Abstract
The aim of the present study was to clarify the effect of low selenium (Se)/high fat on the mRNA expression of selenoproteins, heat shock proteins (HSPs) and cytokines in pig peripheral blood lymphocytes. Forty crossbred boar piglets with healthy lean body weights of 10 kg were randomly divided into four treatment groups (group C, group L-Se, group H-fat, and group L-Se-H-fat) (n = 10/group) and fed with the corresponding diet for 16 weeks. The pig peripheral blood lymphocytes were extracted, and the mRNA expression of selenoproteins, HSPs, and cytokines was measured. Most mRNA levels for selenoproteins decreased in group L-Se, group H-fat, and group L-Se-H-fat, except Gpx1, Gpx2, Selt, and Selm, which were elevated in group H-fat. At the same time, low-Se/high-fat diet increased the expression of HSPs (HSP40, HSP60, HSP70, and HSP90) and inflammatory cytokines (IL-1α, IL-1β, IL-6, IL-8, IL-9, iNOS, COX-2, NF-κB, and TNF-α) in group L-Se, group H-fat, and group L-Se-H-fat, and genes in group L-Se-H-fat showed greater increases. Also, low-Se/high-fat diet inhibits the expression of TGF-β1 and IFN-γ. In summary, a low-Se/high-fat diet can cause relevant selenoprotein expression changes and promote the expression of pro-inflammatory factors and HSPs, and low Se enhances the expression of HSPs and inflammation factors induced by high fat. This information is helpful for understanding the effects of low-Se and high-fat diet on pig peripheral blood lymphocytes.
Similar content being viewed by others
References
Larsen CT, Pierson FW, Gross WB (1997) Effect of dietary selenium on the response of stressed and unstressed chickens to Escherichia coli challenge and antigen. Biol Trace Elem Res 58(3):169–176
Wuryastuti H, Stowe HD, Bull RW, Miller ER (1993) Effects of vitamin E and selenium on immune responses of peripheral blood, colostrum, and milk leukocytes of sows. J Anim Sci 71(9):2464–2472
Chang WP, Hom JS, Dietert RR, Jr CG, Marsh JA (1994) Effect of dietary vitamin E and selenium deficiency on chicken splenocyte proliferation and cell surface marker expression. Immunopharmacol Immunotoxicol 16(2):203–223
Eskew ML, Scholz RW, Reddy CC, Todhunter DA, Zarkower A (1985) Effects of vitamin E and selenium deficiencies on rat immune function. Immunology 54(1):173–180
Swiatkiewicz S, Arczewska-Wlosek A, Jozefiak D (2015) The relationship between dietary fat sources and immune response in poultry and pigs: an updated review. Livest Sci 180:237–246
Luo J, Huang F, Xiao C, Fang Z, Peng J, Jiang S (2013) Responses of growth performance and Proinflammatory cytokines expression to fish oil supplementation in lactation sows’ and/or weaned piglets’ diets. Biomed Res Int (2013):905–918
Makki K, Froguel P, Wolowczuk I (2013) Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm 2013(5091):139–239
Rocha V, Folco E, Sukhova G, Shimizu K, Gotsman I, Vernon A, Libby P (2008) Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 103(5):467–476
Cancello R, Clément K (2006) Review article: is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. BJOG Int J Obstet Gynaecol 113(10):1141–1147
Kollmorgen GM, Sansing WA, Lehman AA, Fischer G, Longley RE, Jr AS, King MM, Mccay PB (1979) Inhibition of lymphocyte function in rats fed higher-fat diets. Cancer Res 39(9):3458–3462
Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee JS, Goldfine AB, Benoist C, Shoelson S (2009) Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15(15):930–939
Williams JH, Ireland HE (2008) Sensing danger--Hsp72 and HMGB1 as candidate signals. J Leukoc Biol 83(3):489–492
Liu CP, Fu J, Xu FP, Wang XS, Li S (2015) The role of heat shock proteins in oxidative stress damage induced by se deficiency in chicken livers. Biometals 28(1):163–173
Guo Y, Zhao P, Guo G, Hu Z, Tian L, Zhang K, Sun Y, Zhang X, Zhang W, Xing M (2015) Effects of arsenic trioxide exposure on heat shock protein response in the immune organs of chickens. Biol Trace Elem Res 169(1):134–141
Yang Z, Liu C, Zheng W, Teng X, Li S (2016) The functions of antioxidants and heat shock proteins are altered in the immune organs of selenium-deficient broiler chickens. Biol Trace Elem Res 169(2):341–351
Lessard M, Yang WC, Elliott GS, Rebar AH, Van Vleet JF, Deslauriers N, Brisson GJ, Schultz RD (1991) Cellular immune responses in pigs fed a vitamin E- and selenium-deficient diet. J Anim Sci 69(4):1575–1582
Luan Y, Zhao J, Yao H, Zhao X, Fan R, Zhao W, Zhang Z, Xu S (2016) Selenium deficiency influences the mRNA expression of Selenoproteins and cytokines in chicken erythrocytes. Biol Trace Elem Res 171(2):427–436
Zhou X, Wang Z, Chen J, Wang W, Song D, Li S, Yang H, Xue S, Chen C (2014) Increased levels of IL-6, IL-1β, and TNF-α in Kashin-Beck disease and rats induced by T-2 toxin and selenium deficiency. Rheumatol Int 34(7):995–1004
Rowntree JE, Hill GM, Hawkins DR, Link JE, Rincker MJ, Bednar GW, Jr KR (2004) Effect of se on selenoprotein activity and thyroid hormone metabolism in beef and dairy cows and calves. J Anim Sci 82(10):2995–3005
Yao HD, Wu Q, Zhang ZW, Shu L, Wang XL, Lei XG, Xu SW (2013) Selenoprotein W serves as an antioxidant in chicken myoblasts. Biochim Biophys Acta 1830(4):3112–3120
Verma S, Hoffmann FW, Kumar M, Huang Z, Roe K, Nguyenwu E, Hashimoto AS, Hoffmann PR (2011) Selenoprotein K knockout mice exhibit deficient calcium flux in immune cells and impaired immune responses. J Immunol 186(4):2127–2137
Shrimali RK, Irons RD, Carlson BA, Sano Y, Gladyshev VN, Park JM, Hatfield DL (2008) Selenoproteins mediate T cell immunity through an antioxidant mechanism. J Biol Chem 283(29):20181–20185
Bokarewa M, Nagaev I, Dahlberg L, Smith U, Tarkowski A (2005) Resistin, an adipokine with potent proinflammatory properties. J Immunol 174(9):5789–5795
Habich C, Sell H (2015) Heat shock proteins in obesity: links to cardiovascular disease. Horm Mol Biol Clin Invest 21(2):117–124
Elyaman W, Bradshaw EM, Uyttenhove C, Dardalhon V, Awasthi A, Imitola J, Bettelli E, Oukka M, Van SJ, Renauld JC (2009) IL-9 induces differentiation of TH17 cells and enhances function of FoxP3+ natural regulatory T cells. Proc Natl Acad Sci U S A 106(31):12885–12890
Kim MS, Yi JM, Kim SH, Hong SH, Kim HM (2004) Madimadi, Korean folk medicine, blocks TNF-alpha, IL-1beta, and IL-8 production by activated human immune cells. Cytokine 25(4):179–186
Kulkarni AB, Karlsson S (1997) Inflammation and TGF beta 1: lessons from the TGF beta 1 null mouse. Res Immunol 148(7):453–456
Li D, Fu Y, Zhang W, Su G, Liu B, Guo M, Li F, Liang D, Liu Z, Zhang X (2013) Salidroside attenuates inflammatory responses by suppressing nuclear factor-κB and mitogen activated protein kinases activation in lipopolysaccharide-induced mastitis in mice. Inflamm Res 62(1):9–15
Abate A, Oberle S, Schröder H (1998) Lipopolysaccharide-induced expression of cyclooxygenase-2 in mouse macrophages is inhibited by chloromethylketones and a direct inhibitor of NF-kappa B translocation. Prostaglandins Other Lipid Mediators 56(5–6):277–290
Lee YW, Han SH, Lee M, Yang KH, Kim HM, Jeon YJ (2000) 2-amino-3-methylimidazo[4,5-f]quinoline inhibits nitric oxide production in lipopolysaccharide-stimulated RAW 264.7 cells by blocking p38 kinase activation. Cancer Lett 156(2):133–139
Nakamura M, Manser T, Pearson GDN, Daley MJ, Gefter ML (1984) Effect of IFN-|[gamma]| on the immune response in vivo and on gene expression in vitro. Nature 307(5949):381–382
Yu D, Zhang Z, Yao H, Li S, Xu SW (2015) The role of selenoprotein W in inflammatory injury in chicken immune tissues and cultured splenic lymphocyte. Biometals 28(1):75–87
Liu Y, Zhao H, Zhang Q, Tang J, Li K, Xia XJ, Wang KN, Li K, Lei XG (2012) Prolonged dietary selenium deficiency or excess does not globally affect selenoprotein gene expression and/or protein production in various tissues of pigs. J Nutr 142(8):1410–1416
Barnes KM, Evenson JK, Raines AM, Sunde RA (2009) Transcript analysis of the selenoproteome indicates that dietary selenium requirements of rats based on selenium-regulated selenoprotein mRNA levels are uniformly less than those based on glutathione peroxidase activity. J Nutr 139(139):199–206
Yao H, Zhao W, Zhao X, Fan R, Khoso PA, Zhang Z, Liu W, Xu S (2014) Selenium deficiency mainly influences the gene expressions of Antioxidative Selenoproteins in chicken muscles. Biol Trace Elem Res 161(3):318–327
Yao H, Fan R, Zhao X, Zhao W, Liu W, Yang J, Sattar H, Zhao J, Zhang Z, Xu S (2016) Selenoprotein W redox-regulated Ca2+ channels correlate with selenium deficiency-induced muscles Ca2+ leak. Oncotarget 7(36):57618–57632
Yao HD, Wu Q, Zhang ZW, Zhang JL, Li S, Huang JQ, Ren FZ, Xu SW, Wang XL, Lei XG (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of se-deficient chicks. J Nutr 143(5):613–619
Strandberg L, Verdrengh M, Enge M, Andersson N, Amu S, Önnheim aK, Benrick A, Brisslert bM, Bylund J, Bokarewa M (2008) Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS One 4(10):e7605 1-10
Yao H, Liu W, Zhao W, Fan R, Zhao X, Khoso PA, Zhang Z, Xu S (2014) Different responses of selenoproteins to the altered expression of selenoprotein W in chicken myoblasts. RSC Adv 4(109):64032–64042
Jiang ZH, Khoso PA, Yao HD, Zhang ZW, Zhang XY, Xu SW (2015) SelW regulates inflammation-related cytokines in response to H2O2 in se-deficient chicken liver. RSC Adv 5(47):37896–37905
Zhao H, Li K, Tang JY, Zhou JC, Wang KN, Xia XJ, Lei XG (2015) Expression of Selenoprotein genes is affected by obesity of pigs fed a high-fat diet. J Nutr 145(7):1394–1401
Sato-Mito N, Suzui M, Yoshino H, Kaburagi T, Sato K (2009) Long term effects of high fat and sucrose diets on obesity and lymphocyte proliferation in mice. J Nutr Health Aging 13(7):602–606
Yang TS, Zhao ZP, Liu TQ, Zhang ZW, Wang PZ, Xiu SW, Lin GX, Shan AS (2017) Oxidative stress induced by se-deficient high-energy diet implicates neutrophil dysfunction via Nrf2 pathway suppression in swine. Oncotarget 8(8):13428–13439
Zhu Y, Lu X, Wu D, Cai S, Li S, Teng X (2013) The effect of manganese-induced cytotoxicity on mRNA expressions of HSP27, HSP40, HSP60, HSP70 and HSP90 in chicken spleen lymphocytes in vitro. Biol Trace Elem Res 156(1):144–152
Khoso PA, Yang Z, Liu C, Li S (2015) Selenoproteins and heat shock proteins play important roles in immunosuppression in the bursa of Fabricius of chickens with selenium deficiency. Cell Stress Chaperones 20(6):967–978
Jin X, Xu Z, Zhao X, Chen M, Xu S (2017) The antagonistic effect of selenium on lead-induced apoptosis via mitochondrial dynamics pathway in the chicken kidney. Chemosphere 180:259–266
Li X, Xing M, Chen M, Zhao J, Fan R, Zhao X, Cao C, Yang J, Zhang Z, Xu S (2017) Effects of selenium-lead interaction on the gene expression of inflammatory factors and selenoproteins in chicken neutrophils. Ecotoxicol Environ Saf 139:447–453
Reddi AS, Bollineni JS (2001) Selenium-deficient diet induces renal oxidative stress and injury via TGF-beta1 in normal and diabetic rats. Kidney Int 59(4):1342–1353
Sandre C, Agay D, Ducros V, Faure H, Cruz C, Alonso A, Chancerelle Y, Roussel AM (2006) Kinetic changes of oxidative stress and selenium status in plasma and tissues following burn injury in selenium-deficient and selenium-supplemented rats. J Trauma 60(3):627–634
Lanneau D, Brunet M, Frisan E, Solary E, Fontenay M, Garrido C (2008) Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med 12(3):743–761
Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362(9382):469–476
Khoso PA, Liu C, Liu C, Khoso MH, Li S (2016) Selenium deficiency activates heat shock protein expression in chicken spleen and thymus. Biol Trace Elem Res 173(2):1–9
Chen X, Zhu YH, Cheng XY, Zhang ZW, Xu SW (2012) The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules 17(12):14565–14572
Zhao J, Xing H, Liu C, Zhang Z, Xu S (2016) Effect of selenium deficiency on nitric oxide and heat shock proteins in chicken erythrocytes. Biol Trace Elem Res 171(1):1–6
Tu Z, Huang D, Yang J, Ojha R, Xiao Y, Liu R, Du C, Shen N, An H, Yu F (2015) Effect of dyslipidemia on intima-media thickness of intra- and extracranial atherosclerosis by regulating the expression of hsp70 in rabbits. Int J Clin Exp Med 8(4):5446–5453
Uyy E, Ivan L, Boteanu RM, Suica VI, Antohe F (2013) High-fat diet alters protein composition of detergent-resistant membrane microdomains. Cell Tissue Res 354(3):771–781
Acknowledgements
This study was supported by the National Natural Science Foundation of China (Grant No. 31472161) and Heilongjiang Key Laboratory for Laboratory Animals and Comparative Medicine.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All procedures used in the present study were approved by the Institutional Animal Care and Use Committee of Northeast Agricultural University.
ᅟ
Conflict of Interest
The authors declare that they have no conflicts of interest.
Additional information
All authors have read the manuscript and have agreed to submit the manuscript in its current form for consideration for publication in this journal.
Rights and permissions
About this article
Cite this article
Liu, T., Yang, T., Pan, T. et al. Effect of Low-Selenium/High-Fat Diet on Pig Peripheral Blood Lymphocytes: Perspectives from Selenoproteins, Heat Shock Proteins, and Cytokines. Biol Trace Elem Res 183, 102–113 (2018). https://doi.org/10.1007/s12011-017-1122-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-017-1122-z