Skip to main content
SpringerLink
Log in

Selenide Chitosan Sulfate Improved the Hepatocyte Activity, Growth Performance, and Anti-oxidation Capacity by Activating the Thioredoxin Reductase of Chickens In Vitro and In Vivo

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Chicken hepatocytes were cultured in vitro and 240 specific pathogen-free (SPF) white leghorns chickens (7 days old) were obtained. The hepatocytes and chickens were randomly allocated to one of six treatment groups: control group; chitosan (COS) group; sodium selenite (Na2SeO3) group; selenide chitosan (COS-Se) group; chitosan sulfate (LS-COS) group; and selenide chitosan sulfate (LS-COS-Se) group. Our results showed that LS-COS-Se increased (P < 0.05) the activities of thioredoxin reductase (TXNRD), anti-superoxide anion radical (antiO2−), and superoxide dismutase (SOD), the mRNA levels of thioredoxin reductase 1 (TXNRD1) and thioredoxin reductase 3 (TXNRD3), and the chicken body weight, but reduced (P < 0.05) the malondialdehyde (MDA) content and the lactate dehydrogenase (LDH) activity. Compared with COS and LS-COS, the LS-COS-Se treatment increased (P < 0.05) the activities of TXNRD, SOD, catalase (CAT), and the mRNA levels of TXNRD1 and TXNRD3, but reduced (P < 0.05) the MDA content in vitro, whereas, in vivo, it increased (P < 0.05) body weight on day 28; the activities of TXNRD, antiO2−, and SOD; and the mRNA levels of TXNRD1 and TXNRD3. Compared with Na2SeO3 and COS-Se, the LS-COS-Se treatment increased (P < 0.05) the TXNRD and SOD activities, the mRNA levels of TXNRD1 and TXNRD3 in vitro, increased (P < 0.05) the chicken body weight on day 28, and the TXNRD, antiO2−, and SOD activities, but reduced (P < 0.05) the MDA content. These results indicated that LS-COS-Se was a useful antioxidant that improved hepatocyte activity, growth performance, and anti-oxidation capacity in hepatocytes (in vitro) and SPF chicken (in vivo) by activating the TXNRD system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  1. Liu L, Wu C, Chen D, Yu B, Huang Z, Luo Y, Zheng P, Mao X, Yu J, Luo J, Yan H, He J (2020) Selenium-enriched yeast alleviates oxidative stress-induced intestinal mucosa disruption in weaned pigs. Oxid Med Cell Longev 2020:5490743. https://doi.org/10.1152/ajpheart.00097.2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hosnedlova B, Kepinska M, Skalickova S, Fernandez C, Nedecky BR, Malevu TD, Sochor J, Baron M, Melcova M, Zidkova J, Kizek R (2017) A summary of new findings on the biological effects of selenium in selected animal species-a critical review. Int J Mol Sci 18(10):2209.2209. https://doi.org/10.3390/ijms18102209

    Article  CAS  Google Scholar 

  3. Rayman MP (2000) The importance of selenium to human health. Lancet 356(9225):233–241. https://doi.org/10.1016/S0140-6736(00)02490-9

    Article  CAS  PubMed  Google Scholar 

  4. Méplan C, Hughes DJ (2020) The role of selenium in health and disease: emerging and recurring trends. Nutrients 12(4):1049. https://doi.org/10.3390/nu12041049

    Article  CAS  PubMed Central  Google Scholar 

  5. Zhang L, Wang YX, Zhou Y, Zheng L, Zhan XA, Pu QH (2014) Different sources of maternal selenium affect selenium retention, antioxidant status, and meat quality of 56-day-old offspring of broiler breeders. Poult Sci 93(9):2210–2219. https://doi.org/10.3382/ps.2013-03605

    Article  CAS  PubMed  Google Scholar 

  6. Zhang S, Xie Y, Li M, Yang H, Li S, Li J, Xu Q, Yang W, Jiang S (2020) Effects of different selenium sources on meat quality and shelf life of fattening pigs. Animals (Basel) 10(4):615. https://doi.org/10.3390/ani10040615

    Article  CAS  Google Scholar 

  7. Yin S, Wang C, Wei J, Wang D, Jin L, Liu J, Wang L, Li Z, Ren A, Yin C (2020) Essential trace elements in placental tissue and risk for fetal neural tube defects. Environ Int 139:105688. https://doi.org/10.1016/j.envint.2020.105688

    Article  CAS  PubMed  Google Scholar 

  8. Rao S, Lin Y, Du Y, He L, Huang G, Chen B, Chen T (2019) Designing multifunctionalized selenium nanoparticles to reverse oxidative stress-induced spinal cord injury by attenuating ROS overproduction and mitochondria dysfunction. J Mater Chem B 7(16):2648–2656. https://doi.org/10.1039/c8tb02520g

    Article  CAS  PubMed  Google Scholar 

  9. Yi HW, Zhu XX, Huang XL, Lai YZ, Tang Y (2020) Selenium-enriched Bifidobacterium longum protected alcohol and high fat diet induced hepatic injury in mice. Chin J Nat Med 18(3):169–177. https://doi.org/10.1016/S1875-5364(20)30018-2

    Article  CAS  PubMed  Google Scholar 

  10. Wu M, Li J, An Y, Li P, Xiong W, Li J, Yan D, Wang M, Zhong G (2019) Chitooligosaccharides prevents the development of colitis-associated colorectal cancer by modulating the intestinal microbiota and mycobiota. Front Microbiol 10:2101. https://doi.org/10.3389/fmicb.2019.02101

    Article  PubMed  PubMed Central  Google Scholar 

  11. Guan G, Azad MAK, Lin Y, Kim SW, Tian Y, Liu G, Wang H (2019) Biological effects and applications of chitosan and chito-oligosaccharides. Front Physiol 10:516. https://doi.org/10.3389/fphys.2019.00516

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sánchez Á, Mengíbar M, Fernández M, Alemany S, Heras A, Acosta N (2018) Influence of preparation methods of chitooligosaccharides on their physicochemical properties and their anti-inflammatory effects in mice and in RAW264.7 macrophages. Mar Drugs 16(11):430. https://doi.org/10.3390/md16110430

    Article  CAS  PubMed Central  Google Scholar 

  13. Dai X, Hou W, Sun Y, Gao Z, Zhu S, Jiang Z (2015) Chitosan oligosaccharides inhibit/disaggregate fibrils and attenuate amyloid β-mediated neurotoxicity. Int J Mol Sci 16(5):10526–10536. https://doi.org/10.3390/ijms160510526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Marmouzi I, Ezzat SM, Salama MM, Merghany RM, Attar AM, El-Desoky AM, Mohamed SO (2019) Recent updates in pharmacological properties of chitooligosaccharides. Biomed Res Int 2019:4568039. https://doi.org/10.1155/2019/4568039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Qin S, Huang B, Ma J, Wang X, Zhang J, Li L, Chen F (2015) Effects of selenium-chitosan on blood selenium concentration, antioxidation status, and cellular and humoral immunity in mice. Biol Trace Elem Res 165(2):145–152. https://doi.org/10.1007/s12011-015-0243-5

    Article  CAS  PubMed  Google Scholar 

  16. Li J, Cheng Y, Chen Y, Qu H, Zhao Y, Wen C, Zhou Y (2019) Dietary chitooligosaccharide inclusion as an alternative to antibiotics improves intestinal morphology, barrier function, antioxidant capacity, and immunity of broilers at early age. Animals (Basel) 9(8):493. https://doi.org/10.3390/ani9080493

    Article  Google Scholar 

  17. Saccoccia F, Angelucci F, Boumis G, Carotti D, Desiato G, Miele AE, Bellelli A (2014) Thioredoxin reductase and its inhibitors. Curr Protein Pept Sci 15(6):621–646. https://doi.org/10.2174/1389203715666140530091910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wu X, Huang K, Wei C, Chen F, Pan C (2010) Regulation of cellular glutathione peroxidase by different forms and concentrations of selenium in primary cultured bovine hepatocytes. J Nutr Biochem 21(2):153–161. https://doi.org/10.1016/j.jnutbio.2008.12.006

    Article  CAS  PubMed  Google Scholar 

  19. Chen F, Zhu L, Qiu H, Qin S (2017) Selenium-enriched Saccharomyces cerevisiae improves growth, antioxidant status and selenoprotein gene expression in Arbor Acres broilers. J Anim Physiol Anim Nutr (Berl) 101(2):259–266. https://doi.org/10.1111/jpn.12571

    Article  CAS  Google Scholar 

  20. Wang G, Zhang J, Dewilde AH, Pal AK, Bello D, Therrien JM, Braunhut SJ, Marx KA (2012) Understanding and correcting for carbon nanotube interferences with a commercial LDH cytotoxicity assay. Toxicology 299(2–3):99–111. https://doi.org/10.1016/j.tox.2012.05.012

    Article  CAS  PubMed  Google Scholar 

  21. Li R, Jia Z, Trush MA (2016) Defining ROS in biology and medicine. React Oxyg Species (Apex) 1(1):9–21. https://doi.org/10.20455/ros.2016.803

    Article  Google Scholar 

  22. Bai K, Hong B, Huang W, He J (2020) Selenium-nanoparticles-loaded chitosan/chitooligosaccharide microparticles and their antioxidant potential: a chemical and in vivo investigation. Pharmaceutics 12(1):43. https://doi.org/10.3390/pharmaceutics12010043

    Article  CAS  PubMed Central  Google Scholar 

  23. Stealey S, Guo X, Majewski R, Dyble A, Lehman K, Wedemeyer M, Steeber DA, Kaltchev MG, Chen J, Zhang W (2020) Calcium-oligochitosan-pectin microcarrier for colonic drug delivery. Pharm Dev Technol 25(2):260–265. https://doi.org/10.1080/10837450.2019.1691591

    Article  CAS  PubMed  Google Scholar 

  24. Bai K, Hong B, He J, Hong Z, Tan R (2017) Preparation and antiOxidant properties of selenium nanoparticles-loaded chitosan microspheres. Int J Nanomedicine 12:4527–4539. https://doi.org/10.2147/IJN.S129958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Liu X, Chen T, Hu Y, Li K, Yan L (2014) Catalytic synthesis and antioxidant activity of sulfated polysaccharide from Momordica charantia L. Biopolymers 101:210–215. https://doi.org/10.2147/IJN.S129958

    Article  CAS  PubMed  Google Scholar 

  26. Deng C, Xu J, Fu H, Chen J, Xu X (2015) Characterization, antioxidant and cytotoxic activity of sulfated derivatives of a water-insoluble polysaccharides from Dictyophora indusiata. Mol Med Rep 11(4):2991–2998. https://doi.org/10.3892/mmr.2014.3060

    Article  CAS  PubMed  Google Scholar 

  27. Wang T, Zhou Y, Xie W, Chen L, Zheng H, Fan L (2012) Preparation and anticoagulant activity of N-succinyl chitosan sulfates. Int J Biol Macromol 51(5):808–814. https://doi.org/10.1016/j.ijbiomac.2012.07.029

    Article  CAS  PubMed  Google Scholar 

  28. Zoidis E, Seremelis I, Kontopoulos N, Danezis GP (2018) Selenium-dependent antioxidant enzymes: actions and properties of selenoproteins. AntiOxidants (Basel) 7(5):66. https://doi.org/10.3390/antiOx7050066

    Article  Google Scholar 

  29. Tinggi U (2018) Selenium: its role as antioxidant in human health. Environ Health Prev Med 13(2):102–108. https://doi.org/10.1007/s12199-007-0019-4

    Article  CAS  Google Scholar 

  30. Surai PF, Kochish II (2019) Nutritional modulation of the antioxidant capacities in poultry: the case of selenium. Poult Sci 98(10):4231–4239. https://doi.org/10.3382/ps/pey406

    Article  CAS  PubMed  Google Scholar 

  31. Peng D, Zhang J, Liu Q (2007) Effect of sodium selenosulfate on restoring activities of selenium-dependent enzymes and selenium retention compared with sodium selenite in vitro and in vivo. Biol Trace Elem Res 117(1–3):77–88. https://doi.org/10.1007/BF02698085

    Article  CAS  PubMed  Google Scholar 

  32. Liu Y, Yu F, Zhang B, Zhou M, Bei Y, Zhang Y, Liang Q, Liu Y (2019) Improving the protective effects of aFGF for peripheral nerve injury repair using sulfated chitooligosaccharides. Asian J Pharm Sci 14(5):511–520. https://doi.org/10.1016/j.ajps.2018.09.007

    Article  PubMed  Google Scholar 

  33. Battin EE, Brumaghim JL (2009) Antioxidant activity of sulfur and selenium: a review of reactive oxygen species scavenging, glutathione peroxidase, and metal-binding antioxidant mechanisms. Cell Biochem Biophys 55(1):1–23. https://doi.org/10.1007/s12013-009-9054-7

    Article  CAS  PubMed  Google Scholar 

  34. Chen F, Hou L, Zhu L, Yang C, Zhu F, Qiu H, Qin S (2020) Effects of selenide chitosan sulfate on glutathione system in hepatocytes and specific pathogen-free chickens. Poult Sci 99(8):3979–3986. https://doi.org/10.1016/j.psj.2020.04.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Guo Y, Yan S, Gong J, Jin L, Shi B (2018) The protective effect of selenium on bovine mammary epithelial cell injury caused by depression of thioredoxin reductase. Biol Trace Elem Res 184(1):75–82. https://doi.org/10.1007/s12011-017-1175-z

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Shandong Major Scientific and Technological Innovation Project (2019JZZY020611), Chinese National Natural Science Foundation (31001093), and Shandong Modern Agricultural Industry Technology System Poultry Innovation Team Projects (SDAIT-11–07).

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Qingdao Agricultural University, Qingdao, 266109, China

    Lele Hou, Lianqin Zhu, Shansong Gao & Fu Chen

  2. Haidu College, Qingdao Agricultural University, Laiyang, 265200, China

    Huiling Qiu

Authors
  1. Lele Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huiling Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lianqin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shansong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors’ contributions are as follows: L.H. designed the study and discussed the results and wrote the paper; H.Q. contributed to the cell and animal experiment; L.Z. contributed to interpretation of findings; S.G. contributed to reviewing of the manuscript; F.C. was the principal investigator and in charge of the whole trial. All authors read and approved the final version of the manuscript. We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.

Corresponding author

Correspondence to Fu Chen.

Ethics declarations

Ethics Approval and Consent to Participate

All animal protocols used in this study were in accordance with the Guidelines for the Care and Use of Animals for Research and Teaching and approved by the Animal Care and Use Committee of Qingdao Agricultural University.

Consent for Publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hou, L., Qiu, H., Zhu, L. et al. Selenide Chitosan Sulfate Improved the Hepatocyte Activity, Growth Performance, and Anti-oxidation Capacity by Activating the Thioredoxin Reductase of Chickens In Vitro and In Vivo. Biol Trace Elem Res 200, 3798–3807 (2022). https://doi.org/10.1007/s12011-021-02962-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02962-1

Keywords

Search

Navigation