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Effect of In Ovo Trace Element Supplementation on Immune-Related Cells of the Small Intestine of Post-hatched Broiler Chicken

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Abstract

Pathological conditions and harmful drugs cause many gastrointestinal diseases in broiler chicken. The current study was conducted to investigate the effect of trace elements zinc (Zn) and selenium (Se) supplementation on histomorphology, immunological role, and functional activity of goblet cells (GCs) of the small intestine. The Alcian blue-periodic acid-Schiff (AB-PAS) was performed to assess the histomorphological changes in GCs, which revealed the regular dispersion with high electron density of GCs throughout the mucosal surface in the supplemented group. However, irregular dispersion with low electron density of GCs was present in the control group. The immunological functional role of GCs within the small intestine was examined by mucicarmine staining, immunohistochemistry, and immunofluorescence. The results showed a high mucin glycol protein secretion in the supplemented group, whereas limited mucin glycol protein secretion in the control group. Furthermore, the biological significance showed a high and low immunoreactivity of Muc2 and Muc13 in the supplemented and control groups, respectively. Immunofluorescence was used to confirm the immunosignaling of Muc2. Results revealed high immunosignaling of Muc2 at the apical part of the small intestine in the supplementation group, while low immunosignaling of Muc2 in the control group. Results suggest that trace element supplementation had significant effect on morphology and immunological role of GCs, which might be essential for immune function and health status of broiler chicken.

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Data Availability

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

References

  1. Juul-Madsen H, Su G, Sørensen P (2004) Influence of early or late start of first feeding on growth and immune phenotype of broilers. Br Poult Sci 45(2):210–222

    Article  CAS  PubMed  Google Scholar 

  2. Uni Z, Ferket P, Tako E, Kedar O (2005) In ovo feeding improves energy status of late-term chicken embryos. Poult Sci 84(5):764–770

    Article  CAS  PubMed  Google Scholar 

  3. Ohta Y, Tsushima N, Koide K, Kidd M, Ishibashi T (1999) Effect of amino acid injection in broiler breeder eggs on embryonic growth and hatchability of chicks. Poult Sci 78(11):1493–1498

    Article  CAS  PubMed  Google Scholar 

  4. Bhanja S, Mandal A (2005) Effect of in ovo injection of critical amino acids on pre-and post-hatch growth, immunocompetence and development of digestive organs in broiler chickens. Asian Australas J Anim Sci 18(4):524–531

    Article  Google Scholar 

  5. Jha R, Singh AK, Yadav S, Berrocoso JFD, Mishra B (2019) Early nutrition programming (in ovo and post-hatch feeding) as a strategy to modulate gut health of poultry. Front Vet Sci 6:82. https://doi.org/10.3389/fvets.2019.00082

  6. Sawosz F, Pineda L, Hotowy A, Hyttel P, Sawosz E, Szmidt M, Niemiec T, Chwalibog A (2012) Nano-nutrition of chicken embryos The effect of silver nanoparticles and glutamine on molecular responses and the morphology of pectoral muscle. Baltic J Comp Clin Syst Biol 2:29–45

    Google Scholar 

  7. Josuha P, Valli C, Balakrishnan V (2016) Effect of in ovo supplementation of nano forms of zinc, copper, and selenium on post-hatch performance of broiler chicken. Vet, World 9(3):287–294

    Article  Google Scholar 

  8. Bartlett J, Smith M (2003) Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poult Sci 82(10):1580–1588

    Article  CAS  PubMed  Google Scholar 

  9. Sunder GS, Panda A, Gopinath N, Rao SR, Raju M, Reddy M, Kumar CV (2008) Effects of higher levels of zinc supplementation on performance, mineral availability, and immune competence in broiler chickens. J Appl Poultry Res 17(1):79–86

    Article  CAS  Google Scholar 

  10. Surai P (2002) Selenium in poultry nutrition 2. Reprod, Egg Meat Qual Pract Appl, World’s Poultry Sci J 58(4):431–450

    Article  Google Scholar 

  11. Dharmani P, Srivastava V, Kissoon-Singh V, Chadee K (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 1(2):123–135

    Article  CAS  PubMed  Google Scholar 

  12. Herbert DBR, Yang J-Q, Hogan SP, Groschwitz K, Khodoun M, Munitz A, Orekov T, Perkins C, Wang Q, Brombacher F (2009) Intestinal epithelial cell secretion of RELM-β protects against gastrointestinal worm infection. J Exp Med 206(13):2947–2957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Johansson ME, Thomsson KA, Hansson GC (2009) Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein. J Proteome Res 8(7):3549–3557

    Article  CAS  PubMed  Google Scholar 

  14. Taupin D, Podolsky DK (2003) Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4(9):721–732

    Article  CAS  PubMed  Google Scholar 

  15. Guy JS (1998) Virus infections of the gastrointestinal tract of poultry. Poult Sci 77(8):1166–1175

    Article  CAS  PubMed  Google Scholar 

  16. Yegani M, Korver D (2008) Factors affecting intestinal health in poultry. Poult Sci 87(10):2052–2063

    Article  CAS  PubMed  Google Scholar 

  17. Contreras-Ruiz L, Ghosh-Mitra A, Shatos MA, Dartt DA, Masli S (2013) Modulation of conjunctival goblet cell function by inflammatory cytokines. Mediators of Inflamm 2013:636812. https://doi.org/10.1155/2013/636812

  18. Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12(5):319–330

    Article  PubMed  PubMed Central  Google Scholar 

  19. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G (2009) Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 15(1):100–113

    Article  PubMed  Google Scholar 

  20. Bhanja S, Mandal A, Johri T (2004) Standardization of injection site, needle length, embryonic age and concentration of amino acids for in ovo injection in broiler breeder eggs. Indian J Poult Sci 39(2):105–111

    Google Scholar 

  21. Tahmasebi S, Toghyani M (2016) Effect of arginine and threonine administered in ovo on digestive organ developments and subsequent growth performance of broiler chickens. J Anim Physiol Anim Nutr (Berl) 100(5):947–956

    Article  CAS  PubMed  Google Scholar 

  22. Luna LG (1968) Manual of histologic staining methods of the Armed Forces Institute of Pathology. In Manual of histologic staining methods of the Armed Forces Institute of Pathology. Google Scholar,  pp xii–258

  23. Osho SO, Wang T, Horn NL, Adeola O (2017) Comparison of goblet cell staining methods in jejunal mucosa of turkey poults. Poult Sci 96:556–59

  24. Hedman HD, Vasco KA, Zhang L (2020) A review of antimicrobial resistance in poultry farming within low-resource settings. Animals 10(8):1264. https://doi.org/10.3390/ani10081264

  25. Bergstrom KS, Kissoon-Singh V, Gibson DL, Ma C, Montero M, Sham HP, Ryz N, Huang T, Velcich A, Finlay BB (2010) Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog 6(5):e1000902

    Article  PubMed  PubMed Central  Google Scholar 

  26. Koninkx J, Mirck M, Hendriks H, Mouwen J, Van Dijk J (1988) Nippostrongylus brasiliensis histochemical changes in the composition of mucins in goblet cells during infection in rats. Exp Parasitol 65(1):84–90

    Article  CAS  PubMed  Google Scholar 

  27. Smirnova MG, Guo L, Birchall JP, Pearson JP (2003) LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol 221(1):42–49

    Article  CAS  PubMed  Google Scholar 

  28. Cornick S, Tawiah A, Chadee K (2015) Roles and regulation of the mucus barrier in the gut. Tissue barriers 3(1–2):e982426

    Article  PubMed  PubMed Central  Google Scholar 

  29. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458(7242):1131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol-Gastrointestinal Liver Physiol 280(5):922–929

    Article  Google Scholar 

  31. Maares M, Keil C, Koza J, Straubing S, Schwerdtle T, Haase H (2018) In vitro studies on zinc binding and buffering by intestinal mucins. Int J Mol Sci 19(9):2662. https://doi.org/10.3390/ijms19092662

  32. Abbasi-Oshaghi E, Mirzaei F, Mirzaei A (2018) Effects of ZnO nanoparticles on intestinal function and structure in normal/high fat diet-fed rats and Caco-2 cells. Nanomedicine (Lond) 13(21):2791–2816

    Article  CAS  PubMed  Google Scholar 

  33. Zhang S, Cheng S, Jiang X, Zhang J, Bai L, Qin X, Zou Z, Chen C (2020) Gut-brain communication in hyperfunction of 5-hydroxytryptamine induced by oral zinc oxide nanoparticles exposure in young mice. Food Chem Toxicol : an Intl J Published Bri Ind Biol Res Assoc 135:110906

    Article  CAS  Google Scholar 

  34. Maares M, Keil C, Straubing S, Robbe-Masselot C, Haase H (2020) Zinc deficiency disturbs mucin expression, O-glycosylation and secretion by intestinal goblet cells. Int J Mol Sci 21(17):6149. https://doi.org/10.3390/ijms21176149

  35. Hafez A, Nassef E, Fahmy M, Elsabagh M (2020) Impact Diet Nano-zinc Oxide On Immune Response Antioxid Def Broiler Chickens 27(16):19108–19114

    CAS  Google Scholar 

  36. Khajeh Bami M, Afsharmanesh M, Espahbodi M, Esmaeilzadeh E (2022) Effects of dietary nano-selenium supplementation on broiler chicken performance meat selenium content, intestinal microflora intestinal morphology and immune response. J Trace Elem Med Biol : Organ Soc Minerals Trace Elem (GMS) 69:126897

    Article  CAS  Google Scholar 

  37. Chen Y, Wu W, Zhou H, Liu X, Li S, Guo Y, Li Y, Wang Y, Yuan J (2022) Selenium nanoparticles improved intestinal health through modulation of the NLRP3 signaling pathway. Front Nutr 9:907386

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gupta BK, Maher DM, Ebeling MC, Stephenson PD, Puumala SE, Koch MR, Aburatani H, Jaggi M, Chauhan SC (2014) Functions and regulation of MUC13 mucin in colon cancer cells. J Gastroenterol 49(10):1378–1391

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Firstly, the authors are thankful to the Central Animal House (CAH) section of Advanced Biological and Animal Research, DUHS, OJHA Campus Karachi, Pakistan, for the great support in data analysis and research sample processing. Additionally, the authors are very grateful to Professor Juan Liu, College of Veterinary Medicine, Southwest University, Chongqing, China, for technical assistance throughout all aspects of our study and for their help in writing the manuscript.

Funding

This work was financially supported by funds from the Pakistan Science Foundation (PSF) Islamabad under the project title “Investigate the effect of in ovo feeding of amino acids and trace elements on immunity and production performance of post-hatch broiler chicken” (award no.: PSF/NSLP/B-LUAWMS (763)).

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  1. Fazul Nabi and Muhammad Asif Arain contribute equally.

Authors and Affiliations

  1. Faculty of Veterinary and Animal Sciences, Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan, Pakistan

    Fazul Nabi, Muhammad Asif Arain & Sarfaraz Ali Fazlani

  2. Department of Traditional Chinese Veterinary Medicine, College of Veterinary Medicine, Southwest University, Chongqing, 402460, China

    Fazul Nabi & Juan Liu

  3. Department of Livestock Management, Sindh Agriculture University, Tandojam, Pakistan

    Mariyam Khalid

  4. Center of Advanced Studies in Vaccinology and Biotechnology (CASVAB), University of Balochistan, Quetta, Pakistan

    Firdous Bugti

  5. Dow Institute for Advanced Biological and Animal Research, Dow University of Health Sciences, Ojha Campus, Karachi, Pakistan

    Sikandar Ali & Syed Khurram Fareed

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  1. Fazul Nabi
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Contributions

F.N. wrote the manuscript text and M.A.A., S.A.F., and M.K. prepared all figures and F.B., S.A., S.K.F., and J.L. reviewed the manuscript.

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Correspondence to Fazul Nabi or Juan Liu.

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Nabi, F., Arain, M.A., Fazlani, S.A. et al. Effect of In Ovo Trace Element Supplementation on Immune-Related Cells of the Small Intestine of Post-hatched Broiler Chicken. Biol Trace Elem Res 201, 4052–4061 (2023). https://doi.org/10.1007/s12011-022-03492-0

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