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Expression of Selenoprotein Genes Is Affected by Heat Stress in IPEC-J2 Cells

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Abstract

The aim of this study was to explore the impacts of heat stress (HS) on expressions of selenoprotein genes in IPEC-J2 cells. Cells were cultured with 5 % CO2-humidified chamber at 37 °C until the cells grew to complete confluence and then exposed to a mild hyperthermia at 41.5 °C (HS) or 37 °C (control) for another 24 h, finally harvested for total RNA or protein extraction. Real-time quantitative PCRs (qPCRs) were performed to compare gene expression of 25 selenoprotein genes, 3 tight junction-related genes, and 10 inflammation-related genes. Protein expressions of heat shock protein 70 (Hsp70) and selenoprotein X and P (SelX and SelP) were also investigated by Western blot. The results showed that HS up-regulated (P < 0.05) Hsp70 and one tight junction-related gene [zonula occludens-1 (Zo-1)] in IPEC-J2 cells. At the same time, HS up-regulated (P < 0.05) 4 selenoprotein genes (Gpx3, Dio2, Selk, Sels) and three inflammation-related genes (Il-6, Icam-1, Tgf-β) and down-regulated (P < 0.05 or as indicated) six selenoprotein genes (Gpx2, Gpx6, Txnrd1, Selh, Selm, Selx) and three inflammation-related genes (Ifn-β, Mcp-1, Tnf-α) in the cells. HS also exhibited impacts on protein expressions, which up-regulated Hsp70, down-regulated SelX, and showed no effect on SelP in IPEC-J2 cells. Our results showed that HS affected the expression of inflammation-related genes and up-regulated gene and protein expressions of Hsp70. The changes of so many selenoprotein genes expression implied a potential link between selenoprotein genes and HS. Moreover, the results provided by this IPEC-J2 model may be used to further study the interactive mechanisms between selenoprotein function and potential intestinal damage induced by HS.

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References

  1. Neimann-Sorensen AT, Derek E (1987) Bioclimatology and the adaptation of livestock. World Anim Sci B5:64–73

    Google Scholar 

  2. Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B et al (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4:1167–1183

    Article  CAS  PubMed  Google Scholar 

  3. Wheelock JB, Rhoads RP, Vanbaale MJ, Sanders SR, Baumgard LH (2010) Effects of heat stress on energetic metabolism in lactating Holstein cows. J Dairy Sci 93:644–655

    Article  CAS  PubMed  Google Scholar 

  4. Baumgard LH, Rhoads RP Jr (2013) Effects of heat stress on postabsorptive metabolism and energetics. Annu Rev Anim Biosci 1:311–337

    Article  PubMed  Google Scholar 

  5. Chand N, Naz S, Khan A, Khan S, Khan RU (2014) Performance traits and immune response of broiler chicks treated with zinc and ascorbic acid supplementation during cyclic heat stress. Int J Biometeorol 58:2153–2157

    Article  PubMed  Google Scholar 

  6. Gao CQ, Zhao YL, Li HC, Sui WG, Yan HC et al (2015) Heat stress inhibits proliferation, promotes growth, and induces apoptosis in cultured Lantang swine skeletal muscle satellite cells. J Zhejiang Univ Sci B 16:549–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. St-Pierre N, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci 86:E52–E77

    Article  Google Scholar 

  8. Pollman D (2010) Seasonal effects on sow herds: Industry experience and management strategies. J Anim Sci 88:9

    Google Scholar 

  9. Lambert G (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci 87:E101–E108

    Article  CAS  PubMed  Google Scholar 

  10. Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE et al (2013) Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8:e70215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tang J, Jiang Y, Tang Y, Chen B, Sun X et al (2013) Effects of propofol on damage of rat intestinal epithelial cells induced by heat stress and lipopolysaccharides. Braz J Med Biol Res 46:507–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gathiram P, Wells M, Brock-Utne J, Gaffin S (1986) Antilipopolysaccharide improves survival in primates subjected to heat stroke. Circ Shock 23:157–164

    Google Scholar 

  13. Gathiram P, Wells M, Brock-Utne J, Gaffin S (1988) Prophylactic corticosteroid increases survival in experimental heat stroke in primates. Aviat Space Environ Med 59:352–355

    CAS  PubMed  Google Scholar 

  14. Habibian M, Ghazi S, Moeini MM (2015) Effects of dietary selenium and vitamin E on growth performance, meat yield, and selenium content and lipid oxidation of breast meat of broilers reared under heat stress. Biol Trace Elem Res. doi:10.1007/s12011-015-0404-6

    Google Scholar 

  15. Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16:705–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Mujahid A, Akiba Y, Toyomizu M (2009) Olive oil-supplemented diet alleviates acute heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am J Physiol Regul Integr Comp Physiol 297:R690–R698

    Article  CAS  PubMed  Google Scholar 

  17. Azad M, Kikusato M, Maekawa T, Shirakawa H, Toyomizu M (2010) Metabolic characteristics and oxidative damage to skeletal muscle in broiler chickens exposed to chronic heat stress. Comp Biochem Physiol A Mol Integr Physiol 155:401–406

    Article  CAS  PubMed  Google Scholar 

  18. Michael T, Sharp A, Klockgether T, Gavrilyuk V, Douglas L (2000) The heat shock response inhibits NF-kappaB activation, nitric oxide synthase type 2 expression, and macrophage/microglial activation in brain. J Cereb Blood Flow Metab 20(5):800–811

    Google Scholar 

  19. Yang L, Tan G-Y, Fu Y-Q, Feng J-H, Zhang M-H (2010) Effects of acute heat stress and subsequent stress removal on function of hepatic mitochondrial respiration, ROS production and lipid peroxidation in broiler chickens. Comp Biochem Physiol Part C: Toxicol Pharmacol 151:204–208

    Google Scholar 

  20. Roman M, Jitaru P, Barbante C (2014) Selenium biochemistry and its role for human health. Metallomics 6:25–54

    Article  CAS  PubMed  Google Scholar 

  21. Liu Y, Zhao H, Zhang Q, Tang J, Li K et al (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 142:1410–1416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhou JC, Zhao H, Li JG, Xia XJ, Wang KN et al (2009) Selenoprotein gene expression in thyroid and pituitary of young pigs is not affected by dietary selenium deficiency or excess. J Nutr 139:1061–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhao H, Li K, Tang JY, Zhou JC, Wang KN et al (2015) Expression of selenoprotein genes is affected by obesity of pigs fed a high-fat diet. J Nutr 145:1394–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Berschneider H (1989) Development of normal cultured small intestinal epithelial cell lines which transport Na and Cl. Gastroenterology 96:A41

    Google Scholar 

  25. Zakrzewski SS, Richter JF, Krug SM, Jebautzke B, Lee IF et al (2013) Improved cell line IPEC-J2, characterized as a model for porcine jejunal epithelium. PLoS One 8, e79643

    Article  PubMed  PubMed Central  Google Scholar 

  26. Paszti-Gere E, Matis G, Farkas O, Kulcsar A, Palocz O et al (2014) The effects of intestinal LPS exposure on inflammatory responses in a porcine enterohepatic co-culture system. Inflammation 37:247–260

    Article  CAS  PubMed  Google Scholar 

  27. Razzuoli E, Villa R, Amadori M (2013) IPEC-J2 cells as reporter system of the anti-inflammatory control actions of interferon-alpha. J Interferon Cytokine Res 33:597–605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Katschinski DM (2004) On heat and cells and proteins. Physiology 19:11–15

    Article  CAS  Google Scholar 

  29. Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710

    Article  CAS  PubMed  Google Scholar 

  30. Mayer M, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA (1992) The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71:97–105

    Article  CAS  PubMed  Google Scholar 

  32. Dieterich A, Troschinski S, Schwarz S, Di Lellis MA, Henneberg A et al (2015) Hsp70 and lipid peroxide levels following heat stress in Xeropicta derbentina (Krynicki 1836) (Gastropoda, Pulmonata) with regard to different colour morphs. Cell Stress Chaperones 20:159–168

    Article  CAS  PubMed  Google Scholar 

  33. Wang X, Yuan B, Dong W, Yang B, Yang Y et al (2014) Induction of heat-shock protein 70 expression by geranylgeranylacetone shows cytoprotective effects in cardiomyocytes of mice under humid heat stress. PLoS One 9, e93536

    Article  PubMed  PubMed Central  Google Scholar 

  34. Chen M, Cai H, Yang JL, Lu CL, Liu T et al (2008) Effect of heat stress on expression of junction-associated molecules and upstream factors androgen receptor and Wilms’ tumor 1 in monkey Sertoli cells. Endocrinology 149:4871–4882

    Article  CAS  PubMed  Google Scholar 

  35. Mailhos C, Howard M, Latchman D (1993) Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 55:621–627

    Article  CAS  PubMed  Google Scholar 

  36. Mosser DD, Martin LH (1992) Induced thermotolerance to apoptosis in a human T lymphocyte cell line. J Cell Physiol 151:561–570

    Article  CAS  PubMed  Google Scholar 

  37. Musch MW, Ciancio M, Sarge K, Chang EB (1996) Induction of heat shock protein 70 protects intestinal epithelial IEC-18 cells from oxidant and thermal injury. Am J Physiol Cell Physiol 270:C429–C436

    CAS  Google Scholar 

  38. Dokladny K, Moseley PL, Ma TY (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290:G204–G212

    Article  CAS  PubMed  Google Scholar 

  39. Koyama H, Omura K, Ejima A, Kasanuma Y, Watanabe C et al (1999) Separation of selenium-containing proteins in human and mouse plasma using tandem high-performance liquid chromatography columns coupled with inductively coupled plasma-mass spectrometry. Anal Biochem 267:84–91

    Article  CAS  PubMed  Google Scholar 

  40. Curran JE, Jowett JB, Elliott KS, Gao Y, Gluschenko K et al (2005) Genetic variation in selenoprotein S influences inflammatory response. Nat Genet 37:1234–1241

    Article  CAS  PubMed  Google Scholar 

  41. Gao Y, Feng HC, Walder K, Bolton K, Sunderland T et al (2004) Regulation of the selenoprotein SelS by glucose deprivation and endoplasmic reticulum stress—SelS is a novel glucose-regulated protein. FEBS Lett 563:185–190

    Article  CAS  PubMed  Google Scholar 

  42. Mittag J, Behrends T, Hoefig CS, Vennström B, Schomburg L (2010) Thyroid hormones regulate selenoprotein expression and selenium status in mice. PLoS One 5, e12931

    Article  PubMed  PubMed Central  Google Scholar 

  43. Schomburg L, Köhrle J (2008) On the importance of selenium and iodine metabolism for thyroid hormone biosynthesis and human health. Mol Nutr Food Res 52:1235–1246

    Article  CAS  PubMed  Google Scholar 

  44. Middleton W (1971) Thyroid hormones and the gut. Gut 12:172–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Muller MJ, Acheson KJ, Jequier E, Burger AG (1988) Effect of thyroid hormones on oxidative and nonoxidative glucose metabolism in humans. Am J Physiol Endocrinol Metabol 255:E146–E152

    CAS  Google Scholar 

  46. de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12:833–845

    PubMed  Google Scholar 

  47. Lu J, Berndt C, Holmgren A (2009) Metabolism of selenium compounds catalyzed by the mammalian selenoprotein thioredoxin reductase. Biochim Et Biophys Acta (BBA)-Gen Subj 1790:1513–1519

    Article  CAS  Google Scholar 

  48. Turanov A, Kehr S, Marino S, Yoo M, Carlson B et al (2010) Mammalian thioredoxin reductase 1: roles in redox homoeostasis and characterization of cellular targets. Biochem J 430:285–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Holmgren A (2000) Antioxidant function of thioredoxin and glutaredoxin systems. Antioxid Redox Signal 2:811–820

    Article  CAS  PubMed  Google Scholar 

  50. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K et al (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal‐regulating kinase (ASK) 1. EMBO J 17:2596–2606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lei XG, Cheng W-H (2005) New roles for an old selenoenzyme: evidence from glutathione peroxidase-1 null and overexpressing mice. J Nutr 135:2295–2298

    CAS  PubMed  Google Scholar 

  52. Lei XG, Cheng W-H, McClung JP (2007) Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nutr 27:41–61

    Article  CAS  PubMed  Google Scholar 

  53. Zhou J, Huang K, Lei XG (2013) Selenium and diabetes—evidence from animal studies. Free Radic Biol Med 65:1548–1556

    Article  CAS  PubMed  Google Scholar 

  54. Burk RF, Hill KE (2009) Selenoprotein P—expression, functions, and roles in mammals. Biochim Et Biophy Acta (BBA) Gen Subj 1790:1441–1447

    Article  CAS  Google Scholar 

  55. Sunde RA, Raines AM, Barnes KM, Evenson JK (2009) Selenium status highly regulates selenoprotein mRNA levels for only a subset of the selenoproteins in the selenoproteome. Biosci Rep 29:329–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Banks WA, Kastin AJ, Gutierrez EG (1994) Penetration of interleukin-6 across the murine blood–brain barrier. Neurosci Lett 179:53–56

    Article  CAS  PubMed  Google Scholar 

  57. Rosette C (2004) Role of ICAM1 in invasion of human breast cancer cells. Carcinogenesis 26:943–950

    Article  Google Scholar 

  58. Hubbard AK, Rothlein R (2000) Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic Biol Med 28:1379–1386

    Article  CAS  PubMed  Google Scholar 

  59. Shi Y, Massagué J (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685–700

    Article  CAS  PubMed  Google Scholar 

  60. Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported partly by the National Natural Science Foundation of China (Nos. 31272468 and 31072043) and by a Research Funding provided by Sichuan Longda Animal Husbandry Science and Technology Co., Ltd (No. 2015SCLD001). We thank Dr Huan Qu in Purdue University for paper correction.

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Authors and Affiliations

  1. Animal Nutrition Institute, Sichuan Agricultural University, No 211 Huimin Road, Chengdu, Sichuan, 611130, China

    Lei Cao, Jiayong Tang, Jingyang Xu, Gang Jia, Guangmang Liu, Xiaoling Chen, Haiying Shang, Jingyi Cai & Hua Zhao

  2. Sichuan Provincial General Station for Animal Husbandry, Chengdu, 610041, China

    Qiang Li

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  1. Lei Cao
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  2. Jiayong Tang
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Lei Cao and Jiayong Tang are co-first authors.

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Cao, L., Tang, J., Li, Q. et al. Expression of Selenoprotein Genes Is Affected by Heat Stress in IPEC-J2 Cells. Biol Trace Elem Res 172, 354–360 (2016). https://doi.org/10.1007/s12011-015-0604-0

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