Study of Monocytes/Macrophages Stimuli as the Targets of Treating Inflammatory Bone Diseases

Author(s): Yuan Liu, Yang Cao, Wanli Smith, Baorong He, Liang Yan*.

Journal Name: Current Drug Targets

Volume 21 , Issue 4 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Inflammation is the most common pathology in many orthopedic diseases, such as: rheumatoid arthritis (RA), osteoarthritis (OA) and other reasons caused osteolysis. The leading factor of inflammation was considered as the differentiation of monocyte and the polarization of macrophage. However, cytokines and different cell models could regulate this progress in some aspects. Therefore, in the current review, we summarize several cytokines and cell models, which could lead to inflammatory orthopedic diseases via regulating monocytes and macrophages. In order to extensively explore the potential therapeutic and medicine targets for inflammation-induced bone diseases.

Keywords: Macrophages, cytokines, rheumatoid arthritis, osteoarthritis, osteolysis, monocyte.

[1]
Bae HC, Park HJ, Wang SY, Yang HR, Lee MC, Han HS. Correction to: Hypoxic condition enhances chondrogenesis in synovium-derived mesenchymal stem cells. Biomater Res 2019; 23: 7.
[http://dx.doi.org/10.1186/s40824-019-0158-x] [PMID: 30873291]
[2]
Daghestani HN, Pieper CF, Kraus VB. Soluble macrophage biomarkers indicate inflammatory phenotypes in patients with knee osteoarthritis. Arthritis Rheumatol 2015; 67(4): 956-65.
[http://dx.doi.org/10.1002/art.39006] [PMID: 25544994]
[3]
Rosa I, Marini M, Guasti D, Ibba-Manneschi L, Manetti M. Morphological evidence of telocytes in human synovium. Sci Rep 2018; 8(1): 3581.
[http://dx.doi.org/10.1038/s41598-018-22067-5] [PMID: 29483562]
[4]
Smith MD, Barg E, Weedon H, et al. Microarchitecture and protective mechanisms in synovial tissue from clinically and arthroscopically normal knee joints. Ann Rheum Dis 2003; 62(4): 303-7.
[http://dx.doi.org/10.1136/ard.62.4.303] [PMID: 12634226]
[5]
Moghaddami M, Cleland LG, Mayrhofer G. MHC II+ CD45+ cells from synovium-rich tissues of normal rats: phenotype, comparison with macrophage and dendritic cell lineages and differentiation into mature dendritic cells in vitro. Int Immunol 2005; 17(8): 1103-15.
[http://dx.doi.org/10.1093/intimm/dxh290] [PMID: 16030130]
[6]
Fujikawa Y, Sabokbar A, Neale S, Athanasou NA. Human osteoclast formation and bone resorption by monocytes and synovial macrophages in rheumatoid arthritis. Ann Rheum Dis 1996; 55(11): 816-22.
[http://dx.doi.org/10.1136/ard.55.11.816] [PMID: 8976638]
[7]
Kurowska-Stolarska M, Alivernini S. Synovial tissue macrophages: friend or foe? RMD Open 2017; 3(2)e000527
[http://dx.doi.org/10.1136/rmdopen-2017-000527] [PMID: 29299338]
[8]
Manferdini C, Paolella F, Gabusi E, et al. From osteoarthritic synovium to synovial-derived cells characterization: synovial macrophages are key effector cells. Arthritis Res Ther 2016; 18: 83.
[http://dx.doi.org/10.1186/s13075-016-0983-4] [PMID: 27044395]
[9]
Smeets TJ, Kraan MC, van Loon ME, Tak PP. Tumor necrosis factor alpha blockade reduces the synovial cell infiltrate early after initiation of treatment, but apparently not by induction of apoptosis in synovial tissue. Arthritis Rheum 2003; 48(8): 2155-62.
[http://dx.doi.org/10.1002/art.11098] [PMID: 12905468]
[10]
Szekanecz Z, Koch AE. Macrophages and their products in rheumatoid arthritis. Curr Opin Rheumatol 2007; 19(3): 289-95.
[http://dx.doi.org/10.1097/BOR.0b013e32805e87ae] [PMID: 17414958]
[11]
Barranco C. Stem cells: Stem cell therapy seems safe in refractory RA. Nat Rev Rheumatol 2016; 12(8): 436.
[http://dx.doi.org/10.1038/nrrheum.2016.105] [PMID: 27334203]
[12]
Ma Y, Pope RM. The role of macrophages in rheumatoid arthritis. Curr Pharm Des 2005; 11(5): 569-80.
[http://dx.doi.org/10.2174/1381612053381927] [PMID: 15720276]
[13]
Bay-Jensen AC, Thudium CS, Gualillo O, Mobasheri A. Biochemical marker discovery, testing and evaluation for facilitating OA drug discovery and development. Drug Discov Today 2018; 23(2): 349-58.
[http://dx.doi.org/10.1016/j.drudis.2017.10.008] [PMID: 29038075]
[14]
Wallace IJ, Worthington S, Felson DT, et al. Knee osteoarthritis has doubled in prevalence since the mid-20th century. Proc Natl Acad Sci USA 2017; 114(35): 9332-6.
[http://dx.doi.org/10.1073/pnas.1703856114] [PMID: 28808025]
[15]
Kan HS, Chan PK, Chiu KY, Yan CH, Yeung SS, Ng YL, et al. Non-surgical treatment of knee osteoarthritis. Hong Kong medical journal = Xianggang yi xue za zhi 2019.
[http://dx.doi.org/10.12809/hkmj187600]
[16]
Iannone F, Lapadula G. Obesity and inflammation--targets for OA therapy. Curr Drug Targets 2010; 11(5): 586-98.
[http://dx.doi.org/10.2174/138945010791011857] [PMID: 20199391]
[17]
Rainbow R, Ren W, Zeng L. Inflammation and joint tissue interactions in OA: Implications for potential therapeutic approaches. Arthritis (Egypt) 2012. 2012741582
[http://dx.doi.org/10.1155/2012/741582] [PMID: 22745906]
[18]
Wood MJ, Leckenby A, Reynolds G, et al. Macrophage proliferation distinguishes 2 subgroups of knee osteoarthritis patients. JCI Insight 2019; 4(2)125325
[http://dx.doi.org/10.1172/jci.insight.125325] [PMID: 30674730]
[19]
Ramshaw HS, Bardy PG, Lee MA, Lopez AF. Chronic myelomonocytic leukemia requires granulocyte-macrophage colony-stimulating factor for growth in vitro and in vivo. Exp Hematol 2002; 30(10): 1124-31.
[http://dx.doi.org/10.1016/S0301-472X(02)00903-7] [PMID: 12384142]
[20]
Lamothe B, Lai Y, Hur L, et al. Deletion of TAK1 in the myeloid lineage results in the spontaneous development of myelomonocytic leukemia in mice. PLoS One 2012; 7(12)e51228
[http://dx.doi.org/10.1371/journal.pone.0051228] [PMID: 23251462]
[21]
Ma XW, Yang LH. [Research Advances of Monocyte/Macrophage in Chronic Lymphocytic Leukemia--Review]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2019; 27(1): 292-6. [Research Advances of Monocyte/Macrophage in Chronic Lymphocytic Leukemia-- Review
[PMID: 30738486]
[22]
Sabir F, Farooq RK, Asim Ur R, Ahmed N. Monocyte as an Emerging Tool for Targeted Drug Delivery: A Review. Curr Pharm Des 2019.
[http://dx.doi.org/10.2174/1381612825666190102104642] [PMID: 30605050]
[23]
Ziegler-Heitbrock L, Ancuta P, Crowe S, et al. Nomenclature of monocytes and dendritic cells in blood. Blood 2010; 116(16): e74-80.
[http://dx.doi.org/10.1182/blood-2010-02-258558] [PMID: 20628149]
[24]
Franzoni G, Graham SP, Giudici SD, et al. Characterization of the interaction of African swine fever virus with monocytes and derived macrophage subsets. Vet Microbiol 2017; 198: 88-98.
[http://dx.doi.org/10.1016/j.vetmic.2016.12.010] [PMID: 28062012]
[25]
Yang J, Zhang L, Yu C, Yang XF, Wang H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res 2014; 2(1): 1.
[http://dx.doi.org/10.1186/2050-7771-2-1] [PMID: 24398220]
[26]
Traunecker E, Gardner R, Fonseca JE, et al. Blocking of LFA-1 enhances expansion of Th17 cells induced by human CD14(+) CD16(++) nonclassical monocytes. Eur J Immunol 2015; 45(5): 1414-25.
[http://dx.doi.org/10.1002/eji.201445100] [PMID: 25678252]
[27]
El-Bassioudni NE, Amin NA, El Amir A, Farid AA, Madkour ME, Atta RI. Down regulation of classical monocytes subset in patients with hcv related liver fibrosis. J Egypt Soc Parasitol 2017; 47(1): 207-10.
[PMID: 30157349]
[28]
Williams H, Cassorla G, Pertsoulis N, Patel V, Vicaretti M, Marmash N, et al. Human classical monocytes display unbalanced M1/M2 phenotype with increased atherosclerotic risk and presence of disease. International angiology a journal of the International Union of Angiology 2017; 36(2): 145-55.
[29]
Bharat A, McQuattie-Pimentel AC, Budinger GRS. Non-classical monocytes in tissue injury and cancer. Oncotarget 2017; 8(63): 106171-2.
[http://dx.doi.org/10.18632/oncotarget.22584] [PMID: 29290937]
[30]
Fukui S, Iwamoto N, Takatani A, et al. M1 and M2 Monocytes in Rheumatoid Arthritis: A Contribution of Imbalance of M1/M2 Monocytes to Osteoclastogenesis. Front Immunol 2018; 8: 1958.
[http://dx.doi.org/10.3389/fimmu.2017.01958] [PMID: 29375576]
[31]
Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010; 32(5): 593-604.
[http://dx.doi.org/10.1016/j.immuni.2010.05.007] [PMID: 20510870]
[32]
Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 2014; 6: 13.
[http://dx.doi.org/10.12703/P6-13] [PMID: 24669294]
[33]
Collison J. Rheumatoid arthritis: Features of synovium in RA remission revealed. Nat Rev Rheumatol 2016; 12(6): 316.
[http://dx.doi.org/10.1038/nrrheum.2016.63] [PMID: 27098906]
[34]
Zhang A, Lee YC. Mechanisms for Joint Pain in Rheumatoid Arthritis (RA): from Cytokines to Central Sensitization. Curr Osteoporos Rep 2018; 16(5): 603-10.
[http://dx.doi.org/10.1007/s11914-018-0473-5] [PMID: 30128836]
[35]
Yoon BR, Yoo SJ. Choi Yh, et al Functional phenotype of synovial monocytes modulating inflammatory T-cell responses in rheumatoid arthritis (RA). PLoS One 2014; 9(10) e109775
[http://dx.doi.org/10.1371/journal.pone.0109775] [PMID: 25329467]
[36]
Manzo A, Bugatti S, Caporali R, Montecucco C. Histopathology of the synovial tissue: perspectives for biomarker development in chronic inflammatory arthritides. Reumatismo 2018; 70(3): 121-32.
[http://dx.doi.org/10.4081/reumatismo.2018.1057] [PMID: 30282438]
[37]
Agarwal SK, Brenner MB. Role of adhesion molecules in synovial inflammation. Curr Opin Rheumatol 2006; 18(3): 268-76.
[http://dx.doi.org/10.1097/01.bor.0000218948.42730.39] [PMID: 16582691]
[38]
Imperatore F, Maurizio J, Vargas Aguilar S, et al. SIRT1 regulates macrophage self-renewal. EMBO J 2017; 36(16): 2353-72.
[http://dx.doi.org/10.15252/embj.201695737] [PMID: 28701484]
[39]
Park SY, Lee SW, Kim HY, et al. SIRT1 inhibits differentiation of monocytes to macrophages: amelioration of synovial inflammation in rheumatoid arthritis. J Mol Med (Berl) 2016; 94(8): 921-31.
[http://dx.doi.org/10.1007/s00109-016-1402-7] [PMID: 26956118]
[40]
Wang R, Dong Z, Lan X, Liao Z, Chen M. Sweroside alleviated lps-induced inflammation via sirt1 mediating nf-κb and foxo1 signaling pathways in raw264.7 cells. Molecules 2019; 24(5)E872
[http://dx.doi.org/10.3390/molecules24050872] [PMID: 30823686]
[41]
Lee N, Kim D, Kim WU. Role of NFAT5 in the immune system and pathogenesis of autoimmune diseases. Front Immunol 2019; 10: 270.
[http://dx.doi.org/10.3389/fimmu.2019.00270] [PMID: 30873159]
[42]
Zappe M, Feldner A, Arnold C, Sticht C, Hecker M, Korff T. NFAT5 Isoform C controls biomechanical stress responses of vascular smooth muscle cells. Front Physiol 2018; 9: 1190.
[http://dx.doi.org/10.3389/fphys.2018.01190] [PMID: 30190682]
[43]
Choi S, You S, Kim D, et al. Transcription factor NFAT5 promotes macrophage survival in rheumatoid arthritis. J Clin Invest 2017; 127(3): 954-69.
[http://dx.doi.org/10.1172/JCI87880] [PMID: 28192374]
[44]
Li J, Hsu HC, Mountz JD. Managing macrophages in rheumatoid arthritis by reform or removal. Curr Rheumatol Rep 2012; 14(5): 445-54.
[http://dx.doi.org/10.1007/s11926-012-0272-4] [PMID: 22855296]
[45]
Liang C, Tian D, Ren X, et al. The development of Bruton’s tyrosine kinase (BTK) inhibitors from 2012 to 2017: A mini-review. Eur J Med Chem 2018; 151: 315-26.
[http://dx.doi.org/10.1016/j.ejmech.2018.03.062] [PMID: 29631132]
[46]
Lou Y, Han X, Kuglstatter A, et al. Structure-based drug design of RN486, a potent and selective Bruton’s tyrosine kinase (BTK) inhibitor, for the treatment of rheumatoid arthritis. J Med Chem 2015; 58(1): 512-6.
[http://dx.doi.org/10.1021/jm500305p] [PMID: 24712864]
[47]
Hartkamp LM, Fine JS, van Es IE, et al. Btk inhibition suppresses agonist-induced human macrophage activation and inflammatory gene expression in RA synovial tissue explants. Ann Rheum Dis 2015; 74(8): 1603-11.
[http://dx.doi.org/10.1136/annrheumdis-2013-204143] [PMID: 24764451]
[48]
MacDonald GI, Augello A, De Bari C. Role of mesenchymal stem cells in reestablishing immunologic tolerance in autoimmune rheumatic diseases. Arthritis Rheum 2011; 63(9): 2547-57.
[http://dx.doi.org/10.1002/art.30474] [PMID: 21647863]
[49]
Lai P, Weng J, Guo L, Chen X, Du X. Novel insights into MSC-EVs therapy for immune diseases. Biomark Res 2019; 7: 6.
[http://dx.doi.org/10.1186/s40364-019-0156-0] [PMID: 30923617]
[50]
Luz-Crawford P, Djouad F, Toupet K, et al. Mesenchymal stem cell-derived interleukin 1 receptor antagonist promotes macrophage polarization and inhibits b cell differentiation. Stem Cells 2016; 34(2): 483-92.
[http://dx.doi.org/10.1002/stem.2254] [PMID: 26661518]
[51]
Maggini J, Mirkin G, Bognanni I, et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 2010; 5(2)e9252
[http://dx.doi.org/10.1371/journal.pone.0009252] [PMID: 20169081]
[52]
Shin TH, Kim HS, Kang TW, et al. Human umbilical cord blood-stem cells direct macrophage polarization and block inflammasome activation to alleviate rheumatoid arthritis. Cell Death Dis 2016; 7(12) e2524
[http://dx.doi.org/10.1038/cddis.2016.442] [PMID: 28005072]
[53]
Obry A, Hardouin J, Lequerré T, et al. Identification of 7 Proteins in Sera of RA Patients with Potential to Predict ETA/MTX Treatment Response. Theranostics 2015; 5(11): 1214-24.
[http://dx.doi.org/10.7150/thno.12403] [PMID: 26379787]
[54]
Zhou Q, Zhou Y, Chen H, Wang Z, Tang Z, Liu J. The efficacy and safety of certolizumab pegol (CZP) in the treatment of active rheumatoid arthritis (RA): a meta-analysis from nine randomized controlled trials. Int J Clin Exp Med 2014; 7(11): 3870-80.
[PMID: 25550895]
[55]
Chopin C, Pauvele L, Jaulerry S, Brochot P, Eschard JP, Salmon JH. [Effectiveness, therapeutic maintenance and reasons for stopping tocilizumab (TCZ): A retrospective and monocentric study in 88 patients followed for rheumatoid arthritis (RA) at the Reims university hospital] Therapie 2018; 73(3): 231-6. [Effectiveness, therapeutic maintenance and reasons for stopping tocilizumab (TCZ): A retrospective and monocentric study in 88 patients followed for rheumatoid arthritis (RA) at the Reims university hospital]
[http://dx.doi.org/10.1016/j.therap.2017.08.004] [PMID: 29146040]
[56]
Degboé Y, Rauwel B, Baron M, et al. Polarization of rheumatoid macrophages by TNF targeting through an IL-10/STAT3 mechanism. Front Immunol 2019; 10: 3.
[http://dx.doi.org/10.3389/fimmu.2019.00003] [PMID: 30713533]
[57]
Charlier E, Deroyer C, Ciregia F, et al. Chondrocyte dedifferentiation and osteoarthritis (OA). Biochem Pharmacol 2019; 165: 49-65.
[http://dx.doi.org/10.1016/j.bcp.2019.02.036] [PMID: 30853397]
[58]
Nwosu LN, Mapp PI, Chapman V, Walsh DA. Relationship between structural pathology and pain behaviour in a model of osteoarthritis (OA). Osteoarthritis Cartilage 2016; 24(11): 1910-7.
[http://dx.doi.org/10.1016/j.joca.2016.06.012] [PMID: 27349460]
[59]
Bloom J, Sun S, Al-Abed Y. MIF, a controversial cytokine: a review of structural features, challenges, and opportunities for drug development. Expert Opin Ther Targets 2016; 20(12): 1463-75.
[http://dx.doi.org/10.1080/14728222.2016.1251582] [PMID: 27762152]
[60]
Grieb G, Kim BS, Simons D, Bernhagen J, Pallua N. MIF and CD74 - suitability as clinical biomarkers. Mini Rev Med Chem 2014; 14(14): 1125-31.
[http://dx.doi.org/10.2174/1389557515666150203143317] [PMID: 25643609]
[61]
Onodera S, Tanji H, Suzuki K, et al. High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints. Cytokine 1999; 11(2): 163-7.
[http://dx.doi.org/10.1006/cyto.1998.0402] [PMID: 10089139]
[62]
Mitchell RA, 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. Proc Natl Acad Sci USA 2002; 99(1): 345-50.
[http://dx.doi.org/10.1073/pnas.012511599] [PMID: 11756671]
[63]
Rowe MA, Harper LR, McNulty MA, et al. reduced osteoarthritis severity in aged mice with deletion of macrophage migration inhibitory factor. Arthritis Rheumatol 2017; 69(2): 352-61.
[http://dx.doi.org/10.1002/art.39844] [PMID: 27564840]
[64]
Spencer LA, Weller PF. Eosinophils and Th2 immunity: contemporary insights. Immunol Cell Biol 2010; 88(3): 250-6.
[http://dx.doi.org/10.1038/icb.2009.115] [PMID: 20065995]
[65]
Liu L, Zhang Y, Zheng X, et al. Eosinophils attenuate arthritis by inducing M2 macrophage polarization via inhibiting the IκB/P38 MAPK signaling pathway. Biochem Biophys Res Commun 2019; 508(3): 894-901.
[http://dx.doi.org/10.1016/j.bbrc.2018.12.010] [PMID: 30528734]
[66]
Mouton AJ, Ma Y, Rivera Gonzalez OJ, et al. Fibroblast polarization over the myocardial infarction time continuum shifts roles from inflammation to angiogenesis. Basic Res Cardiol 2019; 114(2): 6.
[http://dx.doi.org/10.1007/s00395-019-0715-4] [PMID: 30635789]
[67]
Ma X, Lu YP, Yang L, et al. Rapamycin and cyclosporine have different effects on expression of Ang-1 and Ang-2 and Tie2 in rat renal allograft with chronic allograft nephropathy. Transplant Proc 2008; 40(8): 2804-7.
[http://dx.doi.org/10.1016/j.transproceed.2008.08.047] [PMID: 18929866]
[68]
Hamilton JA, Tak PP. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases. Arthritis Rheum 2009; 60(5): 1210-21.
[http://dx.doi.org/10.1002/art.24505] [PMID: 19404968]
[69]
Krausz S, Garcia S, Ambarus CA, et al. Angiopoietin-2 promotes inflammatory activation of human macrophages and is essential for murine experimental arthritis. Ann Rheum Dis 2012; 71(8): 1402-10.
[http://dx.doi.org/10.1136/annrheumdis-2011-200718] [PMID: 22730375]
[70]
Lin H, Ho AS, Haley-Vicente D, et al. Cloning and characterization of IL-1HY2, a novel interleukin-1 family member. J Biol Chem 2001; 276(23): 20597-602.
[http://dx.doi.org/10.1074/jbc.M010095200] [PMID: 11278614]
[71]
Boutet MA, Bart G, Penhoat M, et al. Distinct expression of interleukin (IL)-36α, β and γ, their antagonist IL-36Ra and IL-38 in psoriasis, rheumatoid arthritis and Crohn’s disease. Clin Exp Immunol 2016; 184(2): 159-73.
[http://dx.doi.org/10.1111/cei.12761] [PMID: 26701127]
[72]
Boutet MA, Najm A, Bart G, et al. IL-38 overexpression induces anti-inflammatory effects in mice arthritis models and in human macrophages in vitro. Ann Rheum Dis 2017; 76(7): 1304-12.
[http://dx.doi.org/10.1136/annrheumdis-2016-210630] [PMID: 28288964]
[73]
Zhang H, Lin C, Zeng C, et al. Synovial macrophage M1 polarisation exacerbates experimental osteoarthritis partially through R-spondin-2. Ann Rheum Dis 2018; 77(10): 1524-34.
[http://dx.doi.org/10.1136/annrheumdis-2018-213450] [PMID: 29991473]
[74]
Yan H, Wang S, Li Z, et al. Rspo2 suppresses CD36-mediated apoptosis in oxidized low density lipoprotein-induced macrophages. Mol Med Rep 2016; 14(4): 2945-52.
[http://dx.doi.org/10.3892/mmr.2016.5642] [PMID: 27571704]
[75]
Roukis TS. Contemporary Management of Displaced Intra-Articular Calcaneal Fractures. Clin Podiatr Med Surg 2019; 36(2): xv-xvi.
[http://dx.doi.org/10.1016/j.cpm.2018.11.001] [PMID: 30784543]
[76]
Popelka V. Current concepts in the treatment of intra-articular calcaneal fractures. Acta Chir Orthop Traumatol Cech 2019; 86(1): 58-64.
[PMID: 30843515]
[77]
Furman BD, Kimmerling KA, Zura RD, et al. Articular ankle fracture results in increased synovitis, synovial macrophage infiltration, and synovial fluid concentrations of inflammatory cytokines and chemokines. Arthritis Rheumatol 2015; 67(5): 1234-9.
[http://dx.doi.org/10.1002/art.39064] [PMID: 25707992]
[78]
Santos Savio A, Machado Diaz AC, Chico Capote A, et al. Differential expression of pro-inflammatory cytokines IL-15Ralpha, IL-15, IL-6 and TNFalpha in synovial fluid from rheumatoid arthritis patients. BMC Musculoskelet Disord 2015; 16: 51.
[http://dx.doi.org/10.1186/s12891-015-0516-3] [PMID: 25879761]
[79]
Marvel D, Gabrilovich DI. Myeloid-derived suppressor cells in the tumor microenvironment: expect the unexpected. J Clin Invest 2015; 125(9): 3356-64.
[http://dx.doi.org/10.1172/JCI80005] [PMID: 26168215]
[80]
Yang M, Liu J, Piao C, Shao J, Du J. ICAM-1 suppresses tumor metastasis by inhibiting macrophage M2 polarization through blockade of efferocytosis. Cell Death Dis 2015; 6e: 1780.
[http://dx.doi.org/10.1038/cddis.2015.144] [PMID: 26068788]
[81]
Jones JD, Sinder BP, Paige D, et al. Trabectedin Reduces Skeletal Prostate Cancer Tumor Size in Association with Effects on M2 Macrophages and Efferocytosis. Neoplasia 2019; 21(2): 172-84.
[http://dx.doi.org/10.1016/j.neo.2018.11.003] [PMID: 30591422]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 4
Year: 2020
Page: [338 - 343]
Pages: 6
DOI: 10.2174/1389450120666191015211737
Price: $65

Article Metrics

PDF: 19
HTML: 3
EPUB: 1