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ISSN : 1598-5504(Print)
ISSN : 2383-8272(Online)
Journal of Agriculture & Life Science Vol.52 No.3 pp.91-102
DOI : https://doi.org/10.14397/jals.2018.52.3.91

Glutamine-supplement Diet Maintains Growth Performance and Reduces Blood Corticosterone Level in Cage-reared Growing Chicks

Minhee Kim1,2, Soonwoong Jung1, Hyeonwi Son1, Hyun Joon Kim1*
1Department of Anatomy and Convergence Medical Science, Bio Anti-Aging Medical Research Center, Institute of Health Sciences, Gyeongsang National University Medical School, Jinju, 52727, Korea
2Gyeongsangnam-do Livestock Veterinary Research Institute, Jinju, 52733, Korea
Corresponding author: Hyun Joon Kim Tel: +82-55-772-8034 Fax: +82-55-772-8039kimhj@gnu.ac.kr
November 7, 2017 November 29, 2017 January 25, 2018

Abstract


Supplementation with glutamine(Gln) has beneficial effects on intestinal and immune functions. Cage-reared chicks suffer from various stressors during early growth, but the effect of Gln supplementation on growth performance and stress hormones is uncertain. We investigated the effect of Gln on growth performance and blood corticosterone levels in Hyline chicks. Groups of 3-day-old chicks were fed one of three diets: normal feed(CTL group), normal feed supplemented with a low level of Gln, or normal feed supplemented with a high level of Gln. Growth and various physiological and biochemical parameters related to stress were assessed. On day 30, after a 24-h fast, blood was analyzed for corticosterone and other parameters, including glutamic oxaloacetic transaminase, gamma-glutamyl transpeptidase, total bilirubin, lactate dehydrogenase, total cholesterol, high-density lipoprotein cholesterol, blood urea nitrogen, blood total protein, and inorganic phosphate. Growth performance was maintained in Gln supplemented groups. The corticosterone level was decreased in the two groups receiving Gln supplementation compared to the CTL, and all other humoral factors did not differ between the groups. We suggest that Gln supplementation is a safe and useful strategy for reducing the effects of stress in cage-reared chicks.



초록


    National Research Foundation of Korea
    2014R1A1A4A01006451
    2015R1A5A2008833 Gyeongsang National University

    Introduction

    Stress is an important factor in the health and productivity of domestic animals. It can affect many physiological processes including growth, metabolism, and immune function, and must be mitigated to maximize productivity. However, a low-stress environment can be difficult to maintain as well as costly. Chickens are particularly susceptible to stress, reported to affect a myriad of physiological parameters: notably, the immune system(Shini & Kaiser, 2009; Gomes et al., 2014; Borsoi et al., 2015) muscle development(Duan et al., 2014; Fu et al., 2014), ovarian function and egg laying(Kim & Choi, 2014), and absorption of nutrients(Sun et al., 2015).

    Corticosterone is the main glucocorticoid in birds and it is often used as an indicator of stressfulness in chickens(Choi, 2007). Corticosterone is secreted by the adrenal glands in response to various stressful stimuli(Sapolsky et al., 2000). Both yarding and caging are common systems for raising chicks, but differ in the stress levels they impose. Raising chicks in cages is more cost effective but more stressful than raising chicks in yards(Sohn et al., 2011); consequently, caged chicks may have higher systemic levels of stress hormones than chicks raised in yards. Of particular concern is that meat and eggs from these chickens may also contain greater concentrations of corticosterone and other stress hormones(Rettenbacher et al., 2005). If so, it would be of value to develop new methods of feeding chicks that would reduce the stress associated with cage rearing. These methods might also be applicable to other rearing methods, such as yarding.

    Glutamine(Gln) is a non-essential amino acid in chickens. It is produced mostly in the liver, muscle, and brain(Patejunas & Young, 1987; Campbell & Smith, 1992). Its synthesis is catalyzed by glutamine synthetase(GS) from glutamate and ammonia, a pathway that can be considered a type of ammonia detoxification process(Limami et al., 2002). Glutamine is the most abundant amino acid in the body and plays several important biological functions. It stabilizes the immune system, strengthens intestinal cells, and protects against the effects of stress(Young et al., 1993). It is also the most important energy source of immune and intestinal cells. If there is a deficiency in this amino acid, these cells become sluggish and they cannot function properly. Several studies show that concentrations of Gln in the body are diminished during times of physical or psychological stress(Hertz & Richardson, 1983; Bowtell et al., 1999). Therefore, Gln supplementation may help animals cope with various stressors.

    Recently, we found that a Gln deficiency in the prefrontal cortex evokes depressive-like behaviors that are like those of a chronic stress-induced depression mouse model. Interestingly, exogenous Gln reverses the depressive-like behaviors(Lee et al., 2013). It was hypothesized that Gln reduced the physiological and behavioral changes induced by chronic stress, partly imposed by housing and feed practices. To our knowledge, there is no evidence as to whether supplementation with Gln would alleviate stress symptoms in chickens. Thus, we undertook this study to evaluate the effect of a diet supplemented with Gln on the stress levels and physiology of cage-reared chicks.

    Materials and Methods

    1 Animals and their care

    Male Hyline chickens were used for the study. They were reared at the animal facility of the Gyeongsangnam-do Livestock Veterinary Research Institute, Republic of Korea. Animal use procedures were performed in accordance with the National Institutes of Health(NIH, Bethesda, MD, USA) guidelines and following a protocol(GLA-100917- M0093) that had been approved by the Gyeongsang National University Institute Animal Care & Use Committee.

    2 Experimental design

    Three-day-old chicks were randomly assigned to one of three groups, with eight chicks per group. The control(CTL) group was fed Nonghyup premium poultry feed, with a protein content >20%(“normal feed”, Nonghyup Co., LTD, Korea). A second group was fed a low-Gln(GL) diet, prepared by supplementing the normal feed with 150 mg Gln/kg. A third group was fed a high-Gln diet(GH), prepared by supplementing the normal diet with 300 mg Gln/kg. The chicks were housed at 25ºC under continuous light in cages of area 0.24 m2(four chicks/cage). Body weight and feed consumption were measured every other day.

    3 Biochemical analyses of blood

    Blood samples were taken when the chicks were 32 days old. Blood was collected after a 24-h fast with a cardiac puncture made with a hypodermic needle and syringe. Five milliliters of blood were drawn from each chick and placed into an evacuated blood collection tube spray-coated with the anticoagulant K2-EDTA and mixed for 5 min. The plasma was separated using centrifugation of the whole blood for 10 min at 3000 rpm and stored at -70ºC until use. Plasma was analyzed with a Fuji Dri-Chem 3500i Biochemistry Analyzer(Fuji Film). Total bilirubin, total cholesterol, high-density lipoprotein cholesterol, uric acid, blood urea nitrogen, total protein, albumin, inorganic phosphate, glutamic oxaloacetic transaminase, gamma-glutamyltranspeptidase, and lactate dehydrogenase activity were assessed.

    4 Glutamine synthetase activity assay

    The glutamine synthetase(GS) activity assay was performed as previously described, with some modifications(Gawronski & Benson, 2004; Son et al., 2015). In brief, brain and liver tissues were homogenized in 50 mM imidazole(pH 7.5) lysis buffer. The solutions for color development were prepared following the method used in the previous report. In a set of reactions, 10 μL crude extract was added to eight PCR strip tubes(Thermo Scientific, UK). The reaction sets were prepared in duplicate to assess non-specific GS activity using methionine sulfoximine. The absorbance was measured at 690 nm with a Microplate Reader(TECAN, Austria).

    5 Western blot analysis

    Western blot analysis was performed as previously described(Son et al., 2015). Five micrograms of protein samples were separated with 10% SDS-PAGE and transferred to nitrocellulose paper. The nitrocellulose membrane was blocked using 5% skim milk and was incubated with anti-GS antibody(1:5000, MAB302, Millipore, USA). The bound antibodies were detected with an ECL detection kit(Pierce, USA). For quantification of the result, each band density was calculated using FUJI-FILM Multi Gauge software, and the density values were normalized using the corresponding α-tubulin density as an internal control.

    6 Enzyme-linked immunosorbent assay(EIA) of plasma corticosterone

    Quantification of plasma corticosterone levels was performed using the corticosterone EIA kit(Cayman, MI, USA) according to the manufacturer’s protocol and as described previously(Kim et al., 2014; Jung et al., 2016).

    7 Hematoxylin and eosin stain

    The chicks were euthanized using CO2 so that the tissues could be examined. Tissues were dissected from the carcasses and were fixed in 4% neutralized paraformaldehyde at 4ºC. They were washed in tap water overnight and cleared sequentially with an ascending alcohol series and xylene. The paraffin was infiltrated under vacuum in an oven and the tissues were embedded into the paraffin blocks. The blocks were sectioned in 10-um thick, stained with Mayer’s hematoxylin and eosin, mounted, and examined under a microscope.

    8 Statistics

    Data were assessed with a GraphPad Prism(ver 5.01). Changes in body weight were analyzed with two-way ANOVA and the Bonferroni post-test. Other variables were analyzed with one-way ANOVA and the Tukey post-test. A P-value less than 0.05 was considered to indicate a statistically significant result.

    Results

    1 Effects of Gln supplement on growth and blood corticosterone

    The overall growth pattern was similar in the three groups: There was an exponential growth phase from day 16 to day 26, after which growth reached a plateau(Fig. 1A). However, body weight of the groups supplemented with Gln was higher than that of the CTL, starting on day 26, and the GL group had significant body weight than the CTL group at day 28 and 30(Fig. 1A), with no remarkable difference in consumption(data not shown).

    Changes in body weight have often been considered a symptom of stress in experimental animal stress models(Joo et al., 2009); however, blood corticosterone is the most important indicator of stress in chicks (Cheng & Muir, 2004; Choi, 2007; Willems et al., 2015). Consequently, we measured blood corticosterone levels(Fig. 1B). Blood corticosterone levels from the CTL groups were higher than those of either of the other two groups. We speculate that exogenous Gln reduced the stress level that occurred during early growth period in these cage-reared chicks.

    2 Effects of Gln-supplementation on liver and brain tissues

    Gln can be synthesized de novo, mainly in the liver and brain tissues. We wished to determine if exogenous Gln supplementation affected endogenous GS activity and expression, and investigated the activity and expression of this enzyme in our experiment, employing a method that has been published previously (Son et al., 2015). Histological examinations of liver and brain were also performed; specifically, to determine if there were deleterious effects from the Gln-supplemented diet in these tissues.

    We did not find any pathological differences in the liver tissues between the groups receiving Gln supplementation and the CTL(Fig. 2A). The hepatocytes appeared healthy, and we observed well-developed, normal sinusoids around the portal vein in sections from all three groups. We also did not detect any differences in GS activity or expression among the groups(Fig. 2B, Fig. 2C).

    In the brain, GS is exclusively expressed in the astrocytes that surround active neurons and vessels, so we sectioned and stained the cortex. In these sections, prominent pyramidal neurons were present in the cortex of all groups. We did not detect any abnormal histological and we could not find any abnormal histological remarks. There was no evidence of neuronal atrophy or tissue damage(Fig. 3A).

    Furthermore, GS activity and expression was apparently unaffected by Gln supplement(Fig. 3B, Fig. 3C).

    3 Effects of Gln-supplementation on aspects of physiology

    We also evaluated liver function with blood biochemical examinations, specifically, activity assays for glutamic oxaloacetic transaminase, gamma-glutamyl transpeptidase, lactate dehydrogenase, and total bilirubin (Table 1). We observed no differences in these liver function indicators among the three groups. Similarly, total cholesterol and high density lipoprotein cholesterol were not different in the CTL group and groups receiving supplement. The results are presented in Table 1. The values that we measured in this study are all within the range of what is considered normal for avian species(Harrison & Lightfoot, 2006).

    To confirm the effects of Gln on kidney and general metabolic functions, we also measured plasma concentrations of total uric acid, blood urea nitrogen, albumin, total protein, calcium, and inorganic phosphate. The groups receiving supplements were not remarkably different than the control group(Table 1). We interpret these results as evidence that exogenous Gln had no deleterious effects on liver or kidney function, or on general metabolism.

    Discussion

    Here, we examined the possible benefits of Gln supplementation in young chicks reared in a stressful environment, which included caging and continuous light. There were at least three benefits. First, the supplement appeared to reduce the effects of stress as detected by lower blood corticosterone levels. Second, Gln had this effect with no harmful effects on a set of physiological parameters, as determined in blood biochemical examinations. Third, supplementation maintained normal growth, despite the stressful conditions.

    It has been shown that non-essential amino acids must be present in the diet for normal growth and maintenance of homeostasis, including Gln and glutamate(Maruyama et al., 1976; Meijer et al., 1995). However, very little attention has been given to the use of non-essential amino acids as dietary supplements over the past 50 years(Watford, 2015). This paucity of information applies to chicks, also, and the recommended diet for chicks includes guidelines only for the essential amino acids lysine, methionine, methionine plus cysteine, threonine, tryptophan, arginine, isoleucine, and valine(Hy-Line, 2016).

    The normal diet used in this study did not contain any information about the content of Gln. The rearing conditions used in this study, continuous lighting and small cages(each bird had 0.06 m2 of cage area), are somewhat stressful to chicks. This resulted in less growth of the CTL group: the average body weight at 4 wk was 256 g(Fig. 1A), which is less than the expected body weight of 260-270 g, reported by Management Guid Hyline (Hy-Line, 2016). In contrast, the average body weight of the GH group was 266 g, which is within the normal body-weight range, while the GL group had a body weight of 281 g(Fig. 1A), higher than normal. Although we did not examine the mechanism of the effect of exogenous Gln on growth, we conclude that supplementation with Gln counteracts the effects of stress on the early growth of cage-reared chicks.

    Glutamine is made from glutamate and ammonia via the action of GS, primarily in skeletal muscle, adipose tissue, the liver, and the brain. Glutamine is also a precursor for a number of biosynthetic pathways required for growth and cell division (Watford, 2015), and exogenous Gln may disturb metabolic processes in these organs, because it has been suggested that Gln synthetase activity and expression in cultured cells is subjected to downregulation in the presence of Gln(Huang et al., 2007). This led us to examine GS expression and activity in both the liver and the brain, as the most important organs of Gln production in the peripheral organs and the central nervous system, respectively(Dennis et al., 2015; Santos et al., 2016). The activity and expression of GS in the groups of chicks that received Gln supplements were similar to those of the CTL group (Fig. 2, Fig. 3). We also examined the blood biochemistry of three groups(Table 1). The results for all the parameters revealed no difference between the three groups, and all the plasma chemistry parameters were data were within the normal ranges(Harrison & Lightfoot, 2006). We conclude that these levels of supplementation that were used in this study are not deleterious to the chicks.

    Cage rearing is widely used in poultry farming in many countries because the labor costs are lower and less space is required than in yard rearing(Lay et al., 2011). However, cage rearing is somewhat stressful: the chicks are in a small space that restricts movement and requires ventilation rather than providing fresh air(Carey, 1987; Brantsaeter et al., 2016). Since it is known that exposure to stress can depress immune system function, farmers usually supplement vaccinations with additional antibiotics to prevent infectious diseases (El-Gohary et al., 2014; Park et al., 2015). Stressors present in the cage environment can also affect feeding behaviors, which results in less feed intake and less weight gain, both of which reduce productivity. It follows that reducing the stresses associated with cage rearing should increase immune functions and food intake, and benefit farmers and consumers.

    If organisms cope with stressors, hypothalamus releases corticotropin releasing hormone to pituitary portal vessels to evoke a burst out of adrenocorticotropic hormone(ACTH) into blood then ACTH stimulates adrenal cortex to increase glucocorticoids, which is so called stress response and corticosterone is the final reactive hormone in the stress response (Sapolsky et al., 2000). Thus blood corticosterone level is a good indicator of stress levels in chickens (Lin et al., 2004; Fraisse & Cockrem, 2006). By this measure, we could suggest that the stress level of the chicks should be decreased by Gln supplementation. An important consequence of this finding is that it might be possible to reduce the frequency and doses of antibiotics in cage-reared chicks that receive Gln supplements because less stress level might be closely related with improvement of immune functions(Baccan et al., 2004; Sasaguri et al., 2016; Simi et al., 2016). This study revealed that Gln supplementation maintained growth performance and reduced blood corticosterone concentrations in stressful conditions, and was not associated with any detectable pathological signs. The study also raises some questions. How does exogenous Gln reduce blood corticosterone level? Why was the body weight of the CTL group less than expected when they received a normal diet? What was the effect of supplementation with Gln on immune function, if any? These are interesting topics for further study. We propose, however, that supplementation with Gln is a safe and effective way to counteract the effects of stress of cage rearing on chicks.

    Acknowledgement

    This research was supported by the Basic Science Research Program through the National Research Foundation of Korea(NRF) funded by the Ministry of Education, Science, and Technology(NRF-2014R1A1A 4A01006451 and NRF-2015R1A5A2008833). This work was also partially supported by the Gyeongsang National University Fund for Professors on Sabbatical Leave, 2016.

    Figure

    JALS-52-91_F1.gif

    Body weight(A) and blood corticosterone level(B) of chicks receiving glutamine(Gln) supplement. The control(CTL) group received a normal diet, the GL group received a low level of supplementation, and the GH group received a higher level of supplementation. Note that body weight gain in the GL group during the last week was significantly greater than that of the CTL group and that plasma corticosterone levels in the groups receiving supplements were significantly lower than the CTL group. Data represent mean±SEM; n= 8 for (A), n= 6 for (B); *p<0.05, **p<0.01.

    JALS-52-91_F2.gif

    Hematoxylin and eosin(H&E)-stained liver sections(A), Western blot analysis of glutamine synthetase(GS) expression(B), and GS activity(C) in liver tissue from chicks receiving glutamine(Gln) supplements. For (A) arrows indicate sinusoids and asterisks(*) showed portal vein, and (B), upper panel: representative western blot result; lower panel: quantitative western blot result. The control(CTL) group received a normal diet, the GL group received a low level of supplementation, and the GH group received a higher level of supplementation. Note that there were no histological differences among the groups, and no significant difference(n.s.) in GS expression or activity. Data in (B) and (C) represent mean±SEM, n= 4 for (B) and (C).

    JALS-52-91_F3.gif

    Hematoxylin and eosin(H&E)-stained brain sections (A), western blot analysis of glutamine synthetase (GS) expression (B), and GS activity (C) in the prefrontal cortex of chicks receiving glutamine(Gln) supplements. For (A) arrows indicate pyramidal neurons, and (B), upper panel: representative western blot result; lower panel: quantitative western blot result. The control(CTL) group received a normal diet, the GL group received a low level of supplementation, and the GH group received a higher level of supplementation. Note that there were no histological differences among the groups, and no significant difference(n.s.) in GS expression or activity. Data represent mean±SEM, n= 4 for (B) and (C).

    Table

    The effects of glutamine diet on blood biochemical parameters1)

    1)Values in each item were analyzed via One-way ANOVA with Post-hoc test but no significant difference was found. All P values from each item were over 0.1.

    Reference

    1. G.C. Baccan , R.D. Oliverra , B. Mantovani (2004) Stress and immunological phagocytosis: possible nongenomic action of corticosterone., Life Sci., Vol.75 ; pp.1357-1368
    2. A Borsoi , WM Quinteiro-Filho , AS Calefi , AJ Ferreira , CS Astolfi-Ferreira , JC Florio (2015) Effects of cold stress and Salmonella Heidelberg infection on bacterial load and immunity of chickens., Avian Pathol., Vol.44 ; pp.490-497
    3. J.L. Bowtell , K. Gelly , M.L. Jackman , A. Patel , M. Simeoni , M.J. Rennie (1999) Effect of oral glutamine on whole body carbohydrate storage during recovery from exhaustive exercise., J. Appl. Physiol., Vol.86 ; pp.1770-1777
    4. M. Brantsaeter , J. Nordgreen , T.B. Rodenburg , F.M. Tahamtani , A. Popova , A.M. Janczak (2016) Exposure to Increased Environmental Complexity during Rearing Reduces Fearfulness and Increases Use of Three-Dimensional Space in Laying Hens(Gallus gallus domesticus)., Front. Vet. Sci., Vol.3 ; pp.14
    5. J.W. Campbell , D.D. Smith Jr (1992) Metabolic compartmentation of vertebrate glutamine synthetase: putative mitochondrial targeting signal in avian liver glutamine synthetase., Mol. Biol. Evol., Vol.9 ; pp.787-805
    6. J.B. Carey (1987) Effects of pullet-stocking density on performance of laying hens., Poult. Sci., Vol.66 ; pp.1283-1287
    7. H.W. Cheng , W.M. Muir (2004) Chronic social stress differentially regulates neuroendocrine responses in laying hens: II. Genetic basis of adrenal responses under three different social conditions., Psychoneuroendocrinology, Vol.29 ; pp.961-971
    8. Y. Choi (2007) Management of Stress in Poultry Production., Korean Society of Poultry Science., Vol.34 ; pp.295-300
    9. R.A. Dennis , U. Ponnappan , R.L. Kodell , K.K. Garner , C.M. Parkes , M.M. Bopp , K.P. Padala , C.A. Peterson , P.R. Padala , D.H. Sullivan (2015) Immune function and muscle adaptations to resistance exercise in older adults: Study protocol for a randomized controlled trial of a nutritional supplement., Trials, Vol.16 ; pp.121
    10. Y. Duan , W. Fu , S. Wang , Y. Ni , R. Zhao (2014) Cholesterol deregulation induced by chronic corticosterone(CORT) stress in pectoralis major of broiler chickens., Comp. Biochem. Physiol. Mol. Integr. Physiol., Vol.176 ; pp.59-64
    11. F.A. El-Gohary , W.E. Huff , G.R. Huff , N.C. Rath , Z.Y. Zhou , A.M. Donoghue (2014) Environmental augmentation with bacteriophage prevents colibacillosis in broiler chickens., Poult. Sci., Vol.93 ; pp.2788-2792
    12. F. Fraisse , J.F. Cockrem (2006) Corticosterone and fear behaviour in white and brown caged laying hens., Br. Poult. Sci., Vol.47 ; pp.110-119
    13. W. Fu , Y. Duan , S. Wand , Y. Ni , R. Grossmann , R. Zhao (2014) Comparative proteomic analysis of the breast muscle response to chronic corticosterone administration in broiler chickens showing long or short tonic immobility., Poult. Sci., Vol.93 ; pp.784-793
    14. J.D. Gawronski , D.R. Benson (2004) Microtiter assay for glutamine synthetase biosynthetic activity using inorganic phosphate detection., Anal. Biochem., Vol.327 ; pp.114-118
    15. A.V. Gomes , W.M. Quinteiro-Filho , A. Ribeiro , V. Ferraz-De-Paula , M.L. Pinheiro , E. Baskeville , A.T. Akamine , C.S. Astolfi-Ferreira , A.J. Ferreira , J. Palermo-Neto (2014) Overcrowding stress decreases macrophage activity and increases Salmonella Enteritidis invasion in broiler chickens., Avian Pathol., Vol.43 ; pp.82-90
    16. G.J. Harrison , T.L. Lightfoot (2006) Clinical avian medicine., Avian Medicine Online by Harrison's Bird Foods,
    17. L. Hertz , J.S. Richardson (1983) Acute and chronic effects of antidepressant drugs on beta-adrenergic function in astrocytes in primary cultures: an indication of glial involvement in affective disorders?, J. Neurosci. Res., Vol.9 ; pp.173-182
    18. Y. Huang , Y. Wang , M. Watford (2007) Glutamine directly downregulates glutamine synthetase protein levles in mouse C2C12 skeletal muscle myotubes., J. Nutr., Vol.137 ; pp.1357-1362
    19. HY-LINE (2016) Management Guide-Hy-Line International, pp. 1-41, www.hyline.com/UserDocs/Pages/BRN_COM_ENG.pdf
    20. Y. Joo , K.M. Choi , Y.H. Lee , G. Kim , D.H. Lee , G.S. Roh , S.S. Kang , G.J. Cho , W.S. Choi , H.J. Kim (2009) Chronic immobilization stress induces anxiety- and depression-like behaviors and decreases transthyretin in the mouse cortex., Neurosci. Lett., Vol.461 ; pp.121-125
    21. S. Jung , H. Son , D.H. Lee , G.S. Roh , S.S. Kang , G.J. Cho , W.S. Choi , H.J. Kim (2016) Decreased levels of RGS4 in the paraventricular nucleus facilitate GABAergic inhibition during the acute stress response., Biochem. Biophys. Res. Commun., Vol.472 ; pp.276-280
    22. G. Kim , S. Jung , H. Son , S. Kim , J. Choi , D.H. Lee , G.S. Roh , S.S. Kang , G.J. Cho , W.S. Choi , H.J. Kim (2014) The GABAB receptor associates with regulators of G-protein signaling 4 protein in the mouse prefrontal cortex and hypothalamus., BMB Rep., Vol.47 ; pp.324-329
    23. J. Kim , Y.H. Choi (2014) Differential abundance of egg white proteins in laying hens treated with corticosterone., J. Agric. Food Chem., Vol.62 ; pp.12346-12359
    24. D.C. Lay Jr, R.M. Fulton , P.Y. Hester , D.M. Karcher , J. Kjaer , J.A. Bm Mench , B.A. Mullens , R.C. Newberry , C.J. Nicol , N.P. O ?(tm)sullivan , R.E. Porter (2011) Hen welfare in different housing systems., Poult. Sci., Vol.90 ; pp.278-294
    25. Y. Lee , H. Son , G. Kim , S. Kim , D.H. Lee , G.S. Roh , S.S. Kang , G.J. Cho , W.S. Choi , H.J. Kim (2013) Glutamine deficiency in the prefrontal cortex increases depressive-like behaviours in male mice., J. Psychiatry Neurosci., Vol.38 ; pp.183-191
    26. A.M. Limami , C. Rouillon , G. Glevarec , A. Gallais , B. Hirel (2002) Genetic and physiological analysis of germination efficiency in maize in relation to nitrogen metabolism reveals the importance of cytosolic glutamine synthetase., Plant Physiol., Vol.130 ; pp.1860-1870
    27. H. Lin , E. Decuypere , J. Buyse (2004) Oxidative stress induced by corticosterone administration in broiler chickens(Gallus gallus domesticus) 2. Shortterm effect. Com. Biochem. Physiol. B Biochem., Mol. Biol., Vol.139 ; pp.745-751
    28. K. Maruyama , M.L. Sunde , A.E. Harper (1976) Is L-glutamic acid nutritionally a dispensable amino acid for the young chick?, Poult. Sci., Vol.55 ; pp.45-60
    29. G.A. Meijer , J. Van Der Meulen , J.G. Bakker , C.J. Van Der Koelen , A.M. Van Vuuren (1995) Free amino acids in plasma and muscle of high yielding dairy cows in early lactation., J. Dairy Sci., Vol.78 ; pp.1131-1141
    30. J.Y. Park , S. Kim , J.Y. Oh , H.R. Kim , I. Jang , H.S. Lee , Y.K. Kwon (2015) Characterization of Clostridium perfringens isolates obtained from 2010 to 2012 from chickens with necrotic enteritis in Korea., Poult. Sci., Vol.94 ; pp.1158-1164
    31. G. Patejunas , A.P. Young (1987) Tissue-specific regulation of avian glutamine synthetase expression during development and in response to glucocorticoid hormones., Mol. Cell. Biol., Vol.7 ; pp.1070-1077
    32. S. Rettenbacher , E. Mostl , R. Hackl , R. Palme (2005) Corticosterone in chicken eggs., Ann. N. Y. Acad. Sci., Vol.1046 ; pp.193-203
    33. AC Santos , CA Correia , DC De Oliveira (2016) Intravenous Glutamine Administration Modulates TNF-alpha/IL-10 Ratio and Attenuates NFkB Phosphorylation in a Protein Malnutrition Model., Inflammation, Vol.39 ; pp.1883-1891
    34. R.M. Sapolsky , L.M. Romero , A.U. Munck (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions., Endocr. Rev., Vol.21 ; pp.55-89
    35. K. Sasaguri , K. Yamada , Y. Narimatsu , M. Oonuki , A. Oishi , K. Koda , K.Y. Kubo , T. Yamamoto , T. Kaoya (2016) Stress-induced galectin-1 influences immune tolerance in the spleen and thymus by modulating CD45 immunoreactive lymphocytes., J. Physiol. Sci., Vol.67 ; pp.489-496
    36. S. Shini , P. Kaiser (2009) Effects of stress, mimicked by administration of corticosterone in drinking water, on the expression of chicken cytokine and chemokine genes in lymphocytes., Stress, Vol.12 ; pp.388-399
    37. S. Simi , V.S. Peter , M.C. Subhash Peter (2016) Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish(Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response., Gen. Comp. Endocrinol., Vol.251 ; pp.94-108
    38. S.H. Sohn , I. Jang , B.R. Son (2011) Effect of housing system of cage and floor on the production performance and stress response in layer., Korean J. Poult. Sci., Vol.38 ; pp.305-313
    39. H. Son , S. Jung , J.Y. Kim , Y.M. Goo , K.M. Cho , D.H. Lee , G.S. Roh , S.S. Kang , G.J. Cho , W.S. Choi , H.J. Kim (2015) Type 1 diabetes alters astrocytic properties related with neurotransmitter supply, causing abnormal neuronal activities., Brain Res., Vol.1602 ; pp.32-43
    40. X. Sun , H. Zhang , A. Sheikhahmadi , Y. Wang , H. Jiao , H. Lin , Z. Song (2015) Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens(Gallus gallus domesticus)., Int. J. Biometeorol., Vol.59 ; pp.127-135
    41. M. Watford (2015) Glutamine and glutamate: Nonessential or essential amino acids?, Animal Nutrition., Vol.1 ; pp.119-122
    42. E. Willems , Y. Wang , A. Koppenol , J. Lesuisse , L. Franssens , E. Decuypere , J. Buyse , N. Everaert (2015) Reduced protein availability by albumen removal during chicken embryogenesis decreases body weight and induces hormonal changes., Exp. Physiol., Vol.100 ; pp.1298-1308
    43. L.S. Young , R. Bye , M. Scheltinga , T.R. Ziegler , D.O. Jacobs , D.W. Wilmore (1993) Patients receiving glutamine-supplemented intravenous feedings report an improvement in mood., JPEN J. Parenter. Enteral Nutr., Vol.17 ; pp.422-427
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