. C. (2021) · Journal of Visualized Experiments · doi:10.3791/62057 · Cited by 1 · see citing works
The many facets of transcriptional regulation by hypoxia-inducible factor-1
Heger, J., & Euler, G. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz079 · Cited by 1 · see citing works
Calcium “stress” adds a third hit in driving heart failure with preserved ejection fraction
Fujita, K., Ellis, M. W., & Sheikh, F. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00075.2023 · Cited by 1 · see citing works
Is it time to consider ethnicity in treatment guidelines?
Mearns, B. M. (2010) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2010.181
Rol de la CaMKII en la injuria irreversible por isquemia y reperfusión
Carlo, M. N. D. (2016) · doi:10.35537/10915/53073
New, L. A. (2014) · The Atrium (University of Guelph)
Bioinformatics of Embryonic Exposures: Lipid Metabolism and Gender as Biomedical Variables
Linask, K. K. (2018) · Translational bioinformatics · doi:10.1007/978-981-13-0620-4_3
RESEARCH ARTICLE Integrative Cardiovascular Physiology and Pathophysiology
Ribeiro, J. C. (2018)
Appropriate selection of a mouse strain in accordance with the vascular properties
Kishi, T. (2020) · Hypertension Research · doi:10.1038/s41440-020-0520-3
Heinis, F. I., Thompson, B. R., Gulati, R., Wheelwright, M., & Metzger, J. M. (2024) · JCI Insight · doi:10.1172/jci.insight.163334
Self-citationBethea, M. M., Cook, T. M., Stafford, P., Knaub, L. A., Martinez, M. E., Schniedewind, B., Christians, U., Hendrix, J. J., Mestroni, L., Graw, S. L., et al. (2025) · Endocrinology · doi:10.1210/endocr/bqaf181
Wang, Z., She, G., Wang, C., Ferens, D. M., Salimova, E., Widdop, R. E., Gaspari, T. A., & Samuel, C. S. (2026) · Life Sciences · doi:10.1016/j.lfs.2026.124472
- Authors
- Barnabei, M. S., Palpant, N. J., & Metzger, J. M.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Metzger, Joseph M.
- Venue
- Physiological Genomics
- Publisher
- American Physiological Society
- Published
- 2010-10
- Volume
- 42A
- Issue
- 2
- Pages
- 103-113
- ISSN
- 1094-8341 (ISSN-L)
- 1531-2267
- PMC
- PMC2957793
- OpenAlex
- W2072625807
- Cited by
- 88
- References
- 62
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 7 · 2022: 5 · 2021: 4 · 2020: 10 · 2019: 3 · 2018: 7 · 2017: 4 · 2016: 11 · 2015: 11 · 2014: 5 · 2013: 7 · 2012: 5
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Physiological Genomics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL059301)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- inbred mouse strains, genetic divergence, cardiac function, C57BL/6J mice, C3H/HeJ, DBA/2J, BALB/cJ, ischemia, acute hypoxia, esmolol, acute decompensated heart failure, genetic modifiers, mouse strain comparison
- MeSH terms
- Adrenergic beta-Antagonists, Animals, Hypoxia, Heart, Heart Function Tests, Hemodynamics, Mice, Inbred Strains, Mice, Transgenic, Myocardial Ischemia, Mice, Embryonic Stem Cells, 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