MIF and CXCL12 in Cardiovascular Diseases: Functional Differences and Similarities
Open accessAbstract
Coronary artery disease (CAD) as part of the cardiovascular diseases is a pathology caused by atherosclerosis, a chronic inflammatory disease of the vessel wall characterized by a massive invasion of lipids and inflammatory cells into the inner vessel layer (intima) leading to the formation of atherosclerotic lesions; their constant growth may cause complications such as flow-limiting stenosis and plaque rupture, the latter triggering vessel occlusion through thrombus formation. Pathophysiology of CAD is complex and over the last years many players have entered the picture. One of the latter being chemokines (small 8-12 kDa cytokines) and their receptors, known to orchestrate cell chemotaxis and arrest. Here, we will focus on the chemokine CXCL12, also known as stromal cell-derived factor 1 (SDF-1) and the chemokine-like function chemokine, macrophage migration-inhibitory factor (MIF). Both are ubiquitously expressed and highly conserved proteins and play an important role in cell homeostasis, recruitment, and arrest through binding to their corresponding chemokine receptors CXCR4 (CXCL12 and MIF), ACKR3 (CXCL12), and CXCR2 (MIF). In addition, MIF also binds to the receptor CD44 and the co-receptor CD74. CXCL12 has mostly been studied for its crucial role in the homing of (hematopoietic) progenitor cells in the bone marrow and their mobilization into the periphery. In contrast to CXCL12, MIF is secreted in response to diverse inflammatory stimuli, and has been associated with a clear pro-inflammatory and pro-atherogenic role in multiple studies of patients and animal models. Ongoing research on CXCL12 points at a protective function of this chemokine in atherosclerotic lesion development. This review will focus on the role of CXCL12 and MIF and their differences and similarities in CAD of high risk patients.
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MIF is a chemokine with pro-inflammatory and pro-atherogenic effects.
“a chemokine with pro-inflammatory and pro-atherogenic effects,51”
From Aortic valve-specific genes dysregulated in calcific aortic valve stenosis as potential biomarkers and therapeutic targets (2025) · cites this paper as [51]
CXCL12 was shown to be expressed in human atherosclerotic lesions.
“CXCL12 is a chemokine involved in inflammatory response, leukocyte chemotaxis, and progenitor cell mobilization, which was shown to be expressed in human atherosclerotic lesions.51”
From Aortic valve-specific genes dysregulated in calcific aortic valve stenosis as potential biomarkers and therapeutic targets (2025) · cites this paper as [51]
CXCL12 is a chemokine involved in inflammatory response, leukocyte chemotaxis, and progenitor cell mobilization.
“CXCL12 is a chemokine involved in inflammatory response, leukocyte chemotaxis, and progenitor cell mobilization”
From Aortic valve-specific genes dysregulated in calcific aortic valve stenosis as potential biomarkers and therapeutic targets (2025) · cites this paper as [51]
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Heart Disease and Stroke Statistics—2013 Update: A Report From the American Heart Association
Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Borden, W. B., Bravata, D. M., Dai, S., Ford, E. S., Fox, C. S., et al. (2013) · Circulation · doi:10.1161/cir.0b013e31828124ad · Cited by 5,292 · see citing works
Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Borden, W. B., Bravata, D. M., Dai, S., Ford, E. S., Fox, C. S., et al. (2013) · Circulation · doi:10.1161/cir.0b013e318282ab8f · Cited by 1,294 · see citing works
Brown, M. S., Ho, Y. K., & Goldstein, J. L. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)70568-7 · Cited by 722 · see citing works
Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis
Drechsler, M., Megens, R. T. A., van Zandvoort, M., Weber, C., & Soehnlein, O. (2010) · Circulation · doi:10.1161/circulationaha.110.961714 · Cited by 698 · see citing works
Self-citationCxcr7 controls neuronal migration by regulating chemokine responsiveness
Sánchez-Alcañiz, J. A., Haege, S., Mueller, W., Pla, R., Mackay, F., Schulz, S., López-Bendito, G., Stumm, R., & Marín, O. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.006 · Cited by 290 · see citing works
Stromal cell-derived factor-1α is cardioprotective after myocardial infarction
Saxena, A., Fish, J. E., White, M. D., Yu, S., Smyth, J. W. P., Shaw, R. M., DiMaio, J. M., & Srivastava, D. (2008) · Circulation · doi:10.1161/circulationaha.107.694992 · Cited by 237 · see citing works
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Research works printed but not linked: 165
- [1]Dahlof B. Cardiovascular disease risk factors: epidemiology and risk assessment. Am J Cardiol (2010) 105(1 Suppl): 3A– 9A. 10.1016/j.amjcard.2009.10.007 20102968 · DOI
- [2]Lloyd-Jones DM Cardiovascular risk prediction: basic concepts, current status, and future directions. Circulation (2010) 121(15): 1768– 77. 10.1161/CIRCULATIONAHA.109.849166 20404268 · DOI · Paper page
- [4]Hansson GK Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med (2005) 352(16): 1685– 95. 10.1056/NEJMra043430 15843671 · DOI · Paper page
- [5]Farouk SS Rader DJ Reilly MP Mehta NN. CXCL12: a new player in coronary disease identified through human genetics. Trends Cardiovasc Med (2010) 20(6): 204– 9. 10.1016/j.tcm.2011.08.002 22137643 PMC3235407 · DOI
- [6]Abi-Younes S Sauty A Mach F Sukhova GK Libby P Luster AD. The stromal cell-derived factor-1 chemokine is a potent platelet agonist highly expressed in atherosclerotic plaques. Circ Res (2000) 86(2): 131– 8. 10.1161/01.RES.86.2.131 10666407 · DOI
- [7]Stellos K Bigalke B Langer H Geisler T Schad A Kogel A Expression of stromal-cell-derived factor-1 on circulating platelets is increased in patients with acute coronary syndrome and correlates with the number of CD34+ progenitor cells. Eur Heart J (2009) 30(5): 584– 93. 10.1093/eurheartj/ehn566 19109356 · DOI
- [8]Rath D Chatterjee M Borst O Muller K Stellos K Mack AF Expression of stromal cell-derived factor-1 receptors CXCR4 and CXCR7 on circulating platelets of patients with acute coronary syndrome and association with left ventricular functional recovery. Eur Heart J (2014) 35(6): 386– 94. 10.1093/eurheartj/eht448 24168792 · DOI
- [9]Damas JK Waehre T Yndestad A Ueland T Muller F Eiken HG Stromal cell-derived factor-1alpha in unstable angina: potential antiinflammatory and matrix-stabilizing effects. Circulation (2002) 106(1): 36– 42. 10.1161/01.CIR.0000020001.09990.90 12093767 · DOI
- [10]Ghasemzadeh N Hritani AW De Staercke C Eapen DJ Veledar E Al Kassem H Plasma stromal cell-derived factor 1alpha/CXCL12 level predicts long-term adverse cardiovascular outcomes in patients with coronary artery disease. Atherosclerosis (2015) 238(1): 113– 8. 10.1016/j.atherosclerosis.2014.10.094 25461737 PMC4721225 · DOI
- [11]Wurster T Stellos K Haap M Seizer P Geisler T Otton J Platelet expression of stromal-cell-derived factor-1 (SDF-1): an indicator for ACS? Int J Cardiol (2013) 164(1): 111– 5. 10.1016/j.ijcard.2011.06.082 21737155 · DOI
- [12]Tereshchenko IP Petrkova J Mrazek F Lukl J Maksimov VN Romaschenko AG The macrophage migration inhibitory factor (MIF) gene polymorphism in Czech and Russian patients with myocardial infarction. Clin Chim Acta (2009) 402(1–2): 199– 202. 10.1016/j.cca.2008.12.034 19167373 · DOI
- [13]Burger-Kentischer A Goebel H Seiler R Fraedrich G Schaefer HE Dimmeler S Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation (2002) 105(13): 1561– 6. 10.1161/01.CIR.0000012942.49244.82 11927523 · DOI
- [14]Kong YZ Huang XR Ouyang X Tan JJ Fingerle-Rowson G Bacher M Evidence for vascular macrophage migration inhibitory factor in destabilization of human atherosclerotic plaques. Cardiovasc Res (2005) 65(1): 272– 82. 10.1016/j.cardiores.2004.09.020 15621056 · DOI
- [15]Müller II Müller KA Schönleber H Karathanos A Schneider M Jorbenadze R Macrophage migration inhibitory factor is enhanced in acute coronary syndromes and is associated with the inflammatory response. PLoS One (2012) 7(6): e38376. 10.1371/journal.pone.0038376 22693633 PMC3367911 · DOI
- [16]Makino A Nakamura T Hirano M Kitta Y Sano K Kobayashi T High plasma levels of macrophage migration inhibitory factor are associated with adverse long-term outcome in patients with stable coronary artery disease and impaired glucose tolerance or type 2 diabetes mellitus. Atherosclerosis (2010) 213(2): 573– 8. 10.1016/j.atherosclerosis.2010.09.004 20934703 · DOI
- [17]Müller II Müller KA Karathanos A Schönleber H Rath D Vogel S Impact of counterbalance between macrophage migration inhibitory factor and its inhibitor gremlin-1 in patients with coronary artery disease. Atherosclerosis (2014) 237(2): 426– 32. 10.1016/j.atherosclerosis.2014.09.010 25463068 · DOI
- [18]Chan W White DA Wang XY Bai RF Liu Y Yu HY Macrophage migration inhibitory factor for the early prediction of infarct size. J Am Heart Assoc (2013) 2(5): e000226. 10.1161/JAHA.113.000226 24096574 PMC3835222 · DOI
- [19]Boekholdt SM Peters RJ Day NE Luben R Bingham SA Wareham NJ Macrophage migration inhibitory factor and the risk of myocardial infarction or death due to coronary artery disease in adults without prior myocardial infarction or stroke: the EPIC-Norfolk prospective population study. Am J Med (2004) 117(6): 390– 7. 10.1016/j.amjmed.2004.04.010 15380495 · DOI
- [20]Rosengren A Hawken S Ounpuu S Sliwa K Zubaid M Almahmeed WA Association of psychosocial risk factors with risk of acute myocardial infarction in 11119 cases and 13648 controls from 52 countries (the INTERHEART study): case-control study. Lancet (2004) 364(9438): 953– 62. 10.1016/S0140-6736(04)17019-0 15364186 · DOI · Paper page
- [21]Yusuf S Hawken S Ounpuu S Dans T Avezum A Lanas F Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet (2004) 364(9438): 937– 52. 10.1016/S0140-6736(04)17018-9 15364185 · DOI · Paper page
- [22]Nahrendorf M Swirski FK. Lifestyle effects on hematopoiesis and atherosclerosis. Circ Res (2015) 116(5): 884– 94. 10.1161/CIRCRESAHA.116.303550 25722442 PMC4347940 · DOI
- [23]Kovacic S Bakran M. Genetic susceptibility to atherosclerosis. Stroke Res Treat (2012) 2012: 362941. 10.1155/2012/362941 22550613 PMC3329672 · DOI
- [24]Zarins CK Giddens DP Bharadvaj BK Sottiurai VS Mabon RF Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res (1983) 53(4): 502– 14. 10.1161/01.RES.53.4.502 6627609 · DOI
- [25]Williams KJ Tabas I The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol (1995) 15(5): 551– 61. 10.1161/01.ATV.15.5.551 7749869 PMC2924812 · DOI · Paper page
- [26]Hansson GK Hermansson A. The immune system in atherosclerosis. Nat Immunol (2011) 12(3): 204– 12. 10.1038/ni.2001 21321594 · DOI
- [27]Glass CK Witztum JL Atherosclerosis. the road ahead. Cell (2001) 104(4): 503– 16. 10.1016/S0092-8674(01)00238-0 11239408 · DOI
- [28]Kunjathoor VV Febbraio M Podrez EA Moore KJ Andersson L Koehn S Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem (2002) 277(51): 49982– 8. 10.1074/jbc.M209649200 12376530 · DOI
- [29]Pluddemann A Neyen C Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods (2007) 43(3): 207– 17. 10.1016/j.ymeth.2007.06.004 17920517 · DOI
- [30]Maxfield FR Tabas I. Role of cholesterol and lipid organization in disease. Nature (2005) 438(7068): 612– 21. 10.1038/nature04399 16319881 · DOI
- [32]Tall AR Yvan-Charvet L Terasaka N Pagler T Wang N. HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab (2008) 7(5): 365– 75. 10.1016/j.cmet.2008.03.001 18460328 · DOI · Paper page
- [33]Wang J Tong C Yan X Yeung E Gandavadi S Hare AA Limiting cardiac ischemic injury by pharmacological augmentation of macrophage migration inhibitory factor-AMP-activated protein kinase signal transduction. Circulation (2013) 128(3): 225– 36. 10.1161/CIRCULATIONAHA.112.000862 23753877 PMC3781594 · DOI
- [34]Murphy AJ Dragoljevic D Tall AR. Cholesterol efflux pathways regulate myelopoiesis: a potential link to altered macrophage function in atherosclerosis. Front Immunol (2014) 5: 490. 10.3389/fimmu.2014.00490 25352845 PMC4195367 · DOI
- [35]McLaren JE Michael DR Ashlin TG Ramji DP. Cytokines, macrophage lipid metabolism and foam cells: implications for cardiovascular disease therapy. Prog Lipid Res (2011) 50(4): 331– 47. 10.1016/j.plipres.2011.04.002 21601592 · DOI
- [36]Passlick B Flieger D Ziegler-Heitbrock HW. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood (1989) 74(7): 2527– 34. 2478233
- [37]Gautier EL Jakubzick C Randolph GJ. Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol (2009) 29(10): 1412– 8. 10.1161/ATVBAHA.108.180505 19759373 PMC2782657 · DOI · Paper page
- [38]Wong KL Tai JJ Wong WC Han H Sem X Yeap WH Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood (2011) 118(5): e16– 31. 10.1182/blood-2010-12-326355 21653326 · DOI
- [39]Zlotnik A Yoshie O Chemokines: a new classification system and their role in immunity. Immunity (2000) 12(2): 121– 7. 10.1016/S1074-7613(00)80165-X 10714678 · DOI
- [40]Geissmann F Jung S Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity (2003) 19(1): 71– 82. 10.1016/S1074-7613(03)00174-2 12871640 · DOI
- [41]Woollard KJ Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat Rev Cardiol (2010) 7(2): 77– 86. 10.1038/nrcardio.2009.228 20065951 PMC2813241 · DOI · Paper page
- [42]Ziegler-Heitbrock L Ancuta P Crowe S Dalod M Grau V Hart DN Nomenclature of monocytes and dendritic cells in blood. Blood (2010) 116(16): e74– 80. 10.1182/blood-2010-02-258558 20628149 · DOI
- [43]Sunderkotter C Nikolic T Dillon MJ Van Rooijen N Stehling M Drevets DA Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol (2004) 172(7): 4410– 7. 10.4049/jimmunol.172.7.4410 15034056 · DOI · Paper page
- [44]Zernecke A Bot I Djalali-Talab Y Shagdarsuren E Bidzhekov K Meiler S Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res (2008) 102(2): 209– 17. 10.1161/CIRCRESAHA.107.160697 17991882 · DOI
- [45]Zernecke A Shagdarsuren E Weber C. Chemokines in atherosclerosis: an update. Arterioscler Thromb Vasc Biol (2008) 28(11): 1897– 908. 10.1161/ATVBAHA.107.161174 18566299 · DOI
- [46]Swirski FK Libby P Aikawa E Alcaide P Luscinskas FW Weissleder R Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest (2007) 117(1): 195– 205. 10.1172/JCI29950 17200719 PMC1716211 · DOI
- [47]Moore KJ Sheedy FJ Fisher EA. Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol (2013) 13(10): 709– 21. 10.1038/nri3520 23995626 PMC4357520 · DOI · Paper page
- [48]Barreiro O Yanez-Mo M Serrador JM Montoya MC Vicente-Manzanares M Tejedor R Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol (2002) 157(7): 1233– 45. 10.1083/jcb.200112126 12082081 PMC2173557 · DOI
- [49]Gerhardt T Ley K. Monocyte trafficking across the vessel wall. Cardiovasc Res (2015) pii: cvv147. 10.1093/cvr/cvv147 25990461 PMC4592323 · DOI
- [50]Weber C Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med (2011) 17(11): 1410– 22. 10.1038/nm.2538 22064431 · DOI · Paper page
- [51]Weber C Fraemohs L Dejana E. The role of junctional adhesion molecules in vascular inflammation. Nat Rev Immunol (2007) 7(6): 467– 77. 10.1038/nri2096 17525755 · DOI
- [52]Carman CV Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol (2004) 167(2): 377– 88. 10.1083/jcb.200404129 15504916 PMC2172560 · DOI
- [53]Johnson JL Newby AC. Macrophage heterogeneity in atherosclerotic plaques. Curr Opin Lipidol (2009) 20(5): 370– 8. 10.1097/MOL.0b013e3283309848 19741337 PMC2850554 · DOI · Paper page
- [54]Shimada K. Immune system and atherosclerotic disease: heterogeneity of leukocyte subsets participating in the pathogenesis of atherosclerosis. Circ J (2009) 73(6): 994– 1001. 10.1253/circj.CJ-09-0277 19430164 · DOI
- [55]Wolfs IM Donners MM de Winther MP. Differentiation factors and cytokines in the atherosclerotic plaque micro-environment as a trigger for macrophage polarisation. Thromb Haemost (2011) 106(5): 763– 71. 10.1160/TH11-05-0320 21947328 · DOI
- [56]Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol (2010) 10(1): 36– 46. 10.1038/nri2675 19960040 PMC2854623 · DOI · Paper page
- [57]Tabas I Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol (2011) 13(3): 184– 90. 10.1038/ncb0311-184 21364565 PMC3107571 · DOI
- [58]Virmani R Burke AP Kolodgie FD Farb A. Vulnerable plaque: the pathology of unstable coronary lesions. J Interv Cardiol (2002) 15(6): 439– 46. 10.1111/j.1540-8183.2002.tb01087.x 12476646 · DOI
- [59]Moore KJ Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell (2011) 145(3): 341– 55. 10.1016/j.cell.2011.04.005 21529710 PMC3111065 · DOI · Paper page
- [60]Lusis AJ. Atherosclerosis. Nature (2000) 407(6801): 233– 41. 10.1038/35025203 11001066 PMC2826222 · DOI
- [61]Blanchet X Langer M Weber C Koenen RR von Hundelshausen P. Touch of chemokines. Front Immunol (2012) 3: 175. 10.3389/fimmu.2012.00175 22807925 PMC3394994 · DOI
- [62]Rajagopalan L Rajarathnam K. Structural basis of chemokine receptor function – a model for binding affinity and ligand selectivity. Biosci Rep (2006) 26(5): 325– 39. 10.1007/s10540-006-9025-9 17024562 PMC2671010 · DOI
- [63]Asare Y Schmitt M Bernhagen J. The vascular biology of macrophage migration inhibitory factor (MIF). Expression and effects in inflammation, atherogenesis and angiogenesis. Thromb Haemost (2013) 109(3): 391– 8. 10.1160/TH12-11-0831 23329140 · DOI
- [64]Bachelerie F Ben-Baruch A Burkhardt AM Combadiere C Farber JM Graham GJ International union of basic and clinical pharmacology. [corrected]. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol Rev (2014) 66(1): 1– 79. 10.1124/pr.113.007724 24218476 PMC3880466 · DOI
- [65]Zernecke A Weber C. Chemokines in atherosclerosis: proceedings resumed. Arterioscler Thromb Vasc Biol (2014) 34(4): 742– 50. 10.1161/ATVBAHA.113.301655 24436368 · DOI
- [66]Zhou Z Subramanian P Sevilmis G Globke B Soehnlein O Karshovska E Lipoprotein-derived lysophosphatidic acid promotes atherosclerosis by releasing CXCL1 from the endothelium. Cell Metab (2011) 13(5): 592– 600. 10.1016/j.cmet.2011.02.016 21531341 · DOI
- [68]Soehnlein O Drechsler M Doring Y Lievens D Hartwig H Kemmerich K Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med (2013) 5(3): 471– 81. 10.1002/emmm.201201717 23417922 PMC3598085 · DOI
- [69]Sheikine Y Hansson GK. Chemokines and atherosclerosis. Ann Med (2004) 36(2): 98– 118. 10.1080/07853890310019961 15119830 · DOI
- [70]Tacke F Alvarez D Kaplan TJ Jakubzick C Spanbroek R Llodra J Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest (2007) 117(1): 185– 94. 10.1172/JCI28549 17200718 PMC1716202 · DOI · Paper page
- [71]Boring L Gosling J Cleary M Charo IF. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature (1998) 394(6696): 894– 7. 10.1038/29788 9732872 · DOI · Paper page
- [72]Serbina NV Pamer EG Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol (2006) 7(3): 311– 7. 10.1038/ni1309 16462739 · DOI
- [73]Landsman L Bar-On L Zernecke A Kim KW Krauthgamer R Shagdarsuren E CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood (2009) 113(4): 963– 72. 10.1182/blood-2008-07-170787 18971423 · DOI
- [74]Potteaux S Combadiere C Esposito B Casanova S Merval R Ardouin P Chemokine receptor CCR1 disruption in bone marrow cells enhances atherosclerotic lesion development and inflammation in mice. Mol Med (2005) 11(1–12): 16– 20. 10.2119/2005-00028.Potteaux 16491201 PMC1449521 · DOI
- [75]Braunersreuther V Zernecke A Arnaud C Liehn EA Steffens S Shagdarsuren E Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol (2007) 27(2): 373– 9. 10.1161/01.ATV.0000253886.44609.ae 17138939 · DOI
- [76]Trogan E Feig JE Dogan S Rothblat GH Angeli V Tacke F Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc Natl Acad Sci U S A (2006) 103(10): 3781– 6. 10.1073/pnas.0511043103 16537455 PMC1450154 · DOI
- [77]Feig JE Rong JX Shamir R Sanson M Vengrenyuk Y Liu J HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc Natl Acad Sci U S A (2011) 108(17): 7166– 71. 10.1073/pnas.1016086108 21482781 PMC3084076 · DOI
- [78]Feig JE Shang Y Rotllan N Vengrenyuk Y Wu C Shamir R Statins promote the regression of atherosclerosis via activation of the CCR7-dependent emigration pathway in macrophages. PLoS One (2011) 6(12): e28534. 10.1371/journal.pone.0028534 22163030 PMC3232231 · DOI
- [79]Luchtefeld M Grothusen C Gagalick A Jagavelu K Schuett H Tietge UJ Chemokine receptor 7 knockout attenuates atherosclerotic plaque development. Circulation (2010) 122(16): 1621– 8. 10.1161/CIRCULATIONAHA.110.956730 20921438 · DOI
- [80]Segers D Lipton JA Leenen PJ Cheng C Tempel D Pasterkamp G Atherosclerotic plaque stability is affected by the chemokine CXCL10 in both mice and humans. Int J Inflam (2011) 2011: 936109. 10.4061/2011/936109 22164344 PMC3227498 · DOI
- [81]Murdoch C Monk PN Finn A. Cxc chemokine receptor expression on human endothelial cells. Cytokine (1999) 11(9): 704– 12. 10.1006/cyto.1998.0465 10479407 · DOI
- [82]Fujiwara K Matsukawa A Ohkawara S Takagi K Yoshinaga M. Functional distinction between CXC chemokines, interleukin-8 (IL-8), and growth related oncogene (GRO)alpha in neutrophil infiltration. Lab Invest (2002) 82(1): 15– 23. 10.1038/labinvest.3780391 11796822 · DOI
- [83]Ali S Lazennec G. Chemokines: novel targets for breast cancer metastasis. Cancer Metastasis Rev (2007) 26(3–4): 401– 20. 10.1007/s10555-007-9073-z 17717637 PMC2668792 · DOI
- [84]Yu L Cecil J Peng SB Schrementi J Kovacevic S Paul D Identification and expression of novel isoforms of human stromal cell-derived factor 1. Gene (2006) 374: 174– 9. 10.1016/j.gene.2006.02.001 16626895 · DOI
- [85]Wang JF Liu ZY Groopman JE. The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion. Blood (1998) 92(3): 756– 64. 9680341
- [86]De La Luz Sierra M Yang F Narazaki M Salvucci O Davis D Yarchoan R Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood (2004) 103(7): 2452– 9. 10.1182/blood-2003-08-2857 14525775 · DOI
- [87]Teicher BA Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res (2010) 16(11): 2927– 31. 10.1158/1078-0432.CCR-09-2329 20484021 · DOI
- [88]Orsini MJ Parent JL Mundell SJ Marchese A Benovic JL. Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization. J Biol Chem (1999) 274(43): 31076– 86. 10.1074/jbc.274.43.31076 10521508 · DOI
- [89]Balabanian K Lagane B Infantino S Chow KY Harriague J Moepps B The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem (2005) 280(42): 35760– 6. 10.1074/jbc.M508234200 16107333 · DOI
- [90]Burns JM Summers BC Wang Y Melikian A Berahovich R Miao Z A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med (2006) 203(9): 2201– 13. 10.1084/jem.20052144 16940167 PMC2118398 · DOI
- [91]Luker KE Steele JM Mihalko LA Ray P Luker GD. Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene (2010) 29(32): 4599– 610. 10.1038/onc.2010.212 20531309 PMC3164491 · DOI
- [92]Naumann U Cameroni E Pruenster M Mahabaleshwar H Raz E Zerwes HG CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One (2010) 5(2): e9175. 10.1371/journal.pone.0009175 20161793 PMC2820091 · DOI
- [94]Uto-Konomi A McKibben B Wirtz J Sato Y Takano A Nanki T CXCR7 agonists inhibit the function of CXCL12 by down-regulation of CXCR4. Biochem Biophys Res Commun (2013) 431(4): 772– 6. 10.1016/j.bbrc.2013.01.032 23333329 · DOI
- [95]Kalatskaya I Berchiche YA Gravel S Limberg BJ Rosenbaum JS Heveker N. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol Pharmacol (2009) 75(5): 1240– 7. 10.1124/mol.108.053389 19255243 · DOI
- [96]Rajagopal S Kim J Ahn S Craig S Lam CM Gerard NP Beta-arrestin but not G protein-mediated signaling by the “decoy” receptor CXCR7. Proc Natl Acad Sci U S A (2010) 107(2): 628– 32. 10.1073/pnas.0912852107 20018651 PMC2818968 · DOI
- [97]Döring Y Pawig L Weber C Noels H. The CXCL12/CXCR4 chemokine ligand/receptor axis in cardiovascular disease. Front Physiol (2014) 5: 212. 10.3389/fphys.2014.00212 24966838 PMC4052746 · DOI
- [98]Guo Y Hangoc G Bian H Pelus LM Broxmeyer HE. SDF-1/CXCL12 enhances survival and chemotaxis of murine embryonic stem cells and production of primitive and definitive hematopoietic progenitor cells. Stem Cells (2005) 23(9): 1324– 32. 10.1634/stemcells.2005-0085 16210409 · DOI
- [99]Mazo IB Massberg S von Andrian UH. Hematopoietic stem and progenitor cell trafficking. Trends Immunol (2011) 32(10): 493– 503. 10.1016/j.it.2011.06.011 21802990 PMC3185129 · DOI
- [100]Dar A Schajnovitz A Lapid K Kalinkovich A Itkin T Ludin A Rapid mobilization of hematopoietic progenitors by AMD3100 and catecholamines is mediated by CXCR4-dependent SDF-1 release from bone marrow stromal cells. Leukemia (2011) 25(8): 1286– 96. 10.1038/leu.2011.62 21494253 PMC4175714 · DOI
- [101]Du F Zhou J Gong R Huang X Pansuria M Virtue A Endothelial progenitor cells in atherosclerosis. Front Biosci (Landmark Ed) (2012) 17: 2327– 49. 10.2741/4055 22652782 PMC3368338 · DOI
- [102]Merkulova-Rainon T Broqueres-You D Kubis N Silvestre JS Levy BI. Towards the therapeutic use of vascular smooth muscle progenitor cells. Cardiovasc Res (2012) 95(2): 205– 14. 10.1093/cvr/cvs097 22354897 · DOI
- [103]Akhtar S Gremse F Kiessling F Weber C Schober A. CXCL12 promotes the stabilization of atherosclerotic lesions mediated by smooth muscle progenitor cells in apoe-deficient mice. Arterioscler Thromb Vasc Biol (2013) 33(4): 679– 86. 10.1161/ATVBAHA.112.301162 23393393 · DOI
- [104]Zoll J Fontaine V Gourdy P Barateau V Vilar J Leroyer A Role of human smooth muscle cell progenitors in atherosclerotic plaque development and composition. Cardiovasc Res (2008) 77(3): 471– 80. 10.1093/cvr/cvm034 18006460 · DOI
- [105]Yao L Heuser-Baker J Herlea-Pana O Iida R Wang Q Zou MH Bone marrow endothelial progenitors augment atherosclerotic plaque regression in a mouse model of plasma lipid lowering. Stem Cells (2012) 30(12): 2720– 31. 10.1002/stem.1256 23081735 PMC3508339 · DOI
- [106]Gupta SK Lysko PG Pillarisetti K Ohlstein E Stadel JM. Chemokine receptors in human endothelial cells. Functional expression of CXCR4 and its transcriptional regulation by inflammatory cytokines. J Biol Chem (1998) 273(7): 4282– 7. 10.1074/jbc.273.7.4282 9461627 · DOI
- [107]Murphy PM Baggiolini M I Charo F Hebert CA Horuk R Matsushima K International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev (2000) 52(1): 145– 76. 10699158
- [108]Bruhl H Cohen CD Linder S Kretzler M Schlondorff D Mack M. Post-translational and cell type-specific regulation of CXCR4 expression by cytokines. Eur J Immunol (2003) 33(11): 3028– 37. 10.1002/eji.200324163 14579271 · DOI
- [109]Nie Y Waite J Brewer F Sunshine MJ Littman DR Zou YR. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J Exp Med (2004) 200(9): 1145– 56. 10.1084/jem.20041185 15520246 PMC2211858 · DOI
- [110]Nemenoff RA Horita H Ostriker AC Furgeson SB Simpson PA VanPutten V SDF-1alpha induction in mature smooth muscle cells by inactivation of PTEN is a critical mediator of exacerbated injury-induced neointima formation. Arterioscler Thromb Vasc Biol (2011) 31(6): 1300– 8. 10.1161/ATVBAHA.111.223701 21415388 PMC3111081 · DOI
- [111]Gupta SK Pillarisetti K Lysko PG. Modulation of CXCR4 expression and SDF-1alpha functional activity during differentiation of human monocytes and macrophages. J Leukoc Biol (1999) 66(1): 135– 43. 10411001
- [112]Tanaka G Nakase I Fukuda Y Masuda R Oishi S Shimura K CXCR4 stimulates macropinocytosis: implications for cellular uptake of arginine-rich cell-penetrating peptides and HIV. Chem Biol (2012) 19(11): 1437– 46. 10.1016/j.chembiol.2012.09.011 23177198 · DOI
- [113]Eash KJ Means JM White DW Link DC. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood (2009) 113(19): 4711– 9. 10.1182/blood-2008-09-177287 19264920 PMC2680371 · DOI · Paper page
- [114]Martin C Burdon PC Bridger G Gutierrez-Ramos JC Williams TJ Rankin SM. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity (2003) 19(4): 583– 93. 10.1016/S1074-7613(03)00263-2 14563322 · DOI
- [115]Li LX Zhang XF Bai X Tong Q. SDF-1 promotes ox-LDL induced vascular smooth muscle cell proliferation. Cell Biol Int (2013) 37(9): 988– 94. 10.1002/cbin.10126 23658061 · DOI
- [116]Melchionna R Porcelli D Mangoni A Carlini D Liuzzo G Spinetti G Laminar shear stress inhibits CXCR4 expression on endothelial cells: functional consequences for atherogenesis. FASEB J (2005) 19(6): 629– 31. 15705741
- [118]Poznansky MC I Olszak T Foxall R Evans RH Luster AD Scadden DT. Active movement of T cells away from a chemokine. Nat Med (2000) 6(5): 543– 8. 10.1038/75022 10802710 · DOI
- [119]Okabe S Fukuda S Kim YJ Niki M Pelus LM Ohyashiki K Stromal cell-derived factor-1alpha/CXCL12-induced chemotaxis of T cells involves activation of the RasGAP-associated docking protein p62Dok-1. Blood (2005) 105(2): 474– 80. 10.1182/blood-2004-03-0843 15345598 · DOI
- [120]Zhang X Nakajima T Goronzy JJ Weyand CM. Tissue trafficking patterns of effector memory CD4+ T cells in rheumatoid arthritis. Arthritis Rheum (2005) 52(12): 3839– 49. 10.1002/art.21482 16329093 · DOI · Paper page
- [121]Klasen C Ohl K Sternkopf M Shachar I Schmitz C Heussen N MIF promotes B cell chemotaxis through the receptors CXCR4 and CD74 and ZAP-70 signaling. J Immunol (2014) 192(11): 5273– 84. 10.4049/jimmunol.1302209 24760155 · DOI
- [122]Kowalska MA Ratajczak J Hoxie J Brass LF Gewirtz A Poncz M Megakaryocyte precursors, megakaryocytes and platelets express the HIV co-receptor CXCR4 on their surface: determination of response to stromal-derived factor-1 by megakaryocytes and platelets. Br J Haematol (1999) 104(2): 220– 9. 10.1046/j.1365-2141.1999.01169.x 10050701 · DOI
- [123]Chatterjee M Gawaz M. Platelet-derived CXCL12 (SDF-1alpha): basic mechanisms and clinical implications. J Thromb Haemost (2013) 11(11): 1954– 67. 10.1111/jth.12404 24024928 · DOI
- [124]Kraemer BF Borst O Gehring EM Schoenberger T Urban B Ninci E PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). J Mol Med (Berl) (2010) 88(12): 1277– 88. 10.1007/s00109-010-0680-8 20852838 · DOI
- [125]Li X Zhu M Penfold ME Koenen RR Thiemann A Heyll K Activation of CXCR7 limits atherosclerosis and improves hyperlipidemia by increasing cholesterol uptake in adipose tissue. Circulation (2014) 129(11): 1244– 53. 10.1161/CIRCULATIONAHA.113.006840 24374972 · DOI
- [126]Lo Celso C Fleming HE Wu JW Zhao CX Miake-Lye S Fujisaki J Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature (2009) 457(7225): 92– 6. 10.1038/nature07434 19052546 PMC2820276 · DOI
- [127]Hu X Dai S Wu WJ Tan W Zhu X Mu J Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation (2007) 116(6): 654– 63. 10.1161/CIRCULATIONAHA.106.672451 17646584 PMC3640445 · DOI
- [128]Askari AT Unzek S Popovic ZB Goldman CK Forudi F Kiedrowski M Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet (2003) 362(9385): 697– 703. 10.1016/S0140-6736(03)14232-8 12957092 · DOI
- [129]Jujo K Hamada H Iwakura A Thorne T Sekiguchi H Clarke T CXCR4 blockade augments bone marrow progenitor cell recruitment to the neovasculature and reduces mortality after myocardial infarction. Proc Natl Acad Sci U S A (2010) 107(24): 11008– 13. 10.1073/pnas.0914248107 20534467 PMC2890743 · DOI
- [130]Jujo K Ii M Sekiguchi H Klyachko E Misener S Tanaka T CXC-chemokine receptor 4 antagonist AMD3100 promotes cardiac functional recovery after ischemia/reperfusion injury via endothelial nitric oxide synthase-dependent mechanism. Circulation (2013) 127(1): 63– 73. 10.1161/CIRCULATIONAHA.112.099242 23204107 PMC3560409 · DOI
- [131]Dai S Yuan F Mu J Li C Chen N Guo S Chronic AMD3100 antagonism of SDF-1alpha-CXCR4 exacerbates cardiac dysfunction and remodeling after myocardial infarction. J Mol Cell Cardiol (2010) 49(4): 587– 97. 10.1016/j.yjmcc.2010.07.010 20655922 PMC3005152 · DOI
- [132]Schober A Knarren S Lietz M Lin EA Weber C. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation (2003) 108(20): 2491– 7. 10.1161/01.CIR.0000099508.76665.9A 14581398 · DOI
- [133]Karshovska E Zagorac D Zernecke A Weber C Schober A A small molecule CXCR4 antagonist inhibits neointima formation and smooth muscle progenitor cell mobilization after arterial injury. J Thromb Haemost (2008) 6(10): 1812– 5. 10.1111/j.1538-7836.2008.03086.x 18647221 · DOI
- [134]Olive M Mellad JA Beltran LE Ma M Cimato T Noguchi AC p21Cip1 modulates arterial wound repair through the stromal cell-derived factor-1/CXCR4 axis in mice. J Clin Invest (2008) 118(6): 2050– 61. 10.1172/JCI31244 18464929 PMC2373418 · DOI
- [135]Noels H Zhou B Tilstam PV Theelen W Li X Pawig L Deficiency of endothelial CXCR4 reduces reendothelialization and enhances neointimal hyperplasia after vascular injury in atherosclerosis-prone mice. Arterioscler Thromb Vasc Biol (2014) 34(6): 1209– 20. 10.1161/ATVBAHA.113.302878 24723559 · DOI
- [136]Massberg S Konrad I Schürzinger K Lorenz M Schneider S Zohlnhoefer D Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med (2006) 203(5): 1221– 33. 10.1084/jem.20051772 16618794 PMC2121205 · DOI
- [137]Subramanian S Liu C Aviv A Ho JE Courchesne P Muntendam P Stromal cell-derived factor 1 as a biomarker of heart failure and mortality risk. Arterioscler Thromb Vasc Biol (2014) 34(9): 2100– 5. 10.1161/ATVBAHA.114.303579 25060794 PMC4142677 · DOI
- [138]Calandra T Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol (2003) 3(10): 791– 800. 10.1038/nri1200 14502271 PMC7097468 · DOI
- [139]Tillmann S Bernhagen J Noels H. Arrest functions of the MIF ligand/receptor axes in atherogenesis. Front Immunol (2013) 4: 115. 10.3389/fimmu.2013.00115 23720662 PMC3655399 · DOI
- [140]David JR Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci U S A (1966) 56(1): 72– 7. 10.1073/pnas.56.1.72 5229858 PMC285677 · DOI
- [141]Calandra T Bernhagen J Mitchell RA Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med (1994) 179(6): 1895– 902. 10.1084/jem.179.6.1895 8195715 PMC2191507 · DOI
- [142]Bacher M Metz CN Calandra T Mayer K Chesney J Lohoff M An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci U S A (1996) 93(15): 7849– 54. 10.1073/pnas.93.15.7849 8755565 PMC38837 · DOI
- [143]Nishihira J Koyama Y Mizue Y. Identification of macrophage migration inhibitory factor (MIF) in human vascular endothelial cells and its induction by lipopolysaccharide. Cytokine (1998) 10(3): 199– 205. 10.1006/cyto.1997.0276 9576065 · DOI
- [144]Wymann D Bluggel M Kalbacher H Blesken T Akdis CA Meyer HE Human B cells secrete migration inhibition factor (MIF) and present a naturally processed MIF peptide on HLA-DRB1*0405 by a FXXL motif. Immunology (1999) 96(1): 1– 9. 10.1046/j.1365-2567.1999.00652.x 10233671 PMC2326723 · DOI
- [145]Chen L Yang G Zhang X Wu J Gu Q Wei M Induction of MIF expression by oxidized LDL via activation of NF-kappaB in vascular smooth muscle cells. Atherosclerosis (2009) 207(2): 428– 33. 10.1016/j.atherosclerosis.2009.05.021 19640536 · DOI
- [146]Simons D Grieb G Hristov M Pallua N Weber C Bernhagen J Hypoxia-induced endothelial secretion of macrophage migration inhibitory factor and role in endothelial progenitor cell recruitment. J Cell Mol Med (2011) 15(3): 668– 78. 10.1111/j.1582-4934.2010.01041.x 20178462 PMC3922388 · DOI
- [147]Calandra T Bernhagen J Metz CN Spiegel LA Bacher M Donnelly T MIF as a glucocorticoid-induced modulator of cytokine production. Nature (1995) 377(6544): 68– 71. 10.1038/377068a0 7659164 · DOI
- [148]Leech M Metz C Hall P Hutchinson P Gianis K Smith M Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum (1999) 42(8): 1601– 8. 10.1002/1529-0131(199908)42:8<1601::AID-ANR6>3.0.CO;2-B 10446857 · DOI
- [149]Calandra T Echtenacher B Roy DL Pugin J Metz CN Hultner L Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med (2000) 6(2): 164– 70. 10.1038/72262 10655104 · DOI
- [150]Mawhinney L Armstrong ME O’Reilly C Bucala R Leng L Fingerle-Rowson G Macrophage migration inhibitory factor (MIF) enzymatic activity and lung cancer. Mol Med (2014) 20: 729– 35. 10.2119/molmed.2014.00136 25826675 PMC4398672 · DOI
- [151]Leng L Metz CN Fang Y Xu J Donnelly S Baugh J MIF signal transduction initiated by binding to CD74. J Exp Med (2003) 197(11): 1467– 76. 10.1084/jem.20030286 12782713 PMC2193907 · DOI · Paper page
- [152]Borghese F Clanchy FI. CD74: an emerging opportunity as a therapeutic target in cancer and autoimmune disease. Expert Opin Ther Targets (2011) 15(3): 237– 51. 10.1517/14728222.2011.550879 21208136 · DOI
- [153]Shi X Leng L Wang T Wang W Du X Li J CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity (2006) 25(4): 595– 606. 10.1016/j.immuni.2006.08.020 17045821 PMC3707630 · DOI
- [154]Bernhagen J Krohn R Lue H Gregory JL Zernecke A Koenen RR MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med (2007) 13(5): 587– 96. 10.1038/nm1567 17435771 · DOI
- [155]Schwartz V Lue H Kraemer S Korbiel J Krohn R Ohl K A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett (2009) 583(17): 2749– 57. 10.1016/j.febslet.2009.07.058 19665027 PMC2911026 · DOI
- [156]Lue H Kapurniotu A Fingerle-Rowson G Roger T Leng L Thiele M Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal (2006) 18(5): 688– 703. 10.1016/j.cellsig.2005.06.013 16122907 · DOI
- [157]Sun J Hartvigsen K Chou MY Zhang Y Sukhova GK Zhang J Deficiency of antigen-presenting cell invariant chain reduces atherosclerosis in mice. Circulation (2010) 122(8): 808– 20. 10.1161/CIRCULATIONAHA.109.891887 20697023 PMC2927799 · DOI
- [158]Chatterjee M Borst O Walker B Fotinos A Vogel S Seizer P Macrophage migration inhibitory factor limits activation-induced apoptosis of platelets via CXCR7-dependent Akt signaling. Circ Res (2014) 115(11): 939– 49. 10.1161/CIRCRESAHA.115.305171 25266363 · DOI
- [159]Lin SG Yu XY Chen YX Huang XR Metz C Bucala R De novo expression of macrophage migration inhibitory factor in atherogenesis in rabbits. Circ Res (2000) 87(12): 1202– 8. 10.1161/01.RES.87.12.1202 11110779 · DOI
- [160]Burger-Kentischer A Gobel H Kleemann R Zernecke A Bucala R Leng L Reduction of the aortic inflammatory response in spontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF). Atherosclerosis (2006) 184(1): 28– 38. 10.1016/j.atherosclerosis.2005.03.028 15921687 · DOI
- [161]Schober A Bernhagen J Thiele M Zeiffer U Knarren S Roller M Stabilization of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation (2004) 109(3): 380– 5. 10.1161/01.CIR.0000109201.72441.09 14691040 · DOI
- [162]Cheng Q McKeown SJ Santos L Santiago FS Khachigian LM Morand EF Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J Immunol (2010) 185(2): 1238– 47. 10.4049/jimmunol.0904104 20554956 · DOI
- [163]Pan JH Sukhova GK Yang JT Wang B Xie T Fu H Macrophage migration inhibitory factor deficiency impairs atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation (2004) 109(25): 3149– 53. 10.1161/01.CIR.0000134704.84454.D2 15197138 · DOI
- [164]Wirtz TH Tillmann S Strussmann T Kraemer S Heemskerk JW Grottke O Platelet-derived MIF: a novel platelet chemokine with distinct recruitment properties. Atherosclerosis (2015) 239(1): 1– 10. 10.1016/j.atherosclerosis.2014.12.039 25561410 · DOI
- [165]Boisvert WA Santiago R Curtiss LK Terkeltaub RA. A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. J Clin Invest (1998) 101(2): 353– 63. 10.1172/JCI1195 9435307 PMC508574 · DOI
- [166]Boisvert WA Rose DM Johnson KA Fuentes ME Lira SA Curtiss LK Up-regulated expression of the CXCR2 ligand KC/GRO-alpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am J Pathol (2006) 168(4): 1385– 95. 10.2353/ajpath.2006.040748 16565511 PMC1606562 · DOI
- [167]Chen Z Sakuma M Zago AC Zhang X Shi C Leng L Evidence for a role of macrophage migration inhibitory factor in vascular disease. Arterioscler Thromb Vasc Biol (2004) 24(4): 709– 14. 10.1161/01.ATV.0000119356.35748.9e 14751814 · DOI
- [168]Noels H Bernhagen J Weber C. Macrophage migration inhibitory factor: a noncanonical chemokine important in atherosclerosis. Trends Cardiovasc Med (2009) 19(3): 76– 86. 10.1016/j.tcm.2009.05.002 19679264 · DOI
- [169]White DA Su Y Kanellakis P Kiriazis H Morand EF Bucala R Differential roles of cardiac and leukocyte derived macrophage migration inhibitory factor in inflammatory responses and cardiac remodelling post myocardial infarction. J Mol Cell Cardiol (2014) 69: 32– 42. 10.1016/j.yjmcc.2014.01.015 24508700 PMC4317300 · DOI
- [170]Liehn EA Kanzler I Konschalla S Kroh A Simsekyilmaz S Sönmez TT Compartmentalized protective and detrimental effects of endogenous macrophage migration-inhibitory factor mediated by CXCR2 in a mouse model of myocardial ischemia/reperfusion. Arterioscler Thromb Vasc Biol (2013) 33(9): 2180– 6. 10.1161/ATVBAHA.113.301633 23868943 PMC4337944 · DOI
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Zamani, P., Houessou, U., Manikpurage, H. D., Li, Z., Dahmene, M., Gaudreault, N., Dagenais, F., Clavel, M.-A., Pibarot, P., Arsenault, B. J., et al. (2025) · Human Genetics and Genomics Advances · doi:10.1016/j.xhgg.2025.100448 · Cited by 3 · see citing works
- Authors
- van der Vorst, E. P. C., Döring, Y., & Weber, C.
- Affiliations
- Ludwig-Maximilians-Universität München (DE)
- Maastricht University (NL)
- Corresponding author
- Döring, Yvonne
- Weber, Christian
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2015
- Volume
- 6
- Pages
- 373-373
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC4508925
- OpenAlex
- W1904549514
- Cited by
- 57
- References
- 6
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 2 · 2023: 2 · 2022: 7 · 2021: 5 · 2020: 3 · 2019: 7 · 2018: 6 · 2017: 7 · 2016: 8 · 2015: 1
- FWCI
- 0.69
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- Deutsches Zentrum für Herz-Kreislaufforschung (MHA VD1.2)
- Deutsche Forschungsgemeinschaft (SFB1123/A1, SFB1123)
- Bundesministerium für Bildung und Forschung (01KU1213A)
- FP7 Ideas: European Research Council (249929)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Macrophage Migration Inhibitory Factor
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- macrophage migration inhibitory factor, CXCL12, coronary artery disease, atherosclerosis, chemokines, chemokine receptors, CXCR4, CXCR7, CXCR2, CD44, CD74, pro-inflammatory effects, atherogenesis
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