Cited by 429Macrophage Migration Inhibitory FactorCardiac Ischemia and ReperfusionMetabolism, Diabetes, and Cancer

The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.

Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart

Miller, Edward J., Li, Ji, Leng, Lin, McDonald, Courtney, Atsumi, Toshiya, Bucala, Richard, Young, Lawrence H.·2008·Nature

DOI 10.1038/nature06504

Open this paper in CoChat — free account

Abstract

Understanding cellular response to environmental stress has broad implications for human disease. AMP-activated protein kinase (AMPK) orchestrates the regulation of energy-generating and -consuming pathways, and protects the heart against ischaemic injury and apoptosis. A role for circulating hormones such as adiponectin and leptin in the activation of AMPK has received recent attention. Whether local autocrine and paracrine factors within target organs such as the heart modulate AMPK is unknown. Here we show that macrophage migration inhibitory factor (MIF), an upstream regulator of inflammation, is released in the ischaemic heart, where it stimulates AMPK activation through CD74, promotes glucose uptake and protects the heart during ischaemia-reperfusion injury. Germline deletion of the Mif gene impairs ischaemic AMPK signalling in the mouse heart. Human fibroblasts with a low-activity MIF promoter polymorphism have diminished MIF release and AMPK activation during hypoxia. Thus, MIF modulates the activation of the cardioprotective AMPK pathway during ischaemia, functionally linking inflammation and metabolism in the heart. We anticipate that genetic variation in MIF expression may impact on the response of the human heart to ischaemia by the AMPK pathway, and that diagnostic MIF genotyping might predict risk in patients with coronary artery disease.

Integrity signals

Registry

Crossref · 10.1038/nature06504

Cites

33 of 33 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase
Minokoshi, Y., Kim, Y.-B., Peroni, O. D., Fryer, L. G. D., Müller, C., Carling, D., & Kahn, B. B. (2002) · Nature · doi:10.1038/415339a · Cited by 2,053
Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase
Hawley, S. A., Pan, D. A., Mustard, K. J., Ross, L., Bain, J., Edelman, A. M., Frenguelli, B. G., & Hardie, D. G. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.009 · Cited by 1,589
MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment
Bernhagen, J., Krohn, R. M., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., et al. (2007) · Nature Medicine · doi:10.1038/nm1567 · Cited by 1,292
Self-citation
MIF Signal Transduction Initiated by Binding to CD74
Leng, L., Metz, C. N., Fang, Y., Xu, J., Donnelly, S., Baugh, J., Delohery, T., Chen, Y., Mitchell, R. A., & Bucala, R. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030286 · Cited by 1,154
Self-citation
MIF as a glucocorticoid-induced modulator of cytokine production
Calandra, T., Bernhagen, J., Metz, C. N., Spiegel, L. A., Bacher, M., Donnelly, T. M., Cerami, A., & Bucala, R. (1995) · Nature · doi:10.1038/377068a0 · Cited by 1,148
Self-citation
The Molecular Basis of Skeletal Muscle Atrophy
Jackman, R. W., & Kandarian, S. C. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00579.2003 · Cited by 1,008
MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia
Bernhagen, J., Calandra, T., Mitchell, R. A., Martin, S. B., Tracey, K. J., Voelter, W., Manogue, K. R., Cerami, A., & Bucala, R. (1993) · Nature · doi:10.1038/365756a0 · Cited by 1,001
Self-citation
The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor.
Calandra, T., Bernhagen, J., Mitchell, R. A., & Bucala, R. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.6.1895 · Cited by 986
Self-citation
Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2–dependent mechanisms
Shibata, R., Sato, K., Pimentel, D. R., Takemura, Y., Kihara, S., Ohashi, K., Funahashi, T., Ouchi, N., & Walsh, K. (2005) · Nature Medicine · doi:10.1038/nm1295 · Cited by 982
Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia
Marsin, A.-S., Bertrand, L., Rider, M. H., Deprez, J., Beauloye, C., Vincent, M. F., den Berghe, G. V., Carling, D., & Hue, L. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00742-9 · Cited by 853

Show all 33 references

Sorted by citations

Items 301–400 of 428

Coculture with hematopoietic stem cells protects cardiomyocytes against apoptosis via paracrine activation of AKT
Rosenberg, M. E., Lutz, M., Kühl, C., Will, R. D., Eckstein, V., Krebs, J., Katus, H. A., & Frey, N. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-115 · Cited by 16
Xenon triggers pro-inflammatory effects and suppresses the anti-inflammatory response compared to sevoflurane in patients undergoing cardiac surgery
Breuer, T., Emontzpohl, C., Coburn, M., Benstoem, C., Rossaint, R., Marx, G., Schälte, G., Bernhagen, J., Bruells, C. S., Goetzenich, A., et al. (2015) · Critical Care · doi:10.1186/s13054-015-1082-7 · Cited by 16
Macrophage migration inhibitory factor induces autophagy to resist hypoxia/serum deprivation-induced apoptosis via the AMP-activated protein kinase/mammalian target of rapamycin signaling pathway
Xia, W., & Hou, M. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4847 · Cited by 16
Intermittent fasting activates macrophage migration inhibitory factor and alleviates high-fat diet-induced nonalcoholic fatty liver disease
Li, D., Dun, Y., Qi, D., Ripley-Gonzalez, J. W., Dong, J., Zhou, N., Qiu, L., Zhang, J., Zeng, T., You, B., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-40373-5 · Cited by 16
P115 promotes growth of gastric cancer through interaction with macrophage migration inhibitory factor
Li, X. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i46.8619 · Cited by 15
Macrophage Migration Inhibitory Factor Induces Contractile and Mitochondria Dysfunction by Altering Cytoskeleton Network in the Human Heart*
Préau, S., Montaigne, D., Modine, T., Fayad, G., Koussa, M., Tardivel, M., Durocher, A., Saulnier, F., Marechal, X., & Nevière, R. (2013) · Critical Care Medicine · doi:10.1097/ccm.0b013e31827c0d8c · Cited by 15
Developmental endothelial locus-1 inhibits MIF production through suppression of NF-κB in macrophages
Lee, S., Kim, D.-Y., KANG, Y.-Y., Kim, H., JANG, J., LEE, M.-N., Oh, G. T., Kang, S., & Choi, E. Y. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.1645 · Cited by 14
MIF gene rs755622 polymorphism positively associated with acute coronary syndrome in Chinese Han population: case–control study
Du, G., Luo, J., Wang, D., Li, Y., Fang, B., Li, X., Gao, X., & Yang, Y. (2020) · Scientific Reports · doi:10.1038/s41598-019-56949-z · Cited by 14
Macrophage migration inhibitory factor promotes expression of GLUT4 glucose transporter through MEF2 and Zac1 in cardiomyocytes
Liang, Y., Yuan, W., Zhu, W., Zhu, J.-N., Lin, Q., Zou, X., Deng, C., Fu, Y., Zheng, X., Yang, M., et al. (2015) · Metabolism · doi:10.1016/j.metabol.2015.09.007 · Cited by 14
The Role of Macrophage Migration Inhibitory Factor in Anesthetic-Induced Myocardial Preconditioning
Goetzenich, A., Kraemer, S., Rossaint, R., Bleilevens, C., Dollo, F., Laura, S., Setareh, R.-A., Beckers, C., Soppert, J., Lue, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092827 · Cited by 14
CD74 Promotes Cyst Growth and Renal Fibrosis in Autosomal Dominant Polycystic Kidney Disease
Zhou, J. X., Cheng, A. S., Chen, L., Li, L. X., Agborbesong, E., Torres, V. E., Harris, P. C., & Li, X. (2024) · Cells · doi:10.3390/cells13060489 · Cited by 13
A MIF‐Derived Cyclopeptide that Inhibits MIF Binding and Atherogenic Signaling via the Chemokine Receptor CXCR2
Krammer, C., Kontos, C., Dewor, M., Hille, K., Volta, B. D., Bounkari, O. E., Taş, K., Sinitski, D., Brandhofer, M., Megens, R. T. A., et al. (2020) · ChemBioChem · doi:10.1002/cbic.202000574 · Cited by 13
In Silico Design for Adenosine Monophosphate‐Activated Protein Kinase Agonist from Traditional Chinese Medicine for Treatment of Metabolic Syndromes
Tang, H., & Chen, C. Y. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/928589 · Cited by 13
Macrophage migration inhibitory factor (MIF) in the development and progression of pulmonary arterial hypertension
Ahmed, M., & Miller, E. J. (2018) · Global Cardiology Science and Practice · doi:10.21542/gcsp.2018.14 · Cited by 13
Self-citation
Prognostic significance and dynamic change of plasma macrophage migration inhibitory factor in patients with acute ST-elevation myocardial infarction
Deng, F., Zhao, Q., Deng, Y., Wu, Y., Zhou, D. F., Liu, W., Yuan, Z., & Zhou, J. (2018) · Medicine · doi:10.1097/md.0000000000012991 · Cited by 13
Palmitate‐mediated induction of neuropeptide Y expression occurs through intracellular metabolites and not direct exposure to proinflammatory cytokines
Tran, A., He, W., Chen, J. T. C., Wellhauser, L., Hopperton, K. E., Bazinet, R. P., & Belsham, D. D. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15504 · Cited by 12
Exploring the potential molecular mechanism of trastuzumab-induced cardiotoxicity based on RNA sequencing and bioinformatics analysis
Hou, H., Xu, Y., Xie, M.-L., & Chen, R. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115388 · Cited by 12
2-(3,4-Dihydro-2H-pyrrolium-1-yl)-3oxoindan-1-olate (DHPO), a novel, synthetic small molecule that alleviates insulin resistance and lipid abnormalities
Kandadi, M. R., Prabhakar, K. R., Unnikrishnan, M. K., Boddu, S. P., Hua, Y., Li, J., Du, ‬., Ren, J. T., & Sreejayan, N. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.09.018 · Cited by 12
Self-citation
Proteomic analysis at the subcellular level for host targets against influenza A virus (H1N1)
Zhao, H., Yang, J., Kang, L., Ding, X., Lin, R., Ma, Y., Liu, J., Zhong, Z., Qian, X., Bo, X., et al. (2013) · Antiviral Research · doi:10.1016/j.antiviral.2013.10.005 · Cited by 12
Systems Level Regulation of Cardiac Energy Fluxes Via Metabolic Cycles: Role of Creatine, Phosphotransfer Pathways, and AMPK Signaling
Saks, V. A., Schlattner, U., Tokarska-Schlattner, M., Wallimann, T., Bagur, R., Zorman, S., Pelosse, M., Santos, P. D. D., Boucher, F. R., Käämbre, T., et al. (2013) · Springer series in biophysics · doi:10.1007/978-3-642-38505-6_11 · Cited by 13
Mannose Binding Lectin and Macrophage Migration Inhibitory Factor Gene Polymorphisms in Turkish Children with Cardiomyopathy: No Association with MBL2 Codon 54 A/B Genotype, but an Association between MIF -173 CC Genotype
Araz, N. Ç., Balcı, S. O., Başpınar, O., Sever, T., Balat, A., & Pehlıvan, S. (2012) · International Journal of Medical Sciences · doi:10.7150/ijms.4787 · Cited by 12
Sauchinone augments cardiomyocyte viability by enhancing autophagy proteins -PI3K, ERK(1/2), AMPK and Beclin-1 during early ischemia-reperfusion injury in vitro.
Thapalia, B. A., Zhou, Z., & Lin, X. (2016) · Europe PMC (PubMed Central) · Cited by 12
Downregulation of adipose LPL by PAR2 contributes to the development of hypertriglyceridemia
Huang, Y., Chen, L., Li, L., Qi, Y., Tong, H., Wu, H., Xu, J., Leng, L., Cheema, S. K., Sun, G., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.173240 · Cited by 11
Self-citation
The therapeutic efficacy and clinical translation of mesenchymal stem cell-derived exosomes in cardiovascular diseases
Zhang, H., Wan, X., Tian, J., An, Z., Liu, L., Zhao, X., Zhou, Y., Zhang, L., Ge, C.-J., & Song, X. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115551 · Cited by 11
Myokines: Do they really exist?
Manabe, Y., Miyatake, S., & Takagi, M. (2012) · The Journal of Physical Fitness and Sports Medicine · doi:10.7600/jpfsm.1.51 · Cited by 11
AMPK and the Atrial Response to Metabolic Inhibition∗
Kim, G. E., & Young, L. H. (2015) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2015.04.054 · Cited by 11
Self-citation
Determining the Optimal Administration Conditions under Which MIF Exerts Neuroprotective Effects by Inducing BDNF Expression and Inhibiting Apoptosis in an In Vitro Stroke Model
Jung, C., Kim, M. H., Kim, Y. Y., Kim, J. A., Ko, E. J., Lee, S. H., & Kim, D. Y. (2021) · Brain Sciences · doi:10.3390/brainsci11020280 · Cited by 10
High expression levels and localization of Sox5 in dilated cardiomyopathy
Liu, Y., Jiang, B., Cao, Y., Chen, W., Yin, L., Xu, Y., & Qiu, Z. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11180 · Cited by 10
Recombinant dsAAV9-mediated Endogenous Overexpression of Macrophage Migration Inhibitory Factor Alleviates Myocardial Ischemia–Reperfusion Injury via Activating AMPK and ERK1/2 Signaling Pathways
Chen, X., Gai, M., He, C., Zhao, B.-H., Liu, F., Ma, X., Ma, Y.-T., Gao, X.-M., & Chen, B. (2025) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-024-07662-1 · Cited by 9
The Role of Macrophage Inhibitory Factor in TAA-Induced Liver Fibrosis in Mice: Modulatory Effects of Betaine
Radosavljević, T. S., Vukićević, D., Djuretić, J., Gopčević, K., Labudović‐Borović, M., Stankovic, S. D., Samardžić, J., Radosavljević, M., Vučević, D. B., & Jakovljevic, V. L. (2024) · Biomedicines · doi:10.3390/biomedicines12061337 · Cited by 10
Functional variants in the promoter region of macrophage migration inhibitory factor rs755622 gene (MIF G173C) among patients with heart failure: Association with echocardiographic indices and disease severity
El-Mahdy, R. I., Saleem, T. H., Essam, O. M., & Algowhary, M. (2020) · Heart & Lung · doi:10.1016/j.hrtlng.2020.07.015 · Cited by 9
Lack of Macrophage Migration Inhibitory Factor Reduces Susceptibility to Ventricular Arrhythmias During the Acute Phase of Myocardial Infarction
Lyu, J., Huang, J. Q., Wu, J., Yu, T., Wei, X., & Lei, Q. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s304553 · Cited by 9
Activity‐Based Proteome Profiling Probes Based on Woodward's Reagent K with Distinct Target Selectivity
Qian, Y., Schürmann, M., Janning, P., Hedberg, C., & Waldmann, H. (2016) · Angewandte Chemie · doi:10.1002/ange.201602666 · Cited by 9
Impact of MIF Gene Promoter Variations on Risk of Rheumatic Heart Disease and Its Age of Onset in Saudi Arabian Patients
Abdallah, A. M., Almazroea, A., Alharbi, W. N. A., Al-Harbi, N. A., El-Dardear, A., Almohammadi, Y., & Al-Harbi, K. M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00098 · Cited by 9
MIF and insulin: Lifetime companions from common genesis to common pathogenesis
Stošić‐Grujičić, S., Saksida, T., Miljković, D. M., & Stojanović, I. (2019) · Cytokine · doi:10.1016/j.cyto.2019.154792 · Cited by 9
Distinct roles of MIF in the pathogenesis of ischemic heart disease
Zhao, L., Zhao, B.-H., Ruze, A., Li, Q., Deng, A.-X., & Gao, X.-M. (2024) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2024.10.005 · Cited by 8
The distinct functions of MIF in inflammatory cardiomyopathy
Pressley, K. R., Naseem, Y., Nalawade, S. A., & Forsthuber, T. G. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1544484 · Cited by 8
Macrophage migration inhibitory factor superfamily in tumor metabolism: mechanistic insights and therapeutic potential
Xie, W., Dong, Y., Lv, J., & Wang, X. (2026) · Biochemical Pharmacology · doi:10.1016/j.bcp.2026.117720 · Cited by 8
Fasudil, a ROCK inhibitor, preserves limb integrity in a mouse model of unilateral critical limb ischemia: Possible interplay of inflammatory and angiogenic signaling pathways
El-Waseif, A. G., Nader, M. A., Salem, H. A., & Elshaer, S. L. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.121019 · Cited by 8
AMPK and O-GlcNAcylation: interplay in cardiac pathologies and heart failure
Vanni, E., Beauloye, C., Horman, S., & Bertrand, L. (2024) · Essays in Biochemistry · doi:10.1042/ebc20240003 · Cited by 8
Increased circulating macrophage migration inhibitory factor levels are associated with coronary artery disease
Yüksel, A., Bilgir, F., Bilgir, O., Çalan, M., & Bozkaya, G. (2015) · Clinics · doi:10.6061/clinics/2015(03)03 · Cited by 8
AMPK Inhibition Enhances the Neurotoxicity of Cu(II) in SH-SY5Y Cells
Lan, A., Xiong, X.-J., Chen, J., Wang, X., Chai, Z., & Hu, Y. (2016) · Neurotoxicity Research · doi:10.1007/s12640-016-9651-3 · Cited by 8
Protective cardiac conditioning by an atypical cytokine
Bernhagen, J. (2019) · Clinical Science · doi:10.1042/cs20190036 · Cited by 8
Association between MIF gene promoter rs755622 and susceptibility to coronary artery disease and inflammatory cytokines in the Chinese Han population
Luo, J., Fang, B., Du, G., Liu, F., Li, Y., Tian, T., Li, X., Gao, X., & Yang, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-87580-6 · Cited by 8
Macrophage Migration Inhibitory Factor Predicts Outcome in Complex Aortic Surgery
Gombert, A., Stoppe, C., Foldenauer, A. C., Schuerholz, T., Martin, L., Kalder, J., Schälte, G., Marx, G., Jacobs, M. J. H. M., & Grommes, J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112374 · Cited by 7
Characteristics of expression of goose invariant chain gene and comparison of its structure among different species
Chen, F., Pan, L., Dai, Y., Ye, H., Liu, S., & Weiwei, Y. (2011) · Poultry Science · doi:10.3382/ps.2010-01336 · Cited by 7
Correlations of MIF polymorphism and serum levels of MIF with glucocorticoid sensitivity of sudden sensorineural hearing loss
Zhu, W.-Y., Jin, X., Ma, Y.-C., & Liu, Z.-B. (2019) · Journal of International Medical Research · doi:10.1177/0300060519893870 · Cited by 7
Chemokine Contribution in Stem Cell Engraftment into the Infarcted Myocardium
Liehn, E. A., Radu, E., & Schuh, A. (2013) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x11308040003 · Cited by 7
MIF Matters: The Macrophage Migration Inhibitory Factor and Kidney Injury
Unruh, M. L., Wagner, B., & Hallows, K. R. (2018) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2018.07.003 · Cited by 7
Macrophage migration inhibitory factor MtMIF3 prevents the premature aging of Medicago truncatula nodules
Wang, L., Yang, J., Tan, W., Guo, Y., Li, J., Duan, C., Wei, G., & Chou, M. (2022) · Plant Cell & Environment · doi:10.1111/pce.14515 · Cited by 6
Self-citation
Macrophage migration inhibitory factor as a therapeutic target in neuro-oncology: A review
Jarmula, J., Lee, J., Lauko, A. J., Rajappa, P., Grabowski, M. M., Dhawan, A., Chen, P., Bucala, R., Vogelbaum, M. A., & Lathia, J. D. (2024) · Neuro-Oncology Advances · doi:10.1093/noajnl/vdae142 · Cited by 6
Self-citation
Sestrin2 serves as a scaffold protein to maintain cardiac energy and metabolic homeostasis during pathological stress
Seale, B. C., Slotabec, L. A., Nguyen, J. D., Wang, H., Patterson, C., Filho, F., Rouhi, N., Adenawoola, M. I., & Li, J. (2024) · The FASEB Journal · doi:10.1096/fj.202401404r · Cited by 6
Self-citation
Macrophage Migration Inhibitory Factor Inhibition Is Deleterious for High-Fat Diet-Induced Cardiac Dysfunction
Palud, A., Marciniak, C., Montaigne, D., Marechal, X., Ballot, C., Hassoun, S. M., Decoster, B., Nevière, R., & Lancel, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058718 · Cited by 6
Antifibrotic role of macrophage migration inhibitory factor: Discovery of an unexpected function
Thủy, L. T. T., Kawada, N., Groszmann, R. J., Iwakiri, Y., & Taddei, T. H. (2012) · Hepatology · doi:10.1002/hep.25605 · Cited by 6
Macrophage migration inhibitory factor in acute kidneyinjury
Du, Y., Hao, H., Ma, H., & Liu, H. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.945827 · Cited by 6
Effects of macrophage migration inhibitory factor on cardiac reperfusion injury in mice with depression induced by constant-darkness
Tao, L., Huang, M., Saroj-Thapa, Wang, J., Wu, S., He, F., Huang, K., Xue, Y., Lingwei-Jin, Liao, L., et al. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.12.039 · Cited by 6
Impaired Myocardial MIF/AMPK Activation Aggravates Myocardial Ischemia Reperfusion Injury in High-Fat Diet-Induced Obesity
Meng, F., Li, D., Song, B., & Li, L. (2019) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530319666190326143254 · Cited by 6
Identification of Hub Genes and Immune Infiltration in Pediatric Biliary Atresia by Comprehensive Bioinformatics Analysis
Li, Y., Ye, H., & Ding, Y.-X. (2022) · Children · doi:10.3390/children9050697 · Cited by 5
Elevated Macrophage Migration Inhibitory Factor 1 Is Associated with Left and Right Ventricular Systolic Dysfunction in Heart Failure with Reduced Ejection Fraction
Szabo, T. M., Vass, M., Germán-Salló, M., Frigy, A., & Nagy, E. E. (2025) · Biomedicines · doi:10.3390/biomedicines13051087 · Cited by 5
Novel function of macrophage migration inhibitory factor in regulating post-infarct inflammation and the therapeutic significance
Zhao, L., Du, G., Ruze, A., Qi, H.-Z., Zhang, C., Li, Q., Deng, A.-X., Zhao, B.-H., Hu, S., Gai, M., et al. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.05.030 · Cited by 5
Graft‐derived macrophage migration inhibitory factor correlates with hepatocellular injury in patients undergoing liver transplantation
Baron‐Stefaniak, J., Schiefer, J., Miller, E. J., Plöchl, W., Krenn, C. G., Berlakovich, G. A., Baron, D. M., & Faybik, P. (2017) · Clinical Transplantation · doi:10.1111/ctr.12982 · Cited by 5
Self-citation
Hypoxia Rapidly Induces the Expression of Cardiomyogenic Factors in Human Adipose-Derived Adherent Stromal Cells
Choi, J., Moon, H., Jung, S. H., Lim, S., Lee, S., Kim, I.-K., Lee, H.-B., Lee, J., Song, B., Kim, S. W., et al. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8081231 · Cited by 5
Macrophage migration inhibitory factor regulates specific innate immune sensor responses in gingival epithelial cells
Kantrong, N., Chang, A. M., Bamashmous, S., Hajjar, A. M., Bucala, R. J., & Darveau, R. P. (2022) · Journal of Periodontology · doi:10.1002/jper.21-0598 · Cited by 5
Self-citation
Relationship Between Serum Macrophage Migration Inhibitory Factor Level and Insulin Resistance, High-Sensitivity C-Reactive Protein and Visceral Fat Mass in Prediabetes
Bilgir, O., Gökçen, B., Bilgir, F., Güler, A., Çalan, M., Yüksel, A., Aslanıpour, B., Akşit, M., & Bozkaya, G. (2017) · The American Journal of the Medical Sciences · doi:10.1016/j.amjms.2017.10.006 · Cited by 5
Myeloid Cells in Myocardial Ischemic Injury: The Role of the Macrophage Migration Inhibitory Factor
Wang, H., Rouhi, N., Slotabec, L. A., Seale, B. C., Wen, C., Filho, F., Adenawoola, M. I., & Li, J. (2024) · Life · doi:10.3390/life14080981 · Cited by 4
Self-citation
Biphasic protective effects of macrophage migration inhibitory factor in ischemia/reperfusion-induced acute kidney injury
Du, Y., Feng, C., Zhou, L., Wang, T., Ma, H., & Liu, H. (2025) · Communications Biology · doi:10.1038/s42003-025-08455-4 · Cited by 4
AMP-Activated Protein Kinase: A Metabolic Stress Sensor in the Heart
Pelosse, M., Tokarska-Schlattner, M., & Schlattner, U. (2015) · Springer eBooks · doi:10.1007/978-3-319-15263-9_10 · Cited by 4
Hydrogels based on schizophyllan
Hou, Y., & Li, J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-95351-1.00003-x · Cited by 4
Self-citation
Single-cell transcriptomics reveals writers of RNA modification-mediated immune microenvironment and cardiac resident Macro-MYL2 macrophages in heart failure
Yang, Y., Li, X.-W., Chen, H., Tang, Q.-D., Li, Y., Xu, J., & Xie, J. (2024) · BMC Cardiovascular Disorders · doi:10.1186/s12872-024-04080-x · Cited by 4
Depression exacerbates myocardial ischemia-reperfusion injury in mice via CNR2 gene and MIF-AMPK signaling pathway
Qian, L., Zhang, S., Lin, C., Lin, J., & Li, Z. (2024) · International Journal of Cardiology · doi:10.1016/j.ijcard.2024.132505 · Cited by 4
Plasma Macrophage Migration Inhibitory Factor Predicts Graft Function Following Kidney Transplantation: A Prospective Cohort Study
Ye, Y., Han, F., Ma, M., Sun, Q., Huang, Z., Zheng, H., Yang, Z., Luo, Z., Liao, T., Li, H., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.708316 · Cited by 4
Diabetes Mellitus and Cardiopulmonary Bypass (CPB): Pathophysiological Mechanisms Related to Inflammation and Cardiovascular Disease
Stougiannou, T. M., Koufakis, T., Παπάνας, Ν., & Karangelis, D. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47110911 · Cited by 3
Macrophage migration inhibitory factor (MIF): can functional insights pave the way for future therapeutics in cardiovascular diseases?
Storozhenko, T. Y., Petyunina, O. V., Berezin, A. A., & Kopytsya, M. P. (2025) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2025.2537414 · Cited by 3
Tetramethylpyrazine (TMP) switches energy signalling from the PKCζ-GLUT4-glucose pathway back to the SIRT1-CD36-fatty acid pathway similar to resveratrol to ameliorate cardiac myocyte lipotoxicity
Chen, Y.-P., Tsai, C.-W., Hsieh, D. J., Shen, C.-Y., Ho, T., Padma, V. V., Kuo, W., & Huang, C. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.09.062 · Cited by 3
Macrophage Inhibitory Factor in Myocardial Oxidative Stress and Inflammation During Thioacetamide-Induced Liver Fibrosis: Modulation by Betaine
Djuretić, J., Filipović, J., Branković, M., Stankovic, S. D., Samardžić, J., Vučević, D. B., & Radosavljević, T. S. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47090728 · Cited by 2
MIF in Atherosclerosis
Noels, H., Bernhagen, J., & Weber, C. (2012) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814335362_0017 · Cited by 2
Early Prediction of a Pre-Symptomatic Neurodegeneration Disorder by Measuring Macrophage Inhibitory Factor Level in Diabetic Patients
Khalil, R. M., Alaa, S., Eissa, H., & Youssef, I. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215561 · Cited by 2
An efficient approach for overproduction of DNA polymerase from Pyrococcus furiosus using an optimized autoinduction system in Escherichia coli
Hadi, M. I., Laksmi, F. A., Helbert, Amalia, A. R., Muhammad, A. D., & Violando, W. A. (2024) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-024-04127-3 · Cited by 2
The Polymorphisms rs2516839 of USF1 and -173G/C of MIF were not Associated with Coronary Artery Disease but Dyslipidemia in a Chinese Population
Gong, C. W. Y. (2014) · Journal of Cardiovascular Diseases & Diagnosis · doi:10.4172/2329-9517.1000177 · Cited by 2
MIF and the Chemokine Axis
Kraemer, S., Weber, C., & Bernhagen, J. (2012) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814335362_0002 · Cited by 2
Constructive feedback on the link between depression and acute myocardial infarction: A response to recent findings
Bilquees, A., Saleem, D., & Aamir, M. (2025) · International Journal of Cardiology · doi:10.1016/j.ijcard.2025.133156 · Cited by 1
The role of macrophage migration inhibitory factor (MIF) in the pathogenesis and progression of cardiovascular disease
Mahabhashyam, S., Harris, J., Bernhagen, J., Vinh, A., & Colafella, K. M. M. (2026) · British Journal of Pharmacology · doi:10.1111/bph.70584 · Cited by 1
Macrophage Migration Inhibitory Factor, the Zelig of Cytokines, Is a Chaperone for SOD1 in Non-Neuronal Cells
Ransohoff, R. M. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.054 · Cited by 1
MIF-Dependent Regulation of Monocyte/Macrophage Polarization
Yaddanapudi, K., & Mitchell, R. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-52354-5_4 · Cited by 1
Physiology of Cardiac Ischemia
Sylvies, F. R., Thomas, G. S., & Ellestad, M. (2018) · Oxford University Press eBooks · doi:10.1093/med/9780190225483.003.0002 · Cited by 1
Aging-associated Alteration in the Cardiac MIF-AMPK Cascade in Response to Ischemic StressPreprint
Ma, H., Wang, J., Lane, E., Leng, L., Wang, W., Ren, J. T., Bucala, R., & Li, J. (2008) · Nature Precedings · doi:10.1038/npre.2008.2466.1 · Cited by 1
Self-citation
Complex cellular physiology underlies the use of FDG-PET imaging in investigating post-infarction remodeling
Miller, E. J. (2020) · Journal of Nuclear Cardiology · doi:10.1007/s12350-019-02008-z · Cited by 1
Self-citation
Macrophage Migration Inhibitory Factor: the Next Adjunct to Reperfusion Therapy in Acute Myocardial Infarction?
Keefe, J. A., & Wehrens, X. H. T. (2025) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-025-07726-w · Cited by 1
Molecular mechanisms of the unconventional secretion of macrophage migration inhibitory factor (MIF)
Merk, M., Baumgärtner, W., & Bernhagen, J. (2008) · RWTH Publications (RWTH Aachen) · Cited by 1
D-Dopachrome tautomerase (D-DT) : functional homologue or cross-regulator of macrophage migration inhibitory factor (MIF)?
Schulte, W., & Bernhagen, J. (2011) · RWTH Publications (RWTH Aachen)
Efeito do hormônio tiroideano na função cardíaca no modelo de isquemia/reperfusão em ratos. Papel do receptor AT2 e da via intracelular AMPK.
Tavares, F. M. (2012) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.42.2012.tde-24072012-131445
Therapeutic Angiogenesis for Critical Limb Ischemia: Complex Mechanisms and Future Challenges
Cao, Y. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-906-8_7
Expressão do complexo receptor CD74 - CD44 para o fator de inibição de migração de macrófagos (MIF) na interface materno placentária em camundongos.
Martucci, M. F. (2011) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.42.2011.tde-26102011-142651
Untersuchungen von Phospho-AMPK α, VEGF-A und VEGF-R2 im Myokard sowie Analysen von morphologischen Veränderungen im Modell der chronischen Herzinsuffizienz induziert durch sequentielle, repetitive koronare Mikroembolisation an der Spezies Schaf
Heidrich, F. (2011) · doi:10.53846/goediss-1059
Function of the CD74 receptor in B cell pro-survival signaling in the context of chronic lymphocytic leukemia
Barthel, R. (2015) · Kölner Universitäts PublikationsServer (Universität zu Köln)
Interplay Between Metabolism and Oncogenic Process: Role of microRNAs
Ambedkar, B. R. (2015)
Genetic and Epigenetic Basis of Myocardial Ischemia and Reperfusion Injury
Karagiannis, T. C., Ververis, K., & Licciardi, P. V. (2013) · CRC Press eBooks · doi:10.1201/b14663-6
MIF in Cardiovascular Disease
Miller, E. J., Qi, D., Li, J., & Young, L. H. (2012) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814335362_0018
Self-citation
Autophagy Networks in Cardiovascular Diseases
Garcı́a, L., Bustamante, M., Pizarro, M., Quiroga, C., Rodriguez, A. E., Westermeier, F., Bernal-Sore, I., Castro, P., Lavandero, S., & Troncoso, R. (2016) · Springer eBooks · doi:10.1007/978-3-319-30079-5_14
AMP-activated protein kinase: a cellular energy sensor with a key role in metabolic disorders and in cancer
Lecture, N. M. (2011)

Authors: Miller, E. J., Li, J., Leng, L., McDonald, C., Atsumi, T., Bucala, R., & Young, L. H.
Affiliations: Yale University (US)
Hokkaido University (JP)
Corresponding author: Young, Lawrence H.
ORCID: Miller, Edward J.
Li, Ji
Leng, Lin
Bucala, Richard
Young, Lawrence H.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2008-01
Volume: 451
Issue: 7178
Pages: 578-582
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature06504
OpenAlex: W2039411604
Cited by: 429
References: 33
Citations by year: 2026: 11 · 2025: 15 · 2024: 14 · 2023: 14 · 2022: 18 · 2021: 22 · 2020: 16 · 2019: 30 · 2018: 29 · 2017: 20 · 2016: 26 · 2015: 33 · 2014: 27 · 2013: 38 · 2012: 34
FWCI: 11.59
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Macrophage Migration Inhibitory Factor
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Ischemia and Reperfusion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: macrophage migration inhibitory factor, AMPK, ischemia-reperfusion injury, CD74, glucose uptake, cardioprotection, inflammation, hypoxia, coronary artery disease, autocrine and paracrine signaling, energy metabolism
MeSH terms: Animals, Hypoxia, Antigens, Differentiation, B-Lymphocyte, Histocompatibility Antigens Class II, Coronary Artery Disease, Enzyme Activation, Genotype, Glucose, Humans, Macrophage Migration-Inhibitory Factors, Multienzyme Complexes, Myocardium, Polymorphism, Genetic, Promoter Regions, Genetic, Signal Transduction, Myocardial Reperfusion Injury, Myocardial Ischemia, Protein Serine-Threonine Kinases, Genetic Predisposition to Disease, Mice, Rats, AMP-Activated Protein Kinases

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

Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks