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

Hai-Yu Shen Yan Zhou Qian-Jin Zhou Ming-Yun Li Jiong Chen

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

大弹涂鱼白细胞介素-34(IL-34)通过集落刺激因子-1受体1 (CSF-1R1) 调节单核/巨噬细胞功能的研究

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

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
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  • 摘要:

    新型细胞因子白细胞介素-34(interleukin-34,IL-34)通过与集落刺激因子-1受体(the colony-stimulating factor-1 receptor,CSF-1R)结合,在先天免疫和炎症中发挥重要作用。目前,关于鱼类IL-34功能的研究还非常有限。本研究鉴定了大弹涂鱼(Boleophthalmus pectinirostris)的IL-34(BpIL-34),在序列和结构与其它已知的IL-34相似,与石斑鱼(Epinephelus coioides)的同源关系最近。mRNA水平的研究发现,BpIL-34能组成型表达于大弹涂鱼的各个组织,以大脑表达水平最高;迟缓爱德华氏菌(Edwardsiella tarda)感染能上调各组织的表达。本研究表达并纯化了BpIL-34的成熟肽(rBpIL-34),制备了抗体。肽N-糖苷酶F酶解发现单核/巨噬细胞的BpIL-34被N-糖基化。体外实验发现rBpIL-34能够增强单核/巨噬细胞的吞噬和杀菌活性,促进肿瘤坏死因子α(BpTNF-α)和BpIL-1β等促炎细胞因子的表达。RNA干扰实验结果表明,敲低大弹涂鱼CSF-1R1(BpCSF-1R1)后,rBpIL-34介导的单核/巨噬细胞功能的强化表现被显著抑制;BpCSF-1R2不具备此功能。综上,BpIL-34能够通过BpCSF-1R1调节大弹涂鱼单核/巨噬细胞的功能。

  • Figure  1.  Multiple alignment of amino acid sequences of BpIL-34 and related fish IL-34 sequences

    Threshold for shading was >60%; similar residues are marked with a gray shadow, identical residues with a black shadow, and alignment gaps with “-”. BpIL-34: Mudskipper IL-34; DrIL-34: Zebrafish IL-34; OmIL-34: Rainbow trout IL-34; SaIL-34: Gilthead seabream IL-34; TrIL-34: Tiger puffer IL-34; SsIL-34: Atlantic salmon IL-34; IpIL-34: Channel catfish IL-34; CcIL-34: Common carp IL-34; OlIL-34: Japanese rice fish IL-34; EcIL-34: Orange-spotted grouper IL-34. Predicted cleavage site for signal peptide is marked as “↓”. Five conserved cysteine residues are marked as “*”. Two cysteine residues joined by solid line represent disulfide bond. Possible N-linked glycosylation sites of BpIL-34 are indicated by “▼”. RKx [R/K] K motif is double underlined. GenBank accession Nos. of sequences used are presented in Table 1.

    Figure  2.  Phylogenetic tree analysis of complete amino acid sequences of IL-34 and CSF-1 using neighbor-joining method

    CSF-1 sequences as an outgroup. Percentage of bootstrap values is shown next to branches based on 1 000 bootstrap replications (shown only when >60%). Scale bar represents number of substitutions per base position. Site of mudskipper IL-34 is indicated by “▲”. GenBank accession Nos. of sequences used are listed in Table 1.

    Figure  3.  qRT-PCR analysis of BpIL-34 mRNA expression in tissues of healthy (A) and Edwardsiella tarda-infected mudskippers (B–E)

    A: BpIL-34 mRNA expression relative to that of Bp18S rRNA was calculated using 2−ΔCT method. Values denoted by different letters are significantly different when compared by ANOVA (P<0.05); n=4. B–E: BpIL-34 mRNA expression relative to that of Bp18S rRNA was calculated using 2−ΔΔCT method. Tissues were collected at 4, 8, 12, and 24 h after bacterial infection. Data are expressed as means±SEM; n=4, *: P<0.05.

    Figure  4.  Prokaryotic expression and Western blot analysis of BpIL-34

    A: SDS-PAGE analysis of prokaryotically expressed rBpIL-34. Lane M: Protein marker; 1, 2: Crude protein extracts from BL21 (DE3) transformed with pET-28a-BpIL-34 plasmid before and after IPTG induction, respectively; 3: Purified rBpIL-34. B: Western blot analysis of BpIL-34 using anti-rBpIL-34 IgG. NC: Negative control; 4: Purified rBpIL-34; 5: Proteins extracted from mudskipper MOs/MФs; 6: Proteins extracted from mudskipper MOs/MФs with PNGase F digestion.

    Figure  5.  Effects of rBpIL-34 on phagocytosis and bacterial killing of Edwardsiella tarda by mudskipper MO/MΦs

    A: Effect of rBpIL-34 on phagocytosis of E. tarda by MOs/MΦs. Mudskipper MOs/MΦs were pre-treated with PBS or rBpIL-34 before adding FITC-E. tarda (MOI=10). After an additional 30 min incubation, phagocytosis of FITC-E. tarda was determined by flow cytometry. MFI is presented as fold-change over the value for PBS-treated group, which was assigned a unit of 100. B: Effect of rBpIL-34 on bacterial killing of E. tarda by MOs/MΦs. MOs/MΦs were infected with live E. tarda after treatment with PBS or rBpIL-34, and viability of E. tarda (MOI=10) was determined by qRT-PCR. Killing of E. tarda by mudskipper MOs/MФs was measured using CFU assay based on a standard curve. Data are expressed as means±SEM; n=4, *: P<0.05.

    Figure  6.  Effects of rBpIL-34 on mRNA expression of BpTNF-α (A), BpIL-1β (B), BpIL-6 (C), BpTGF-β (D), and BpIL-10 (E) in mudskipper MOs/MΦs

    MOs/MΦs were treated with rBpIL-34 for 12 h. PBS-treated group was used as the control. mRNA expression levels of selected cytokines were normalized to those of Bp18S rRNA. Data are expressed as means±SEM; n=4, *: P<0.05.

    Figure  7.  RNAi-mediated gene knockdown of BpCSF-1R1 and BpCSF-1R2 in mudskipper MOs/MФs

    A: qRT-PCR analysis of mRNA expression of BpCSF-1R1 and BpCSF-1R2 in primary MOs/MФs. B: qRT-PCR analysis of BpCSF-1R1 transcripts in BpCSF-1R1si- or BpCSF-1R2si-transfected MOs/MФs. C: qRT-PCR analysis of BpCSF-1R2 transcripts in BpCSF-1R1si- or BpCSF-1R2si-transfected MOs/MФs. MsiRNA-transfected MOs/MФs group was used as the control. mRNA levels of BpCSF-1R1 and BpCSF-1R2 were normalized to those of Bp18S rRNA. Data are expressed as means±SEM; n=4, *: P<0.05.

    Figure  8.  Effects of BpCSF-1R1 and BpCSF-1R2 knockdown on rBpIL-34-enhanced phagocytosis and bacterial killing of Edwardsiella tarda by mudskipper MOs/MΦs

    A: Effect of BpCSF-1R1 or BpCSF-1R2 knockdown on rBpIL-34-enhanced phagocytosis of E. tarda by mudskipper MOs/MΦs. After transfection with BpCSF-1R1si, BpCSF-1R2si, or MsiRNA (control) for 48 h, mudskipper MOs/MФs were treated with rBpIL-34 for 12 h. Normal MOs/MΦs treated with rBpIL-34 (rBpIL-34 group) were used as controls. Thereafter, FITC-E. tarda were added at a MOI of 10 and incubated for an additional 30 min. Phagocytosis of FITC-E. tarda was determined by flow cytometry. Mean fluorescence intensity (MFI) is presented as a fold-change over value for rBpIL-34 group, which was assigned a value of 100. B: Effect of BpCSF-1R1 and BpCSF-1R2 knockdown on rBpIL-34-enhanced bacterial killing of E. tarda by mudskipper MOs/MΦs. After transfection with BpCSF-1R1si, BpCSF-1R2si, or MsiRNA for 48 h, mudskipper MOs/MФs were treated with rBpIL-34 for 12 h. Normal MOs/MΦs treated with rBpIL-34 (rBpIL-34 group) were used as controls. Live E. tarda were added at a MOI of 10 and incubated for an additional 30 min. Killing of E. tarda by mudskipper MOs/MФs was measured using a CFU assay based on standard curve. Data are expressed as means±SEM; n=4, *: P<0.05.

    Figure  9.  Effects of BpCSF-1R1 and BpCSF-1R2 knockdown on rBpIL-34-altered mRNA expression of selected cytokines in MOs/MФs

    Mudskipper MOs/MФs were pre-treated with BpCSF-1R1si, BpCSF-1R2si, or MsiRNA (control) and further incubated with rBpIL-34 for 12 h. MsiRNA-treated group was used as the control. mRNA levels of BpTNF-α (A), BpIL-1β (B), BpIL-6 (C), BpTGF-β (D), and BpIL-10 (E) were normalized to those of Bp18S rRNA. Data are expressed as means±SEM; n=4, *: P<0.05.

    Table  1.   IL-34 and CSF-1 sequences used for multiple sequence alignment and phylogenetic tree analysis

    GenBank accession No.SpeciesGene
    Latin nameEnglish name
    XM_020935293Boleophthalmus pectinirostrisMudskipperIL-34
    NM_001128701Danio rerioZebrafishIL-34
    KM350155Epinephelus coioidesOrange-spotted grouperIL-34
    NM_001257301Oncorhynchus mykissRainbow troutIL-34
    XM_030427145Sparus aurataGilthead seabreamIL-34
    NM_001305607Takifugu rubripesTiger pufferIL-34
    XM_020104586Paralichthys olivaceusJapanese flounderIL-34
    XM_019360775Oreochromis niloticusNile tilapiaIL-34
    XM_010743578Larimichthys croceaLarge yellow croakerIL-34
    XM_014124241Salmo salarAtlantic salmonIL-34
    XM_017465109Ictalurus punctatusChannel catfishIL-34
    XM_019087026Cyprinus carpioCommon carpIL-34
    XM_011476357Oryzias latipesJapanese rice fishIL-34
    XM_027161223Tachysurus fulvidracoYellow catfishIL-34
    XM_013138989Esox luciusNorthern pikeIL-34
    XM_026287434Carassius auratusGoldfishIL-34
    XM_007249177Astyanax mexicanusMexican tetraIL-34
    MK297321Ctenopharyngodon idellaGrass carpIL-34
    XM_020456685Oncorhynchus kisutchCoho salmonIL-34
    XM_024802984Maylandia zebraZebra mbunaIL-34
    NM_152456Homo sapiensHumanIL-34
    NM_001135100Mus musculusMouseIL-34
    NM_001025766Rattus norvegicusRatIL-34
    NM_001285975Sus scrofaPigIL-34
    XM_022419217Canis lupus familiarisDogIL-34
    XM_023637306Equus caballusHorseIL-34
    XM_018260639Xenopus laevisAfrican clawed frogIL-34
    XM_003641892Gallus gallusChickenIL-34
    XM_019535589Crocodylus porosusCrocodileIL-34
    NM_001100324Bos taurusCattleIL-34
    NM_001114480Danio rerioZebrafishCSF-1
    NM_001080076Danio rerioZebrafishCSF-1-2
    NM_001124394Oncorhynchus mykissRainbow troutCSF-1
    NM_001160476Oncorhynchus mykissRainbow troutCSF-1-2
    KM350156Epinephelus coioidesOrange-spotted grouperCSF-1-2
    NM_001280600Xenopus laevisAfrican clawed frogCSF-1
    XM_017000369Homo sapiensHumanCSF-1
    XM_024984551Bos taurusCattleCSF-1
    XM_008761428Rattus norvegicusRatCSF-1
    NM_001113530Mus musculusMouseCSF-1
    NM_001193295Gallus gallusChickenCSF-1
    下载: 导出CSV

    Table  2.   Oligonucleotide primers used in the qRT-PCR analysis of mudskipper genes

    GeneGenBank accession No.PrimerNucleotide sequence (5′–3′)
    BpIL-34XM_020935293BpIL-34RFGCAGGAGCTTCCAGAGTCAG
    BpIL-34RRCCTCCAATGGGACCTGTCAC
    BpIL-1βKX492895BpIL-1βFACGAGTGGTGAATGTGGTCA
    BpIL-1βRGAACTGAGGTTGTGCTGCAA
    BpTNF-αKX492896BpTNF-αFGGACAACAACGAGATCGTGA
    BpTNF-αRGTTCCACCGTGTGACTGATG
    BpIL-6XM_020932674BpIL-6FGCAGCACGTCAGAAGATGAGA
    BpIL-6RTCTCTGAGAAACTCGTGCAGC
    BpTGF-βXM_020928521BpTGF-βFTCAAAGGACACTTGCACAGC
    BpTGF-βRCAGGGCCAAGATCTGTGAAT
    BpIL-10XM_020936977BpIL-10FGTGGAGGGGTTCCCTCTAAG
    BpIL-10RGTGCGGAGGTAAAAGCTCAG
    Bp18S rRNA KX492897Bp18SFGGCCGTTCTTAGTTGGTGGA
    Bp18SRCCCGGACATCTAAGGGCATC
    BpCSF-1R1XM_020921963BpCSF-1R1FGGCCCACGTGTAAGGAGAAT
    BpCSF-1R1RTACTCCTCCCTCTGCACCTC
    BpCSF-1R2XM_020941064BpCSF-1R2FGTCTTGAGGTTGGACTCGGG
    BpCSF-1R2RCTCACACCTGTCGGTGAGTC
    下载: 导出CSV
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