Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
Dietary Zn proteinate alleviates heat stress-induced intestinal integrity disruption possibly by promoting cell proliferation via related signaling pathways in the jejunum of broilers

Yangyang Hu1*, Weizhen Song1, Weiyun Zhang1, Xin Du1, Xi Lin2, Hsiao-Ching Liu2, Jack Odle2, Miles Todd See2, Xiaoyan Cui1, Tingting Li1, Shengchen Wang1, Xiudong Liao3, Liyang Zhang3, Yun Hu1#, Xugang Luo1#

Poultry Mineral Nutrition Laboratory, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China

Department of Animal Science, North Carolina State University, Raleigh, NC 27695, USA

Mineral Nutrition Research Division, State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

热应激(Heat stress, HS)可引起肉仔鸡小肠完整性的破坏。本研究揭示饲粮添加锌(Zinc, Zn),尤其是添加中等螯合强度蛋白锌(Zinc proteinate with moderate chelation strength, Zn-Prot M)缓解HS引起的肉鸡小肠完整性破坏方面的功效和可能的机制。采用22日龄爱拔益加(AA)肉仔公鸡进行本试验,试验期为22-42日龄,共21天。采用HS条件下的1(对照组) + 2(Zn) × 2(Zn添加水平)5个处理组的两因子完全随机试验设计与常温条件下的1(对照组) + 1(将鸡只采食量控制到与HS对照组鸡只相同的配对组)2个处理组的单因子完全随机试验设计。因此,本试验共有7个处理组设置本试验HS条件为9:00-17:0034±1°C8 h d-1,其余时间段温度为28±1°C;常温条件为23±1°C24 h d-1。以上HS和常温条件下的相对湿度均保持在55±5%。在HS条件下,添加的2Zn源分别为ZnSO4.7H2O(ZnSO4)Zn-Prot M;在以ZnSO4添补Zn而满足22-42日龄肉仔鸡Zn营养需要量(65 mg/kg)作为对照组的基础上,设置的2个饲粮Zn添加水平分别为3060 mg kg-1。结果表明,HS显著降低小肠绒毛高度(Villus height, VH)绒毛高度/隐窝深度(Villus height/crypt depth, VH/CD和绒毛表面积(Villus surface area, VSA)、空肠增殖细胞核抗原(Proliferating cell nuclear antigen, PCNA)阳性细胞数量磷脂酰肌醇3-激酶(Phosphatidylinositol 3-kinase, PI3K)丝氨酸苏氨酸激酶(Serine threonine kinase, AKT)细胞外调节蛋白激酶(Extracellular regulated protein kinase, ERK)蛋白激酶C(Protein kinase C, PKC)G蛋白偶联受体39(G protein-coupled receptor 39, GPR39)、磷酸化PI3K(p-PI3K)/PI3Kp-AKT/AKTp-ERK/ERK和磷脂酶C(Phospholipase C, PLC)β1/2mRNA或蛋白表达水平以及PLC活性(P<0.05);而明显增加了小肠CD、空肠P38丝裂原活化蛋白激酶(P38 mitogen activated protein kinase, P38MAPK)C-Jun氨基末端激酶(C-jun N-terminal kinase, JNK)1/2p-JNK/JNK mRNA或蛋白表达水平(P<0.05)。以上研究结果表明,饲粮添加Zn,尤其是以Zn-Prot M形式添加60 mg kg-1 Zn,可能通过热应激肉仔鸡空肠GPR39/PLC β1介导的PI3K/AKTMAPK信号通路促进细胞增殖而缓解HS诱导的小肠损伤。这一发现也凸显了Zn-Prot M作为一种新型有机锌添加剂的潜力,它可以通过加强细胞修复来减轻HS引起的肉仔鸡肠道损伤,从而为改善肉仔鸡肠道健康和提高生产效率提供了一种新的营养策略。



Abstract  

Heat stress (HS) can induce the disruption of small intestinal integrity in broilers. Here we examined the efficacies and possible mechanismof zinc proteinate with moderate chelation strength (Zn-Prot M) compared to ZnSO4.7H2O (ZnSO4) in alleviating HS-induced disruption of small intestinal integrity in broilers. The experiment included 7 treatments. Twenty two-d-old birds were randomly allotted into 1 of 5 treatments under high temperature (HT, 9:00-17:00: 34±1°C, 8 h d-1; 17:00–9:00: 28±1°C) with 1 control (HT-CON) plus 2 [dietary Zn sources, Zn-Prot M and ZnSO4] × 2 [added Zn levels, 30 and 60 mg kg-1] factorial arrangement, and 1 of 2 treatments under normal temperature (NT) with the control (NT-CON) and pair-feeding matched to HT-CON (NT-PF). The results showed that HS dramatically reduced (P<0.05) small intestinal villus height (VH), VH/crypt depth (CD) and villus surface area (VSA), the amount of proliferating cell nuclear antigen (PCNA) positive cells, mRNA or protein expression levels of phosphatidylinositol 3-kinase (PI3K), serine threonine kinase (AKT), extracellular regulated protein kinase (ERK), protein kinase C (PKC), G protein-coupled receptor 39 (GPR39), phosphorylated PI3K (p-PI3K)/PI3K, p-AKT/AKT, p-ERK/ERK and phospholipase C (PLC) β1/2, and PLC activity. HS also remarkably increased (P<0.05) small intestinal CD and mRNA or protein levels of P38 mitogen activated protein kinase (P38 MAPK), C-jun N-terminal kinase (JNK)1/2 and p-JNK/JNK in the jejunum of heat stressed (HS) broilers. However, dietary supplementation with Zn, especially organic Zn as Zn-Prot M at 60 mg kg-1, significantly increased (P<0.05) small intestinal VH, VH/CD and VSA, as well as the amount of PCNA positive cells, PLC activity, mRNA expression levels of PI3K, AKT, GPR39 and PLC β1, protein expression levels of p-PI3K/PI3K, p-AKT/AKT, p-ERK/ERK, GPR39 and PLC β1, and decreased (P<0.05) small intestinal CDJNK2 mRNA expression level and p-JNK/JNK protein expression level in the jejunum of HS broilers. These results suggest that dietary supplemental Zn, especially 60 mg Zn kg-1 as Zn-Prot M, can effectively alleviate HS-induced small intestinal injury possibly by promoting cellular proliferation via the GPR39/PLC β1-mediated PI3K/AKT or MAPK pathwayin the jejunum of HS broilers.

Keywords:  Zn-Prot M       heat stressed broiler       small intestinal integrity       cellular proliferation       GPR39/PLC β1-mediated PI3K/AKT or MAPK pathways  
Online: 16 May 2025  
Fund: 

This work was supported by the Key International Cooperation Program of the National Natural Science Foundation of China (32120103011), the Jiangsu Shuang Chuang Tuan Dui program (JSSCTD202147), the Jiangsu Shuang Chuang Ren Cai program (JSSCRC2021541) and the Initiation Funds of Yangzhou University for Distinguished Scientists.

About author:  Yangyang Hu, E-mail: 1481447880@qq.com; #Correspondences Yun Hu, Email: huyun@yzu.edu.cn; Xugang Luo, E-mail: wlysz@263.net

Cite this article: 

Yangyang Hu, Weizhen Song, Weiyun Zhang, Xin Du, Xi Lin, Hsiao-Ching Liu, Jack Odle, Miles Todd See, Xiaoyan Cui, Tingting Li, Shengchen Wang, Xiudong Liao, Liyang Zhang, Yun Hu, Xugang Luo. 2025. Dietary Zn proteinate alleviates heat stress-induced intestinal integrity disruption possibly by promoting cell proliferation via related signaling pathways in the jejunum of broilers. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.05.012

Abuajamieh M, Abdelqader A, Irshaid R, Hayajneh F M F, Al-Khaza'leh J M, Al-Fataftah A R. 2020. Effects of organic zinc on the performance and gut integrity of broilers under heat stress conditions. Archives Animal Breeding, 63, 125-135.

Alagbe E O, Schulze H, Adeola O. 2023. Growth performance, nutrient digestibility, intestinal morphology, cecal mucosal cytokines and serum antioxidant responses of broiler chickens to dietary enzymatically treated yeast and coccidia challenge. Journal of Animal Science and Biotechnology, 14, 57-69.

Alcantara E H, Shin M Y, Feldmann J, Nixon G F, Beattie J H, Kwun I S. 2013. Long-term zinc deprivation accelerates rat vascular smooth muscle cell proliferation involving the down-regulation of JNK1/2 expression in MAPK signaling. Atherosclerosis, 228, 46-52.

Alhenaky A, Abdelqader A, Abuajamieh M, Al-Fataftah A R. 2017. The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. Journal of Thermal Biology, 70, 9-14.

Asraf H, Salomon S, Nevo A, Sekler I, Mayer D, Hershfinkel M. 2013. The ZnR/GPR39 interacts with the casr to enhance signaling in prostate and salivary epithelia. Journal of Cellular Physiology, 229, 868-877.

Azriel-Tamir H, Sharir H, Schwartz B, Hershfinkel M. 2004. Extracellular zinc triggers ERK-dependent activation of Na+/H+ exchange in colonocytes mediated by the zinc-sensing receptor. Journal of Biological Chemistry, 279, 51804-51816.

Bortoluzzi C, Vieira B S, Applegate T J. 2020. Influence of dietary zinc, copper, and manganese on the intestinal health of broilers under eimeria challenge. Frontiers in Veterinary Science, 7, 13-19.

Branca J J V, Carrino D, Paternostro F, Morucci G, Fiorillo C, Nicoletti C, Gulisano M, Ghelardini C, Manneili L D C, Becatti M, Pacini A. 2022. The protection of zinc against acute cadmium exposure: A morphological and molecular study on a BBB in vitro model. Cells, 11, 1646.

Brzozowa-Zasada M, Piecuch A, Michalski M, Matysiak N, Kucharzewski M, Los M J. 2023. The clinical application of immunohistochemical expression of notch 4 protein in patients with colon adenocarcinoma. International Journal of Molecular Sciences, 24, 7502.

Castro F L S, Kim H Y, Hong Y G, Kim W K. 2019. The effect of total sulfur amino acid levels on growth performance, egg quality, and bone metabolism in laying hens subjected to high environmental temperature. Poultry Science, 98, 4982-4993.

Chen F M, Chen J Y, Chen Q H, Yang L Y, Yin J, Li Y H, Huang X G. 2021. Lactobacillus delbrueckii protected intestinal integrity, alleviated intestinal oxidative damage, and activated toll-like receptor–bruton’s tyrosine kinase–nuclear factor erythroid 2-related factor 2 pathway in weaned piglets challenged with lipopolysaccharide. Antioxidants, 10, 468.

Cohen L, Azriel-Tamir H, Arotsker N, Sekler I, Hershfinkel M. 2012. Zinc sensing receptor signaling, mediated by GPR39, reduces butyrate-induced cell death in HT29 colonocytes via upregulation of clusterin. PLoS One, 7, e35482.

Cohen L, Sekler I, Hershfinkel M. 2014. The zinc sensing receptor, ZnR/GPR39, controls proliferation and differentiation of colonocytes and thereby tight junction formation in the colon. Cell Death and Disease, 5, e1307.

Dong X Y, Tang S Q, Zhang W, Gao W H, Chen Y F. 2016. GPR39 activates proliferation and differentiation of porcine intramuscular preadipocytes through targeting the PI3K/AKT cell signaling pathway. Journal of Receptors and Signal Transduction, 36, 130-138.

Dou T F, Yan S X, Liu L X, Wang K, Jian Z H, Xu Z Q, Zhao J Y, Wang Q T, Sun S C, Talpur M Z, Duan X H, Gu D H, He Y, Du Y, Abdulwahid A M, Li Q H, Rong H, Cao W N, Su Z C, Zhao G P, Liu R R, Zhao S M, Huang Y, te Pas M F W, Ge C R, Jia J J. 2022. Integrative analysis of transcriptomics and metabolomics to reveal the melanogenesis pathway of muscle and related meat characters in wuliangshan black-boned chickens. BMC Genomics, 23, 173.

Fournier M N, Lee B Y, Banasr M, Elsayed M H, Duman R S. 2012. Vascular endothelial growth factor regulates adult hippocampal cell proliferation through MEK/ERK-and PI3K/Akt-dependent signaling. Neuropharmacology, 63, 642-652.

Ganaie A H, Ghasura R S, Mir N A, Bumla N A, Sankar G, Wani S A. 2013. Biochemical and physiological changes during thermal stress in bovines: A review. Iranian Journal of Applied Animal Science, 3, 423-430.

Goor A V, Bolek K J, Ashwell C M, Persia M E, Rothschild M F, Schmidt C J, Lamont S J. 2015. Identification of quantitative trait loci for body temperature, body weight, breast yield, and digestibility in an advanced intercross line of chickens under heat stress. Genetics Selection Evolution, 47, 96.

He X F, Lu Z, Ma B B, Zhang L, Li J L, Jiang Y, Zhou G H, Gao F. 2018. Effects of chronic heat exposure on growth performance, intestinal epithelial histology, appetite-related hormones and genes expression in broilers. Journal of the Science of Food and Agriculture, 98, 4471-4478.

Hershfinkel M, Moran A, Grossman N, Sekler I. 2001. A zinc-sensing receptor triggers the release of intracellular Ca2+ and regulates ion transport. Proceedings of the National Academy of Sciences of the United States of America, 98, 11749–11754.

Holst B, Holliday N D, Bach A, Elling C E, Cox H M, Schwartz T W. 2004. Common structural basis for constitutive activity of the ghrelin receptor family. Journal of Biological Chemistry, 279, 53806-53817.

Holwerda R A, Albin R C, Madsen F C. 1995. Chelation effectiveness of zinc proteinates demonstrated. Feedstuffs, 67, 12-13.

Hosseindoust A, Oh S M, Ko H S, Jeon S A O, Ha S H, Jang A, Son J S, Kim G Y, Kang H K, Kim J S. 2020. Muscle antioxidant activity and meat quality are altered by supplementation of astaxanthin in broilers exposed to high temperature. Antioxidants, 9, 1032.

Hu Y, Huang Y H, Wang C L, Zhang W Y, Qu Y C, Li D, Wu W, Gao F Y, Zhu L, Wu B X, Zhang L Y, Cui X Y, Li T T, Geng Y Q, Liao X D, Luo X D. 2023. The organic zinc with moderate chelation strength enhances the expression of related transporters in the jejunum and ileum of broilers. Poultry Science, 102, 102477.

Hu Y Y, Yang K, Zhang W Y, Xue M X, Li T T, Wang S C, Cui X Y, Zhang L Y, Hu Y, Luo X G. 2024a. Dietary Zn deficiency inhibits cell proliferation via the GPR39-mediated suppression of the PI3K/AKT/mTOR signaling pathway in the jejunum of broilers. Animals, 14, 979-989.

Hu Y Y, Zhang W Y, Yang K, Lin X, Liu H C, Odle J, See M T, Cui X Y, Li T T, Wang S C, Liao X D, Zhang L Y, Li S F, Hu Y, Luo X G. 2024b. Dietary Zn proteinate with moderate chelation strength alleviates heat stress-induced intestinal barrier function damage by promoting expression of tight junction proteins via the A20/NF-κB p65/MMP-2 pathway in the jejunum of broilers. Journal of Animal Science and Biotechnology, 15, 115.

Huang L, Cao C Y, Lin X X, Lu L, Lin X, Liu H C, Odle J, See M T, Zhang L Y, Wu W, Luo X G, Liao X D. 2024. Zinc alleviates thermal stress-induced damage to the integrity and barrier function of cultured chicken embryonic primary jejunal epithelial cells via the MAPK and PI3K/AKT/mTOR signaling pathways. Poultry Science, 103, 103696.

Huang Y L, Lu L, Luo X G, Liu B. 2007. An optimal dietary zinc level of broiler chicks fed a corn-soybean meal diet. Poultry Science, 86, 2582-2589.

Huang Y L, Lu L, Li S F, Luo X G, Liu B. 2009. Relative bioavailabilities of organic zinc sources with different chelation strengths for broilers fed a conventional corn-soybean meal diet. Journal of Animal Science, 87, 2038-2046.

Huang Y L, Lu L, Xie J J, Li S F, Li X L, Liu S B, Zhang L Y, Xi L, Luo X G. 2013. Relative bioavailabilities of organic zinc sources with different chelation strengths for broilers fed diets with low or high phytate content. Animal Feed Science and Technology, 179, 144-148.

Inatomi T, Otomaru K. 2018. Effect of dietary probiotics on the semen traits and antioxidative activity of male broiler breeders. Scientific Reports, 8, 5974.

Jin X J, Song Y F, An Z L, Wu S S, Cai D H, Fu Y, Zhang C J, Chen L C, Tang W, Zheng Z Q, Lu H S, Lian J F. 2022. A predictive model for prognosis and therapeutic response in hepatocellular carcinoma based on a panel of three MED8-related immunomodulators. Frontiers in Oncology, 12, 868411.

Kidd M T, Ferket P R, Qureshi M A. 1996. Zinc metabolism with special reference to its role in immunity. World's Poultry Science Journal, 52, 309-324.

Kouti V, Papazoglou L, Flaskos J, Angelopoulou K, Karkavelas G, Rallis T. 2011. Ursodeoxycholic acid promotes intestinal adaptation in a cat model of short bowel syndrome. Fundamental and Clinical Pharmacology, 25, 734-742.

Li J Y, Ren K K, Zhang W J, Xiao L, Wu H Y, Liu Q Y, Ding T, Zhang X C, Nie W J, Ke Y, Deng K Y, Liu Q W, Xin H B. 2019. Human amniotic mesenchymal stem cells and their paracrine factors promote wound healing by inhibiting heat stress-induced skin cell apoptosis and enhancing their proliferation through activating PI3K/AKT signaling pathway. Stem Cell Research & Therapy, 10, 247.

Liang D, Yang M W, Guo B L, Cao J J, Yang L, Guo X D. 2012. Zinc upregulates the expression of osteoprotegerin in mouse osteoblasts MC3T3-E1 through PKC/MAPK pathways. Biological Trace Element Research, 146, 340-348.

Liao X D, Li A, Lu L, Liu S B, Li S F, Zhang L Y, Wang G Y, Luo X G. 2013. Optimal dietary zinc levels of broiler chicks fed a corn–soybean meal diet from 22 to 42 days of age. Animal Production Science, 53, 388-394.

Liao X D, Liu G Q, Sun G M, Sun X M, Liu T, Lu L, Zhang L Y, Zhang M H, Guo Y L, Luo X G. 2021. Determination of optimal dietary selenium levels by full expression of selenoproteins in various tissues of broilers from 1 to 21 d of age. Animal Nutrition, 7, 1133-1144.

Liu L W, Yao J H, Li Z L, Zu G, Feng D C, Li Y, Qasim W, Zhang S, Li T, Zeng H Z, Tian X F. 2018. miR-381-3p knockdown improves intestinal epithelial proliferation and barrier function after intestinal ischemia/reperfusion injury by targeting nurr1. Cell Death and Disease, 9, 411.

Liu T, Zou L, Ji X, Xiao G. 2022. Chicken skin-derived collagen peptides chelated zinc promotes zinc absorption and represses tumor growth and invasion in vivo by suppressing autophagy. Frontiers in Nutrition, 9, 960926.

Liu X X, Li H R, Lu A, Zhong Y G, Hou X L, Wang N, Jia D, Zan J L, Zhao H, Xu J Q, Liu F H. 2012. Reduction of intestinal mucosal immune function in heat-stressed rats and bacterial translocation. International Journal of Hyperthermia, 28, 756-765.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.

Lu Z, He X F, Ma B B, Zhang L, Li J L, Jiang Y, Zhou G H, Gao F. 2019. The alleviative effects and related mechanisms of taurine supplementation on growth performance and carcass characteristics in broilers exposed to chronic heat stress. Poultry Science, 98, 878-886.

MAPRC (Ministry of Agriculture and Rural Affairs of China). 2004. Feeding Standard of Chicken. Beijing, China. (in Chinese)

Mo J W, Wang Z J, Liu Q C, Li Z H, Nie Q H. 2022. Construction and analysis of disuse atrophy model of the gastrocnemius muscle in chicken. International Journal of Molecular Sciences, 23, 6892.

Nanto-Hara F, Kikusato M, Ohwada S, Toyomizu M. 2020. Heat stress directly affects intestinal integrity in broiler chickens. Journal of Poultry Science, 57, 284-290.

Neto B J, Stefan V, Mendonça B B, Bloise W, Castro A V B. 1995. The essential role of zinc in growth. Nutrition Research, 15, 335-358.

Ohashi K, Nagata Y, Wada E, Zammit P S, Shiozuka M, Matsuda R. 2015. Zinc promotes proliferation and activation of myogenic cells via the PI3K/Akt and ERK signaling cascade. Experimental Cell Research, 333, 228-237.

Paiva D, Walk C, McElroy A. 2014. Dietary calcium, phosphorus, and phytase effects on bird performance, intestinal morphology, mineral digestibility, and bone ash during a natural necrotic enteritis episode. Poultry Science, 93, 2752-2762.

Qu H Y, Sun H B, Wang X P. 2018. Neogenin-1 promotes cell proliferation, motility, and adhesion by up-regulation of zinc finger e-box binding homeobox 1 via activating the rac1/PI3K/AKT pathway in gastric cancer cells. Cellular Physiology and Biochemistry, 48, 1457-1467.

Sahin K, Orhan C, Akdemir F, Tuzcu M, Ali S, Sahin N. 2011. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Animal Feed Science and Technology, 165, 230-237.

Santos R R, Awati A, Hil R V D, Zijderveld M H G T, Koolmees P A, Gremmels J F. 2015. Quantitative histo-morphometric analysis of heat-stress-related damage in the small intestines of broiler chickens. Avian Pathology, 44, 19-22.

Satianrapapong W, Pongkorpsakol P, Muanprasat C C. 2020. A G-protein coupled receptor 39 agonist stimulates proliferation of keratinocytes via an ERK-dependent pathway. Biomedicine & Pharmacotherapy, 127, 110160.

Shah M, Zaneb H, Masood S, Khan R U, Mobashar M, Khan I, Din S, Khan M S, Rehman H U, Tinelli A. 2020. Single or combined applications of zinc and multi-strain probiotic on intestinal histomorphology of broilers under cyclic heat stress. Probiotics and Antimicrobial Proteins, 12, 473-480.

Shao Y X, Lei Z, Wolf P G, Gao Y, Guo Y M, Zhang B K. 2017a. Zinc supplementation, via GPR39, upregulates PKC zeta to protect intestinal barrier integrity in caco-2 cells challenged by salmonella enterica serovar typhimurium. Journal of Nutrition, 147, 1282-1289.

Siddiqui S H, Kang D, Park J, Khan M S, Shim K. 2020. Chronic heat stress regulates the relation between heat shock protein and immunity in broiler small intestine. Scientific Reports, 10, 18872.

Sun L K, Wang L, Chen T X, Yao B W, Wang Y F, Li Q, Yang W, Liu Z K. 2019. microRNA-1914, which is regulated by lncRNA DUXAP10, inhibits cell proliferation by targeting the GPR39-mediated PI3K/AKT/mTOR pathway in HCC. Journal of Cellular and Molecular Medicine, 23, 8292-8304.

Sunuwar L, Asraf H, Donowitz M, Sekler I, Hershfinkel M. 2017. The Zn2+-sensing receptor, ZnR/GPR39, upregulates colonocytic Cl- absorption, via basolateral KCC1, and reduces fluid loss. Biochimica Et Biophysica Acta-molecular Basis of Disease, 1863, 947-960.

Teegala L R, Elshoweikh Y, Gudneppanavar R, Thodeti S, Pokhrel S, Southard E, Thodeti C K, Paruchuri S A-O. 2022. Protein kinase C α and β compensate for each other to promote stem cell factor-mediated KIT phosphorylation, mast cell viability and proliferation. Federation of American Societies for Experimental Biology, 36, e22273.

Varasteh S, Braber S, Akbari P, Garssen J, Fink-Gremmels J. 2015. Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLoS One, 10, e0138975.

Wales S Q, Pandiscia A, Kulka M, Sanchez G, Randazzo W. 2023. Challenges for estimating human norovirus infectivity by viability RT-qPCR as compared to replication in human intestinal enteroids. International Journal of Food Microbiology, 23, 110507.

Waseem T, Duxbury M, Ashley S W, Robinson M K. 2014. Ghrelin promotes intestinal epithelial cell proliferation through PI3K/Akt pathway and EGFR trans-activation both converging to ERK 1/2 phosphorylation. Peptides, 52, 113-121.

Watermann B T, Daehne B, Sievers S, Dannenberg R, Overbeke J C, Klijnstra J W, Heemken O. 2005. Bioassays and selected chemical analysis of biocide-free antifouling coatings. Chemosphere, 60, 1530-1541.

Wu T, Li K, Yi D, Wang L, Zhao D, Lv Y A, Zhang L, Chen H B, Ding B Y, Hou Y Q, Wu G Y. 2018. Dietary supplementation with trihexanoin enhances intestinal function of weaned piglets. International Journal of Molecular Sciences, 19, 3277.

Xia P P, Yan L, Ji X D, Wu Y P, Lian S Q, Zhu G Q. 2022. Functions of the zinc-sensing receptor GPR39 in regulating intestinal health in animals. International Journal of Molecular Sciences, 23, 12133.

Yang P C, He S H, Zheng P Y. 2007. Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function. Journal of Gastroenterology and Hepatology, 22, 1823-1831.

Yu J, Liu F H, Yin P, Zhao H, Luan W L, Hou X L, Zhong Y G, Jia D, Zan J L, Ma W R, Shu B C, Xu J Q. 2012. Involvement of oxidative stress and mitogen-activated protein kinase signaling pathways in heat stress-induced injury in the rat small intestine. Stress, 16, 99-113.

Yu Y, Lu L, Wang R L, Xi L, Luo X G, Liu B. 2010. Effects of zinc source and phytate on zinc absorption by in situ ligated intestinal loops of broilers. Poultry Science, 89, 2157-2165.

Zan G X, Qin Y C, Xie W W, Gao C Q, Yan H C, Wang X Q, Zhou J Y. 2023. Heat stress disrupts intestinal stem cell migration and differentiation along the crypt–villus axis through FAK signaling. Biochimica et Biophysica Acta, 1870, 119431.

Zhang J Q, Li Z H, Yu C Y, Liu H J, Zhou B B, Zhang X H, Wang T, Wang C. 2022. Efficiency of using zinc oxide nanoparticle as a substitute to antibiotic growth promoter and zinc sulphate for growth performance, antioxidant capacity, immunity and intestinal barrier function in broilers. Italian Journal of Animal Science, 21, 562-576.

Zhang L L, Xing D, Gao X J, Wu S N. 2009. Low-power laser irradiation promotes cell proliferation by activating PI3K/Akt pathway. Journal of Cellular Physiology, 219, 553-562.

Zhang W, Liu H T. 2002. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Research, 12, 9-18.

Zhang Y F, Xie L Y, Ding X Q, Wang Y Y, Xu Y B, Li D L, Liang S, Wang Y X, Zhang L, Fu A K, Zhan X A. 2022. Mechanisms underlying the protective effect of maternal zinc (ZnSO4 or Zn-Gly) against heat stress-induced oxidative stress in chicken embryo. Antioxidants, 11, 1699-1713.

Zhou J Y, Lin H L, Wang Z, Zhang S W, Huang D G, Gao C Q, Yan H C, Wang X Q. 2020. Zinc L-Aspartate enhances intestinal stem cell activity to protect the integrity of the intestinal mucosa against deoxynivalenol through activation of the Wnt/β-catenin signaling pathway. Environmental Pollution, 262, 114290.

Zhu D H, Su Y C, Zheng Y F, Fu B M, Tang L P, Qin Y X. 2018. Zinc regulates vascular endothelial cell activity through zinc-sensing receptor ZnR/GPR39. American Journal of Physiology-Cell Physiology, 314, C404-C414.

Zhu X P, Shang X G, Lin G Z, Li H J, Feng X, Zhang H H. 2021. Effects of zinc glycinate on growth performance, serum biochemical indexes, and intestinal morphology of yellow feather broilers. Biological Trace Element Research, 200, 4089-4097.

No related articles found!
No Suggested Reading articles found!