Volume 41 Issue 2
Mar.  2020
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Hai-Yu Shen, Yan Zhou, Qian-Jin Zhou, Ming-Yun Li, Jiong Chen. Mudskipper interleukin-34 modulates the functions of monocytes/macrophages via the colony-stimulating factor-1 receptor 1. Zoological Research, 2020, 41(2): 123-137. doi: 10.24272/j.issn.2095-8137.2020.026
Citation: Hai-Yu Shen, Yan Zhou, Qian-Jin Zhou, Ming-Yun Li, Jiong Chen. Mudskipper interleukin-34 modulates the functions of monocytes/macrophages via the colony-stimulating factor-1 receptor 1. Zoological Research, 2020, 41(2): 123-137. doi: 10.24272/j.issn.2095-8137.2020.026

Mudskipper interleukin-34 modulates the functions of monocytes/macrophages via the colony-stimulating factor-1 receptor 1

doi: 10.24272/j.issn.2095-8137.2020.026
Funds:  The study was supported by the National Natural Science Foundation of China (31972821; 31772876), the Program of Zhejiang Provincial Natural Science Foundation of China (LZ18C190001), Science and Technology Department of Zhejiang Province (LGN18C180002), Natural Science Foundation of Ningbo City (2018A610342), and the K.C. Wong Magna Fund in Ningbo University
More Information
  • Interleukin-34 (IL-34) is a novel cytokine that plays an important role in innate immunity and inflammatory processes by binding to the colony-stimulating factor-1 receptor (CSF-1R). However, information on the function of IL-34 in fish remains limited. In the present study, we identified an IL-34 homolog from mudskippers (Boleophthalmus pectinirostris). In silico analysis showed that the mudskipper IL-34 (BpIL-34) was similar to other known IL-34 variants in sequence and structure and was most closely related to an orange-spotted grouper (Epinephelus coioides) homolog. BpIL-34 transcripts were constitutively expressed in various tissues, with the highest level of expression found in the brain. Edwardsiella tarda infection significantly up-regulated the mRNA expression of BpIL-34 in the mudskipper tissues. The recombinant mature BpIL-34 peptide (rBpIL-34) was purified and used to produce anti-rBpIL-34 IgG. Western blot analysis combined with PNGase F digestion revealed that native BpIL-34 in monocytes/macrophages (MOs/MФs) was N-glycosylated. In vitro, rBpIL-34 treatment enhanced the phagocytotic and bactericidal activity of mudskipper MOs/MФs, as well as the mRNA expression of pro-inflammatory cytokines like tumor necrosis factor α (BpTNF-α) and BpIL-1β in these cells. Furthermore, the knockdown of mudskipper CSF-1R1 (BpCSF-1R1), but not mudskipper BpCSF-1R2, significantly inhibited the rBpIL-34-mediated enhanced effect on MO/MФ function. In conclusion, our results indicate that mudskipper BpIL-34 modulates the functions of MOs/MФs via BpCSF-1R1.

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  • [1]
    Baghdadi M, Umeyama Y, Hama N, Kobayashi T, Han N, Wada H, Seino KI. 2018. Interleukin-34, a comprehensive review. Journal of Leukocyte Biology, 104(5): 931−951. doi: 10.1002/JLB.MR1117-457R
    [2]
    Chen J, Chen Q, Lu XJ, Chen J. 2016a. The protection effect of LEAP-2 on the mudskipper (Boleophthalmus pectinirostris) against Edwardsiella tarda infection is associated with its immunomodulatory activity on monocytes/macrophages. Fish & Shellfish Immunology, 59: 66−76.
    [3]
    Chen J, Nie L, Chen J. 2018. Mudskipper (Boleophthalmus pectinirostris) hepcidin-1 and hepcidin-2 present different gene expression profile and antibacterial activity and possess distinct protective effect against Edwardsiella tarda infection. Probiotics and Antimicrobial Proteins, 10(2): 176−185. doi: 10.1007/s12602-017-9352-0
    [4]
    Chen K, Shi YH, Chen J, Li MY. 2019. A soluble FcγR homolog inhibits IgM antibody production in ayu spleen cells. Zoological Research, 40(5): 404−415. doi: 10.24272/j.issn.2095-8137.2019.056
    [5]
    Chen Q, Lu XJ, Chen J. 2015. Identification and functional characterization of the CSF1R gene from grass carp Ctenopharyngodon idellus and its use as a marker of monocytes/macrophages. Fish & Shellfish Immunology, 45(2): 386−398.
    [6]
    Chen Q, Lu XJ, Li MY, Chen J. 2016b. Molecular cloning, pathologically-correlated expression and functional characterization of the colonystimulating factor 1 receptor (CSF-1R) gene from a teleost, Plecoglossus altivelis. Zoological Research, 37(2): 96−102.
    [7]
    Cheng ST, Tang H, Ren JH, Chen X, Huang AL, Chen J. 2017. Interleukin-34 inhibits hepatitis B virus replication in vitro and in vivo. PLoS One, 12(6): e0179605. doi: 10.1371/journal.pone.0179605
    [8]
    Chihara T, Suzu S, Hassan R, Chutiwitoonchai N, Hiyoshi M, Motoyoshi K, Kimura F, Okada S. 2010. IL-34 and M-CSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death & Differentiation, 17(12): 1917−1927.
    [9]
    Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER. 2002. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood, 99(1): 111−120. doi: 10.1182/blood.V99.1.111
    [10]
    Dan XM, Zhong ZP, Li YW, Luo XC, Li AX. 2013. Cloning and expression analysis of grouper (Epinephelus coioides) M-CSFR gene post Cryptocaryon irritans infection and distribution of M-CSFR+ cells. Fish & Shellfish Immunology, 35(2): 240−248.
    [11]
    Ding FF, Li CH, Chen J. 2019. Molecular characterization of the NK-lysin in a teleost fish, Boleophthalmus pectinirostris: Antimicrobial activity and immunomodulatory activity on monocytes/macrophages. Fish & Shellfish Immunology, 92: 256−264.
    [12]
    Droin N, Solary E. 2010. Editorial: CSF1R, CSF-1, and IL-34, a "ménage à trois" conserved across vertebrates. Journal of Leukocyte Biology, 87(5): 745−747. doi: 10.1189/jlb.1209780
    [13]
    Eda H, Zhang J, Keith RH, Michener M, Beidler DR, Monahan JB. 2010. Macrophage-colony stimulating factor and interleukin-34 induce chemokines in human whole blood. Cytokine, 52(3): 215−220. doi: 10.1016/j.cyto.2010.08.005
    [14]
    Felix J, Elegheert J, Gutsche I, Shkumatov AV, Wen YR, Bracke N, Pannecoucke E, Vandenberghe I, Devreese B, Svergun DI, Pauwels E, Vergauwen B, Savvides SN. 2013. Human IL-34 and CSF-1 establish structurally similar extracellular assemblies with their common hematopoietic receptor. Structure, 21(4): 528−539. doi: 10.1016/j.str.2013.01.018
    [15]
    Franzè E, Monteleone I, Cupi ML, Mancia P, Caprioli F, Marafini I, Colantoni A, Ortenzi A, Laudisi F, Sica G, Sileri P, Pallone F, Monteleone G. 2015. Interleukin-34 sustains inflammatory pathways in the gut. Clinical Science, 129(3): 271−280. doi: 10.1042/CS20150132
    [16]
    Grayfer L, Robert J. 2014. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34. Journal of Leukocyte Biology, 96(6): 1143−1153. doi: 10.1189/jlb.4A0614-295R
    [17]
    Grayfer L, Robert J. 2015. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages. Journal of Leukocyte Biology, 98(4): 641−649. doi: 10.1189/jlb.4AB0315-117RR
    [18]
    Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, Leboeuf M, Kündig TM, Frei K, Ginhoux F, Merad M, Becher B. 2012. Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity, 37(6): 1050−1060. doi: 10.1016/j.immuni.2012.11.001
    [19]
    Guan F, Lu XJ, Li CH, Chen J. 2017. Molecular characterization of mudskipper (Boleophthalmus pectinirostris) hypoxia-inducible factor-1α (HIF-1α) and analysis of its function in monocytes/macrophages. PLoS One, 12(5): e0177960. doi: 10.1371/journal.pone.0177960
    [20]
    Honda T, Nishizawa T, Uenobe M, Kohchi C, Kuroda A, Ototake M, Nakanishi T, Yokomizo Y, Takahashi Y, Inagawa H, Soma GI. 2005. Molecular cloning and expression analysis of a macrophage-colony stimulating factor receptor-like gene from rainbow trout, Oncorhynchus mykiss. Molecular Immunology, 42(1): 1−8. doi: 10.1016/j.molimm.2004.07.002
    [21]
    Huang ZL, Chen S, Liu JC, Xiao J, Yan J, Feng H. 2015. IFNa of black carp is an antiviral cytokine modified with N-linked glycosylation. Fish & Shellfish Immunology, 46(2): 477−485.
    [22]
    Jeannin P, Paolini L, Adam C, Delneste Y. 2018. The roles of CSFs on the functional polarization of tumor-associated macrophages. The FEBS Journal, 285(4): 680−699. doi: 10.1111/febs.14343
    [23]
    Jiang YY, Chen JH, Yen K, Xu J. 2019. Ectopically expressed IL-34 can efficiently induce macrophage migration to the liver in zebrafish. Zebrafish, 16(2): 165−170. doi: 10.1089/zeb.2018.1685
    [24]
    Jin SJ, Sonobe Y, Kawanokuchi J, Horiuchi H, Cheng Y, Wang Y, Mizuno T, Takeuchi H, Suzumura A. 2014. Interleukin-34 restores blood-brain barrier integrity by upregulating tight junction proteins in endothelial cells. PLoS One, 9(12): e115981. doi: 10.1371/journal.pone.0115981
    [25]
    Katzenback BA, Belosevic M. 2012. Colony-stimulating factor-1 receptor protein expression is a specific marker for goldfish (Carassius auratus L.) macrophage progenitors and their differentiated cell types. Fish & Shellfish Immunology, 32(3): 434−445.
    [26]
    Kim JI, Turka LA. 2015. Transplant tolerance: a new role for IL-34. Journal of Clinical Investigation, 125(10): 3751−3753. doi: 10.1172/JCI84010
    [27]
    Lenzo JC, Turner AL, Cook AD, Vlahos R, Anderson GP, Reynolds EC, Hamilton JA. 2012. Control of macrophage lineage populations by CSF-1 receptor and GM-CSF in homeostasis and inflammation. Immunology & Cell Biology, 90(4): 429−440.
    [28]
    Lin HS, Lee E, Hestir K, Leo C, Huang MM, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D, Hollenbaugh D, Linnemann T, Qin MM, Wong J, Chu KT, Doberstein SK, Williams LT. 2008. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science, 320(5877): 807−811. doi: 10.1126/science.1154370
    [29]
    Liu H, Leo C, Chen XY, Wong BR, Williams LT, Lin HS, He XL. 2012. The mechanism of shared but distinct CSF-1R signaling by the non-homologous cytokines IL-34 and CSF-1. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1824(7): 938−945. doi: 10.1016/j.bbapap.2012.04.012
    [30]
    Lu XJ, Chen J. 2019. Specific function and modulation of teleost monocytes/macrophages: polarization and phagocytosis. Zoological Research, 40(3): 146−150. doi: 10.24272/j.issn.2095-8137.2019.035
    [31]
    Ma XL, Lin WY, Chen YM, Stawicki S, Mukhyala K, Wu Y, Martin F, Bazan JF, Starovasnik MA. 2012. Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R. Structure, 20(4): 676−687. doi: 10.1016/j.str.2012.02.010
    [32]
    Masteller EL, Wong BR. 2014. Targeting IL-34 in chronic inflammation. Drug Discovery Today, 19(8): 1212−1216. doi: 10.1016/j.drudis.2014.05.016
    [33]
    Mo ZQ, Li YW, Zhou L, Li AX, Luo XC, Dan XM. 2015. Grouper (Epinephelus coioides) IL-34/MCSF2 and MCSFR1/MCSFR2 were involved in mononuclear phagocytes activation against Cryptocaryon irritans infection. Fish & Shellfish Immunology, 43(1): 142−149.
    [34]
    Mulero I, Pilar Sepulcre M, Roca FJ, Meseguer J, García-Ayala A, Mulero V. 2008. Characterization of macrophages from the bony fish gilthead seabream using an antibody against the macrophage colony-stimulating factor receptor. Developmental & Comparative Immunology, 32(10): 1151−1159.
    [35]
    Nakamichi Y, Udagawa N, Takahashi N. 2013. IL-34 and CSF-1: similarities and differences. Journal of Bone and Mineral Metabolism, 31(5): 486−495. doi: 10.1007/s00774-013-0476-3
    [36]
    Nandi S, Gokhan S, Dai XM, Wei SW, Enikolopov G, Lin HS, Mehler MF, Stanley ER. 2012. The CSF-1 receptor ligands IL-34 and CSF-1 exhibit distinct developmental brain expression patterns and regulate neural progenitor cell maintenance and maturation. Developmental Biology, 367(2): 100−113. doi: 10.1016/j.ydbio.2012.03.026
    [37]
    Neves F, Abrantes J, Steinke JW, Esteves PJ. 2014. Maximum-likelihood approaches reveal signatures of positive selection in IL genes in mammals. Innate Immunity, 20(2): 184−191. doi: 10.1177/1753425913486687
    [38]
    Ogryzko NV, Renshaw SA, Wilson HL. 2014. The IL-1 family in fish: swimming through the muddy waters of inflammasome evolution. Developmental & Comparative Immunology, 46(1): 53−62.
    [39]
    Peyraud F, Cousin S, Italiano A. 2017. CSF-1R inhibitor development: current clinical status. Current Oncology Reports, 19(11): 70. doi: 10.1007/s11912-017-0634-1
    [40]
    Rieger AM, Konowalchuk JD, Havixbeck JJ, Robbins JS, Smith MK, Lund JM, Barreda DR. 2013. A soluble form of the CSF-1 receptor contributes to the inhibition of inflammation in a teleost fish. Developmental & Comparative Immunology, 39(4): 438−446.
    [41]
    Rieger AM, Hanington PC, Belosevic M, Barreda DR. 2014. Control of CSF-1 induced inflammation in teleost fish by a soluble form of the CSF-1 receptor. Fish & Shellfish Immunology, 41(1): 45−51.
    [42]
    Rieger AM, Havixbeck JJ, Belosevic M, Barreda DR. 2015. Teleost soluble CSF-1R modulates cytokine profiles at an inflammatory site, and inhibits neutrophil chemotaxis, phagocytosis, and bacterial killing. Developmental & Comparative Immunology, 49(2): 259−266.
    [43]
    Roca FJ, Sepulcre MP, López-Castejón G, Meseguer J, Mulero V. 2006. The colony-stimulating factor-1 receptor is a specific marker of macrophages from the bony fish gilthead seabream. Molecular Immunology, 43(9): 1418−1423. doi: 10.1016/j.molimm.2005.07.028
    [44]
    Secombes CJ. 2016. What's new in fish cytokine research?. Fish & Shellfish Immunology, 53: 1−3.
    [45]
    Secombes CJ, Zou J. 2017. Evolution of interferons and interferon receptors. Frontiers in Immunology, 8: 209.
    [46]
    Ségaliny AI, Brion R, Brulin B, Maillasson M, Charrier C, Téletchéa S, Heymann D. 2015. IL-34 and M-CSF form a novel heteromeric cytokine and regulate the M-CSF receptor activation and localization. Cytokine, 76(2): 170−181. doi: 10.1016/j.cyto.2015.05.029
    [47]
    Slaven EM, Lopez FA, Hart SM, Sanders CV. 2001. Myonecrosis caused by Edwardsiella tarda: a case report and case series of extraintestinal E. tarda infections. Clinical Infectious Diseases, 32(10): 1430−1433. doi: 10.1086/320152
    [48]
    Suzumura A. 2013. Neuron-microglia interaction in neuroinflammation. Current Protein & Peptide Science, 14(1): 16−20.
    [49]
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731−2739. doi: 10.1093/molbev/msr121
    [50]
    Truong AD, Hong Y, Lee J, Lee K, Kil DY, Lillehoj HS, Hong YH. 2018. Interleukin-34 regulates Th1 and Th17 cytokine production by activating multiple signaling pathways through CSF-1R in chicken cell lines. International Journal of Molecular Sciences, 19(6): 1665. doi: 10.3390/ijms19061665
    [51]
    Vasek MJ, Garber C, Dorsey D, Durrant DM, Bollman B, Soung A, Yu JS, Perez-Torres C, Frouin A, Wilton DK, Funk K, DeMasters BK, Jiang XP, Bowen JR, Mennerick S, Robinson JK, Garbow JR, Tyler KL, Suthar MS, Schmidt RE, Stevens B, Klein RS. 2016. A complement-microglial axis drives synapse loss during virus-induced memory impairment. Nature, 534(7608): 538−543. doi: 10.1038/nature18283
    [52]
    Wang LP, Jiang LH, Wu CW, Lou B. 2018. Molecular characterization and expression analysis of large yellow croaker (Larimichthys crocea) interleukin-12A, 16 and 34 after poly I: C and Vibrio anguillarum challenge. Fish & Shellfish Immunology, 74: 84−93.
    [53]
    Wang TH, Kono T, Monte MM, Kuse H, Costa MM, Korenaga H, Maehr T, Husain M, Sakai M, Secombes CJ. 2013. Identification of IL-34 in teleost fish: differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor. Molecular Immunology, 53(4): 398−409. doi: 10.1016/j.molimm.2012.09.008
    [54]
    Wang TH, Secombes CJ. 2013. The cytokine networks of adaptive immunity in fish. Fish & Shellfish Immunology, 35(6): 1703−1718.
    [55]
    Wang YM, Szretter KJ, Vermi W, Gilfillan S, Rossini C, Cella M, Barrow AD, Diamond MS, Colonna M. 2012. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nature Immunology, 13(8): 753−760. doi: 10.1038/ni.2360
    [56]
    Wang YM, Colonna M. 2014. Interkeukin-34, a cytokine crucial for the differentiation and maintenance of tissue resident macrophages and Langerhans cells. European Journal of Immunology, 44(6): 1575−1581. doi: 10.1002/eji.201344365
    [57]
    Williams H, Brenner S, Venkatesh B. 2002. Identification and analysis of additional copies of the platelet-derived growth factor receptor and colony stimulating factor 1 receptor genes in fugu. Gene, 295(2): 255−264. doi: 10.1016/S0378-1119(02)00736-9
    [58]
    Wu Y, Zhou YC, Cao ZJ, Sun Y, Chen Y, Xiang YJ, Wang L, Zhang SN, Guo WL. 2019. Comparative analysis of the expression patterns of IL-1β, IL-11, and IL-34 in golden pompano (Trachinotus ovatus) following different pathogens challenge. Fish & Shellfish Immunology, 93: 863−870.
    [59]
    Xu TT, Zhang XH. 2014. Edwardsiella tarda: an intriguing problem in aquaculture. Aquaculture, 431: 129−135. doi: 10.1016/j.aquaculture.2013.12.001
    [60]
    Xue YJ, Jiang XY, Gao JD, Li X, Xu JW, Wang JY, Gao Q, Zou J. 2019. Functional characterisation of interleukin 34 in grass carp Ctenopharyngodon idella. Fish & Shellfish Immunology, 92: 91−100.
    [61]
    You XX, Bian C, Zan QJ, Xu X, Liu X, Chen JM, Wang JT, Qiu Y, Li WJ, Zhang XH, Sun Y, Chen SX, Hong WS, Li YX, Cheng SF, Fan GY, Shi CC, Liang J, Tom Tang Y, Yang CY, Ruan ZQ, Bai J, Peng C, Mu Q, Lu J, Fan MJ, Yang S, Huang ZY, Jiang XT, Fang XD, Zhang GJ, Zhang Y, Polgar G, Yu H, Li J, Liu ZJ, Zhang GQ, Ravi V, Coon SL, Wang J, Yang HM, Venkatesh B, Wang J, Shi Q. 2014. Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes. Nature Communications, 5(1): 5594. doi: 10.1038/ncomms6594
    [62]
    You XX, Chen JM, Bian C, Yi YH, Ruan ZQ, Li J, Zhang XH, Yu H, Xu JM, Shi Q. 2018. Transcriptomic evidence of adaptive tolerance to high environmental ammonia in mudskippers. Genomics, 110(6): 404−413. doi: 10.1016/j.ygeno.2018.09.001
    [63]
    Zhou J, Sun XY, Zhang J, Yang Y, Chen DP, Cao J. 2018. IL-34 regulates IL-6 and IL-8 production in human lung fibroblasts via MAPK, PI3K-Akt, JAK and NF-κB signaling pathways. International Immunopharmacology, 61: 119−125. doi: 10.1016/j.intimp.2018.05.023
    [64]
    Zou J, Secombes CJ. 2016. The function of fish cytokines. Biology, 5(2): 23. doi: 10.3390/biology5020023
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