Abstract
Although it has been reported that selenium (Se) deficiency can trigger inflammation, however, there are few reports on the effect of Se on the function of mouse peritoneal macrophages. Herein, we examined the expression of inflammatory factors, oxidative stress levels, and phagocytosis for primary-cultured peritoneal macrophages using control and Se-deficient groups. Our results revealed that Se deficiency induced the accumulation of oxygen free radicals and weakened antioxidant capacity. Se deficiency also significantly increased the expression of inflammation factors including iNOS, IL-1β, IL-12, IL-10, PTGe, and NF-κB. Meanwhile, Se suppression restrained macrophage production of TNF-α. The results of the phagocytosis assay demonstrated that Se deficiency inhibited the phagocytosis of macrophages. In conclusion, Se-deficient macrophages undergo severe inflammation through the NF-κB pathway due to the accumulation of oxygen free radicals and are hindered in their phagocytic capacity.
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Abbreviations
- GSH-Px:
-
glutathione peroxidase
- CAT:
-
catalase
- MDA:
-
malondialdehyde
- iNOS:
-
induced nitric oxide synthase
- SOD:
-
superoxide dismutase
- T-AOC:
-
total antioxidant capability
- TNF-α:
-
tumor necrosis factor
- PTGEs:
-
prostaglandin e synthetase
- iNOS:
-
inducible nitric oxide synthase
- NF-κB:
-
nuclear factor kappa-light-chain-enhancer of activated B cells
- IL-1β:
-
interleukin-1β
- IL-10:
-
interleukin-10
- IL-12:
-
interleukin-12
- GAPDH:
-
glyceraldehyde-3-phosphate dehydrogenase
References
Yang J, Hamid S, Liu Q, Cai JZ, Xu SW, Zhang ZW (2017) Gene expression of selenoproteins can be regulated by thioredoxin(Txn) silence in chicken cardiomyocytes. J Inorg Biochem 177:118–126
Yang J, Zhang Y, Hamid S, Cai JZ, Liu Q, Li H, Zhao R, Wang H, Xu S, Zhang Z (2017) Interplay between autophagy and apoptosis in selenium deficient cardiomyocytes in chicken. J Inorg Biochem 170:17–25
Ishihara H, Kanda F, Matsushita T, Chihara K, Itoh K (1999) White muscle disease in humans: myopathy caused by selenium deficiency in anorexia nervosa under long term total parenteral nutrition. J Neurol Neurosurg Psychiatry 67:829–830
Burk RF, Hill KE, Awad JA, Morrow JD, Lyons PR (1995) Liver and kidney necrosis in selenium-deficient rats depleted of glutathione. LAB INVEST; a jour of tech meth and patho 72:723–730
Ip C, ., Sinha DK. Enhancement of mammary tumorigenesis by dietary selenium deficiency in rats with a high polyunsaturated fat intake. Cancer Res 1981;41:31
Reddi AS, Bollineni JS (2001) Selenium-deficient diet induces renal oxidative stress and injury via TGF-β1 in normal and diabetic rats. Kidney Int 59:1342–1353
Yang T, Cao C, Jie Y, Liu T, Xin GL, Zhang Z et al (2017) miR-200a-5p regulates myocardial necroptosis induced by Se deficiency via targeting RNF11. Redox Biol 15:159–169
Khoso PA, Yang Z, Liu C, Li S (2015) Selenium deficiency downregulates selenoproteins and suppresses immune function in chicken thymus. Biol Trace Elem Res 167:48–55
Contempre B, Dumont JE, Denef JF, Many MC (1995) Effects of selenium deficiency on thyroid necrosis, fibrosis and proliferation: a possible role in myxoedematous cretinism. Eur J Endocrinol 133:99–109
Stabel PDJR (1990) Effect of in vitro selenium repletion on bovine lymphocyte proliferation. Nutr Res 10:1053–1059
Dworkin BM (1994) Selenium deficiency in HIV infection and the acquired immunodeficiency syndrome (AIDS). Chem Biol Interact 91:181–186
Ongele E, Ashraf M, Nesbitt R, Humphrey P, Lee C (2002) Effects of selenium deficiency in the development of trypanosomes and humoral immune responses in mice infected with Trypanosoma musculi. Parasitol Res 88:540–545
Ben-Nun A, Cohen IR (1982) Genes of the major histocompatibility complex control transmission of information between initiator and recruited T lymphocyte[J]. Adv Exp Med Biol 149(5):635
Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32:593–604
Zhang Z, Liu Q, Cai J, Yang J, Shen Q, Xu S (2017) Chlorpyrifos exposure in common carp (Cyprinus carpio L.) leads to oxidative stress and immune responses. Fish & shellfish immunol 67:604–611
Liu F, Wang XY, Zhou XP, Liu ZP, Song XB, Wang ZY, Wang L (2017) Cadmium disrupts autophagic flux by inhibiting cytosolic Ca2+−dependent autophagosome-lysosome fusion in primary rat proximal tubular cells. Toxicology 383:13–23
Liu G, Wang ZK, Wang ZY, Yang DB, Liu ZP, Wang L (2016) Mitochondrial permeability transition and its regulatory components are implicated in apoptosis of primary cultures of rat proximal tubular cells exposed to lead. Arch Toxicol 90:1193–1209
Zhang ZW, Zheng Z, Cai JZ, Liu Q, Yang J, Gong YF, Wu M, Shen Q, Xu S (2017) Effect of cadmium on oxidative stress and immune function of common carp (Cyprinus carpio L.) by transcriptome analysis. Aquat Toxicol 192:171–177
Wang Y, Zhao H, Liu J, Shao Y, Li J, Luo L, Xing M (2018) Copper and arsenic-induced oxidative stress and immune imbalance are associated with activation of heat shock proteins in chicken intestines. Int Immunopharmacol 60:64–75
Wang Y, Zhao H, Shao Y, Liu J, Li J, Luo L, Xing M (2018) Copper (II) and/or arsenite-induced oxidative stress cascades apoptosis and autophagy in the skeletal muscles of chicken. Chemosphere 206:597–605
Yao HD, Wu Q, Zhang ZW, Li S, Wang XL, Lei XG et al (1830) Selenoprotein W serves as an antioxidant in chicken myoblasts. Biochim Biophys Acta 2013:3112–3120
Liu T, Yang T, Xu Z, Tan S, Pan T, Wan N, Li S (2018) MicroRNA-193b-3p regulates hepatocyte apoptosis in selenium-deficient broilers by targeting MAML1. J Inorg Biochem 186:235–245
Chi Q, Chi X, Hu X, Wang S, Zhang H, Li S (2018) The effects of atmospheric hydrogen sulfide on peripheral blood lymphocytes of chickens: perspectives on inflammation, oxidative stress and energy metabolism. Environ Res 167:1–6
Kaushal N, Gandhi UH, Nelson SM, Narayan V, Prabhu KS (2012) Selenium and inflammation[M]// selenium: its molecular biology and role in human health. Springer, New York
Mattmiller SA, Carlson BA, Sordillo LM (2013) Regulation of inflammation by selenium and selenoproteins: impact on eicosanoid biosynthesis. J of Nutr Sci 2(2). https://doi.org/10.1017/jns.2013.17
Yan J, Zheng Y, Min Z, Ning Q, Lu S (2013) Selenium effect on selenoprotein transcriptome in chondrocytes. Biometals 26:285–296
Shi-Wen X, Hai-Dong Y, Jian Z, Zi-Wei Z, Jin-Tao W, Jiu-Li Z et al (2013) The oxidative damage and disbalance of calcium homeostasis in brain of chicken induced by selenium deficiency. Biol Trace Elem Res 151:225–233
Cao C, Fan R, Chen M, Li X, Xing M, Zhu F et al (2017) Inflammatory response occurs in veins of broiler chickens treated with a selenium deficiency diet. Biol Trace Elem Res 183:1–9
Fan R, Cao C, Xia Z, Shi Q, Zhao J, Xu S (2017) Downregulated long noncoding RNA ALDBGALG0000005049 induces inflammation in chicken muscle suffered from selenium deficiency by regulating stearoyl-CoA desaturase. Oncotarget 8:52761–52774
Rao L, Puschner B, Prolla T (2001) Gene expression profiling of low selenium status in the mouse intestine: transcriptional activation of genes linked to DNA damage, cell cycle control and oxidative stress. J Nutr 131:3175–3181
Burk RF, Hill KE, Nakayama A, Mostert V, Levander XA, Motley AK, Johnson DA, Johnson JA, Freeman ML, Austin LM (2008) Selenium deficiency activates mouse liver Nrf2–ARE but vitamin E deficiency does not. Free Radic Biol Med 44:1617–1623
Roman M, Jitaru P, Barbante C (2013) Selenium biochemistry and its role for human health. Metallomics: Inte Bio Sci 6:25–54
Malá S, Kovářů F, Mišurová Ľ, Pavlata L, Dvořák R, Číž M (2009) Influence of selenium on innate immune response in kids. Folia Microbiol 54:545
Arthur JR, McKenzie RC, Beckett GJ (2003) Selenium in the immune system. J Nutr 133:1457S–1459S
Gebhart GF, Schmidt RF (2013) Immunocompetent cells. Ency Pain 958
Fogg DK, Claire S, Chaouki M, Steffen J, Pierre A, Littman DR et al (2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311:83–87
Ganz T (1993) Macrophage function. New Horiz 1:23–27
Stacia CK, Shen-An H, Kruzel MC, Amitava D, Actor JK (2008) Immune modulation of macrophage pro-inflammatory response by goldenseal and Astragalus extracts. J Med Food 11:493–498
Shilo S, Aharoni-Simon M, Tirosh O (2005) Selenium attenuates expression of MnSOD and uncoupling protein 2 in J774.2 macrophages: molecular mechanism for its cell-death and antiinflammatory activity. Antioxid Redox Signal 7:276–286
Gyang EO, Stevens JB, Olson WG, Tsitsamis SD, Usenik EA (2012) Effects of selenium-vitamin E injection on polymorphonucleated leukocytes phagocytosis and killing Staphylococcus aureus. Am J Vet Res 45:175–177
Prabhu KS, Zamamiri-Davis F, Stewart JB, Thompson JT, Sordillo LM, Reddy CC (2002) Selenium deficiency increases the expression of inducible nitric oxide synthase in RAW 264.7 macrophages: role of nuclear factor-kappaB in up-regulation. Biochem J 366:203–209
Carlson BA, Yoo MH, Sano Y, Sengupta A, Jin YK, Irons R et al (2009) Selenoproteins regulate macrophage invasiveness and extracellular matrix-related gene expression. Bmc Immunology 10:57
Vunta H, Belda BJ, Arner RJ, Channa Reddy C, Vanden Heuvel JP, Sandeep Prabhu K (2010) Selenium attenuates pro-inflammatory gene expression in macrophages. Mol Nutr Food Res 52:1316–1323
Zheng JC, Huang Y, Tang K, Cui M, Niemann D, Lopez A, Morgello S, Chen S (2008) HIV-1-infected and/or immune-activated macrophages regulate astrocyte CXCL8 production through IL-1beta and TNF-alpha: involvement of mitogen-activated protein kinases and protein kinase R. J Neuroimmunol 200:100–110
Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805–820
Christensen MJ, Nartey ET, Hada AL, Legg RL, Barzee BR (2007) High selenium reduces NF-kappaB-regulated gene expression in uninduced human prostate cancer cells. Nutr Cancer 58:197–204
Du Q, Yao H, Yao L, Zhang Z, Lei X, Xu S (2016) Selenium deficiency influences the expression of selenoproteins and inflammatory cytokines in chicken aorta vessels. Biol Trace Elem Res 173:1–13
Yilma AN, Singh SR, Fairley SJ, Taha MA, Dennis VA (2012, (2012-2-19)) The anti-inflammatory cytokine, interleukin-10, inhibits inflammatory mediators in human epithelial cells and mouse macrophages exposed to live and UV-inactivated Chlamydia trachomatis. Mediat Inflamm 2012(2012):520174
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The study was supported by the Earmarked Fund for China Agriculture Research System (No. CARS 35) and the Students Innovative Training (SIPT) program of Northeast Agricultural University (No. 201810224213).
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All procedures used in this study were approved by the Institutional Animal Care and Use Committee of Northeast Agricultural University (SRM-11).
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Xu, J., Gong, Y., Sun, Y. et al. Impact of Selenium Deficiency on Inflammation, Oxidative Stress, and Phagocytosis in Mouse Macrophages. Biol Trace Elem Res 194, 237–243 (2020). https://doi.org/10.1007/s12011-019-01775-7
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DOI: https://doi.org/10.1007/s12011-019-01775-7