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CXCR3.1 and CXCR3.2 Differentially Contribute to Macrophage Polarization in Teleost Fish

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CXCR3.1 and CXCR3.2 Differentially Contribute to Macrophage Polarization in Teleost Fish CXCR3.1 and CXCR3.2 Differentially Contribute to Macrophage Polarization in Teleost Fish This information is current as Xin-Jiang Lu, Qiang Chen, Ye-Jing Rong, Feng Chen and of September 29, 2021. Jiong Chen J Immunol 2017; 198:4692-4706; Prepublished online 12 May 2017; doi: 10.4049/jimmunol.1700101 http://www.jimmunol.org/content/198/12/4692 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2017/05/12/jimmunol.170010 Material 1.DCSupplemental http://www.jimmunol.org/ References This article cites 69 articles, 17 of which you can access for free at: http://www.jimmunol.org/content/198/12/4692.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 29, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2017 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology CXCR3.1 and CXCR3.2 Differentially Contribute to Macrophage Polarization in Teleost Fish Xin-Jiang Lu, Qiang Chen, Ye-Jing Rong, Feng Chen, and Jiong Chen The study of multiple copies of chemokine receptor genes in various teleosts has long appealed to investigators seeking to understand the evolution of the immune system. The CXCR CXCR3 gene has two isoforms, CXCR3.1 and CXCR3.2, which are both expressed in macrophages. The distinct roles of teleost CXCR3s have not been identified previously. In this article, we found that CXCR3.1 and CXCR3.2 differentially contributed to macrophage polarization in the teleosts: ayu (Plecoglossus altivelis), grass carp (Ctenopharyngodon idella), and spotted green pufferfish (Tetraodon nigroviridis). In ayu macrophages, the P. altivelis CXCR3.1 (PaCXCR3.1) gene was constitutively expressed, whereas the P. altivelis CXCR3.2 (PaCXCR3.2) gene was induced postinfection with Escherichia coli. Upon E. coli infection, PaCXCR3.1+ and PaCXCR3.2+ macrophages showed an M1 and an M2 phenotype, respectively. CXCL9– 11-like proteins mediated M1 and M2 polarization by interacting with the PaCXCR3.1 and PaCXCR3.2 proteins on macrophages, Downloaded from respectively. The transcription factors P. altivelis STAT1 and P. altivelis STAT3 were activated in PaCXCR3.1+ and PaCXCR3.2+ macrophages, respectively. Furthermore, the prognosis of septic ayu adoptively transferred with PaCXCR3.2+ macrophages was improved. Our data reveal a previously unknown mechanism for macrophage polarization, suggesting that redundant genes may regulate crucial functions in the teleost immune system. The Journal of Immunology, 2017, 198: 4692–4706. n mammals, the chemokine receptor CXCR3 exists as a polarization in a mouse cancer model (7). Two CXCR3 isoforms http://www.jimmunol.org/ single gene and is preferentially expressed on immune cells are found in poikilothermic vertebrates, including teleosts (bony I to aid in cell migration to the sites of inflammation (1). The fishes), amphibians, and reptiles (8, 9). CXCR3.1 (CXCR3b) and primary ligands of CXCR3 are CXCL9, CXCL10, and CXCL11 CXCR3.2 (CXCR3a) are found in zebrafish, Japanese ricefish, and (2, 3). CXCL10/CXCR3 interactions drive the proinflammatory tetraodon (10). In Japanese ricefish, CXCR3.2 is a marker of in- effector Th1 polarization of T cells, whereas CXCL11/CXCR3 nate immune cells (10). In zebrafish, CXCR3.2 mediates macro- binding induces an immune-tolerant state that is characterized phage chemotaxis to the sites of bacterial infection (11). Similarly, by anti-inflammatory Th2 polarization (4, 5). CXCR3 has been in rainbow trout, CXCR3.1 and CXCR3.2 are mainly expressed in detected in a small subset of peripheral blood monocytes and a macrophages (12). We ask why two CXCR3 genes exist in teleost high percentage of monocytes recruited to inflammatory sites (6). fish. The cost–benefit trade-off of a given trait is optimized by by guest on September 29, 2021 Although CXCR3 is not a classic marker for macrophage polari- maximizing the benefit while minimizing the cost (13). Thus, we zation, its deficiency has been shown to promote macrophage M2 hypothesized that, in teleosts, the two isoforms of CXCR3 may confer a specific benefit by regulating macrophage function. Macrophages are present in most vertebrate tissues and perform Laboratory of Biochemistry and Molecular Biology, Ningbo University, Ningbo functions encompassing host defense and tissue homeostasis (14, 315211, People’s Republic of China 15). The inflammatory state of macrophages plays an important Received for publication January 23, 2017. Accepted for publication April 18, 2017. role in pathogen clearance (16, 17), and their polarization to dif- This work was supported by the Program for the National Natural Science Founda- ferent inflammatory phenotypes depends on environmental cues or tion of China (Grants 31372555 and 31472300), the Zhejiang Provincial Natural Science Foundation of China (Grant LZ13C190001), the Young Talent Cultivation pathophysiologic conditions (18). The classically activated mac- Project of the Zhejiang Association for Science and Technology (Grant 2016YCGC003), rophages (M1 type) are induced by LPS and IFN-g and express National 111 Project of China, the LiDakSum Marine Biopharmaceutical Development Fund, and the K.C. Wong Magna Fund at Ningbo University. proinflammatory mediators. The alternatively activated macro- phages (M2 type) are induced by IL-4 and IL-13 and express high The sequences presented in this article have been submitted to GenBank (https:// www.ncbi.nlm.nih.gov/genbank/) under accession numbers JP725619, KY081643, levels of anti-inflammatory mediators. Macrophage polarization KJ130413, KU362928, KU362929, JP742610, and JP722452. is also regulated by soluble proteins, intracellular signals, and Address correspondence and reprint requests to Prof. Jiong Chen, Ningbo University, transcription factors. Galectin-dependent regulatory signaling 818 Fenghua Road, Ningbo 315211, Zhejiang, People’s Republic of China. E-mail stimulates M2-type macrophage polarization (19). TLR signaling address: [email protected] activates the STAT1 protein to skew macrophage function toward The online version of this article contains supplemental material. the M1 phenotype, whereas the activation of STAT3 by IL-4 and Abbreviations used in this article: CiCXCR3.1, C. idella CXCR3.1; CiCXCR3.2, C. idella CXCR3.2; iNOS, inducible NO synthase; IsoIgG, mouse isotype IgG; MEGA, IL-13 skews macrophage function toward the M2 phenotype (20). molecular evolutionary genetics analysis; MOI, multiplicity of infection; NAC, N-acetyl The ablation of protein kinase Ba (Akt1) and protein kinase Bb cysteine; PaCSFR1, P. altivelis M-CSFR; PaCXCL9–11l1, P. altivelis CXCL9–11l1; (Akt2) differentially affects macrophage polarization (21). Similar PaCXCL9–11l2, P. altivelis CXCL9–11l2; PaCXCL9–11l3, P. altivelis CXCL9–11l3; PaCXCR3.1, P. altivelis CXCR3.1; PaCXCR3.2, P. altivelis CXCR3.2; PaIL-10, to those in mammals, macrophages in teleost fish are differen- P. altivelis IL-10; PaIL-12p40a, P. altivelis IL-12p40a; PaIL-12p40c, P. altivelis IL- tiated from hematopoietic stem/progenitor cells and perform 12p40c; PaIL-1b, P. altivelis IL-1b;PaSTAT1,P. altivelis STAT1; PaSTAT3, P. altivelis STAT3; PaTGF-b, P. altivelis TGF-b;PaTNF,P. altivelis TNF; P/S, penicillin/streptomycin; functions such as phagocytosis, bacterial killing, and cytokine RNAi, RNA interference; ROS, reactive oxygen species; RT-qPCR, real-time quantitative production (22–24). However, they possess additional functions PCR; siRNA, small interfering RNA; TnCXCR3.1, T. nigroviridis CXCR3.1; TnCXCR3.2, and regulatory mechanisms that differ from those in mammals. T. nigroviridis CXCR3.2. For example, teleost macrophages express novel cytokines to re- Copyright Ó 2017 by The American Association of Immunologists, Inc. 0022-1767/17/$30.00 gulate inflammatory reactions (25, 26) and are poorly activated by www.jimmunol.org/cgi/doi/10.4049/jimmunol.1700101 The Journal of Immunology 4693 TNF (27). Head kidney–derived macrophages in teleosts show transcriptomic data were deposited in the Gene Expression Omnibus functional polarization upon differential stimulation (28, 29). (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE40221 Furthermore, teleost macrophages have been shown to polarize (22). PCR, cloning, and sequencing were used to confirm the authenticity of these sequences. The similarity between the obtained sequences and into a continuum of different activation states ranging from innate other known sequences was analyzed using the basic local alignment search to alternative activation (30). Thus, it is essential to understand the tool (http://blast.ncbi.nlm.nih.gov/blast.cgi). Multiple sequence alignments signaling mechanisms that regulate macrophage phenotypes, be- were generated using ClustalW (http://clustalw.ddbj.nig.ac.jp/). Phylogenetic cause macrophage polarization plays an important role in systemic and molecular evolutionary analyses
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