REVIEW

Effects and Mechanism of Weaning Stress on Immune System in Young Ruminants

  • ZHANG Qian ,
  • LI Fadi ,
  • LI Fei
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  • 1. Key State Laboratory of Agro-Ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China;
    2. Biotechnology Engineering Laboratory of Gansu Meat Sheep Breeding, Minqin 733300, China

Received date: 2016-01-21

  Online published: 2016-07-28

Abstract

The digestive and immune systems have not yet developed completely, when young ruminants were weaned. Weaning stress leaded to adolescent alterations in hormone levels and immune function, which could suppress immune system and cause inflammatory response, consequently restricted their growth and increased the risk of disease in ruminants. In this article, the effects and mechanism of weaning stress on the immune system in young ruminants were discussed, focusing on glucocorticoid, immune cell, acute phase proteins and related cytokine, with the aim of providing a scientific basis for the relevant research.

Cite this article

ZHANG Qian , LI Fadi , LI Fei . Effects and Mechanism of Weaning Stress on Immune System in Young Ruminants[J]. Chinese Journal of Animal Nutrition, 2016 , 28(7) : 1988 -1997 . DOI: 10.3969/j.issn.1006-267x.2016.07.003

References

[1] ENRÍQUEZ D,HÖTZEL M J,UNGERFELD R.Minimising the stress of weaning of beef calves:a review[J].Acta Veterinaria Scandinavica,2011,53(1):28.
[2] GREENWOOD P L,CAFE L M.Prenatal and pre-weaning growth and nutrition of cattle:long-term consequences for beef production[J].Animal,2007,1(9):1283-1296.
[3] O'LOUGHLIN A,MCGEE M,DOYLE S,et al.Biomarker responses to weaning stress in beef calves[J].Research in Veterinary Science,2014,97(2):458-463.  
[4] LAMBERTZ C,FARKE-RÖVER A,GAULY M.Effects of sex and age on behavior and weight gain in beef calves after abrupt weaning[J].Animal Science Journal,2015,86(3):345-350.  
[5] OBRIST P A,GAEBELEIN C J,TELLER E S,et al.The relationship among heart rate,carotid dP/dt,and blood pressure in humans as a function of the type of stress[J].Psychophysiology,1978,15(2):102-115.  
[6] GREENWOOD P L,CAFE L M,HEARNSHAW H,et al.Consequences of nutrition and growth retardation early in life for growth and composition of cattle and eating quality of beef[J].Recent Advances in Animal Nutrition in Australia,2005,15:183-195.
[7] HULBERT L E,COBB C J,CARROLL J A,et al.The effects of early weaning on innate immune responses of Holstein calves[J].Journal of Dairy Science,2011,94(5):2545-2556.  
[8] CALLAN R J,GARRY F B.Biosecurity and bovine respiratory disease[J].Veterinary Clinics of North America:Food Animal Practice,2002,18(1):57-77.  
[9] DUFF G C,GALYEAN M L.Board-invited review:recent advances in management of highly stressed,newly received feedlot cattle[J].Journal of Animal Science,2007,85(3):823-840.
[10] SNOWDER G.Genetics,environment and bovine respiratory disease[J].Animal Health Research Reviews,2009,10(2):117-119.  
[11] NOCEK J E,BRAUND D G,WARNER R G.Influence of neonatal colostrum administration,immunoglobulin,and continued feeding of colostrum on calf gain,health,and serum protein[J].Journal of Dairy Science,1984,67(2):319-333.  
[12] XU R J.Development of the newborn GI tract and its relation to colostrum/milk intake:a review[J].Reproduction Fertility and Development,1996,8(1):35-48.  
[13] HICKEY M C,DRENNAN M,EARLEY B.The effect of abrupt weaning of suckler calves on the plasma concentrations of cortisol,catecholamines,leukocytes,acute-phase proteins and in vitro interferon-gamma production[J].Journal of Animal Science,2003,81(11):2847-2855.
[14] KIM M H,YANG J Y,UPADHAYA S D,et al.The stress of weaning influences serum levels of acute-phase proteins,iron-binding proteins,inflammatory cytokines,cortisol,and leukocyte subsets in Holstein calves[J].Journal of Veterinary Science,2011,12(2):151-157.  
[15] LYNCH E M,EARLEY B,MCGEE M,et al.Effect of abrupt weaning at housing on leukocyte distribution,functional activity of neutrophils,and acute phase protein response of beef calves[J].BMC Veterinary Research,2010,6(1):39.
[16] LYNCH E M,EARLEY B,MCGEE M,et al.Characterisation of physiological and immunological responses in beef cows to abrupt weaning and subsequent housing[J].BMC Veterinary Research,2010,6(1):37.
[17] LYNCH E M,MCGEE M,DOYLE S,et al.Effect of post-weaning management practices on physiological and immunological responses of weaned beef calves[J].Irish Journal of Agricultural and Food Research,2011,50(2):161-174.
[18] LYNCH E M,MCGEE M,DOYLE S,et al.Effect of pre-weaning concentrate supplementation on peripheral distribution of leukocytes,functional activity of neutrophils,acute phase protein and behavioural responses of abruptly weaned and housed beef calves[J].BMC Veterinary Research,2012,8(1):1.
[19] O'LOUGHLIN A,LYNN D J,MCGEE M,et al.Transcriptomic analysis of the stress response to weaning at housing in bovine leukocytes using RNA-seq technology[J].BMC Genomics,2012,13(1):250.
[20] O'LOUGHLIN A,MCGEE M,WATERS S M,et al.Examination of the bovine leukocyte environment using immunogenetic biomarkers to assess immunocompetence following exposure to weaning stress[J].BMC Veterinary Research,2011,7(1):45.
[21] PAZIRANDEH A,XUE Y,PRESTEGAARD T,et al.Effects of altered glucocorticoid sensitivity in the T cell lineage on thymocyte and T cell homeostasis[J].The FASEB Journal,2002,16(7):727-729.
[22] BOMMHARDT U,BEYER M,HüNIG T,et al.Molecular and cellular mechanisms of T cell development[J].Cellular and Molecular Life Sciences CMLS,2004,61(3):263-280.  
[23] FRAKER P J,KING L E.Reprogramming of the immune system during zinc deficiency[J].Annual Review of Nutrition,2004,24(1):277-298.  
[24] BIOLATTI B,BOLLO E,CANNIZZO F T,et al.Effects of low-dose dexamethasone on thymus morphology and immunological parameters in veal calves[J].Journal of Veterinary Medicine Series A,2005,52(4):202-208.  
[25] BISWAS R,ROY T,CHATTOPADHYAY U.Prolactin induced reversal of glucocorticoid mediated apoptosis of immature cortical thymocytes is abrogated by induction of tumor[J].Journal of Neuroimmunology,2006,171(1/2):120-134.
[26] RODRIGUES-MASCARENHAS S,FERNANDES DOS SANTOS N,RUMJANEK V M.Synergistic effect between ouabain and glucocorticoids for the induction of thymic atrophy[J].Bioscience Reports,2006,26(2):159-169.  
[27] GLASER R,KIECOLT-GLASER J K.Stress-induced immune dysfunction:implications for health[J].Nature Reviews Immunology,2005,5(3):243-251.  
[28] MINTON J E,PARSONS K M.Adrenocorticotropic hormone and cortisol response to corticotropin-releasing factor and lysine vasopressin in pigs[J].Journal of Animal Science,1993,71(3):724-729.
[29] RIVIER C,VALE W.Interaction of corticotropin-releasing factor and arginine vasopressin on adrenocorticotropin secretion in vivo[J].Endocrinology,1983,113(3):939-942.  
[30] WATABE T,TANAKA K,KUMAGAE M,et al.Role of endogenous arginine vasopressin in potentiating corticotropin-releasing hormone-stimulated corticotropin secretion in man[J].The Journal of Clinical Endocrinology & Metabolism,1988,66(6):1132-1137.  
[31] AUPHAN N,DIDONATO J A,ROSETTE C,et al.Immunosuppression by glucocorticoids:inhibition of NF-κB activity through induction of IκB synthesis[J].Science,1995,270(5234):286-290.  
[32] WRIGHTON C J,HOFER-WARBINEK R,MOLL T,et al.Inhibition of endothelial cell activation by adenovirus-mediated expression of I kappa B alpha,an inhibitor of the transcription factor NF-kappa B[J].Journal of Experimental Medicine,1996,183(3):1013-1022.  
[33] CONNOR T J,BREWER C,KELLY J P,et al.Acute stress suppresses pro-inflammatory cytokines TNF-α and IL-1β independent of a catecholamine-driven increase in IL-10 production[J].Journal of Neuroimmunology,2005,159(1/2):119-128.
[34] CURTIN N M,BOYLE N T,MILLS K H G,et al.Psychological stress suppresses innate IFN-γ production via glucocorticoid receptor activation:reversal by the anxiolytic chlordiazepoxide[J].Brain,Behavior,and Immunity,2009,23(4):535-547.  
[35] MARX J.Immunology:how the glucocorticoids suppress immunity[J].Science,1995,270(5234):232-233.  
[36] MELTZER J C,MACNEIL B J,SANDERS V,et al.Stress-induced suppression of in vivo splenic cytokine production in the rat by neural and hormonal mechanisms[J].Brain,Behavior,and Immunity,2004,18(3):262-273.  
[37] CARROLL J A,ARTHINGTON J D,CHASE C C.Early weaning alters the acute-phase reaction to an endotoxin challenge in beef calves[J].Journal of Animal Science,2009,87(12):4167-4172.  
[38] HU X Y,LI W P,MENG C,et al.Inhibition of IFN-γ signaling by glucocorticoids[J].Journal of Immunology,2003,170(9):4833-4839.  
[39] JOHNSON J D,O'CONNOR K A,DEAK T,et al.Prior stressor exposure sensitizes LPS-induced cytokine production[J].Brain,Behavior,and Immunity,2002,16(4):461-476.  
[40] GOUJON E,PARNET P,LAYE S,et al.Stress downregulates lipopolysaccharide-induced expression of proinflammatory cytokines in the spleen,pituitary,and brain of mice[J].Brain,Behavior,and Immunity,1995,9(4):292-303.  
[41] ZAHOREC R.Ratio of neutrophil to lymphocyte counts-rapid and simple parameter of systemic inflammation and stress in critically ill[J].Bratislavské Lekárske Listy,2001,102(1):5-14.
[42] DHABHAR F S.A hassle a day may keep the pathogens away:the fight-or-flight stress response and the augmentation of immune function[J].Integrative and Comparative Biology,2009,49(3):215-236.  
[43] TEMPELMAN R J,SAAMA P M,FREEMAN A E,et al.Genetic variation in bovine neutrophil sensitivity to glucocorticoid challenge[J].Acta Agriculturae Scandinavica,Section A-Animal Science,2002,52(4):189-202.  
[44] SAUL A N,OBERYSZYN T M,DAUGHERTY C,et al.Chronic stress and susceptibility to skin cancer[J].Journal of the National Cancer Institute,2005,97(23):1760-1767.  
[45] JONES M L,ALLISON R W.Evaluation of the ruminant complete blood cell count[J].Veterinary Clinics of North America:Food Animal Practice,2007,23(3):377-402.  
[46] EMLEN W,CARL V,BURDICK G.Mechanism of transfer of immune complexes from red blood cell CR1 to monocytes[J].Clinical & Experimental Immunology,1992,89(1):8-17.
[47] LAZARUS A H,ELLIS J,SEMPLE J W,et al.Comparison of platelet immunity in patients with SLE and with ITP[J].Transfusion Science,2000,22(1/2):19-27.
[48] LIPPI G,FRANCHINI M.Platelets and immunity:the interplay of mean platelet volume in health and disease[J].Expert Review of Hematology,2015,8(5):555-557.  
[49] WAZNA E.Platelet-mediated regulation of immunity[J].Postepy Higieny Ⅰ Medycyny Doswiadczalnej,2006,60:265-277.
[50] GARRAUD O,COGNASSE F.Platelet immunology and the immune response[J].Transfusion Clinique et Biologique,2009,16(2):106-117.  
[51] MCDOWELL G H.Hormonal control of glucose homoeostasis in ruminants[J].Proceedings of the Nutrition Society,1983,42(2):149-167.  
[52] SHOELSON S E,LEE J,GOLDFINE A B.Inflammation and insulin resistance[J].Journal of Clinical Investigation,2006,116(7):1793-1801.  
[53] AKBARI H,DALIR-NAGHADEH B,ASRI-REZAEI S,et al.Experimental hyperlipidemia induces insulin resistance in sheep[J].Domestic Animal Endocrinology,2015,53:95-102.
[54] VOSOOGHI-POOSTINDOZ V,FOROUGHI A R,DELKHOROSHAN A,et al.Effects of different levels of protein with or without probiotics on growth performance and blood metabolite responses during pre- and post-weaning phases in male Kurdi lambs[J].Small Ruminant Research,2014,117(1):1-9.  
[55] BACH A,DOMINGO L,MONTORO C,et al.Short communication:insulin responsiveness is affected by the level of milk replacer offered to young calves[J].Journal of Dairy Science,2013,96(7):4634-4637.  
[56] GODSON D L,BACA-ESTRADA M E,VAN KESSEL A G,et al.Regulation of bovine acute phase responses by recombinant interleukin-1 beta[J].Canadian Journal of Veterinary Research,1995,59(4):249-255.
[57] GRUYS E,TOUSSAINT M J,NIEWOLD T A,et al.Acute phase reaction and acute phase proteins[J].Journal of Zhejiang University:Science B,2005,6(11):1045-1056.
[58] PETERSEN H H,NIELSEN J P,HEEGAARD P M H.Application of acute phase protein measurements in veterinary clinical chemistry[J].Veterinary Research,2004,35(2):163-187.  
[59] CARROLL J A,FORSBERG N E.Influence of stress and nutrition on cattle immunity[J].Veterinary Clinics of North America:Food Animal Practice,2007,23(1):105-149.  
[60] ARTHINGTON J D,EICHERT S D,KUNKLE W E,et al.Effect of transportation and commingling on the acute-phase protein response,growth,and feed intake of newly weaned beef calves[J].Journal of Animal Science,2003,81(5):1120-1125.
[61] HORADAGODA N U,KNOX K M G,GIBBS H A,et al.Acute phase proteins in cattle:discrimination between acute and chronic inflammation[J].Veterinary Record,1999,144(16):437-441.  
[62] MORINOBU A,KUMAGAI S.Cytokine measurement at a single-cell level to analyze human Th1 and Th2 cells[J].The Japanese Journal of Clinical Pathology,1998,46(9):908-914.
[63] BOEHM U,KLAMP T,GROOT M,et al.Cellular responses to interferon-γ[J].Annual Review of Immunology,1997,15(1):749-795.  
[64] SPORER K R B,BURTON J L,EARLEY B,et al.Transportation stress in young bulls alters expression of neutrophil genes important for the regulation of apoptosis,tissue remodeling,margination,and anti-bacterial function[J].Veterinary Immunology and Immunopathology,2007,118(1/2):19-29.
[65] BAILEY M T,KINSEY S G,PADGETT D A,et al.Social stress enhances IL-1β and TNF-α production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b+ cells[J].Physiology & Behavior,2009,98(3):351-358.  
[66] NAGATA S,GOLSTEIN P.The Fas death factor[J].Science,1995,267(5203):1449-1456.  
[67] KIM J M,KIM S S,LEE Y D.Fas-associated factor 1 promotes in neurofibrillary tangle-mediated cell death of basal forebrain cholinergic neurons in P301L transgenic mice[J].Neuroreport,2015,26(13):767-772.
[68] SPORER K R B,XIAO L,TEMPELMAN R J,et al.Transportation stress alters the circulating steroid environment and neutrophil gene expression in beef bulls[J].Veterinary Immunology and Immunopathology,2008,121(3/4):300-320.
[69] YIN D L,TUTHILL D,MUFSON R A,et al.Chronic restraint stress promotes lymphocyte apoptosis by modulating CD95 expression[J].Journal of Experimental Medicine,2000,191(8):1423-1428.  
[70] YIN D L,ZHANG Y,STUART C,et al.Chronic restraint stress modulates expression of genes in murine spleen[J].Journal of Neuroimmunology,2006,177(1/2):11-17.
[71] COQUERET O.New roles for p21 and p27 cell-cycle inhibitors:a function for each cell compartment[J].Trends in Cell Biology,2003,13(2):65-70.  
[72] HINGORANI R,BI B Y,DAO T,et al.CD95/Fas signaling in T lymphocytes induces the cell cycle control protein p21cip-1/WAF-1,which promotes apoptosis[J].The Journal of Immunology,2000,164(8):4032-4036.  
[73] GAN L,LI L W.Regulations and roles of the interleukin-1 receptor associated kinases (IRAKs) in innate and adaptive immunity[J].Immunologic Research,2006,35(3):295-302.  
[74] LEHNARDT S,LACHANCE C,PATRIZI S,et al.The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS[J].Journal of Neuroscience,2002,22(7):2478-2486.
[75] ZHANG Y,WOODRUFF M,ZHANG Y,et al.Toll-like receptor 4 mediates chronic restraint stress-induced immune suppression[J].Journal of Neuroimmunology,2008,194(1/2):115-122.
[76] ZHANG Y,ZHANG Y,MIAO J Y,et al.Chronic restraint stress promotes immune suppression through Toll-like receptor 4-mediated phosphoinositide 3-kinase signaling[J].Journal of Neuroimmunology,2008,204(1/2):13-19.
[77] SHAHRARA S,PARK C C,TEMKIN V,et al.RANTES modulates TLR4-induced cytokine secretion in human peripheral blood monocytes[J].Journal of Immunology,2006,177(8):5077-5087.  
[78] LU Y C,YEH W C,OHASHI P S.LPS/TLR4 signal transduction pathway[J].Cytokine,2008,42(2):145-151.  
[79] SEKI E,DE MINICIS S,ÖSTERREICHER C H,et al.TLR4 enhances TGF-β signaling and hepatic fibrosis[J].Nature Medicine,2007,13(11):1324-1332.  
[80] KANSAS G S.Selectins and their ligands:current concepts and controversies[J].Blood,1996,88(9):3259-3287.
[81] WEBER P S D,TOELBOELL T,CHANG L C,et al.Mechanisms of glucocorticoid-induced down-regulation of neutrophil L-selectin in cattle:evidence for effects at the gene-expression level and primarily on blood neutrophils[J].Journal of Leukocyte Biology,2004,75(5):815-827.
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