Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens

Broiler chickens are highly sensitive to high ambient temperatures due to their feathers, lack of skin sweat glands, and high productivity. Heat stress (HS) is a major concern for the poultry industry because it negatively affects growth as well as immune functions, which increase the potential risk...

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Main Authors: Ryota Hirakawa, Siti Nurjanah, Kyohei Furukawa, Atsushi Murai, Motoi Kikusato, Tomonori Nochi, Masaaki Toyomizu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fvets.2020.00046/full
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author Ryota Hirakawa
Ryota Hirakawa
Siti Nurjanah
Siti Nurjanah
Kyohei Furukawa
Kyohei Furukawa
Atsushi Murai
Motoi Kikusato
Motoi Kikusato
Tomonori Nochi
Tomonori Nochi
Tomonori Nochi
Masaaki Toyomizu
Masaaki Toyomizu
author_facet Ryota Hirakawa
Ryota Hirakawa
Siti Nurjanah
Siti Nurjanah
Kyohei Furukawa
Kyohei Furukawa
Atsushi Murai
Motoi Kikusato
Motoi Kikusato
Tomonori Nochi
Tomonori Nochi
Tomonori Nochi
Masaaki Toyomizu
Masaaki Toyomizu
author_sort Ryota Hirakawa
collection DOAJ
description Broiler chickens are highly sensitive to high ambient temperatures due to their feathers, lack of skin sweat glands, and high productivity. Heat stress (HS) is a major concern for the poultry industry because it negatively affects growth as well as immune functions, which increase the potential risk of infectious disease outbreaks. Therefore, it is vital to elucidate HS's effect on the avian immune system, especially considering the global rise in average surface temperature. Our study identified a series of immunological disorders in heat-stressed broiler chickens. We exposed 22-day-old broiler chickens to a continuous HS condition (34.5 ± 0.5°C) for 14 days and immunized them with a prototype bovine serum albumin (BSA) antigen. The plasma and lymphoid tissues (thymus, bursa of Fabricius, and spleen) were harvested at the end of the experiments to investigate the induction of BSA-specific immune responses. Our results revealed that plasma titers of immunoglobulin (Ig)Y, IgM, and IgA antibodies specific for BSA were lower than those of thermoneutral chickens immunized with BSA. Furthermore, the spleens of the heat-stressed broiler chickens displayed severe depression of Bu1+ B cells and CD3+ T cells, including CD4+ T cells and CD8+ T cells, and lacked a fully developed germinal center (GC), which is crucial for B cell proliferation. These immunological abnormalities might be associated with severe depression of CD4−CD8− or CD4+CD8+ cells, which are precursors of either helper or killer T cells in the thymus and Bu1+ B cells in the bursa of Fabricius. Importantly, HS severely damaged the morphology of the thymic cortex and bursal follicles, where functional maturation of T and B cells occur. These results indicate that HS causes multiple immune abnormalities in broiler chickens by impairing the developmental process and functional maturation of T and B cells in both primary and secondary lymphoid tissues.
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spelling doaj.art-d5317191ef6146bf80d3d85e1f1079e32022-12-21T19:41:56ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692020-02-01710.3389/fvets.2020.00046477021Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler ChickensRyota Hirakawa0Ryota Hirakawa1Siti Nurjanah2Siti Nurjanah3Kyohei Furukawa4Kyohei Furukawa5Atsushi Murai6Motoi Kikusato7Motoi Kikusato8Tomonori Nochi9Tomonori Nochi10Tomonori Nochi11Masaaki Toyomizu12Masaaki Toyomizu13Laboratory of Animal Nutrition, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLaboratory of Animal Nutrition, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLaboratory of Animal Nutrition, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLaboratory of Animal Nutrition, Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, JapanLaboratory of Animal Nutrition, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLaboratory of Functional Morphology, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Research and Development Center for Mucosal Vaccine, Institute of Medical Science, The University of Tokyo, Tokyo, JapanLaboratory of Animal Nutrition, Division of Life Sciences, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanInternational Education and Research Center for Food and Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanBroiler chickens are highly sensitive to high ambient temperatures due to their feathers, lack of skin sweat glands, and high productivity. Heat stress (HS) is a major concern for the poultry industry because it negatively affects growth as well as immune functions, which increase the potential risk of infectious disease outbreaks. Therefore, it is vital to elucidate HS's effect on the avian immune system, especially considering the global rise in average surface temperature. Our study identified a series of immunological disorders in heat-stressed broiler chickens. We exposed 22-day-old broiler chickens to a continuous HS condition (34.5 ± 0.5°C) for 14 days and immunized them with a prototype bovine serum albumin (BSA) antigen. The plasma and lymphoid tissues (thymus, bursa of Fabricius, and spleen) were harvested at the end of the experiments to investigate the induction of BSA-specific immune responses. Our results revealed that plasma titers of immunoglobulin (Ig)Y, IgM, and IgA antibodies specific for BSA were lower than those of thermoneutral chickens immunized with BSA. Furthermore, the spleens of the heat-stressed broiler chickens displayed severe depression of Bu1+ B cells and CD3+ T cells, including CD4+ T cells and CD8+ T cells, and lacked a fully developed germinal center (GC), which is crucial for B cell proliferation. These immunological abnormalities might be associated with severe depression of CD4−CD8− or CD4+CD8+ cells, which are precursors of either helper or killer T cells in the thymus and Bu1+ B cells in the bursa of Fabricius. Importantly, HS severely damaged the morphology of the thymic cortex and bursal follicles, where functional maturation of T and B cells occur. These results indicate that HS causes multiple immune abnormalities in broiler chickens by impairing the developmental process and functional maturation of T and B cells in both primary and secondary lymphoid tissues.https://www.frontiersin.org/article/10.3389/fvets.2020.00046/fullheat stressbroiler chickensimmunitybursa of fabriciusthymusspleen
spellingShingle Ryota Hirakawa
Ryota Hirakawa
Siti Nurjanah
Siti Nurjanah
Kyohei Furukawa
Kyohei Furukawa
Atsushi Murai
Motoi Kikusato
Motoi Kikusato
Tomonori Nochi
Tomonori Nochi
Tomonori Nochi
Masaaki Toyomizu
Masaaki Toyomizu
Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
Frontiers in Veterinary Science
heat stress
broiler chickens
immunity
bursa of fabricius
thymus
spleen
title Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
title_full Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
title_fullStr Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
title_full_unstemmed Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
title_short Heat Stress Causes Immune Abnormalities via Massive Damage to Effect Proliferation and Differentiation of Lymphocytes in Broiler Chickens
title_sort heat stress causes immune abnormalities via massive damage to effect proliferation and differentiation of lymphocytes in broiler chickens
topic heat stress
broiler chickens
immunity
bursa of fabricius
thymus
spleen
url https://www.frontiersin.org/article/10.3389/fvets.2020.00046/full
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