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Research Article

Transcriptomic Network Support Distinct Roles of Classical and Non-Classical Monocytes in Human

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Pages 470-489 | Accepted 03 Mar 2014, Published online: 14 Apr 2014

REFERENCES

  • Geissmann F, Manz MG, Jung S, Development of monocytes, macrophages, and dendritic cells. Science 2010;327:656–661.
  • Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5:953–964.
  • Staples KJ, Smallie T, Williams LM, IL-10 induces IL-10 in primary human monocyte-derived macrophages via the transcription factor Stat3. J Immunol 2007;178:4779–4785.
  • Ziegler-Heitbrock HW. The biology of the monocyte system. Eur J Cell Biol 1989;49:1–12.
  • Ziegler-Heitbrock L, Hofer TP. Toward a refined definition of monocyte subsets. Front Immunol 2013;4:23.
  • Wong KL, Tai JJ, Wong WC, Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 2011;118:e16–31.
  • Sunderkotter C, Nikolic T, Dillon MJ, Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004;172:4410–4417.
  • Nahrendorf M, Pittet MJ, Swirski FK. Monocytes: protagonists of infarct inflammation and repair after myocardial infarction. Circulation 2010;121:2437–2445.
  • Nahrendorf M, Swirski FK, Aikawa E, The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007;204:3037–3047.
  • Cooper DL, Martin SG, Robinson JI, FcgammaRIIIa expression on monocytes in rheumatoid arthritis: role in immune-complex stimulated TNF production and non-response to methotrexate therapy. PloS one 2012;7:e28918.
  • Yona S, Jung S. Monocytes: subsets, origins, fates and functions. Curr Opin Hematol 2010;17:53–59.
  • Komano Y, Nanki T, Hayashida K, Identification of a human peripheral blood monocyte subset that differentiates into osteoclasts. Arthritis Res Ther 2006;8:R152.
  • Lari R, Kitchener PD, Hamilton JA. The proliferative human monocyte subpopulation contains osteoclast precursors. Arthritis Res Ther 2009;11:R23.
  • Jakubzick C, Gautier EL, Gibbings SL, Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 2013;39:599–610.
  • Ancuta P, Liu KY, Misra V, Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+and CD16- monocyte subsets. BMC Genomics 2009;10:403.
  • Frankenberger M, Hofer TP, Marei A, Transcript profiling of CD16-positive monocytes reveals a unique molecular fingerprint. Eur J Immunol 2012;42:957–974.
  • Haniffa M, Shin A, Bigley V, Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103 +nonlymphoid dendritic cells. Immunity 2012;37:60–73.
  • Ingersoll MA, Spanbroek R, Lottaz C, Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 2010;115:e10–e19.
  • Cai H, Chen H, Yi T, VennPlex–a novel Venn diagram program for comparing and visualizing datasets with differentially regulated datapoints. PloS One 2013;8:e53388.
  • Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 2006;7:311–317.
  • Tsou CL, Peters W, Si Y, Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007;117:902–909.
  • Combadiere C, Potteaux S, Rodero M, Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 2008;117:1649–1657.
  • Swirski FK, Libby P, Aikawa E, Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007;117:195–205.
  • Swirski FK, Nahrendorf M, Etzrodt M, Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009;325:612–616.
  • Jia T, Serbina NV, Brandl K, Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol 2008;180:6846–6853.
  • Scott HM, Flynn JL. Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect Immun 2002;70:5946–5954.
  • Peters W, Cyster JG, Mack M, CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J Immunol 2004;172:7647–7653.
  • Bouchon A, Dietrich J, Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J Immunol 2000;164:4991–4995.
  • Dower K, Ellis DK, Saraf K, Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide. J Immunol 2008;180:3520–3534.
  • Gibot S, Massin F, Marcou M, TREM-1 promotes survival during septic shock in mice. Eur J Immunol 2007;37:456–466.
  • Shi C, Velazquez P, Hohl TM, Monocyte trafficking to hepatic sites of bacterial infection is chemokine independent and directed by focal intercellular adhesion molecule-1 expression. J Immunol 2010;184:6266–6274.
  • Potteaux S, Gautier EL, Hutchison SB, Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression. J Clin Invest 2011;121:2025–2036.
  • Auffray C, Fogg D, Garfa M, Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007;317:666–670.
  • Krieglstein CF, Anthoni C, Laukotter MG, Effect of anti-CD11b (alphaM-MAC-1) and anti-CD54 (ICAM-1) monoclonal antibodies on indomethacin induced chronic ileitis in rats. Int J Colorectal Dis 1999;14:219–223.
  • Park-Min KH, Lee EY, Moskowitz NK, Negative regulation of osteoclast precursor differentiation by CD11b and beta2 integrin-B-cell lymphoma 6 signaling. J Bone Miner Res : the official journal of the American Society for Bone and Mineral Research. 2013;28:135–149.
  • Hayashi H, Nakahama K, Sato T, The role of Mac-1 (CD11b/CD18) in osteoclast differentiation induced by receptor activator of nuclear factor-kappaB ligand. FEBS Lett 2008;582:3243–3248.
  • Charles JF, Hsu LY, Niemi EC, Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function. J Clin Invest 2012;122:4592–4605.
  • Chiu YG, Shao T, Feng C, CD16 (FcRgammaIII) as a potential marker of osteoclast precursors in psoriatic arthritis. Arthritis Res Ther 2010;12:R14.
  • Byon CH, Sun Y, Chen J, Runx2-upregulated receptor activator of nuclear factor kappaB ligand in calcifying smooth muscle cells promotes migration and osteoclastic differentiation of macrophages. Arterioscler Thromb Vasc Biol 2011;31:1387–1396.
  • Enomoto H, Shiojiri S, Hoshi K, Induction of osteoclast differentiation by Runx2 through receptor activator of nuclear factor-kappa B ligand (RANKL) and osteoprotegerin regulation and partial rescue of osteoclastogenesis in Runx2-/- mice by RANKL transgene. J Biol Chem 2003;278:23971–23977.
  • Egawa M, Mukai K, Yoshikawa S, Inflammatory monocytes recruited to allergic skin acquire an anti-inflammatory M2 phenotype via basophil-derived interleukin-4. Immunity 2013;38:570–580.
  • Arnold L, Henry A, Poron F, Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 2007;204:1057–1069.
  • Leach ST, Mitchell HM, Geczy CL, S100 calgranulin proteins S100A8, S100A9 and S100A12 are expressed in the inflamed gastric mucosa of Helicobacter pylori-infected children. Can J Gastroenterol = Journal canadien de gastroenterologie. 2008;22:461–464.
  • Lutzow YC, Donaldson L, Gray CP, Identification of immune genes and proteins involved in the response of bovine mammary tissue to Staphylococcus aureus infection. BMC Vet Res 2008;4:18.
  • Meijer B, Gearry RB, Day AS. The role of S100A12 as a systemic marker of inflammation. Int J Inflamm 2012;2012:907078.
  • Nakashima K, Nakatsuka K, Yamashita K, An in vitro model of cartilage degradation by chondrocytes in a three-dimensional culture system. Int J Biomed Sci : IJBS. 2012;8:249–257.
  • Foell D, Wittkowski H, Kessel C, Proinflammatory S100A12 can activate human monocytes via Toll-like receptor 4. Am J Respir Crit Care Med 2013;187:1324–1334.
  • Britsch S. The neuregulin-I/ErbB signaling system in development and disease. Adv Anat Embryol Cell Biol 2007;190:1–65.
  • Chua YL, Ito Y, Pole JC, The NRG1 gene is frequently silenced by methylation in breast cancers and is a strong candidate for the 8p tumour suppressor gene. Oncogene 2009;28:4041–4052.
  • Mei L, Xiong WC. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008;9:437–452.
  • Sheng Q, Liu X, Fleming E, An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 2010;17:298–310.
  • Marballi K, Quinones MP, Jimenez F, In vivo and in vitro genetic evidence of involvement of neuregulin 1 in immune system dysregulation. J Mol Med (Berl) 2010;88:1133–1141.
  • Walss-Bass C, Liu W, Lew DF, A novel missense mutation in the transmembrane domain of neuregulin 1 is associated with schizophrenia. Biol Psychiatry 2006;60:548–553.
  • Hanninen K, Katila H, Saarela M, Interleukin-1 beta gene polymorphism and its interactions with neuregulin-1 gene polymorphism are associated with schizophrenia. Eur Arch Psychiatry Clin Neurosci 2008;258:10–15.
  • Xu M, He L. Convergent evidence shows a positive association of interleukin-1 gene complex locus with susceptibility to schizophrenia in the Caucasian population. Schizophr Res 2010;120:131–142.
  • Calvo M, Zhu N, Tsantoulas C, Neuregulin-ErbB signaling promotes microglial proliferation and chemotaxis contributing to microgliosis and pain after peripheral nerve injury. J Neurosci : the official journal of the Society for Neuroscience. 2010;30:5437–5450.
  • Kettle R, Simmons J, Schindler F, Regulation of neuregulin 1beta1-induced MUC5AC and MUC5B expression in human airway epithelium. Am J Respir Cell Mol Biol 2010;42:472–481.
  • Shirakabe K, Wakatsuki S, Kurisaki T, Fujisawa-Sehara A. Roles of Meltrin beta/ADAM19 in the processing of neuregulin. J Biol Chem 2001;276:9352–9358.
  • Fernandes-Alnemri T, Wu J, Yu JW, The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ 2007;14:1590–1604.
  • Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005;73:1907–1916.
  • Lee GS, Subramanian N, Kim AI, The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 2012;492:123–127.
  • Rossol M, Pierer M, Raulien N, Extracellular Ca2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat Commun 2012;3: 1329.
  • Masters SL, Dunne A, Subramanian SL, Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 2010;11:897–904.
  • Zaki MH, Vogel P, Malireddi RK, The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell 2011;20:649–660.
  • Lich JD, Williams KL, Moore CB, Monarch-1 suppresses non-canonical NF-kappaB activation and p52-dependent chemokine expression in monocytes. J Immunol 2007;178:1256–1260.
  • Williams KL, Lich JD, Duncan JA, The CATERPILLER protein monarch-1 is an antagonist of toll-like receptor-, tumor necrosis factor alpha-, and Mycobacterium tuberculosis-induced pro-inflammatory signals. J Biol Chem 2005;280:39914–39924.
  • Ruffell D, Mourkioti F, Gambardella A, A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc Natl Acad Sci USA 2009;106:17475–17480.
  • Mascanfroni ID, Yeste A, Vieira SM, IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol 2013;14:1054–1063.
  • Frostegard J, Nilsson J, Haegerstrand A, Oxidized low density lipoprotein induces differentiation and adhesion of human monocytes and the monocytic cell line U937. Proc Natl Acad Sci USA 1990;87:904–908.
  • Hayden JM, Brachova L, Higgins K, Induction of monocyte differentiation and foam cell formation in vitro by 7-ketocholesterol. J Lipid Res 2002;43:26–35.
  • Paulson KE, Zhu SN, Chen M, Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Cir Res 2010;106:383–390.
  • Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006;177:7303–7311.
  • Kzhyshkowska J, Gratchev A, Goerdt S. Stabilin-1, a homeostatic scavenger receptor with multiple functions. J Cell Mol Med 2006;10:635–649.
  • Chinetti-Gbaguidi G, Baron M, Bouhlel MA, Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARgamma and LXRalpha pathways. Cir Res 2011;108:985–995.
  • Rubic T, Lorenz RL. Downregulated CD36 and oxLDL uptake and stimulated ABCA1/G1 and cholesterol efflux as anti-atherosclerotic mechanisms of interleukin-10. Cardiovasc Res 2006;69:527–535.
  • Trigatti B, Covey S, Rizvi A. Scavenger receptor class B type I in high-density lipoprotein metabolism, atherosclerosis and heart disease: lessons from gene-targeted mice. Biochem Soc Trans 2004;32:116–120.
  • Zalewski A, Macphee C. Role of lipoprotein-associated phospholipase A2 in atherosclerosis: biology, epidemiology, and possible therapeutic target. Arterioscler Thromb Vasc Biol 2005;25:923–931.
  • Tjoelker LW, Wilder C, Eberhardt C, Anti-inflammatory properties of a platelet-activating factor acetylhydrolase. Nature 1995;374:549–553.
  • Du Y, Yang M, Wei W, Macrophage VLDL receptor promotes PAFAH secretion in mother's milk and suppresses systemic inflammation in nursing neonates. Nat Commun 2012;3:1008.
  • Ancuta P, Rao R, Moses A, Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med 2003;197:1701–1707.
  • Landsman L, Bar-On L, Zernecke A, CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 2009;113:963–972.
  • Randolph GJ, Sanchez-Schmitz G, Liebman RM, Schakel K. The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J Exp Med 2002;196:517–527.
  • Sanchez-Torres C, Garcia-Romo GS, Cornejo-Cortes MA, CD16+and CD16- human blood monocyte subsets differentiate in vitro to dendritic cells with different abilities to stimulate CD4+T cells. Int Immunol 2001;13:1571–1581.
  • Kramer PR, Winger V, Reuben J. PI3K limits TNF-alpha production in CD16-activated monocytes. Eur J Immunol 2009;39:561–570.
  • Shalova IN, Kajiji T, Lim JY, CD16 regulates TRIF-dependent TLR4 response in human monocytes and their subsets. J Immunol 2012;188:3584–3593.
  • Liu Y, Yang B, Ma J, Interleukin-21 maintains the expression of CD16 on monocytes via the production of IL-10 by human naive CD4+ T cells. Cell Immunol 2011;267:102–108.
  • Seeling M, Hillenhoff U, David JP, Inflammatory monocytes and Fcgamma receptor IV on osteoclasts are critical for bone destruction during inflammatory arthritis in mice. Proc Natl Acad Sci U S A 2013;110:10729–10734.
  • Cros J, Cagnard N, Woollard K, Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010;33:375–386.
  • Zhang JY, Zou ZS, Huang A, Hyper-activated pro-inflammatory CD16 monocytes correlate with the severity of liver injury and fibrosis in patients with chronic hepatitis B. PloS One 2011;6:e17484.
  • Ancuta P, Kunstman KJ, Autissier P, CD16+ monocytes exposed to HIV promote highly efficient viral replication upon differentiation into macrophages and interaction with T cells. Virology 2006;344:267–276.
  • Tippett E, Cheng WJ, Westhorpe C, Differential expression of CD163 on monocyte subsets in healthy and HIV-1 infected individuals. PloS One 2011;6:e19968.
  • Moestrup SK, Moller HJ. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 2004;36:347–354.
  • Philippidis P, Mason JC, Evans BJ, Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Cir Res 2004;94:119–126.
  • Azeredo EL, Neves-Souza PC, Alvarenga AR, Differential regulation of toll-like receptor-2, toll-like receptor-4, CD16 and human leucocyte antigen-DR on peripheral blood monocytes during mild and severe dengue fever. Immunology 2010;130:202–216.
  • Vaggi F, Disanza A, Milanesi F, The Eps8/IRSp53/VASP network differentially controls actin capping and bundling in filopodia formation. PLoS Comput Biol 2011;7:e1002088.
  • Chang EJ, Ha J, Oerlemans F, Brain-type creatine kinase has a crucial role in osteoclast-mediated bone resorption. Nat Med 2008;14:966–972.
  • Menna E, Zambetti S, Morini R, Eps8 controls dendritic spine density and synaptic plasticity through its actin-capping activity. EMBO J 2013;32:1730–1744.
  • Chen YR, Feng F, Wang L, Deletion of RBP-J in dendritic cells compromises TLR-mediated DC activation accompanied by abnormal cytoskeleton reorganization. Mol Biol Rep 2013;40:1531–1539.
  • Frittoli E, Matteoli G, Palamidessi A, The signaling adaptor Eps8 is an essential actin capping protein for dendritic cell migration. Immunity 2011;35:388–399.
  • Bournier O, Kroviarski Y, Rotter B, Spectrin interacts with EVL (Enabled/vasodilator-stimulated phosphoprotein-like protein), a protein involved in actin polymerization. Biol Cell / under the auspices of the European Cell Biology Organization. 2006;98:279–293.
  • Furman C, Sieminski AL, Kwiatkowski AV, Ena/VASP is required for endothelial barrier function in vivo. J Cell Biol 2007;179:761–775.
  • Block J, Breitsprecher D, Kuhn S, FMNL2 drives actin-based protrusion and migration downstream of Cdc42. Curr Biol: CB. 2012;22:1005–1012.
  • Kitzing TM, Wang Y, Pertz O, Formin-like 2 drives amoeboid invasive cell motility downstream of RhoC. Oncogene 2010;29:2441–2448.
  • Dawson JC, Bruche S, Spence HJ, Mtss1 promotes cell-cell junction assembly and stability through the small GTPase Rac1. PloS One 2012;7:e31141.
  • Liu K, Wang G, Ding H, Downregulation of metastasis suppressor 1(MTSS1) is associated with nodal metastasis and poor outcome in Chinese patients with gastric cancer. BMC Cancer 2010;10:428.
  • Arima M, Fukuda T. Prostaglandin D2 receptors DP and CRTH2 in the pathogenesis of asthma. Curr Mol Med 2008;8:365–375.
  • Yue L, Durand M, Lebeau Jacob MC, Prostaglandin D2 induces apoptosis of human osteoclasts by activating the CRTH2 receptor and the intrinsic apoptosis pathway. Bone 2012;51:338–346.
  • Jin C, Wu L, Li J, Multiple signaling pathways are involved in the interleukine-4 regulated expression of DC-SIGN in THP-1 cell line. J Biomed Biotechnol 2012;2012:357060.
  • Wang M, Zhang J, Telljohann R, Chronic matrix metalloproteinase inhibition retards age-associated arterial proinflammation and increase in blood pressure. Hypertension 2012;60:459–466.
  • Li W, Kornmark L, Jonasson L, Cathepsin L is significantly associated with apoptosis and plaque destabilization in human atherosclerosis. Atherosclerosis 2009;202:92–102.
  • Baumgrass R, Williamson MK, Price PA. Identification of peptide fragments generated by digestion of bovine and human osteocalcin with the lysosomal proteinases cathepsin B, D, L, H, and S. J Bone Miner Res: the official journal of the American Society for Bone and Mineral Research. 1997;12:447–455.
  • Gerber A, Welte T, Ansorge S, Buhling F. Expression of cathepsins B and L in human lung epithelial cells is regulated by cytokines. Adv Exp Med Biol 2000;477:287–292.
  • Schedel J, Seemayer CA, Pap T, Targeting cathepsin L (CL) by specific ribozymes decreases CL protein synthesis and cartilage destruction in rheumatoid arthritis. Gene Ther 2004;11:1040–1047.
  • Yang X, Karuturi RK, Sun F, CDKN1C (p57) is a direct target of EZH2 and suppressed by multiple epigenetic mechanisms in breast cancer cells. PloS One 2009;4:e5011.
  • Kuang SQ, Fang Z, Zweidler-McKay PA, Epigenetic inactivation of Notch-Hes pathway in human B-cell acute lymphoblastic leukemia. PloS One 2013;8:e61807.
  • El Yakoubi W, Borday C, Hamdache J, Hes4 controls proliferative properties of neural stem cells during retinal ontogenesis. Stem Cells 2012;30:2784–2795.
  • Keller UB, Old JB, Dorsey FC, Myc targets Cks1 to provoke the suppression of p27Kip1, proliferation and lymphomagenesis. EMBO J 2007;26:2562–2574.
  • Shi L, Wang S, Zangari M, Over-expression of CKS1B activates both MEK/ERK and JAK/STAT3 signaling pathways and promotes myeloma cell drug-resistance. Oncotarget 2010;1:22–33.
  • Meffre E, Nussenzweig MC. Deletion of immunoglobulin beta in developing B cells leads to cell death. Proc Natl Acad Sci U S A 2002;99:11334–11339.
  • Anbazhagan K, Rabbind Singh, A., Isabelle, P., Human pre-B cell receptor signal transduction: evidence for distinct roles of PI3kinase and MAP-kinase signalling pathways. Immuni Inflamm and Dis 1: 26–36. 2013;1:26–36.
  • Yamazaki T, Kurosaki T. Contribution of BCAP to maintenance of mature B cells through c-Rel. Nat Immunol 2003;4:780–786.
  • Matsumura T, Oyama M, Kozuka-Hata H, Identification of BCAP-(L) as a negative regulator of the TLR signaling-induced production of IL-6 and IL-10 in macrophages by tyrosine phosphoproteomics. Biochem Biophys Res Commun 2010;400:265–270.

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