Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks

Nutritional stimulation of the developing small intestine of chick embryos can be conducted by in-ovo feeding (IOF). We hypothesized that IOF of glutamine and leucine can enhance small intestinal development by promoting proliferation and differentiation of multipotent small intestinal epithelial ce...

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Main Authors: Naama Reicher, Tal Melkman-Zehavi, Jonathan Dayan, Eric A. Wong, Zehava Uni
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2022-03-01
Series:Animal Nutrition
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405654521001566
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author Naama Reicher
Tal Melkman-Zehavi
Jonathan Dayan
Eric A. Wong
Zehava Uni
author_facet Naama Reicher
Tal Melkman-Zehavi
Jonathan Dayan
Eric A. Wong
Zehava Uni
author_sort Naama Reicher
collection DOAJ
description Nutritional stimulation of the developing small intestine of chick embryos can be conducted by in-ovo feeding (IOF). We hypothesized that IOF of glutamine and leucine can enhance small intestinal development by promoting proliferation and differentiation of multipotent small intestinal epithelial cells. Broiler embryos (n = 128) were subject to IOF of glutamine (IOF-Gln), leucine (IOF-Leu), NaCl (IOF-NaCl) or no injection (control) at embryonic d 17 (E 17). Multipotent, progenitor and differentiated cells were located and quantified in the small intestinal epithelium between E 17 and d 7 after hatch (D 7) in all treatment groups by immunofluorescence of SRY-box transcription factor 9 (Sox9) and proliferating cell nuclear antigen (PCNA), in-situ hybridization of leucine-rich repeat containing G-protein coupled receptor 5 (Lgr5) and peptide transporter 1 (PepT1) and histochemical goblet cell staining. The effects of IOF treatments at E 19 (48 h post-IOF), in comparison to control embryos, were as follows: total cell counts increased by 40%, 33% and 19%, and multipotent cell counts increased by 52%, 50% and 38%, in IOF-Gln, IOF-Leu and IOF-NaCl embryos, respectively. Only IOF-Gln embryos exhibited a significance, 36% increase in progenitor cell counts. All IOF treatments shifted Lgr5+ stem cell localizations to villus bottoms. The differentiated, PepT1+ region of the villi was 1.9 and 1.3-fold longer in IOF-Gln and IOF-Leu embryos, respectively, while goblet cell densities decreased by 20% in IOF-Gln embryos. Post–hatch, crypt and villi epithelial cell counts were significantly higher IOF-Gln chicks, compared to control chicks (P < 0.05). We conclude IOF of glutamine stimulates small intestinal maturation and functionality during the peri-hatch period by promoting multipotent cell proliferation and differentiation, resulting in enhanced compartmentalization of multipotent and differentiated cell niches and expansions of the absorptive surface area.
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spelling doaj.art-ad72269bc6954667bc4dfd6539f39a802022-12-22T03:13:56ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452022-03-01891101Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicksNaama Reicher0Tal Melkman-Zehavi1Jonathan Dayan2Eric A. Wong3Zehava Uni4Department of Animal Science, The Robert H. Smith, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, IsraelDepartment of Animal Science, The Robert H. Smith, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, IsraelDepartment of Animal Science, The Robert H. Smith, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, IsraelDepartment of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA 24061, USADepartment of Animal Science, The Robert H. Smith, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel; Corresponding author.Nutritional stimulation of the developing small intestine of chick embryos can be conducted by in-ovo feeding (IOF). We hypothesized that IOF of glutamine and leucine can enhance small intestinal development by promoting proliferation and differentiation of multipotent small intestinal epithelial cells. Broiler embryos (n = 128) were subject to IOF of glutamine (IOF-Gln), leucine (IOF-Leu), NaCl (IOF-NaCl) or no injection (control) at embryonic d 17 (E 17). Multipotent, progenitor and differentiated cells were located and quantified in the small intestinal epithelium between E 17 and d 7 after hatch (D 7) in all treatment groups by immunofluorescence of SRY-box transcription factor 9 (Sox9) and proliferating cell nuclear antigen (PCNA), in-situ hybridization of leucine-rich repeat containing G-protein coupled receptor 5 (Lgr5) and peptide transporter 1 (PepT1) and histochemical goblet cell staining. The effects of IOF treatments at E 19 (48 h post-IOF), in comparison to control embryos, were as follows: total cell counts increased by 40%, 33% and 19%, and multipotent cell counts increased by 52%, 50% and 38%, in IOF-Gln, IOF-Leu and IOF-NaCl embryos, respectively. Only IOF-Gln embryos exhibited a significance, 36% increase in progenitor cell counts. All IOF treatments shifted Lgr5+ stem cell localizations to villus bottoms. The differentiated, PepT1+ region of the villi was 1.9 and 1.3-fold longer in IOF-Gln and IOF-Leu embryos, respectively, while goblet cell densities decreased by 20% in IOF-Gln embryos. Post–hatch, crypt and villi epithelial cell counts were significantly higher IOF-Gln chicks, compared to control chicks (P < 0.05). We conclude IOF of glutamine stimulates small intestinal maturation and functionality during the peri-hatch period by promoting multipotent cell proliferation and differentiation, resulting in enhanced compartmentalization of multipotent and differentiated cell niches and expansions of the absorptive surface area.http://www.sciencedirect.com/science/article/pii/S2405654521001566ChickIntestinal developmentProliferationDifferentiationMultipotent cellIn-ovo feeding
spellingShingle Naama Reicher
Tal Melkman-Zehavi
Jonathan Dayan
Eric A. Wong
Zehava Uni
Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
Animal Nutrition
Chick
Intestinal development
Proliferation
Differentiation
Multipotent cell
In-ovo feeding
title Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
title_full Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
title_fullStr Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
title_full_unstemmed Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
title_short Nutritional stimulation by in-ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
title_sort nutritional stimulation by in ovo feeding modulates cellular proliferation and differentiation in the small intestinal epithelium of chicks
topic Chick
Intestinal development
Proliferation
Differentiation
Multipotent cell
In-ovo feeding
url http://www.sciencedirect.com/science/article/pii/S2405654521001566
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