Supplementation of reduced protein diets with l-arginine and l-citrulline for broilers challenged with subclinical necrotic enteritis. 3. Immunological parameters and gene expression
Hiep Thi Dao
A B , Nishchal K. Sharma A , Sarbast K. Kheravii A , Emma J. Bradbury C , Shu-Biao Wu A and Robert A. Swick A *
+ Author Affiliations
- Author Affiliations
A School of Environmental and Rural Science, Faculty of Science, Agriculture, Business and Law, University of New England, Armidale, NSW 2351, Australia.
B Faculty of Animal Science, Vietnam National University of Agriculture, Trau Quy Town, Gia Lam District, Hanoi 100000, Vietnam.
C Ridley AgriProducts, Melbourne, Vic. 3000, Australia.
Animal Production Science 62(13) 1266-1279 https://doi.org/10.1071/AN21395
Submitted: 28 July 2021 Accepted: 23 May 2022 Published: 1 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: The impact of necrotic enteritis (NE) on acute-phase proteins, interleukins, blood mineral profiles, and gene expression have not been well documented.
Aims: This study aimed to determine the effects of l-arginine (Arg) or l-citrulline (Cit) supplementation on serum immunological parameters, serum mineral composition and gene expression in broilers fed reduced-protein diets (RP) during subclinical NE challenge.
Methods: Ross 308 cockerels (n = 720) were randomly assigned to six experimental treatments, with eight replicates of 15 birds per pen. The treatments were standard protein without and with NE challenge (SP−, SP+); reduced protein (2% points lower crude protein) without and with NE challenge (RP−, RP+), RP plus added Arg (103% of Ross 308 requirement) with NE challenge (RPA+) and RPC+ where supplemental Arg in RPA+ was replaced with Cit. A 2 × 2 factorial arrangement was employed for the first four treatments. Additionally, treatments SP+, RP+, RPA+, and RPC+ were analysed by one-way ANOVA.
Key results: The NE × protein interactions indicated that serum calcium concentration decreased in birds fed the RP diets only when challenged with NE (P < 0.05). The NE × protein interactions showed that the NE challenge downregulated the mRNA expression of jejunal y+ L amino acid transporter-2, and mucin 2 only in birds fed the RP diets (P < 0.05). Feeding the RP decreased expression of catenin alpha 1, but increased expression of claudin 5 and tight junction protein genes compared with the SP (P < 0.05). Birds in the RPC+ treatment had increased gene expression of tight junction protein and claudin 5 compared with the SP+ treatment (P < 0.05).
Conclusions: Dietary protein level and infection with NE both have an impact on immune response and expression of genes involved in immunity and nutrient digestibility. In part replacement of Arg with Cit in the RPC diet may have beneficial effects on gene expression in NE-challenged birds.
Implications: Feeding RP diets may alleviate a decline in growth during subclinical NE by increasing gene expression of tight junction proteins compared with the SP diets.
Keywords: alpha-1 acid glycoprotein, arginine, calcium, citrulline, interleukins, low protein, minerals, ovotransferrin.
References
Aviagen (2014a) ‘Ross 308 broiler management handbook.’ (Ross Breeders Ltd: Newbridge, Midlothian, Scotland)Aviagen (2014b) ‘Ross 308 broiler nutrition specification.’ (Ross Breeders Ltd: Newbridge, Midlothian, Scotland)
Bahri S, Zerrouk N, Aussel C, Moinard C, Crenn P, Curis E, Chaumeil J-C, Cynober L, Sfar S (2013) Citrulline: from metabolism to therapeutic use. Nutrition 29, 479–484.
| Citrulline: from metabolism to therapeutic use.Crossref | GoogleScholarGoogle Scholar | 23022123PubMed |
Barekatain R, Nattrass G, Tilbrook AJ, Chousalkar K, Gilani S (2019a) Reduced protein diet and amino acid concentration alter intestinal barrier function and performance of broiler chickens with or without synthetic glucocorticoid. Poultry Science 98, 3662–3675.
| Reduced protein diet and amino acid concentration alter intestinal barrier function and performance of broiler chickens with or without synthetic glucocorticoid.Crossref | GoogleScholarGoogle Scholar | 30597073PubMed |
Barekatain R, Chrystal PV, Howarth GS, McLaughlan CJ, Gilani S, Nattrass GS (2019b) Performance, intestinal permeability, and gene expression of selected tight junction proteins in broiler chickens fed reduced protein diets supplemented with arginine, glutamine, and glycine subjected to a leaky gut model. Poultry Science 98, 6761–6771.
| Performance, intestinal permeability, and gene expression of selected tight junction proteins in broiler chickens fed reduced protein diets supplemented with arginine, glutamine, and glycine subjected to a leaky gut model.Crossref | GoogleScholarGoogle Scholar | 31328774PubMed |
Bhatt T, Rizvi A, Batta SPR, Kataria S, Jamora C (2013) Signaling and mechanical roles of E-cadherin. Cell Communication & Adhesion 20, 189–199.
| Signaling and mechanical roles of E-cadherin.Crossref | GoogleScholarGoogle Scholar |
Braun JS, Novak R, Gao G, Murray PJ, Shenep JL (1999) Pneumolysin, a protein toxin of Streptococcus pneumoniae, induces nitric oxide production from macrophages. Infection and Immunity 67, 3750–3756.
| Pneumolysin, a protein toxin of Streptococcus pneumoniae, induces nitric oxide production from macrophages.Crossref | GoogleScholarGoogle Scholar | 10417133PubMed |
Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A (2005) Interferon-γ induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. The FASEB Journal 19, 923–933.
| Interferon-γ induces internalization of epithelial tight junction proteins via a macropinocytosis-like process.Crossref | GoogleScholarGoogle Scholar | 15923402PubMed |
Coleman JW (2001) Nitric oxide in immunity and inflammation. International Immunopharmacology 1, 1397–1406.
| Nitric oxide in immunity and inflammation.Crossref | GoogleScholarGoogle Scholar | 11515807PubMed |
Collier CT, Hofacre CL, Payne AM, Anderson DB, Kaiser P, Mackie RI, Gaskins HR (2008) Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Veterinary Immunology and Immunopathology 122, 104–115.
| Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth.Crossref | GoogleScholarGoogle Scholar | 18068809PubMed |
Dao HT, Sharma NK, Bradbury EJ, Swick RA (2021a) Response of meat chickens to different sources of arginine in low-protein diets. Journal of Animal Physiology and Animal Nutrition 105, 731–746.
| Response of meat chickens to different sources of arginine in low-protein diets.Crossref | GoogleScholarGoogle Scholar | 33410556PubMed |
Dao HT, Sharma NK, Bradbury EJ, Swick RA (2021b) Effects of l-arginine and l-citrulline supplementation in reduced protein diets for broilers under normal and cyclic warm temperature. Animal Nutrition 7, 927–938.
| Effects of l-arginine and l-citrulline supplementation in reduced protein diets for broilers under normal and cyclic warm temperature.Crossref | GoogleScholarGoogle Scholar | 34703910PubMed |
Dao HT, Sharma NK, Daneshmand A, Kumar A, Bradbury EJ, Wu S-B, Swick RA (2022a) Supplementation of reduced protein diets with l-arginine and l-citrulline for broilers challenged with subclinical necrotic enteritis. 1. Growth, carcass yield, and intestinal lesion scores. Animal Production Science
| Supplementation of reduced protein diets with l-arginine and l-citrulline for broilers challenged with subclinical necrotic enteritis. 1. Growth, carcass yield, and intestinal lesion scores.Crossref | GoogleScholarGoogle Scholar |
Dao HT, Sharma NK, Barekatain R, Kheravii SK, Bradbury EJ, Wu S-B, Swick RA (2022b) Supplementation of reduced protein diets with l-arginine and l-citrulline for broilers challenged with subclinical necrotic enteritis. 2. Intestinal permeability, microbiota, and short-chain fatty acid production. Animal Production Science
| Supplementation of reduced protein diets with l-arginine and l-citrulline for broilers challenged with subclinical necrotic enteritis. 2. Intestinal permeability, microbiota, and short-chain fatty acid production.Crossref | GoogleScholarGoogle Scholar |
Emami NK, Calik A, White MB, Young M, Dalloul RA (2019) Necrotic enteritis in broiler chickens: the role of tight junctions and mucosal immune responses in alleviating the effect of the disease. Microorganisms 7, 231
| Necrotic enteritis in broiler chickens: the role of tight junctions and mucosal immune responses in alleviating the effect of the disease.Crossref | GoogleScholarGoogle Scholar |
Fan SP, Liberman Z, Keysar B, Kinzler KD (2015) The exposure advantage: early exposure to a multilingual environment promotes effective communication. Psychological Science 26, 1090–1097.
| The exposure advantage: early exposure to a multilingual environment promotes effective communication.Crossref | GoogleScholarGoogle Scholar | 25956911PubMed |
Fernandez A, Verde MT, Gascon M, Ramos J, Gomez J, Luco DF, Chavez G (1994) Variations of clinical biochemical parameters of laying hens and broiler chickens fed aflatoxin-containing feed. Avian Pathology 23, 37–47.
| Variations of clinical biochemical parameters of laying hens and broiler chickens fed aflatoxin-containing feed.Crossref | GoogleScholarGoogle Scholar | 18671070PubMed |
Flak TA, Goldman WE (1999) Signalling and cellular specificity of airway nitric oxide production in pertussis. Cellular Microbiology 1, 51–60.
| Signalling and cellular specificity of airway nitric oxide production in pertussis.Crossref | GoogleScholarGoogle Scholar | 11207540PubMed |
Fu WJ, Haynes TE, Kohli R, Hu J, Shi W, Spencer TE, Carroll RJ, Meininger CJ, Wu G (2005) Dietary l-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. The Journal of Nutrition 135, 714–721.
| Dietary l-arginine supplementation reduces fat mass in Zucker diabetic fatty rats.Crossref | GoogleScholarGoogle Scholar | 15795423PubMed |
Gasbarrini G, Montalto M (1999) Structure and function of tight junctions. Role in intestinal barrier. Italian Journal of Gastroenterology and Hepatology 31, 481–488.
Gharib-Naseri K, Kheravii SK, Keerqin C, Morgan N, Swick RA, Choct M, Wu S-B (2019) Two different Clostridium perfringens strains produce different levels of necrotic enteritis in broiler chickens. Poultry Science 98, 6422–6432.
| Two different Clostridium perfringens strains produce different levels of necrotic enteritis in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 31424518PubMed |
Gharib-Naseri K, de Paula Dorigam JC, Doranalli K, Kheravii S, Swick RA, Choct M, Wu S-B (2020) Modulations of genes related to gut integrity, apoptosis, and immunity underlie the beneficial effects of Bacillus amyloliquefaciens CECT 5940 in broilers fed diets with different protein levels in a necrotic enteritis challenge model. Journal of Animal Science and Biotechnology 11, 104
| Modulations of genes related to gut integrity, apoptosis, and immunity underlie the beneficial effects of Bacillus amyloliquefaciens CECT 5940 in broilers fed diets with different protein levels in a necrotic enteritis challenge model.Crossref | GoogleScholarGoogle Scholar | 33088501PubMed |
Gilbert ER, Li H, Emmerson DA, Webb KE, Wong EA (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poultry Science 86, 1739–1753.
| Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers.Crossref | GoogleScholarGoogle Scholar | 17626820PubMed |
Gilbert ER, Li H, Emmerson DA, Webb KE, Wong EA (2008) Dietary protein quality and feed restriction influence abundance of nutrient transporter mRNA in the small intestine of broiler chicks. The Journal of Nutrition 138, 262–271.
| Dietary protein quality and feed restriction influence abundance of nutrient transporter mRNA in the small intestine of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 18203889PubMed |
Guo S, Liu D, Zhao X, Li C, Guo Y (2014) Xylanase supplementation of a wheat-based diet improved nutrient digestion and mRNA expression of intestinal nutrient transporters in broiler chickens infected with Clostridium perfringens. Poultry Science 93, 94–103.
| Xylanase supplementation of a wheat-based diet improved nutrient digestion and mRNA expression of intestinal nutrient transporters in broiler chickens infected with Clostridium perfringens.Crossref | GoogleScholarGoogle Scholar | 24570428PubMed |
Guo W, Wang P, Liu Z-H, Ye P (2018) Analysis of differential expression of tight junction proteins in cultured oral epithelial cells altered by Porphyromonas gingivalis, Porphyromonas gingivalis lipopolysaccharide, and extracellular adenosine triphosphate. International Journal of Oral Science 10, e8
| Analysis of differential expression of tight junction proteins in cultured oral epithelial cells altered by Porphyromonas gingivalis, Porphyromonas gingivalis lipopolysaccharide, and extracellular adenosine triphosphate.Crossref | GoogleScholarGoogle Scholar | 29319048PubMed |
Hangalapura BN, Kaiser MG, van der Poel JJ, Parmentier HK, Lamont SJ (2006) Cold stress equally enhances in vivo pro-inflammatory cytokine gene expression in chicken lines divergently selected for antibody responses. Developmental & Comparative Immunology 30, 503–511.
| Cold stress equally enhances in vivo pro-inflammatory cytokine gene expression in chicken lines divergently selected for antibody responses.Crossref | GoogleScholarGoogle Scholar |
He F, Wu C, Li P, Li N, Zhang D, Zhu Q, Ren W, Peng Y (2018) Functions and signaling pathways of amino acids in intestinal inflammation. BioMed Research International 2018, 1–13.
| Functions and signaling pathways of amino acids in intestinal inflammation.Crossref | GoogleScholarGoogle Scholar |
Hilliar M, Keerqin C, Girish CK, Barekatain R, Wu S-B, Swick RA (2020) Reducing protein and supplementing crystalline amino acids, to alter dietary amino acid profiles in birds challenged for subclinical necrotic enteritis. Poultry Science 99, 2048–2060.
| Reducing protein and supplementing crystalline amino acids, to alter dietary amino acid profiles in birds challenged for subclinical necrotic enteritis.Crossref | GoogleScholarGoogle Scholar | 32241490PubMed |
Igwe AO, Ihedioha JI, Okoye JOA (2018) Changes in serum calcium and phosphorus levels and their relationship to egg production in laying hens infected with velogenic Newcastle disease virus. Journal of Applied Animal Research 46, 523–528.
| Changes in serum calcium and phosphorus levels and their relationship to egg production in laying hens infected with velogenic Newcastle disease virus.Crossref | GoogleScholarGoogle Scholar |
Jiang WG (1996) E-cadherin and its associated protein catenins, cancer invasion and metastasis. British Journal of Surgery 83, 437–446.
| E-cadherin and its associated protein catenins, cancer invasion and metastasis.Crossref | GoogleScholarGoogle Scholar | 8665230PubMed |
Jin S, Moujahid EME, Duan Z, Zheng J, Qu L, Xu G, Yang N, Chen S (2016) Association of AMPK subunit gene polymorphisms with growth, feed intake, and feed efficiency in meat-type chickens. Poultry Science 95, 1492–1497.
| Association of AMPK subunit gene polymorphisms with growth, feed intake, and feed efficiency in meat-type chickens.Crossref | GoogleScholarGoogle Scholar | 27143764PubMed |
Jobgen W, Meininger CJ, Jobgen SC, Li P, Lee M-J, Smith SB, Spencer TE, Fried SK, Wu G (2009) Dietary l-arginine supplementation reduces white fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. The Journal of Nutrition 139, 230–237.
| Dietary l-arginine supplementation reduces white fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats.Crossref | GoogleScholarGoogle Scholar | 19106310PubMed |
Lassala A, Bazer FW, Cudd TA, Li P, Li X, Satterfield MC, Spencer TE, Wu G (2009) Intravenous administration of l-citrulline to pregnant ewes is more effective than l-arginine for increasing arginine availability in the fetus. The Journal of Nutrition 139, 660–665.
| Intravenous administration of l-citrulline to pregnant ewes is more effective than l-arginine for increasing arginine availability in the fetus.Crossref | GoogleScholarGoogle Scholar | 19225132PubMed |
Latorre JD, Adhikari B, Park SH, Teague KD, Graham LE, Mahaffey BD, Baxter MFA, Hernandez-Velasco X, Kwon YM, Ricke SC, Bielke LR, Hargis BM, Tellez G (2018) Evaluation of the epithelial barrier function and ileal microbiome in an established necrotic enteritis challenge model in broiler chickens. Frontiers in Veterinary Science 5, 199
| Evaluation of the epithelial barrier function and ileal microbiome in an established necrotic enteritis challenge model in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 30186844PubMed |
Le Floc’h N, Melchior D, Obled C (2004) Modifications of protein and amino acid metabolism during inflammation and immune system activation. Livestock Production Science 87, 37–45.
| Modifications of protein and amino acid metabolism during inflammation and immune system activation.Crossref | GoogleScholarGoogle Scholar |
Lee YS, Lee SH, Gadde UD, Oh ST, Lee SJ, Lillehoj HS (2018) Allium hookeri supplementation improves intestinal immune response against necrotic enteritis in young broiler chickens. Poultry Science 97, 1899–1908.
| Allium hookeri supplementation improves intestinal immune response against necrotic enteritis in young broiler chickens.Crossref | GoogleScholarGoogle Scholar | 29538713PubMed |
Li YP, Bang DD, Handberg KJ, Jorgensen PH, Zhang MF (2005) Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus. Veterinary Microbiology 110, 155–165.
| Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus.Crossref | GoogleScholarGoogle Scholar | 16159698PubMed |
Lindholm-Perry AK, Kuehn LA, Oliver WT, Kern RJ, Cushman RA, Miles JR, McNeel AK, Freetly HC (2014) DNA polymorphisms and transcript abundance of PRKAG2 and phosphorylated AMP-activated protein kinase in the rumen are associated with gain and feed intake in beef steers. Animal Genetics 45, 461–472.
| DNA polymorphisms and transcript abundance of PRKAG2 and phosphorylated AMP-activated protein kinase in the rumen are associated with gain and feed intake in beef steers.Crossref | GoogleScholarGoogle Scholar | 24730749PubMed |
Marinkovic S, Jahreis GP, Wong GG, Baumann H (1989) IL-6 modulates the synthesis of a specific set of acute phase plasma proteins in vivo. The Journal of Immunology 142, 808–812.
Meng Q, Cooney M, Yepuri N, Cooney RN (2017) l-arginine attenuates Interleukin-1β (IL-1β) induced Nuclear Factor Kappa-Beta (NF-κB) activation in Caco-2 cells. PLoS ONE 12, e0174441
| l-arginine attenuates Interleukin-1β (IL-1β) induced Nuclear Factor Kappa-Beta (NF-κB) activation in Caco-2 cells.Crossref | GoogleScholarGoogle Scholar | 28334039PubMed |
Murata H, Shimada N, Yoshioka M (2004) Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal 168, 28–40.
| Current research on acute phase proteins in veterinary diagnosis: an overview.Crossref | GoogleScholarGoogle Scholar | 15158206PubMed |
Nafari SB (2019) Metabolism of energy and implementation of net energy system in laying hens. PhD thesis, University of New England, NSW, Australia.
NHMRC (2013) ‘Australian code of practice for the care and use of animals for scientific purposes.’ 8th edn. (The National Health and Medical Research Council: Australia)
Obst BS, Diamond J (1992) Ontogenesis of intestinal nutrient transport in domestic chickens (Gallus gallus) and its relation to growth. The Auk 109, 451–464.
| Ontogenesis of intestinal nutrient transport in domestic chickens (Gallus gallus) and its relation to growth.Crossref | GoogleScholarGoogle Scholar |
O’Reilly EL, Eckersall PD (2014) Acute phase proteins: a review of their function, behaviour and measurement in chickens. World’s Poultry Science Journal 70, 27–44.
| Acute phase proteins: a review of their function, behaviour and measurement in chickens.Crossref | GoogleScholarGoogle Scholar |
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.
| Dietary calcium, phosphorus, and phytase effects on bird performance, intestinal morphology, mineral digestibility, and bone ash during a natural necrotic enteritis episode.Crossref | GoogleScholarGoogle Scholar | 25143591PubMed |
Paris NE, Wong EA (2013) Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria maxima-infected chickens. Poultry Science 92, 1331–1335.
| Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria maxima-infected chickens.Crossref | GoogleScholarGoogle Scholar | 23571343PubMed |
Park SS, Lillehoj HS, Allen PC, Park DW, FitzCoy S, Bautista DA, Lillehoj EP (2008) Immunopathology and cytokine responses in broiler chickens coinfected with Eimeria maxima and Clostridium perfringens with the use of an animal model of necrotic enteritis. Avian Diseases 52, 14–22.
| Immunopathology and cytokine responses in broiler chickens coinfected with Eimeria maxima and Clostridium perfringens with the use of an animal model of necrotic enteritis.Crossref | GoogleScholarGoogle Scholar | 18459290PubMed |
Reeds PJ, Fjeld CR, Jahoor F (1994) Do the differences between the amino acid compositions of acute-phase and muscle proteins have a bearing on nitrogen loss in traumatic states? The Journal of Nutrition 124, 906–910.
| Do the differences between the amino acid compositions of acute-phase and muscle proteins have a bearing on nitrogen loss in traumatic states?Crossref | GoogleScholarGoogle Scholar | 7515956PubMed |
Rodgers NJ, Swick RA, Geier MS, Moore RJ, Choct M, Wu S-B (2015) A multifactorial analysis of the extent to which Eimeria and fishmeal predispose broiler chickens to necrotic enteritis. Avian Diseases 59, 38–45.
| A multifactorial analysis of the extent to which Eimeria and fishmeal predispose broiler chickens to necrotic enteritis.Crossref | GoogleScholarGoogle Scholar | 26292532PubMed |
Sakaguchi T, Gu X, Golden HM, Suh E, Rhoads DB, Reinecker H-C (2002) Cloning of the human claudin-2 5′-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1α. Journal of Biological Chemistry 277, 21361–21370.
| Cloning of the human claudin-2 5′-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1α.Crossref | GoogleScholarGoogle Scholar | 11934881PubMed |
Saleem G (2013) Necrotic enteritis, disease induction, predisposing factors and novel biochemical markers in broilers chickens. PhD thesis, University of Glasgow, UK.
Sanderink G-J, Artur Y, Siest G (1988) Human aminopeptidases: a review of the literature. Journal of Clinical Chemistry and Clinical Biochemistry 26, 795–807.
| Human aminopeptidases: a review of the literature.Crossref | GoogleScholarGoogle Scholar |
Schroder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-γ: an overview of signals, mechanisms and functions. Journal of Leukocyte Biology 75, 163–189.
| Interferon-γ: an overview of signals, mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 14525967PubMed |
Sovran B, Lu P, Loonen LMP, Hugenholtz F, Belzer C, Stolte EH, Boekschoten MV, van Baarlen P, Smidt H, Kleerebezem M, de Vos P, Renes IB, Wells JM, Dekker J (2016) Identification of commensal species positively correlated with early stress responses to a compromised mucus barrier. Inflammatory Bowel Diseases 22, 826–840.
| Identification of commensal species positively correlated with early stress responses to a compromised mucus barrier.Crossref | GoogleScholarGoogle Scholar | 26926038PubMed |
Su CL, Austic RE (1999) The recycling of l-citrulline to l-arginine in a chicken macrophage cell line. Poultry Science 78, 353–355.
| The recycling of l-citrulline to l-arginine in a chicken macrophage cell line.Crossref | GoogleScholarGoogle Scholar | 10090261PubMed |
Su S, Miska KB, Fetterer RH, Jenkins MC, Wong EA (2014) Expression of digestive enzymes and nutrient transporters in Eimeria acervulina-challenged layers and broilers. Poultry Science 93, 1217–1226.
| Expression of digestive enzymes and nutrient transporters in Eimeria acervulina-challenged layers and broilers.Crossref | GoogleScholarGoogle Scholar | 24795315PubMed |
Tan J, Applegate TJ, Liu S, Guo Y, Eicher SD (2014) Supplemental dietary l-arginine attenuates intestinal mucosal disruption during a coccidial vaccine challenge in broiler chickens. British Journal of Nutrition 112, 1098–1109.
| Supplemental dietary l-arginine attenuates intestinal mucosal disruption during a coccidial vaccine challenge in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 25181320PubMed |
Tosi MF (2005) Innate immune responses to infection. Journal of Allergy and Clinical Immunology 116, 241–249.
| Innate immune responses to infection.Crossref | GoogleScholarGoogle Scholar | 16083775PubMed |
Verrey F, Closs EI, Wagner CA, Palacin M, Endou H, Kanai Y (2004) CATs and HATs: the SLC7 family of amino acid transporters. Pflügers Archiv 447, 532–542.
| CATs and HATs: the SLC7 family of amino acid transporters.Crossref | GoogleScholarGoogle Scholar | 14770310PubMed |
Wade B, Keyburn A (2015) The true cost of necrotic enteritis. World Poultry 31, 16–17.
Wu S-B, Rodgers NJ, Cui G, Sun Y, Choct M (2016) Dynamics of intestinal metabolites and morphology in response to necrotic enteritis challenge in broiler chickens. Avian Pathology 45, 346–356.
| Dynamics of intestinal metabolites and morphology in response to necrotic enteritis challenge in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 27245303PubMed |
Xue G-D, Wu S-B, Choct M, Swick RA (2017) Effects of yeast cell wall on growth performance, immune responses and intestinal short chain fatty acid concentrations of broilers in an experimental necrotic enteritis model. Animal Nutrition 3, 399–405.
| Effects of yeast cell wall on growth performance, immune responses and intestinal short chain fatty acid concentrations of broilers in an experimental necrotic enteritis model.Crossref | GoogleScholarGoogle Scholar | 29767160PubMed |
Yang F, Lei X, Rodriguez-Palacios A, Tang C, Yue H (2013) Selection of reference genes for quantitative real-time PCR analysis in chicken embryo fibroblasts infected with avian leukosis virus subgroup J. BMC Research Notes 6, 402
| Selection of reference genes for quantitative real-time PCR analysis in chicken embryo fibroblasts infected with avian leukosis virus subgroup J.Crossref | GoogleScholarGoogle Scholar | 24099561PubMed |
Yun CH, Lillehoj HS, Lillehoj EP (2000) Intestinal immune responses to coccidiosis. Developmental & Comparative Immunology 24, 303–324.
| Intestinal immune responses to coccidiosis.Crossref | GoogleScholarGoogle Scholar |
Zanu HK, Kheravii SK, Morgan NK, Bedford MR, Swick RA (2020a) Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. Serum calcium and phosphorus, and bone mineralization. Poultry Science 99, 3617–3627.
| Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. Serum calcium and phosphorus, and bone mineralization.Crossref | GoogleScholarGoogle Scholar | 32616258PubMed |
Zanu HK, Keerqin C, Kheravii SK, Morgan N, Wu S-B, Bedford MR, Swick RA (2020b) Influence of meat and bone meal, phytase, and antibiotics on broiler chickens challenged with subclinical necrotic enteritis: 2. Intestinal permeability, organ weights, hematology, intestinal morphology, and jejunal gene expression. Poultry Science 99, 2581–2594.
| Influence of meat and bone meal, phytase, and antibiotics on broiler chickens challenged with subclinical necrotic enteritis: 2. Intestinal permeability, organ weights, hematology, intestinal morphology, and jejunal gene expression.Crossref | GoogleScholarGoogle Scholar | 32359594PubMed |
Zhang B, Gan L, Shahid MS, Lv Z, Fan H, Liu D, Guo Y (2019) In vivo and in vitro protective effect of arginine against intestinal inflammatory response induced by Clostridium perfringens in broiler chickens. Journal of Animal Science and Biotechnology 10, 73
| In vivo and in vitro protective effect of arginine against intestinal inflammatory response induced by Clostridium perfringens in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 31428367PubMed |
Zulkifli I, Najafi P, Nurfarahin AJ, Soleimani AF, Kumari S, Aryani AA, O’Reilly EL, Eckersall PD (2014) Acute phase proteins, interleukin 6, and heat shock protein 70 in broiler chickens administered with corticosterone. Poultry Science 93, 3112–3118.
| Acute phase proteins, interleukin 6, and heat shock protein 70 in broiler chickens administered with corticosterone.Crossref | GoogleScholarGoogle Scholar | 25306460PubMed |
