Abstract
Bovine respiratory disease complex (BRD), a major economic concern to the beef cattle industry all over the world, is triggered by physical, biological and psychological stresses. It is becoming noticeable that the key to reducing BRD appears to be centered at reducing the response to stress. The aims of the present study were to detect individual variations in the stress response of newly received young calves through their leukocyte heat shock protein (Hsp) response, selected neutrophil-related gene expression and oxidative stress, and relate them to pulmonary adhesions at slaughter, an indicative sign of clinical and subclinical episodes of BRD at an early age. Differential expression patterns of Hsp60 and Hsp70A1A were revealed in newly received calves 1 h, 5 h and 1 day after arrival, distinguishing between stress-responsive and non-stress-responsive individuals. Plasma cortisol was also indicative of stress-responsive and non-stress-responsive individuals, 1 h and 5 h after arrival. At the longer term, β-glycan levels were highest 7 days after arrival and significantly correlated with an adhesion-free phenotype at slaughter. Oxidative stress responses, measured through the oxidation products of the exogenous linoleoyl tyrosine (LT) marker, revealed that hydroperoxidation and epoxidation of membranes may readily occur. Based on the LT oxidation products and levels of β-glycan, we present a discriminant analysis model, according to which vulnerable individuals may be predicted at near 100% probability 7 days after arrival. Since clinical signs of BRD may often go undetected in feedlot calves, such a model, after its examination in large-scale experiments, may be a reliable tool for an early prediction of subclinical signs of BRD.
Similar content being viewed by others
References
Aich P, Jalal S, Czuba C, Schatte G, Herzog K, Olson DJH, Ross ARS, Potter AA, Babiuk LA, Griebel P (2007) Comparative approaches to the investigation of responses to stress and viral infection in cattle. OMICS 11(4):413–434
Asea A, Rehli M, Kabingu E, Boch JA, Baré O, Auron PE, Stevenson MA, Calderwood SK (2002) Novel signal transduction pathway utilized by extracellular HSP70. J Biol Chem 277:15028–15034
Bao E, Sultan KR, Nowak B, Hartung J (2008) Expression and distribution of heat shock proteins in the heart of transported pigs. Cell Stress Chaperones 13:459–466
Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int Immunol 12:1539–1546
Blecha F, Boyles SL, Riley JG (1984) Shipping suppresses lymphocyte blastogenic responses in Angus and Brahman Angus feeder calves. J Anim Sci 59(3):576–583
Brosh A, Lidski I, Nitsan Z (1992) The effect of the fat level in milk replacer on its digestibility and performance of suckling calves. Meshek Habakar VeHahalav Heker Uma'as 14:25–31 (in Hebrew)
Buckham Sporer KR, Burton JL, Earley B, Crowe MA (2007) Transportation stress in young bulls alters expression of neutrophil genes important for the regulation of apoptosis, tissue remodeling, margination, and anti-bacterial function. Vet Immun Immunopath 118:19–29
Burton JL, Madsen SA, Chang LC, Weber PSD, Buckham KR, van Dorp R, Hickey MC, Earley B (2005) Gene expression signatures in neutrophils exposed to glucocorticoids: a new paradigm to help explain “neutrophil dysfunction” in parturient dairy cows. Vet Immun Immunopath 105:197–219
Campisi J, Leem TH, Fleshner M (2003) Stress-induced extracellular Hsp72 is functionally significant danger signal to the immune system. Cell Stress Chaperones 8:272–286
Chang LC, Madsen SA, Toelboell T, Weber PSD, Burton JL (2004) Effects of glucocorticoids on Fas gene expression in bovine blood neutrophils. J Endocrinol 183:569–583
Chen W, Syldath U, Bellmann K, Burkart V, Kolb H (1999) Human 60-kDa heat shock protein: a danger signal to the innate immune system. J Immunol 162(6):3212–3219
Chirase NK, Greene LW, Purdy CW, Loan RW, Briggs RE, McDowell LR (2001) Effect of environmental stressors on ADG, serum retinol and α-tocopherol concentrations, and incidence of bovine respiratory disease of feeder steers (abstr). J Anim Sci 79(suppl 1):188
Chirase NK, Greene LW, Purdy CW, Loan RW, Auvermann BW, Parker DB, Walborg EF Jr, Stevenson DE, Xu Y, Klaunig JE (2004) Effect of transport stress on respiratory disease, serum antioxidant status, and serum concentrations of lipid peroxidation biomarkers in beef cattle. Am J Vet Res 65:860–864
Cobb JM, Steptoe A (1996) Psychosocial stress and susceptibility to upper respiratory tract illness in an adult population sample. Psychosom Med 58:404–412
Craig EA, Lindquist S (1988) The heat shock proteins. Annu Rev Genet 22:631–677
Eustace BK, Jay DG (2004) Extracellular roles for the molecular chaperone Hsp90. Cell Cycle 3:1098–1100
Fligiel SEG, Standiford T, Fligiel HM, Tashkin D, Strieter RM, Warner RL, Johnson KJ, Varani J (2006) Matrix metalloproteinases and matrix metalloproteinase inhibitors in acute lung injury. Hum Pathol 37:422–430
Freestone PPE, Sandrini SM, Haigh RD, Lyte M (2008) Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 16:55–64
Gardner BA, Dolezal HG, Bryant LK, Owens FN, Smith RA (1999) Health of finishing steers: effects on performance, carcass traits and meat tenderness. J Anim Sci 77:3168–3175
Gupta S, Earley B, Crowe MA (2007) Effect of 12-h road transportation on physiological, immunological, and haematological parameters in bulls housed at different space allowances. Vet J 173:605–616
Haddad JJ, Saadé NE, Safieh-Garabedian B (2002) Cytokines and neuron-immune–endocrine interactions: a role for the hypothalamic–pituitary–adrenal revolving axis. J Neuroimmunol 133(1–2):1–19
Hickey MC, Drennan M, Earley B (2003) 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 Anim Sci 81:2847–2855
Hodgson PD, Aich P, Manuja A, Hokamp K, Roche FM, Brinkman FSL, Potter A, Babiuk LA, Griebel PJ (2005) Effect of stress on viral–bacterial synergy in bovine respiratory disease: novel mechanisms to regulate inflammation. Comp Funct Genom 6:244–250
Hutcheson DP, Cole NA (1985) Vitamin E and selenium for yearling feedlot cattle (abstr). Fed Proc 44:549
Inanami O, Shiga A, Okada K, Sato R, Miyake Y, Kuwabara M (1999) Lipid peroxides and antioxidants in serum of neonatal calves. Am J Vet Res 60:452–457
Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukok Biol 79:425–434
Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S (1993) Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90:770–774
Lekeux P, Hajer R, Breukink HJ (1984) Effect of somatic growth on pulmonary function values in healthy Friesian cattle. Am J Vet Res 45:2003–2007
Letterio JJ, Roberts AB (1998) Regulation of immune responses by TGFβ. Annu Rev Immunol 16:137–161
Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631–677
Miller JK, Brzezinska-Slebodzinska E (1993) Oxidative stress, antioxidants and animal function. J Dairy Sci 76:2812–2823
Minton JE (1994) Function of the hypothalamus–pituitary–adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim Sci 72:1891–1898
Morimoto RI, Santoro MG (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16:833–838
Murata H, Takahashi H, Matsumoto H (1987) The effects of road transportation on peripheral blood lymphocyte subpopulations, lymphocyte blastogenesis and neutrophil function in calves. Br Vet J 143:166–174
Nguyen J, Knapnougel P, Lesavre P, Bauvois B (2005) Inhibition of matrix metalloproteinase-9 by interferons and TGF-β1 through distinct signalings accounts for reduced monocyte invasiveness. FEBS Lett 579:5487–5493
Ogawa K, Chen F, Kuang C, Chen Y (2004) Suppression of matrix metalloproteinase-9 transcription by transforming growth factor beta is mediated by a nuclear factor-kappaB site. Biochem J 381:413–422
Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476
Preisler MT, Weber PSD, Tempelman RJ, Erskine RJ, Hunt H, Burton JL (2000) Glucocorticoid receptor down-regulation in neutrophils of periparturient cows. Am J Vet Res 61:14–19
Radostits OM, Gay CC, Blood DC, Hinchcliff KW (2000) Veterinary medicine: a textbook of the diseases of cattle, sheep, pigs, goats and horses, 9th edn. W.B. Saunders, London
Reiche EMV, Nunes SOV, Morimoto HK (2004) Stress, depression, the immune system, and cancer. Lancet Oncol 5:617–625
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Salak-Johnson JL, McGlone JJ (2007) Making sense of apparently conflicting data: stress and immunity in swine and cattle. J Anim Sci 85(E. Suppl):E81–E88
Shull MM, Kier OI, AB PS, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D et al (1992) Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693–699
Snowder GD, Van Vleck LD, Cundiff LV, Bennett GL, Koohmaraie M, Dikeman ME (2007) Bovine respiratory disease in feedlot cattle: phenotypic, environmental, and genetic correlations with growth, carcass, and longissimus palatability traits. J Anim Sci 85:1885–1892
Sohn EJ, Paape MJ, Connor EE, Bannerman DD, Fetterer RH, Peters RR (2007) Bacterial lipopolysaccharide stimulates bovine neutrophil production of TNF-α, IL-1β, IL-12 and INF-γ. Vet Res 38:809–818
Szuchman A, Aviram M, Soliman K, Tamir S, Vaya J (2006) Exogenous N-linoleoyl tyrosine marker as a tool for the characterization of cellular oxidative stress in macrophages. Free Radic Res 40(1):41–52
Szuchman A, Aviram M, Ramadan M, Soliman K, Vaya J (2008) Characterization of oxidative stress in blood from diabetic vs. hypercholesterolaemic patients, using a novel synthesized marker. Biomarkers 13:119–131
Thompson PN, Stone A, Schultheiss WA (2006) Use of treatment records and lung lesion scoring to estimate the effect of respiratory disease on growth during early and late finishing periods in South African feedlot cattle. J Anim Sci 84:488–498
Weber PSD, Madsen SA, Smith GW, Ireland JJ, Burton JL (2001) Pre-translational regulation of neutrophila l-selectin in glucocorticoid-challenged cattle. Vet Immunol Immunopathol 83:213–240
Weber PSD, Toelboell T, Chang L-C, Tirrell JD, Saama PM, Smith GW, Burton JL (2004) 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 Leukoc Biol 75:815–827
Weber PSD, Madsen-Bouterse SA, Rosa GJM, Sipkovsky S, Ren X, Almeida PE, Kruska R, Halgren RG, Barrick JL, Burton JL (2006) Analysis of the bovine neutrophil transcriptome during glucocorticoid treatment. Physiol Genom 28(1):97–112
Welch WJ (1990) The mammalian stress response: cell physiology and biochemistry of stress proteins. In: Morimoto RI, Tissieres A, Georgopolous C (eds) Stress proteins in biology and medicine. Cold Spring Harbor, New York, pp 223–278
Williams JHH, Ireland E (2008) Sensing danger—Hsp72 and HMGB1 as candidate signals. J Leukoc Biol 83:489–492
Wittum TE, Woolen NE, Perino LJ, Littledike ET (1996) Relationship among treatment for respiratory tract disease, pulmonary lesions evident at slaughter, and rate of weight gain in feedlot cattle. JAVMA 209:814–818
Yagi Y, Shiono H, Chikayama Y, Ohnuma A, Nakamura I, Yayou K-I (2004) Transportation stress increases somatic cell counts in milk, and enhances the migration capacity of peripheral blood neutrophils of dairy cows. Clin Pathol 66(4):381–387
Yates WDG (1982) A review of infectious bovine rhinotracheitis, shipping fever pneumonia and viral–bacterial synergism in respiratory disease of cattle. Can J Comp Med 46:225–263
Zhu L, Bao E, Zhao R, Hartung J (2009) Expression of heat shock protein 60 in the tissues of transported piglets. Cell Stress Chaperones 14:61–69
Acknowledgements
This research was supported by funds from the Israeli Milk Marketing Board and Northern R&D. Contribution No. 555/09 from the ARO, the Volcani Center, Bet Dagan, Israel.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Eitam, H., Vaya, J., Brosh, A. et al. Differential stress responses among newly received calves: variations in reductant capacity and Hsp gene expression. Cell Stress and Chaperones 15, 865–876 (2010). https://doi.org/10.1007/s12192-010-0195-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-010-0195-9