|
|
|
| Research Progress of Macrophage Migration Inhibitory Factor Regulating Cell Senescence |
LI Yu-jin1,WANG Jie1,WANG Ya-ni2,WANG Yao2,MENG Jia-min2,ZHANG Hong-bing2,**( ) |
1 College of Life Science, Northwest University, Xi’an 710069, China
2 The First Affiliated Hospital of Northwest University, Xi’an First Hospital, Eye Institute of Shaanxi Province, Xi’an 710002, China |
|
|
|
Abstract Macrophage migration inhibitory factor (MIF) is a widely expressed pleiotropic cytokine that controls various biological functions of cells, including cell proliferation, differentiation, survival and apoptosis. Recent studies have found that MIF is closely associated with cell senescence, suggesting that MIF may regulate cell senescence. To further understand the mechanism of cell senescence, the role of MIF in cell senescence and its mechanism in recent studies was summarized in this article, which includes how MIF controls senescence related gene expression, especially in hypoxia and oxidative stress conditions. The complex regulatory mechanisms of aging related diseases in the context of MIF functional polymorphism were further analyzed. Finally, the development and application of bioengineering products of MIF and its receptors were introduced. It lays a foundation for further study on the mechanism of MIF regulating cell senescence.
|
|
Received: 17 August 2022
Published: 31 March 2023
|
|
|
|
Corresponding Authors:
**Hong-bing ZHANG
E-mail: zhanghongbing01@163.com
|
|
|
| [1] |
Jankauskas S S, Wong D W L, Bucala R, et al. Evolving complexity of MIF signaling. Cellular Signalling, 2019, 57: 76-88.
doi: S0898-6568(19)30015-4
pmid: 30682543
|
|
|
| [2] |
Harris J, VanPatten S, Deen N S, et al. Rediscovering MIF: new tricks for an old cytokine. Trends in Immunology, 2019, 40(5): 447-462.
doi: S1471-4906(19)30043-2
pmid: 30962001
|
|
|
| [3] |
Wirtz T H, Saal A, Bergmann I, et al. Macrophage migration inhibitory factor exerts pro-proliferative and anti-apoptotic effects via CD 74 in murine hepatocellular carcinoma. British Journal of Pharmacology, 2021, 178(22): 4452-4467.
doi: 10.1111/bph.v178.22
|
|
|
| [4] |
Sikora E, Bielak-Żmijewska A, Mosieniak G. What is and what is not cell senescence. Postepy Biochemii, 2018, 64(2): 110-118.
doi: 10.18388/pb.2018_120
pmid: 30656893
|
|
|
| [5] |
Antelo-Iglesias L, Picallos-Rabina P, Estévez-Souto V, et al. The role of cellular senescence in tissue repair and regeneration. Mechanisms of Ageing and Development, 2021, 198: 111528.
doi: 10.1016/j.mad.2021.111528
|
|
|
| [6] |
von Kobbe C. Cellular senescence: a view throughout organismal life. Cellular and Molecular Life Sciences, 2018, 75(19): 3553-3567.
doi: 10.1007/s00018-018-2879-8
pmid: 30030594
|
|
|
| [7] |
Zhang Y L, Zhu W W, He H W, et al. Macrophage migration inhibitory factor rejuvenates aged human mesenchymal stem cells and improves myocardial repair. Aging, 2019, 11(24): 12641-12660.
doi: 10.18632/aging.v11i24
|
|
|
| [8] |
Xia W Z, Hou M. Macrophage migration inhibitory factor rescues mesenchymal stem cells from doxorubicin-induced senescence though the PI3K-Akt signaling pathway. International Journal of Molecular Medicine, 2018, 41(2): 1127-1137.
doi: 10.3892/ijmm.2017.3282
pmid: 29207187
|
|
|
| [9] |
Hu Y W, Xia W Z, Hou M. Macrophage migration inhibitory factor serves a pivotal role in the regulation of radiation-induced cardiac senescencethrough rebalancing the microRNA-34a/sirtuin 1 signaling pathway. International Journal of Molecular Medicine, 2018, 42(5): 2849-2858.
|
|
|
| [10] |
Lan H Y. Role of macrophage migration inhibition factor in kidney disease. Nephron Experimental Nephrology, 2008, 109(3): e79-e83.
doi: 10.1159/000145463
|
|
|
| [11] |
Deo R C. Machine learning in medicine. Circulation, 2015, 132(20): 1920-1930.
doi: 10.1161/CIRCULATIONAHA.115.001593
pmid: 26572668
|
|
|
| [12] |
Chen C A, Chang J M, Yang Y L, et al. Macrophage migration inhibitory factor regulates integrin-β1 and cyclin D 1 expression via ERK pathway in podocytes. Biomedicine & Pharmacotherapy, 2020, 124: 109892.
doi: 10.1016/j.biopha.2020.109892
|
|
|
| [13] |
Su H T, Na N, Zhang X D, et al. The biological function and significance of CD 74 in immune diseases. Inflammation Research, 2017, 66(3): 209-216.
doi: 10.1007/s00011-016-0995-1
|
|
|
| [14] |
Kleemann R, Hausser A, Geiger G, et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature, 2000, 408(6809): 211-216.
doi: 10.1038/35041591
|
|
|
| [15] |
Nguyen M T, Lue H Q, Kleemann R, et al. The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis. The Journal of Immunology, 2003, 170(6): 3337-3347.
doi: 10.4049/jimmunol.170.6.3337
|
|
|
| [16] |
Yoshihisa Y, Rehman M U, Kondo T, et al. Role of macrophage migration inhibitory factor in heat-induced apoptosis in keratinocytes. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 2016, 30(11): 3870-3877.
doi: 10.1096/fsb2.v30.11
|
|
|
| [17] |
Schröder B. The multifaceted roles of the invariant chain CD74:more than just a chaperone. Biochimica et Biophysica Acta, 2016, 1863(6 Pt A): 1269-1281.
doi: 10.1016/j.bbamcr.2016.03.026
pmid: 27033518
|
|
|
| [18] |
Bruchez A, Sha K, Johnson J, et al. MHC class II transactivator CIITA induces cell resistance to Ebola virus and SARS-like coronaviruses. Science, 2020, 370(6513): 241-247.
doi: 10.1126/science.abb3753
pmid: 32855215
|
|
|
| [19] |
Lee S, Yu Y, Trimpert J, et al. Virus-induced senescence is a driver and therapeutic target in COVID-19. Nature, 2021, 599(7884): 283-289.
doi: 10.1038/s41586-021-03995-1
|
|
|
| [20] |
Evangelou K, Veroutis D, Paschalaki K, et al. Pulmonary infection by SARS-CoV-2 induces senescence accompanied by an inflammatory phenotype in severe COVID-19: possible implications for viral mutagenesis. European Respiratory Journal, 2022, 60(2): 2102951.
doi: 10.1183/13993003.02951-2021
|
|
|
| [21] |
Wei W Q, Ji S P. Cellular senescence: molecular mechanisms and pathogenicity. Journal of Cellular Physiology, 2018, 233(12): 9121-9135.
doi: 10.1002/jcp.26956
pmid: 30078211
|
|
|
| [22] |
Childs B G, Durik M, Baker D J, et al. Cellular senescence in aging and age-related disease: from mechanisms to therapy. Nature Medicine, 2015, 21(12): 1424-1435.
doi: 10.1038/nm.4000
pmid: 26646499
|
|
|
| [23] |
Liu R M, Liu G. Cell senescence and fibrotic lung diseases. Experimental Gerontology, 2020, 132: 110836.
doi: 10.1016/j.exger.2020.110836
|
|
|
| [24] |
Hernandez-Segura A, Nehme J, Demaria M. Hallmarks of cellular senescence. Trends in Cell Biology, 2018, 28(6): 436-453.
doi: S0962-8924(18)30020-5
pmid: 29477613
|
|
|
| [25] |
Kumari R, Jat P. Mechanisms of cellular senescence: cell cycle arrest and senescence associated secretory phenotype. Frontiers in Cell and Developmental Biology, 2021, 9: 645593.
doi: 10.3389/fcell.2021.645593
|
|
|
| [26] |
Rajendran P, Alzahrani A M, Hanieh H N, et al. Autophagy and senescence: a new insight in selected human diseases. Journal of Cellular Physiology, 2019, 234(12): 21485-21492.
doi: 10.1002/jcp.28895
pmid: 31144309
|
|
|
| [27] |
Wang Y Y, Hu Y Z, Wang H M, et al. Deficiency of MIF accentuates overloaded compression-induced nucleus pulposus cell oxidative damage via depressing mitophagy. Oxidative Medicine and Cellular Longevity, 2021, 2021: 6192498.
|
|
|
| [28] |
Welford S M, Bedogni B, Gradin K, et al. HIF1α delays premature senescence through the activation of MIF. Genes & Development, 2006, 20(24): 3366-3371.
doi: 10.1101/gad.1471106
|
|
|
| [29] |
Ohta S, Misawa A, Fukaya R, et al. Macrophage migration inhibitory factor (MIF) promotes cell survival and proliferation of neural stem/progenitor cells. Journal of Cell Science, 2012, 125(Pt 13): 3210-3220.
doi: 10.1242/jcs.102210
pmid: 22454509
|
|
|
| [30] |
Palumbo S, Tsai T L, Li W J. Macrophage migration inhibitory factor regulates AKT signaling in hypoxic culture to modulate senescence of human mesenchymal stem cells. Stem Cells and Development, 2014, 23(8): 852-865.
doi: 10.1089/scd.2013.0294
pmid: 24274936
|
|
|
| [31] |
Xu X H, Pang J J, Chen Y G, et al. Macrophage migration inhibitory factor (MIF) deficiency exacerbates aging-induced cardiac remodeling and dysfunction despite improved inflammation: role of autophagy regulation. Scientific Reports, 2016, 6: 22488.
doi: 10.1038/srep22488
pmid: 26940544
|
|
|
| [32] |
Mohamad Kamal N S, Safuan S, Shamsuddin S, et al. Aging of the cells: insight into cellular senescence and detection Methods. European Journal of Cell Biology, 2020, 99(6): 151108.
doi: 10.1016/j.ejcb.2020.151108
|
|
|
| [33] |
Fukaya R, Ohta S, Yaguchi T, et al. MIF maintains the tumorigenic capacity of brain tumor-initiating cells by directly inhibiting p53. Cancer Research, 2016, 76(9): 2813-2823.
doi: 10.1158/0008-5472.CAN-15-1011
pmid: 26980763
|
|
|
| [34] |
Xia W Z, Zhuang L, Hou M. Role of lincRNA-p21 in the protective effect of macrophage inhibition factor against hypoxia/serum deprivation-induced apoptosis in mesenchymal stem cells. International Journal of Molecular Medicine, 2018, 42(4): 2175-2184.
|
|
|
| [35] |
Sauler M, Leng L, Trentalange M, et al. Macrophage migration inhibitory factor deficiency in chronic obstructive pulmonary disease. American Journal of Physiology Lung Cellular and Molecular Physiology, 2014, 306(6): L487-L496.
doi: 10.1152/ajplung.00284.2013
|
|
|
| [36] |
Petrenko O, Moll U M. Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Molecular Cell, 2005, 17(2): 225-236.
pmid: 15664192
|
|
|
| [37] |
Sasaki Y, Kasuya K, Nishihira J, et al. Suppression of tumor growth through introduction of an antisense plasmid of macrophage migration inhibitory factor. International Journal of Molecular Medicine, 2002, 10(5): 579-583.
pmid: 12373295
|
|
|
| [38] |
Wen F Y, Zheng J, Yu J, et al. Macrophage migration inhibitory factor in the regulation of myoblast proliferation and differentiation. Bioscience, Biotechnology, and Biochemistry, 2016, 80(7): 1313-1320.
doi: 10.1080/09168451.2016.1153951
|
|
|
| [39] |
Guo P, Wang J, Liu J X, et al. Macrophage immigration inhibitory factor promotes cell proliferation and inhibits apoptosis of cervical adenocarcinoma. Tumor Biology, 2015, 36(7): 5095-5102.
doi: 10.1007/s13277-015-3161-4
|
|
|
| [40] |
Lan H B, Wang N, Chen Y, et al. Macrophage migration inhibitory factor (MIF) promotes rat airway muscle cell proliferation and migration mediated by ERK1/2 and FAK signaling. Cell Biology International, 2018, 42(1): 75-83.
doi: 10.1002/cbin.10863
pmid: 28851074
|
|
|
| [41] |
Vizcaíno C, Mansilla S, Portugal J. Sp1 transcription factor: a long-standing target in cancer chemotherapy. Pharmacology & Therapeutics, 2015, 152: 111-124.
|
|
|
| [42] |
Shrestha S, Adhikary G, Naselsky W, et al. ACTL6A suppresses p21Cip1 tumor suppressor expression to maintain an aggressive mesothelioma cancer cell phenotype. Oncogenesis, 2021, 10(10): 70.
doi: 10.1038/s41389-021-00362-7
pmid: 34689163
|
|
|
| [43] |
Xia W Z, Zhang F Y, Xie C Y, et al. Macrophage migration inhibitory factor confers resistance to senescence through CD74-dependent AMPK-FOXO3a signaling in mesenchymal stem cells. Stem Cell Research & Therapy, 2015, 6(1): 82.
|
|
|
| [44] |
Zhuang L, Xia W Z, Chen D D, et al. Exosomal LncRNA-NEAT1 derived from MIF-treated mesenchymal stem cells protected against doxorubicin-induced cardiac senescence through sponging miR-221-3p. Journal of Nanobiotechnology, 2020, 18(1): 157.
doi: 10.1186/s12951-020-00716-0
pmid: 33129330
|
|
|
| [45] |
Ma H, Wang J Y, Thomas D P, et al. Impaired macrophage migration inhibitory factor-AMP-activated protein kinase activation and ischemic recovery in the senescent heart. Circulation, 2010, 122(3): 282-292.
doi: 10.1161/CIRCULATIONAHA.110.953208
pmid: 20606117
|
|
|
| [46] |
Sergiev P V, Dontsova O A, Berezkin G V. Theories of aging: an ever-evolving field. Acta Naturae, 2015, 7(1): 9-18.
pmid: 25926998
|
|
|
| [47] |
Kaspar J W, Niture S K, Jaiswal A K. Nrf2: INrf 2 (Keap1) signaling in oxidative stress. Free Radical Biology and Medicine, 2009, 47(9): 1304-1309.
doi: 10.1016/j.freeradbiomed.2009.07.035
pmid: 19666107
|
|
|
| [48] |
Kimura H, Sato Y, Tajima Y, et al. BTZO-1, a cardioprotective agent, reveals that macrophage migration inhibitory factor regulates ARE-mediated gene expression. Chemistry & Biology, 2010, 17(12): 1282-1294.
doi: 10.1016/j.chembiol.2010.10.011
|
|
|
| [49] |
Mitchell R A, Liao H, Chesney J, et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53:regulatory role in the innate immune response. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(1): 345-350.
|
|
|
| [50] |
Koga K, Kenessey A, Powell S R, et al. Macrophage migration inhibitory factor provides cardioprotection during ischemia/reperfusion by reducing oxidative stress. Antioxidants & Redox Signaling, 2011, 14(7): 1191-1202.
|
|
|
| [51] |
Cotzomi-Ortega I, Rosas-Cruz A, Ramírez-Ramírez D, et al. Autophagy inhibition induces the secretion of macrophage migration inhibitory factor (MIF) with autocrine and paracrine effects on the promotion of malignancy in breast cancer. Biology, 2020, 9(1): 20.
doi: 10.3390/biology9010020
|
|
|
| [52] |
Rojas-Sanchez G, García-Miranda A, Montes-Alvarado J B, et al. Chloroquine induces ROS-mediated macrophage migration inhibitory factor secretion and epithelial to mesenchymal transition in ER-positive breast cancer cell lines. Journal of Mammary Gland Biology and Neoplasia, 2021, 26(4): 341-355.
doi: 10.1007/s10911-021-09503-5
pmid: 34813005
|
|
|
| [53] |
Ke Q D, Costa M. Hypoxia-inducible factor-1 (HIF-1). Molecular Pharmacology, 2006, 70(5): 1469-1480.
doi: 10.1124/mol.106.027029
pmid: 16887934
|
|
|
| [54] |
Fu H, Luo F M, Yang L, et al. Hypoxia stimulates the expression of macrophage migration inhibitory factor in human vascular smooth muscle cells via HIF-1alpha dependent pathway. BMC Cell Biology, 2010, 11: 66.
doi: 10.1186/1471-2121-11-66
pmid: 20727156
|
|
|
| [55] |
Alonso D, Serrano E, Bermejo F J, et al. HIF-1α-regulated MIF activation and Nox2-dependent ROS generation promote Leishmania amazonensis killing by macrophages under hypoxia. Cellular Immunology, 2019, 335: 15-21.
doi: S0008-8749(18)30312-5
pmid: 30384962
|
|
|
| [56] |
Safi W, Kraus A, Grampp S, et al. Macrophage migration inhibitory factor is regulated by HIF-1α and cAMP and promotes renal cyst cell proliferation in a macrophage-independent manner. Journal of Molecular Medicine, 2020, 98(11): 1547-1559.
doi: 10.1007/s00109-020-01964-1
|
|
|
| [57] |
Li J, Zhang J H, Xie F J, et al. Macrophage migration inhibitory factor promotes Warburg effect via activation of the NF-κB/HIF-1α pathway in lung cancer. International Journal of Molecular Medicine, 2018, 41(2): 1062-1068.
|
|
|
| [58] |
Hofmann E, Soppert J, Ruhl T, et al. The role of macrophage migration inhibitory factor in adipose-derived stem cells under hypoxia. Frontiers in Physiology, 2021, 12: 638448.
doi: 10.3389/fphys.2021.638448
|
|
|
| [59] |
Oda S, Oda T, Nishi K, et al. Macrophage migration inhibitory factor activates hypoxia-inducible factor in a p53-dependent manner. PLoS One, 2008, 3(5): e2215.
|
|
|
| [60] |
Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nature Reviews Immunology, 2003, 3(10): 791-800.
doi: 10.1038/nri1200
pmid: 14502271
|
|
|
| [61] |
Sumaiya K, Langford D, Natarajaseenivasan K, et al. Macrophage migration inhibitory factor (MIF): a multifaceted cytokine regulated by genetic and physiological strategies. Pharmacology & Therapeutics, 2022, 233: 108024.
|
|
|
| [62] |
Basile M S, Battaglia G, Bruno V, et al. The dichotomic role of macrophage migration inhibitory factor in neurodegeneration. International Journal of Molecular Sciences, 2020, 21(8): 3023.
doi: 10.3390/ijms21083023
|
|
|
| [63] |
Sinitski D, Kontos C, Krammer C, et al. Macrophage migration inhibitory factor (MIF)-based therapeutic concepts in atherosclerosis and inflammation. Thrombosis and Haemostasis, 2019, 119(4): 553-566.
doi: 10.1055/s-0039-1677803
pmid: 30716779
|
|
|
| [64] |
Sauler M, Bucala R, Lee P J. Role of macrophage migration inhibitory factor in age-related lung disease. American Journal of Physiology Lung Cellular and Molecular Physiology, 2015, 309(1): L1-L10.
doi: 10.1152/ajplung.00339.2014
|
|
|
| [65] |
Nobre C C G, de Araújo J M G, Allyrio Araújo de Medeiros Fernandes T, et al. Macrophage migration inhibitory factor (MIF): biological activities and relation with cancer. Pathology & Oncology Research, 2017, 23(2): 235-244.
|
|
|
| [66] |
Li S Y, Nie K, Zhang Q X, et al. Macrophage migration inhibitory factor mediates neuroprotective effects by regulating inflammation, apoptosis and autophagy in Parkinson’s disease. Neuroscience, 2019, 416: 50-62.
doi: 10.1016/j.neuroscience.2019.05.052
|
|
|
| [67] |
Zhang S, Zhao J H, Zhang Y H, et al. Upregulation of MIF as a defense mechanism and a biomarker of Alzheimer’s disease. Alzheimer’s Research & Therapy, 2019, 11(1): 54.
|
|
|
| [68] |
Jung H, Seong H A, Ha H. Critical role of cysteine residue 81 of macrophage migration inhibitory factor (MIF) in MIF-induced inhibition of p53 activity. Journal of Biological Chemistry, 2008, 283(29): 20383-20396.
doi: 10.1074/jbc.M800050200
pmid: 18502749
|
|
|
| [69] |
Zhang J N, Zhang G B, Yang S M, et al. Macrophage migration inhibitory factor regulating the expression of VEGF-C through MAPK signal pathways in breast cancer MCF-7 cell. World Journal of Surgical Oncology, 2016, 14(1): 51.
doi: 10.1186/s12957-016-0797-5
|
|
|
| [70] |
Garcia-Gerique L, García M, Garrido-Garcia A, et al. MIF/CXCR4 signaling axis contributes to survival, invasion, and drug resistance of metastatic neuroblastoma cells in the bone marrow microenvironment. BMC Cancer, 2022, 22(1): 669.
doi: 10.1186/s12885-022-09725-8
pmid: 35715791
|
|
|
| [71] |
Bernhagen J, Krohn R, Lue H Q, et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nature Medicine, 2007, 13(5): 587-596.
doi: 10.1038/nm1567
pmid: 17435771
|
|
|
| [72] |
Miller E J, Li J, Leng L, et al. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature, 2008, 451(7178): 578-582.
doi: 10.1038/nature06504
|
|
|
| [73] |
Fallica J, Boyer L, Kim B, et al. Macrophage migration inhibitory factor is a novel determinant of cigarette smoke-induced lung damage. American Journal of Respiratory Cell and Molecular Biology, 2014, 51(1): 94-103.
doi: 10.1165/rcmb.2013-0371OC
pmid: 24490973
|
|
|
| [74] |
Mathew B, Jacobson J R, Siegler J H, et al. Role of migratory inhibition factor in age-related susceptibility to radiation lung injury via NF-E2-related factor-2 and antioxidant regulation. American Journal of Respiratory Cell and Molecular Biology, 2013, 49(2): 269-278.
doi: 10.1165/rcmb.2012-0291OC
pmid: 23526214
|
|
|
| [75] |
Kariya S, Okano M, Maeda Y, et al. Role of macrophage migration inhibitory factor in age-related hearing loss. Neuroscience, 2014, 279: 132-138.
doi: 10.1016/j.neuroscience.2014.08.042
pmid: 25194790
|
|
|
| [76] |
Rowe M A, Harper L R, McNulty M A, et al. Reduced osteoarthritis severity in aged mice with deletion of macrophage migration inhibitory factor. Arthritis & Rheumatology (Hoboken, N J), 2017, 69(2): 352-361.
|
|
|
| [77] |
Liu M, Xie Z K, Sun G, et al. Macrophage migration inhibitory factor may play a protective role in osteoarthritis. Arthritis Research & Therapy, 2021, 23(1): 59.
|
|
|
| [78] |
Ashcroft G S, Mills S J, Lei K J, et al. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. The Journal of Clinical Investigation, 2003, 111(9): 1309-1318.
doi: 10.1172/JCI16288
|
|
|
| [79] |
Mahalingam D, Patel M R, Sachdev J C, et al. Phase I study of imalumab (BAX69), a fully human recombinant antioxidized macrophage migration inhibitory factor antibody in advanced solid tumours. British Journal of Clinical Pharmacology, 2020, 86(9): 1836-1848.
doi: 10.1111/bcp.v86.9
|
|
|
| [80] |
Hussain F, Freissmuth M, Völkel D, et al. Human anti-macrophage migration inhibitory factor antibodies inhibit growth of human prostate cancer cells in vitro and in vivo. Molecular Cancer Therapeutics, 2013, 12(7): 1223-1234.
doi: 10.1158/1535-7163.MCT-12-0988
pmid: 23619302
|
|
|
| [81] |
Stein R, Smith M R, Chen S S, et al. Combining milatuzumab with bortezomib, doxorubicin, or dexamethasone improves responses in multiple myeloma cell lines. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research, 2009, 15(8): 2808-2817.
doi: 10.1158/1078-0432.CCR-08-1953
|
|
|
| [82] |
Ladikou E E, Chevassut T, Pepper C J, et al. Dissecting the role of the CXCL12/CXCR4 axis in acute myeloid leukaemia. British Journal of Haematology, 2020, 189(5): 815-825.
doi: 10.1111/bjh.16456
pmid: 32135579
|
|
|
| [83] |
Ghobrial I M, Liu C J, Redd R A, et al. A phase Ib/II trial of the first-in-class anti-CXCR4 antibody ulocuplumab in combination with lenalidomide or bortezomib plus dexamethasone in relapsed multiple myeloma. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research, 2020, 26(2): 344-353.
doi: 10.1158/1078-0432.CCR-19-0647
|
|
|
| [84] |
Treon S P, Meid K, Hunter Z R, et al. Phase1 study of ibrutinib and the CXCR4 antagonist ulocuplumab in CXCR4-mutated Waldenström macroglobulinemia. Blood, 2021, 138(17): 1535-1539.
|
|
|
| [85] |
Kashyap M K, Kumar D, Jones H, et al. Ulocuplumab (BMS-936564/MDX1338): a fully human anti-CXCR4 antibody induces cell death in chronic lymphocytic leukemia mediated through a reactive oxygen species-dependent pathway. Oncotarget, 2016, 7(3): 2809-2822.
doi: 10.18632/oncotarget.6465
pmid: 26646452
|
|
|
| [86] |
Cheng Z Q, Zhou S Y, Wang X F, et al. Characterization and application of two novel monoclonal antibodies against human CXCR4: cell proliferation and migration regulation for glioma cell line in vitro by CXCR4/SDF-1alpha signal. Hybridoma (2005), 2009, 28(1): 33-41.
doi: 10.1089/hyb.2008.0069
|
|
|
| [87] |
Kok T, Wasiel A A, Cool R H, et al. Small-molecule inhibitors of macrophage migration inhibitory factor (MIF) as an emerging class of therapeutics for immune disorders. Drug Discovery Today, 2018, 23(11): 1910-1918.
doi: S1359-6446(17)30581-0
pmid: 29936245
|
|
|
| [88] |
Liu Y Y, Liu Y N, Wang Q F, et al. MIF inhibitor ISO-1 alleviates severe acute pancreatitis-associated acute kidney injury by suppressing the NLRP 3 inflammasome signaling pathway. International Immunopharmacology, 2021, 96: 107555.
doi: 10.1016/j.intimp.2021.107555
|
|
|
| [89] |
Cheng B, Wang Q F, Song Y D, et al. MIF inhibitor, ISO-1, attenuates human pancreatic cancer cell proliferation, migration and invasion in vitro, and suppresses xenograft tumour growth in vivo. Scientific Reports, 2020, 10: 6741.
doi: 10.1038/s41598-020-63778-y
pmid: 32317702
|
|
|
| [90] |
Zheng L, Gao J W, Jin K T, et al. Macrophage migration inhibitory factor (MIF) inhibitor 4-IPP suppresses osteoclast formation and promotes osteoblast differentiation through the inhibition of the NF-κB signaling pathway. The FASEB Journal, 2019, 33(6): 7667-7683.
doi: 10.1096/fsb2.v33.6
|
|
|
| [91] |
Wang J P, Hu W M, Wang K S, et al. Repertaxin, an inhibitor of the chemokine receptors CXCR1 and CXCR2, inhibits malignant behavior of human gastric cancer MKN45 cells in vitro and in vivo and enhances efficacy of 5-fluorouracil. International Journal of Oncology, 2016, 48(4): 1341-1352.
doi: 10.3892/ijo.2016.3371
|
|
|
| [92] |
Bai F W, Asojo O A, Cirillo P, et al. A novel allosteric inhibitor of macrophage migration inhibitory factor (MIF). The Journal of Biological Chemistry, 2012, 287(36): 30653-30663.
doi: 10.1074/jbc.M112.385583
|
|
|
| [93] |
Martin P, Furman R R, Rutherford S, et al. Phase I study of the anti-CD 74 monoclonal antibody milatuzumab (hLL1) in patients with previously treated B-cell lymphomas. Leukemia & Lymphoma, 2015, 56(11): 3065-3070.
|
|
|
| [94] |
Van Bockstaele F, Holz J B, Revets H. The development of nanobodies for therapeutic applications. Current Opinion in Investigational Drugs (London, England: 2000), 2009, 10(11): 1212-1224.
|
|
|
| [95] |
Xu J L, Xu K, Jung S, et al. Nanobodies from camelid mice and llamas neutralize SARS-CoV-2 variants. Nature, 2021, 595(7866): 278-282.
doi: 10.1038/s41586-021-03676-z
|
|
|
| [96] |
Xiang Y F, Nambulli S, Xiao Z Y, et al. Versatile and multivalent nanobodies efficiently neutralize SARS-CoV-2. Science, 2020, 370(6523): 1479-1484.
doi: 10.1126/science.abe4747
pmid: 33154108
|
|
|
| [97] |
Sparkes A, De Baetselier P, Brys L, et al. Novel half-life extended anti-MIF nanobodies protect against endotoxic shock. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 2018, 32(6): 3411-3422.
doi: 10.1096/fsb2.v32.6
|
|
|
| [98] |
Xiao Z P, Song S S, Chen D, et al. Proteolysis targeting Chimera (PROTAC) for macrophage migration inhibitory factor (MIF) has anti-proliferative activity in lung cancer cells. Angewandte Chemie (International Ed in English), 2021, 60(32): 17514-17521.
doi: 10.1002/anie.v60.32
|
|
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
