MicroRNA-regulated B cells in obesity-Immunometabolism-CSCIED科技核心评价数据库-手机版

MicroRNA-regulated B cells in obesity

MicroRNA-regulated B cells in obesity

ES评分 0 浏览量：1029 下载量：0

DOI	10.1097/IN9.0000000000000005
刊名	Immunometabolism IJ
年，卷(期)	2022, 4(3)
作者	Matz, Alyssa J.; Qu, Lili; Karlinsey, Keaton; Zhou, Beiyan,
作者单位	[Matz, Alyssa J.; Qu, Lili; Karlinsey, Keaton; Zhou, Beiyan] Univ Connecticut, Sch Med, Dept Immunol, Farmington, CT 06269 USA; [Zhou, Beiyan] Univ Connecticut, Inst Syst Genom, Farmington, CT USA
摘要	Obesity is a prevalent health risk by inducing chronic, low-grade inflammation and insulin resistance, in part from adipose tissue inflammation perpetuated by activated B cells and other resident immune cells. However, regulatory mechanisms controlling B-cell actions in adipose tissue remain poorly understood, limiting therapeutic innovations. MicroRNAs are potent regulators of immune cell dynamics through fine-tuning a network of downstream genes in multiple signaling pathways. In particular, miR-150 is crucial to B-cell development and suppresses obesity-associated inflammation via regulating adipose tissue B-cell function. Herein, we review the effect of microRNAs on B-cell development, activation, and function and highlight miR-150-regulated B-cell actions during obesity which modulate systemic inflammation and insulin resistance. In this way, we hope to promote translational discoveries that mitigate obesity-induced health risks by targeting microRNA-regulated B-cell actions.
Abstract	Obesity is a prevalent health risk by inducing chronic, low-grade inflammation and insulin resistance, in part from adipose tissue inflammation perpetuated by activated B cells and other resident immune cells. However, regulatory mechanisms controlling B-cell actions in adipose tissue remain poorly understood, limiting therapeutic innovations. MicroRNAs are potent regulators of immune cell dynamics through fine-tuning a network of downstream genes in multiple signaling pathways. In particular, miR-150 is crucial to B-cell development and suppresses obesity-associated inflammation via regulating adipose tissue B-cell function. Herein, we review the effect of microRNAs on B-cell development, activation, and function and highlight miR-150-regulated B-cell actions during obesity which modulate systemic inflammation and insulin resistance. In this way, we hope to promote translational discoveries that mitigate obesity-induced health risks by targeting microRNA-regulated B-cell actions.
关键词	B cell; microRNA; adipose tissue; obesity
KeyWord	B cell; microRNA; adipose tissue; obesity
基金项目
页码	1-6

参考文献
相关文献

[1]. Field AE, Coakley EH, Must A, et al. Impact of overweight on the risk of developing common chronic diseases during a 10-year period. Arch Intern Med. 2001;161:1581–6. doi: 10.1001/archinte.161.13.1581.

[2]. Afshin A, Forouzanfar MH, et al.; GBD 2015 Obesity Collaborators. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377:13–27.

[3]. Juonala M, Magnussen CG, Berenson GS, et al. Childhood adiposity, adult adiposity, and cardiovascular risk factors. N Engl J Med. 2011;365:1876–85.

[4]. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest. 2003;112:1821–30.

[5]. Fleischman A, Shoelson SE, Bernier R, et al. Salsalate improves glycemia and inflammatory parameters in obese young adults. Diabetes Care. 2008;31:289–94.

[6]. Stanley TL, Zanni MV, Johnsen S, et al. TNF-alpha antagonism with etanercept decreases glucose and increases the proportion of high molecular weight adiponectin in obese subjects with features of the metabolic syndrome. J Clin Endocrinol Metab. 2011;96:146.

[7]. Hauser TH, Salastekar N, Schaefer EJ, et al. Effect of targeting inflammation with salsalate: the TINSAL-CVD randomized clinical trial on progression of coronary plaque in overweight and obese patients using statins. JAMA Cardiol. 2016;1:413–23.

[8]. Oral EA, Reilly SM, Gomez AV, et al. Inhibition of IKKvarepsilon and TBK1 improves glucose control in a subset of patients with type 2 diabetes. Cell Metab. 2017;26:157–70.e7.

[9]. DeFuria J, Belkina AC, Jagannathan-Bogdan M, et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc Natl Acad Sci USA. 2013;110:5133–8.

[10]. Winer DA, Winer S, Shen L, et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med. 2011;17:610–7.

[11]. Karl M, Hasselwander S, Zhou Y, et al. Dual roles of B lymphocytes in murine models of diet-induced non-alcoholic fatty liver disease. Hepatology. 2022. doi: 10.1002/hep.32428.

[12]. Ying W, Tseng A, Chang RC, et al. miR-150 regulates obesity-associated insulin resistance by controlling B cell functions. Sci Rep. 2016;6:20176.

[13]. Luck H, Khan S, Kim JH, et al. Gut-associated IgA(+) immune cells regulate obesity-related insulin resistance. Nat Commun. 2019;10:3650.

[14]. Visness CM, London SJ, Daniels JL, et al. Association of obesity with IgE levels and allergy symptoms in children and adolescents: results from the national health and nutrition examination survey 2005-2006. J Allergy Clin Immunol. 2009;123:1163–4.

[15]. McDonnell ME, Ganley-Leal LM, Mehta A, et al. B lymphocytes in human subcutaneous adipose crown-like structures. Obesity. 2012;20:1372–8.

[16]. Zhou B, Wang S, Mayr C, et al. miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci USA. 2007;104:7080–5.

[17]. Musilova K, Devan J, Cerna K, et al. miR-150 downregulation contributes to the high-grade transformation of follicular lymphoma by upregulating FOXP1 levels. Blood. 2018;132:2389–400.

[18]. Mraz M, Chen L, Rassenti LZ, et al. miR-150 influences B-cell receptor signaling in chronic lymphocytic leukemia by regulating expression of GAB1 and FOXP1. Blood. 2014;124:84–95.

[19]. Mehta A, Baltimore D. MicroRNAs as regulatory elements in immune system logic. Nat Rev Immunol. 2016;16:279–94.

[20]. Hammond SM, Boettcher S, Caudy AA, et al. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science. 2001;293:1146–50.

[21]. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15:509–24.

[22]. Kawamata T, Seitz H, Tomari Y. Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat Struct Mol Biol. 2009;16:953–60.

[23]. Landgraf P, Rusu M, Sheridan R, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.

[24]. Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875–86.

[25]. Neilsen CT, Goodall GJ, Bracken CP. IsomiRs—the overlooked repertoire in the dynamic microRNAome. Trends Genet. 2012;28:544–9.

[26]. Lewis BP, Shih IH, Jones-Rhoades MW, et al. Prediction of mammalian microRNA targets. Cell. 2003;115:787–98.

[27]. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15–20.

[28]. Miranda KC, Huynh T, Tay Y, et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell. 2006;126:1203–17.

[29]. McGeary SE, Lin KS, Shi CY, et al. The biochemical basis of microRNA targeting efficacy. Science. 2019;366:eaav1741.

[30]. Chen Y, Wang X. miRDB: an online database for prediction of functional microRNA targets. Nucleic Acids Res. 2020;48:D127–31.

[31]. Krek A, Grün D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet. 2005;37:495–500.

[32]. Paraskevopoulou MD, Georgakilas G, Kostoulas N, et al. DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows. Nucleic Acids Res. 2013;41:169.

[33]. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–33.

[34]. Dong JT, Boyd JC, Frierson HF Jr. Loss of heterozygosity at 13q14 and 13q21 in high grade, high stage prostate cancer. Prostate. 2001;49:166–71.

[35]. Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA. 2002;99:15524–9.

[36]. Klein U, Lia M, Crespo M, et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell. 2010;17:28–40.

[37]. Calin GA, Liu CG, Sevignani C, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci USA. 2004;101:11755–60.

[38]. Iqbal J, Shen Y, Huang X, et al. Global microRNA expression profiling uncovers molecular markers for classification and prognosis in aggressive B-cell lymphoma. Blood. 2015;125:1137–45.

[39]. Gonzalez-Martin A, Adams BD, Lai M, et al. The microRNA miR-148a functions as a critical regulator of B cell tolerance and autoimmunity. Nat Immunol. 2016;17:433–40.

[40]. Monsálvez V, Montes-Moreno S, Artiga MJ, et al. MicroRNAs as prognostic markers in indolent primary cutaneous B-cell lymphoma. Mod Pathol. 2013;26:171–81.

[41]. Xiao C, Calado DP, Galler G, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-myb. Cell. 2007;131:146–59.

[42]. Cron MA, Maillard S, Truffault F, et al. Causes and consequences of miR-150-5p dysregulation in myasthenia gravis. Front Immunol. 2019;10:539.

[43]. Fiorillo AA, Heier CR, Huang YF, et al. Estrogen receptor, inflammatory, and FOXO transcription factors regulate expression of myasthenia gravis-associated circulating microRNAs. Front Immunol. 2020;11:151.

[44]. Xing L, Xu W, Qu Y, et al. miR-150 regulates B lymphocyte in autoimmune hemolytic anemia/evans syndrome by c-myb. Int J Hematol. 2018;107:666–72.

[45]. Rao DS, OʼConnell RM, Chaudhuri AA, et al. MicroRNA-34a perturbs B lymphocyte development by repressing the forkhead box transcription factor Foxp1. Immunity. 2010;33:48–59.

[46]. Guo Q, Zhang J, Li J, et al. Forced miR-146a expression causes autoimmune lymphoproliferative syndrome in mice via downregulation of Fas in germinal center B cells. Blood. 2013;121:4875–83.

[47]. Hou G, Harley ITW, Lu X, et al. SLE non-coding genetic risk variant determines the epigenetic dysfunction of an immune cell specific enhancer that controls disease-critical microRNA expression. Nat Commun. 2021;12:135.Google Scholar
[48]. Pichiorri F, Suh SS, Ladetto M, et al. MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc Natl Acad Sci USA. 2008;105:12885–90.

[49]. Li Y, Shi Y, McCaw L, et al. Microenvironmental interleukin-6 suppresses toll-like receptor signaling in human leukemia cells through miR-17/19A. Blood. 2015;126:766–8.

[50]. Thai TH, Calado DP, Casola S, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316:604–8.

[51]. Teng G, Hakimpour P, Landgraf P, et al. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity. 2008;28:621–9.

[52]. Dorsett Y, McBride KM, Jankovic M, et al. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity. 2008;28:630–8.

[53]. Lu D, Nakagawa R, Lazzaro S, et al. The miR-155-PU.1 axis acts on Pax5 to enable efficient terminal B cell differentiation. J Exp Med. 2014;211:2183–98.

[54]. Thai TH, Patterson HC, Pham DH, et al. Deletion of microRNA-155 reduces autoantibody responses and alleviates lupus-like disease in the Fas(lpr) mouse. Proc Natl Acad Sci USA. 2013;110:20194–9.Google Scholar
[55]. Costinean S, Sandhu SK, Pedersen IM, et al. Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of emicro-MiR-155 transgenic mice. Blood. 2009;114:1374–82.

[56]. Dagan LN, Jiang X, Bhatt S, et al. miR-155 regulates HGAL expression and increases lymphoma cell motility. Blood. 2012;119:513–20.Google Scholar
[57]. Jiang D, Aguiar RC. MicroRNA-155 controls RB phosphorylation in normal and malignant B lymphocytes via the noncanonical TGF-β1/SMAD5 signaling module. Blood. 2014;123:86–93.Google Scholar
[58]. Sandhu SK, Volinia S, Costinean S, et al. miR-155 targets histone deacetylase 4 (HDAC4) and impairs transcriptional activity of B-cell lymphoma 6 (BCL6) in the eμ-miR-155 transgenic mouse model. Proc Natl Acad Sci USA. 2012;109:20047–52.Google Scholar
[59]. Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol. 2002;20:253–300.

[60]. Yuan J, Nguyen CK, Liu X, et al. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science. 2012;335:1195–200.

[61]. Zhou Y, Li YS, Bandi SR, et al. Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J Exp Med. 2015;212:569–80.

[62]. Hardy RR, Carmack CE, Shinton SA, et al. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med. 1991;173:1213–25.

[63]. Li YS, Wasserman R, Hayakawa K, et al. Identification of the earliest B lineage stage in mouse bone marrow. Immunity. 1996;5:527–35.

[64]. Meffre E, Casellas R, Nussenzweig MC. Antibody regulation of B cell development. Nat Immunol. 2000;1:379–85.

[65]. Coffman RL, Weissman IL. Immunoglobulin gene rearrangement during pre-B cell differentiation. J Mol Cell Immunol. 1983;1:31–41.

[66]. Hombach J, Tsubata T, Leclercq L, et al. Molecular components of the B-cell antigen receptor complex of the IgM class. Nature. 1990;343:760–2.

[67]. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol. 2001;19:595–621.

[68]. Chen CZ, Li L, Lodish HF, et al. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004;303:83–6.

[69]. Ludwig N, Leidinger P, Becker K, et al. Distribution of miRNA expression across human tissues. Nucleic Acids Res. 2016;44:3865–77.

[70]. Lu J, Guo S, Ebert BL, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14:843–53.

[71]. Bezman NA, Chakraborty T, Bender T, et al. miR-150 regulates the development of NK and iNKT cells. J Exp Med. 2011;208:2717–31.

[72]. Kim N, Kim M, Yun S, et al. MicroRNA-150 regulates the cytotoxicity of natural killers by targeting perforin-1. J Allergy Clin Immunol. 2014;134:195–203.

[73]. Ghisi M, Corradin A, Basso K, et al. Modulation of microRNA expression in human T-cell development: targeting of NOTCH3 by miR-150. Blood. 2011;117:7053–62.

[74]. Bousquet M, Zhuang G, Meng C, et al. miR-150 blocks MLL-AF9-associated leukemia through oncogene repression. Mol Cancer Res. 2013;11:912–22.

[75]. Ito M, Teshima K, Ikeda S, et al. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T-cell lymphoma. Blood. 2014;123:1499–511.

[76]. Thomas MD, Kremer CS, Ravichandran KS, et al. C-myb is critical for B cell development and maintenance of follicular B cells. Immunity. 2005;23:275–86.

[77]. Havelange V, Garzon R. MicroRNAs: emerging key regulators of hematopoiesis. Am J Hematol. 2010;85:935–42.

[78]. Nemazee D. Mechanisms of central tolerance for B cells. Nat Rev Immunol. 2017;17:281–94.

[79]. Hou G, Harley ITW, Lu X, et al. SLE non-coding genetic risk variant determines the epigenetic dysfunction of an immune cell specific enhancer that controls disease-critical microRNA expression. Nat Commun. 2021;12:135.

[80]. Taganov KD, Boldin MP, Chang KJ, et al. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA. 2006;103:12481–6.

[81]. Wu XN, Ye YX, Niu JW, et al. Defective PTEN regulation contributes to B cell hyperresponsiveness in systemic lupus erythematosus. Sci Transl Med. 2014;6:246ra99.

[82]. Cyster JG, Allen CDC. B cell responses: cell interaction dynamics and decisions. Cell. 2019;177:524–40.

[83]. Cancro MP. Age-associated B cells. Annu Rev Immunol. 2020;38:315–40.

[84]. Yuseff MI, Pierobon P, Reversat A, et al. How B cells capture, process and present antigens: a crucial role for cell polarity. Nat Rev Immunol. 2013;13:475–86.

[85]. Dunand-Sauthier I, Santiago-Raber ML, Capponi L, et al. Silencing of c-fos expression by microRNA-155 is critical for dendritic cell maturation and function. Blood. 2011;117:4490–500.

[86]. Mari L, Hoefnagel SJM, Zito D, et al. microRNA 125a regulates MHC-I expression on esophageal adenocarcinoma cells, associated with suppression of antitumor immune response and poor outcomes of patients. Gastroenterology. 2018;155:784–98.

[87]. Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol. 2012;30:221–41.

[88]. de Yébenes VG, Belver L, Pisano DG, et al. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J Exp Med. 2008;205:2199–206.

[89]. Lin J, Lwin T, Zhao JJ, et al. Follicular dendritic cell-induced microRNA-mediated upregulation of PRDM1 and downregulation of BCL-6 in non-Hodgkin’s B-cell lymphomas. Leukemia. 2011;25:145–52.

[90]. Puissegur MP, Eichner R, Quelen C, et al. B-cell regulator of immunoglobulin heavy-chain transcription (bright)/ARID3a is a direct target of the oncomir microRNA-125b in progenitor B-cells. Leukemia. 2012;26:2224–32.

[91]. Tan LP, Wang M, Robertus JL, et al. miRNA profiling of B-cell subsets: specific miRNA profile for germinal center B cells with variation between centroblasts and centrocytes. Lab Invest. 2009;89:708–16.

[92]. Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science. 2007;316:608–11.

[93]. Keim C, Kazadi D, Rothschild G, et al. Regulation of AID, the B-cell genome mutator. Genes Dev. 2013;27:1–17.

[94]. Vigorito E, Kohlhaas S, Lu D, et al. miR-155: an ancient regulator of the immune system. Immunol Rev. 2013;253:146–57.

[95]. Tsiantoulas D, Perkmann T, Afonyushkin T, et al. Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies. J Lipid Res. 2015;56:440–8.

[96]. Amendt T, Allies G, Nicolò A, et al. Autoreactive antibodies control blood glucose by regulating insulin homeostasis. Proc Natl Acad Sci USA. 2022;119:e2115695119.

引用本文

Matz, Alyssa J.; Qu, Lili; Karlinsey, Keaton; Zhou, Beiyan. MicroRNA-regulated B cells in obesity [J]. Immunometabolism. 2022; 4; (3). 1 - 6.

文献评论

相关学者

相关机构