香鱼IGF-1基因特性及其对单核巨噬细胞的功能调控
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摘要
胰岛素样生长因子1 (insulin-like growth factor-1, IGF-1)是重要的内分泌激素,不仅调控细胞生长和分化,还参与免疫系统调节。为研究鱼类IGF-1在机体抗菌免疫中发挥的作用,探寻IGF-1对鱼类单核巨噬细胞的调控机制,本研究从香鱼(Plecoglossus altivelis)转录组数据中获得PaIGF-1的cDNA序列(GenBank No. MK005188)。序列全长929 bp,包含1个ORF,编码171个氨基酸,预测分子量为18.86 kD。PaIGF-1氨基酸序列相对保守,与大西洋鲑(Salmo salar) IGF-1具有最高的同源性(77%)。qRT-PCR分析显示,PaIGF-1主要在香鱼肝脏、体肾、头肾和肠道中表达;感染鳗弧菌(Vibrio anguillarum)后,脾脏中PaIGF-1表达在感染8 h显著上调,头肾中PaIGF-1表达在感染24 h显著上调,而在鳃和肝中的表达没有改变。利用原核表达系统诱导表达并纯化PaIGF-1重组蛋白(recombinant PaIGF-1, rPaIGF-1),以rPaIGF-1孵育单核巨噬细胞,发现r PaIGF-1可显著增强单核巨噬细胞的吞噬能力,但其杀菌作用不受影响;qRTPCR分析显示,rPaIGF-1可显著上调单核巨噬细胞中抑炎因子白介素(interleukin, IL)-10和转化生长因子β(transforming growth factorβ, TGF-β)的表达,下调促炎因子IL-1β和肿瘤坏死因子α(tumor necrosis factorα, TNF-α)的表达;最后,利用r PaIGF-1分别孵育单核巨噬细胞PaCXCR (C-X-C chemokine receptor)3.1+和PaCXCR3.2+,发现r PaIGF-1促进PaCXCR3.2+中PaSTAT3的磷酸化,而对PaCXCR3.1+中PaSTAT1和PaSTAT3的磷酸化水平没有影响。以特异性siRNA抑制PaSTAT3表达,可显著下调rPaIGF-1处理的PaCXCR3.2+中IL-10和TGF-β的表达,表明r PaIGF-1可能通过激活PaSTAT3而抑制单核巨噬细胞的炎症水平。本研究为深入探讨香鱼IGF-1在宿主抗菌免疫中发挥作用的机制提供了基础资料。
Insulin-like growth factor-1(IGF-1) is an important endocrine hormone which regulates cell growth and differentiation, and participates in the regulation of immune system. To investigate the mechanisms of IGF-1 in regulating fish immune response to pathogens and explore the regulation mechanism of IGF-1 on fish monocytes/macrophages(MO/MΦ), the present study got Plecoglossus altivelis PaIGF-1 cDNA sequence(GenBank No. MK005188) from transcriptome data. The sequence had 929 bp in length,contained an ORF which encoded a protein of 171 amino acids with the molecular weight of 18.86 kD. The amino acid sequence of PaIGF-1 was relatively conservative, sequence comparison showed that PaIGF-1 shared 77% amino acid sequence identity with Atlantic salmon(Salmo salar). Analysis of qRT-PCR showed that the expression of PaIGF-1 was in a high level in liver, trunk kidney, head kidney and intestine. After infected with Vibrio anguillarum, the expression of PaIGF-1 increased at 8 h in spleen, and increased at 24 h in head kidney, and there was no change in gill and liver. Furthermore, prokaryotic expression system was used to induce the expression and purification of PaIGF-1 recombinant protein(rPaIGF-1), and the mononuclear macrophages were incubated with rPaIGF-1. It was found that rPaIGF-1 increased the phagocytic activity of ayu MO/MΦ and had no effect on bacterial killing. Additionally, the qRT-PCR analysis showed that rPaIGF-1 increased the expression of interleukin-10(IL-10) and transforming growth factor-β(TGF-β), suppressed the expression of IL-1β and tumor necrosis factor-α(TNF-α) in ayu MO/MФ infected with V. anguillarum. Finally,mononuclear macrophages PaCXCR(C-X-C chemokine receptor) 3.1+and PaCXCR3.2+were incubated with rPaIGF-1. It was found that r PaIGF-1 promoted the phosphorylation of PaSTAT3 in PaCXCR3.2+but had no effect on the phosphorylation levels of PaSTAT1 and PaSTAT3 in PaCXCR3.1+. Inhibition of PaSTAT3 expression by specific siRNA could significantly down-regulate the expression of IL-10 and TGF-β in PaCXCR3.2+treated with r PaIGF-1 which indicated that r PaIGF-1 might inhibit the inflammatory response of ayu MO/MΦ through activating PaSTAT3. The above research provides a theoretical basis to study PaIGF-1 function and related mechanism in regulating fish immune response to pathogens.
Insulin-like growth factor-1(IGF-1) is an important endocrine hormone which regulates cell growth and differentiation, and participates in the regulation of immune system. To investigate the mechanisms of IGF-1 in regulating fish immune response to pathogens and explore the regulation mechanism of IGF-1 on fish monocytes/macrophages(MO/MΦ), the present study got Plecoglossus altivelis PaIGF-1 cDNA sequence(GenBank No. MK005188) from transcriptome data. The sequence had 929 bp in length,contained an ORF which encoded a protein of 171 amino acids with the molecular weight of 18.86 kD. The amino acid sequence of PaIGF-1 was relatively conservative, sequence comparison showed that PaIGF-1 shared 77% amino acid sequence identity with Atlantic salmon(Salmo salar). Analysis of qRT-PCR showed that the expression of PaIGF-1 was in a high level in liver, trunk kidney, head kidney and intestine. After infected with Vibrio anguillarum, the expression of PaIGF-1 increased at 8 h in spleen, and increased at 24 h in head kidney, and there was no change in gill and liver. Furthermore, prokaryotic expression system was used to induce the expression and purification of PaIGF-1 recombinant protein(rPaIGF-1), and the mononuclear macrophages were incubated with rPaIGF-1. It was found that rPaIGF-1 increased the phagocytic activity of ayu MO/MΦ and had no effect on bacterial killing. Additionally, the qRT-PCR analysis showed that rPaIGF-1 increased the expression of interleukin-10(IL-10) and transforming growth factor-β(TGF-β), suppressed the expression of IL-1β and tumor necrosis factor-α(TNF-α) in ayu MO/MФ infected with V. anguillarum. Finally,mononuclear macrophages PaCXCR(C-X-C chemokine receptor) 3.1+and PaCXCR3.2+were incubated with rPaIGF-1. It was found that r PaIGF-1 promoted the phosphorylation of PaSTAT3 in PaCXCR3.2+but had no effect on the phosphorylation levels of PaSTAT1 and PaSTAT3 in PaCXCR3.1+. Inhibition of PaSTAT3 expression by specific siRNA could significantly down-regulate the expression of IL-10 and TGF-β in PaCXCR3.2+treated with r PaIGF-1 which indicated that r PaIGF-1 might inhibit the inflammatory response of ayu MO/MΦ through activating PaSTAT3. The above research provides a theoretical basis to study PaIGF-1 function and related mechanism in regulating fish immune response to pathogens.
引文
华益民,林浩然.2001.草鱼IGF-ⅠcDNA的克隆和在原核生物中的表达[J].动物学报,47(3):274-279.(Hua YM,Lin H R.2001.Cloning and expression in prokaryote of grass carp IGF-ⅠcDNA[J].Acta Zoologica Sinica,47(3):274-279.)
李长红,陈炯,史雨红,等.2009.宁海地区香鱼弧菌病病原菌鉴定[J].微生物学报,49(7):931-937.(Li C Y,Chen J,Shi Y H,et al.2009.Identification of pathogenic bacteria of Vibrio in ayu in Ninghai area[J].Acta Microbiologica Sinica,49(7):931-937.)
邹晓岚,叶茸茸,王洋,等.2018.胰岛素样生长因子-1及其受体在肿瘤中的研究进展[J].重庆医学,47(18):2474-2479.(Zou X L,Ye R R,Wang W,et al.2018.Progress in research of insulin-like growth factor-1 and its receptor in tumors[J].Chongqing Medicine,47(18):2474-2479.)
Akdis M,Aab A,Altunbulakli C,et al.2016.Interleukins(from IL-1 to IL-38),interferons,transforming growth factorβ,and TNF-α:Receptors,functions,and roles in diseases[J].Journal of Allergy and Clinical Immunology,138(4):984-1010.
Anne-Constance F,Oliver F,Bernd K,et al.2016.Endocrine and local IGF-I in the bony fish immune System[J].Biology,5(1):1-13.
Baer C,Squadrito M L,Laoui D,et al.2016.Suppression of microRNA activity amplifies IFN-γ-induced macrophage activation and promotes anti-tumour immunity[J].Nature Cell Biology,18(7):790-802.
Bo Y X,Song X H,Wu K,et al.2015.Characterization of interleukin-1βas a proinflammatory cytokine in grass carp(Ctenopharyngodon idella)[J].Fish&Shellfish Immunology,46(2):584-595.
Caldarone E M,Maclean S A,Beckman B R.2016.Evaluation of nucleic acids and plasma IGF1 levels for estimating short-term responses of postsmolt Atlantic salmon(Salmo salar)to food availability[J].Fishery Bulletin,114(3):288-301.
Cao Q P,Duguay S J,Plisetskaya E,et al.1989.Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA[J].Molecular Endocrinology,3(12):2005-2010.
Chen M H,Lin G,Gong H,et al.2001.The characterization of prepro-insulin-like growth factor-1 Ea-2 expression and insulin-like growth factor-1 genes(devoid 81 bp)in the zebrafish(Danio rerio)[J].Gene,268(1-2):67-75.
Crisafi F,Denaro R,Genovese M,et al.2011.Comparison of16S rDNA and toxR genes as targets for detection of Vibrio anguillarum in Dicentrarchus labrax kidney and liver[J].Research in Microbiology,162(3):223-230.
Eppler E,Berishvili G,Mazel P,et al.2010.Distinct organspecific up-and down-regulation of IGF-Ⅰand IGF-Ⅱm RNA in various organs of a GH-overexpressing transgenic Nile tilapia[J]Transgenic Research,19(2):231-240.
Geertz R,Kiess W,Kessler U,et al.1997.Expression of IGFreceptors on alveolar macrophages:IGF-induced changes in InsPi formation,[Ca2+]i,and pHi[J].Molecular&Cellular Biochemistry,177(1-2):33-45.
González-Stegmaier R,Guzmán F,Albericio F,et al.2015.Asynthetic peptide derived from the D1 domain of flagellin induced the expression of proinflammatory cytokines in fish macrophages[J].Fish&Shellfish Immunology,47(1):239-244.
Guan F,Lu X J,Li C H,et al.2017.Molecular characterization of mudskipper(Boleophthalmus pectinirostris)hypoxia-inducible factor-1α(HIF-1α)and analysis of its function in monocytes/macrophages[J].PLoS One,12(5):e0177960.
He Y Q,Chen J,Lu X J,et al.2013.Characterization of P2X7R and its function in the macrophages of ayu,Plecoglossus altivelis[J].PLoS One,8(2):e57505.
Hua Q X,Mayer J P,Jia W,et al.2006.The folding nucleus of the insulin superfamily:A flexible peptide model foreshadows the native state[J].Journal of Biological Chemistry,281(38):28131-28142.
Irmawati,Alimuddin,Zairin M,et al.2016.Molecular cloning and sequence analysis of insulin-like growth factors-1 cDNA of giant gourami,Osphronemus goramy[J].Aquaculture,Aquarium,Conservation&Legislation-International Journal of the Bioflux Society,9(1):174-183.
Jansen M,van Schaik F M,Ricker A T,et al.1983.Sequence of cDNA encoding human insulin-like growth factorⅠprecursor[J].Nature,306(5943):609-611.
Jiang Y,Husain M,Qi Z,et al.2015.Identification and expression analysis of two interleukin-23α(p19)isoforms,in rainbow trout Oncorhynchus mykiss and Atlantic salmon Salmo salar[J].Molecular Immunology,66(2):216-228.
Jie C,Qiang C,Lu X J,et al.2016.The protection effect of LEAP-2 on the mudskipper(Boleophthalmus pectinirostris)against Edwardsiella tarda infection is associated with its immunomodulatory activity on monocytes/macrophages[J].Fish&Shellfish Immunology,59:66-76.
Kai J E,Clifford M A,Hedrick R P,et al.2008.Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pesticides and Infectious hematopoietic necrosis virus(IHNV)[J].Fish&Shellfish Immunology,25(5):508-516.
Kashima H,Shiozawa T,Miyamoto T,et al.2009.Autocrine stimulation of IGF1 in estrogen-induced growth of endometrial carcinoma cells:Involvement of the mitogen-activated protein kinase pathway followed by up-regulation of cyclin D1 and cyclin E[J].Endocrine Related Cancer,16(1):113-122.
Lawrence T,Natoli G.2011.Transcriptional regulation of macrophage polarization:Enabling diversity with identity[J].Nature Reviews Immunology,11(11):750-761.
Lu X J,Chen Q,Rong Y J,et al.2017.CXCR3.1 and CX-CR3.2 differentially contribute to macrophage polarization in teleost fish[J].Journal of Immunology,198(12):4692-4706.
LU X J,Zhang H,Yang G J,et al.2016.Comparative transcriptome analysis on the alteration of gene expression in ayu(Plecoglossusal tivelis)larvae associated with salinity change[J].Zoological Research,37(3):126-135.
Ma Q,Liu S F,Zhuang Z M,et al.2011.Molecular cloning,expression analysis of insulin-like growth factorⅠ(IGF-Ⅰ)gene and IGF-Ⅰserum concentration in female and male Tongue sole(Cynoglossus semilaevis)[J].Comparative Biochemistry&Physiology Part B,160(4):208-214.
Ma W,Wu J,Zhang J,et al.2016.Sex differences in the expression of GH/IGF axis genes underlie sexual size dimorphism in the yellow catfish(Pelteobagrus fulvidraco)[J].Science China Life Sciences,59(4):431-433.
O'Connor J C,Mccusker R H,Strle K,et al.2008.Regulation of IGF-I function by proinflammatory cytokines:At the interface of immunology and endocrinology[J].Cellular Immunology,252(1):91-110.
Pérez L,Ortiz-Delgado J B,Manchado M.2016.Molecular characterization and transcriptional regulation by GHand GnRH of insulin-like growth factorsⅠandⅡin white seabream(Diplodus sargus)[J].Gene,578(2):251-262.
Piazzon M C,Savelkoul H F J,Pietretti D,et al.2015.CarpⅠIL10 has anti-inflammatory activities on phagocytes,promotes proliferation of memory T cells,and regulates B cell differentiation and antibody secretion[J].The Journal of Immunology,194(1):187-199.
Ponce M,Infante C,Funes V,et al.2008.Molecular characterization and gene expression analysis of insulin-like growth factorsⅠandⅡin the redbanded seabream,Pagrus auriga:Transcriptional regulation by growth hormone[J].Comparative Biochemistry&Physiology Part B Biochemistry&Molecular Biology,150(4):418-426.
Sica A,Mantovani A.2012.Macrophage plasticity and polarization:In vivo veritas[J].Journal of Clinical Investigation,122(3):787-795.
Sitjàbobadilla A,Calduchginer J,Saeravila A,et al.2008.Chronic exposure to the parasite Enteromyxum leei(Myxozoa:Myxosporea)modulates the immune response and the expression of growth,redox and immune relevant genes in gilthead sea bream,Sparus aurata L.[J].Fish&Shellfish Immunology,24(5):610-619.
Spadaro O,Camell C D,Bosurgi L,et al.2017.IGF1 shapes macrophage activation in response toimmunometabolic challenge[J].Cell Reports,19(2):225-234.
Tamura K,Peterson D,Peterson N,et al.2011.MEGA5:Molecular evolutionary genetics analysis using maximum likelihood,evolutionary distance,and maximum parsimony methods[J].Molecular Biology&Evolution,28(10):2731-2739.
Tsai T C,Shih C C,Chien H P,et al.2018.Anti-apoptotic effects of IGF-Ⅰon mortality and dysmorphogenesis in tbx5-deficient zebrafish embryos[J].BMC Developmental Biology,18(1):5-20.
Vikes?V,Nankervis L,Rem?S C,et al.2015.Pre and postprandial regulation of ghrelin,amino acids and IGF1 in Atlantic salmon(Salmo salar L.)at optimal and elevated seawater temperatures[J].Aquaculture,438(438):159-169.
Vong Q P,Chan K M,Cheng C H.2003.Quantification of common carp(Cyprinus carpio)IGF-Ⅰand IGF-ⅡmRNA by real-time PCR:Differential regulation of expression by GH[J].Journal of Endocrinology,178(3):513-521.
Wallenius K,Sj?gren K,Peng X D,et al.2001.Liver-derived IGF-Ⅰregulates GH secretion at the pituitary level in mice[J].Endocrinology,142(11):4762-4770.
Wenger M,Shved N,Akgül G,et al.2014.Developmental oestrogen exposure differentially modulates IGF-Ⅰand TNF-αexpression levels in immune organs of Yersinia ruckeri-challenged young adult rainbow trout(Oncorhynchus mykiss)[J].General&Comparative Endocrinology,205:168-175.
Wu J,Shi Y H,Zhang X H,et al.2015.Molecular characterization of an IL-1βgene from the large yellow croaker(Larimichthys crocea)and its effect on fish defense against Vibrio alginolyticus infection[J].Zoological Research,36(3):133-141.
Xu X G,Hu J F,Ma J X,et al.2016.Essential Roles of TIM-1 and TIM-4 homologs in adaptive humoral immunity in a zebrafish model[J].Journal of Immunology,196(4):1686-1700.
Yildirimaksoy M,Beck B H.2017.Antimicrobial activity of chitosan and a chitosan oligomer against bacterial pathogens of warmwater fish[J].Journal of Applied Microbiology,122(6):1570-1578.
李长红,陈炯,史雨红,等.2009.宁海地区香鱼弧菌病病原菌鉴定[J].微生物学报,49(7):931-937.(Li C Y,Chen J,Shi Y H,et al.2009.Identification of pathogenic bacteria of Vibrio in ayu in Ninghai area[J].Acta Microbiologica Sinica,49(7):931-937.)
邹晓岚,叶茸茸,王洋,等.2018.胰岛素样生长因子-1及其受体在肿瘤中的研究进展[J].重庆医学,47(18):2474-2479.(Zou X L,Ye R R,Wang W,et al.2018.Progress in research of insulin-like growth factor-1 and its receptor in tumors[J].Chongqing Medicine,47(18):2474-2479.)
Akdis M,Aab A,Altunbulakli C,et al.2016.Interleukins(from IL-1 to IL-38),interferons,transforming growth factorβ,and TNF-α:Receptors,functions,and roles in diseases[J].Journal of Allergy and Clinical Immunology,138(4):984-1010.
Anne-Constance F,Oliver F,Bernd K,et al.2016.Endocrine and local IGF-I in the bony fish immune System[J].Biology,5(1):1-13.
Baer C,Squadrito M L,Laoui D,et al.2016.Suppression of microRNA activity amplifies IFN-γ-induced macrophage activation and promotes anti-tumour immunity[J].Nature Cell Biology,18(7):790-802.
Bo Y X,Song X H,Wu K,et al.2015.Characterization of interleukin-1βas a proinflammatory cytokine in grass carp(Ctenopharyngodon idella)[J].Fish&Shellfish Immunology,46(2):584-595.
Caldarone E M,Maclean S A,Beckman B R.2016.Evaluation of nucleic acids and plasma IGF1 levels for estimating short-term responses of postsmolt Atlantic salmon(Salmo salar)to food availability[J].Fishery Bulletin,114(3):288-301.
Cao Q P,Duguay S J,Plisetskaya E,et al.1989.Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA[J].Molecular Endocrinology,3(12):2005-2010.
Chen M H,Lin G,Gong H,et al.2001.The characterization of prepro-insulin-like growth factor-1 Ea-2 expression and insulin-like growth factor-1 genes(devoid 81 bp)in the zebrafish(Danio rerio)[J].Gene,268(1-2):67-75.
Crisafi F,Denaro R,Genovese M,et al.2011.Comparison of16S rDNA and toxR genes as targets for detection of Vibrio anguillarum in Dicentrarchus labrax kidney and liver[J].Research in Microbiology,162(3):223-230.
Eppler E,Berishvili G,Mazel P,et al.2010.Distinct organspecific up-and down-regulation of IGF-Ⅰand IGF-Ⅱm RNA in various organs of a GH-overexpressing transgenic Nile tilapia[J]Transgenic Research,19(2):231-240.
Geertz R,Kiess W,Kessler U,et al.1997.Expression of IGFreceptors on alveolar macrophages:IGF-induced changes in InsPi formation,[Ca2+]i,and pHi[J].Molecular&Cellular Biochemistry,177(1-2):33-45.
González-Stegmaier R,Guzmán F,Albericio F,et al.2015.Asynthetic peptide derived from the D1 domain of flagellin induced the expression of proinflammatory cytokines in fish macrophages[J].Fish&Shellfish Immunology,47(1):239-244.
Guan F,Lu X J,Li C H,et al.2017.Molecular characterization of mudskipper(Boleophthalmus pectinirostris)hypoxia-inducible factor-1α(HIF-1α)and analysis of its function in monocytes/macrophages[J].PLoS One,12(5):e0177960.
He Y Q,Chen J,Lu X J,et al.2013.Characterization of P2X7R and its function in the macrophages of ayu,Plecoglossus altivelis[J].PLoS One,8(2):e57505.
Hua Q X,Mayer J P,Jia W,et al.2006.The folding nucleus of the insulin superfamily:A flexible peptide model foreshadows the native state[J].Journal of Biological Chemistry,281(38):28131-28142.
Irmawati,Alimuddin,Zairin M,et al.2016.Molecular cloning and sequence analysis of insulin-like growth factors-1 cDNA of giant gourami,Osphronemus goramy[J].Aquaculture,Aquarium,Conservation&Legislation-International Journal of the Bioflux Society,9(1):174-183.
Jansen M,van Schaik F M,Ricker A T,et al.1983.Sequence of cDNA encoding human insulin-like growth factorⅠprecursor[J].Nature,306(5943):609-611.
Jiang Y,Husain M,Qi Z,et al.2015.Identification and expression analysis of two interleukin-23α(p19)isoforms,in rainbow trout Oncorhynchus mykiss and Atlantic salmon Salmo salar[J].Molecular Immunology,66(2):216-228.
Jie C,Qiang C,Lu X J,et al.2016.The protection effect of LEAP-2 on the mudskipper(Boleophthalmus pectinirostris)against Edwardsiella tarda infection is associated with its immunomodulatory activity on monocytes/macrophages[J].Fish&Shellfish Immunology,59:66-76.
Kai J E,Clifford M A,Hedrick R P,et al.2008.Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pesticides and Infectious hematopoietic necrosis virus(IHNV)[J].Fish&Shellfish Immunology,25(5):508-516.
Kashima H,Shiozawa T,Miyamoto T,et al.2009.Autocrine stimulation of IGF1 in estrogen-induced growth of endometrial carcinoma cells:Involvement of the mitogen-activated protein kinase pathway followed by up-regulation of cyclin D1 and cyclin E[J].Endocrine Related Cancer,16(1):113-122.
Lawrence T,Natoli G.2011.Transcriptional regulation of macrophage polarization:Enabling diversity with identity[J].Nature Reviews Immunology,11(11):750-761.
Lu X J,Chen Q,Rong Y J,et al.2017.CXCR3.1 and CX-CR3.2 differentially contribute to macrophage polarization in teleost fish[J].Journal of Immunology,198(12):4692-4706.
LU X J,Zhang H,Yang G J,et al.2016.Comparative transcriptome analysis on the alteration of gene expression in ayu(Plecoglossusal tivelis)larvae associated with salinity change[J].Zoological Research,37(3):126-135.
Ma Q,Liu S F,Zhuang Z M,et al.2011.Molecular cloning,expression analysis of insulin-like growth factorⅠ(IGF-Ⅰ)gene and IGF-Ⅰserum concentration in female and male Tongue sole(Cynoglossus semilaevis)[J].Comparative Biochemistry&Physiology Part B,160(4):208-214.
Ma W,Wu J,Zhang J,et al.2016.Sex differences in the expression of GH/IGF axis genes underlie sexual size dimorphism in the yellow catfish(Pelteobagrus fulvidraco)[J].Science China Life Sciences,59(4):431-433.
O'Connor J C,Mccusker R H,Strle K,et al.2008.Regulation of IGF-I function by proinflammatory cytokines:At the interface of immunology and endocrinology[J].Cellular Immunology,252(1):91-110.
Pérez L,Ortiz-Delgado J B,Manchado M.2016.Molecular characterization and transcriptional regulation by GHand GnRH of insulin-like growth factorsⅠandⅡin white seabream(Diplodus sargus)[J].Gene,578(2):251-262.
Piazzon M C,Savelkoul H F J,Pietretti D,et al.2015.CarpⅠIL10 has anti-inflammatory activities on phagocytes,promotes proliferation of memory T cells,and regulates B cell differentiation and antibody secretion[J].The Journal of Immunology,194(1):187-199.
Ponce M,Infante C,Funes V,et al.2008.Molecular characterization and gene expression analysis of insulin-like growth factorsⅠandⅡin the redbanded seabream,Pagrus auriga:Transcriptional regulation by growth hormone[J].Comparative Biochemistry&Physiology Part B Biochemistry&Molecular Biology,150(4):418-426.
Sica A,Mantovani A.2012.Macrophage plasticity and polarization:In vivo veritas[J].Journal of Clinical Investigation,122(3):787-795.
Sitjàbobadilla A,Calduchginer J,Saeravila A,et al.2008.Chronic exposure to the parasite Enteromyxum leei(Myxozoa:Myxosporea)modulates the immune response and the expression of growth,redox and immune relevant genes in gilthead sea bream,Sparus aurata L.[J].Fish&Shellfish Immunology,24(5):610-619.
Spadaro O,Camell C D,Bosurgi L,et al.2017.IGF1 shapes macrophage activation in response toimmunometabolic challenge[J].Cell Reports,19(2):225-234.
Tamura K,Peterson D,Peterson N,et al.2011.MEGA5:Molecular evolutionary genetics analysis using maximum likelihood,evolutionary distance,and maximum parsimony methods[J].Molecular Biology&Evolution,28(10):2731-2739.
Tsai T C,Shih C C,Chien H P,et al.2018.Anti-apoptotic effects of IGF-Ⅰon mortality and dysmorphogenesis in tbx5-deficient zebrafish embryos[J].BMC Developmental Biology,18(1):5-20.
Vikes?V,Nankervis L,Rem?S C,et al.2015.Pre and postprandial regulation of ghrelin,amino acids and IGF1 in Atlantic salmon(Salmo salar L.)at optimal and elevated seawater temperatures[J].Aquaculture,438(438):159-169.
Vong Q P,Chan K M,Cheng C H.2003.Quantification of common carp(Cyprinus carpio)IGF-Ⅰand IGF-ⅡmRNA by real-time PCR:Differential regulation of expression by GH[J].Journal of Endocrinology,178(3):513-521.
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