Abstract
Selection for higher production rate in cattle inhabiting challenging habitats may be considered disadvantageous because of possible deleterious effects on immunity and reproduction and, consequently, on calf crop percentage. In Israel, free-grazing high productive beef cows experience reduction in nutritional quality of forage during up to 8 months of the year. As milk production by dams dictates calf performance, dam’s nutritional needs and rebreeding rates, the aim of the present study was to test how lactating beef cows deal with combined caloric and protein stress both at the productive and self protective levels. For this purpose, we studied the effect of long-term caloric stress on milk characteristics and gene expression of stress and milk components producing proteins. Lactating dams responded to caloric stress by decreased body weight, milk, and milk protein production. To compensate for total energy loses in milk, they produced milk of higher fat concentration and shifted the proportions of its fatty acids towards long and unsaturated ones. This was reflected by increased mRNA transcription of the fatty acid binding protein. Prolonged low-energy diet promoted cell-specific heat shock protein (Hsp) response; whereas significant increase of Hsp90 but unchanged levels of Hsp70 proteins were observed in white blood cells, the expression of Hsp70 in milk somatic cells was markedly attenuated, in parallel with a marked increase of αs1-casein expression. At the mammary gland level, these results may indicate a decrease in turnover of proteins and a shift to an exclusive expression of milk components producing factors. Similar responses to caloric stress were revealed also in ketotic dairy cows. Ketosis promoted a shift towards long and unsaturated fatty acids and an increased expression of αs1-casein in milk somatic cells. These findings may reflect an evolutionary-preserved mechanism in lactating cows for coping with caloric restriction. Overall, our results provide an index to test suitability of beef cattle breeds to inadequate caloric demands.
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References
Aharoni Y, Brosh A, Orlov A, Shargal E, Gutman M (2004) Energy balance of grazing beef cows in Mediterranean pasture, the effects of stocking rate and season: 1. Digesta kinetics, faecal output and digestible dry mater intake. Livest Prod Sci 90:89–100, doi:10.1016/j.livprodsci.2004.03.007
Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes—integrating cell survival and death. J Biosci 32:595–610, doi:10.1007/s12038-007-0059-3
Association of Official Analytical Chemists (1990) Official methods of analysis, 15th edn. AOAC, Arlington, VA
Baumgard LH, Corl BA, Dwyer DA, Saebo A, Bauman DE (2000) Identification of the conjugated linoleic isomer that inhibits milk fat synthesis. Am J Physiol 278:R179–R184
Baumgard LH, Matitashvili E, Corl BA, Dwyer DA, Bauman DE (2002) trans-10, cis-12 conjugated linoleic acid decreases lipogenic rates and expression of genes involved in milk lipid synthesis in dairy cows. J Dairy Sci 85:2155–2163
Benson ME, Henry MJ, Cardellino RA (1999) Comparison of weigh-suckle-weigh and machine milking for measuring ewe milk production. J Anim Sci 77:2330–2335
Boutinaud M, Rulquin H, Keisler DH, Djiane J, Jammes H (2002) Use of somatic cells from goat milk for dynamic studies of gene expression in the mammary gland. J Anim Sci 80:1258–1269
Brosh A, Aharoni Y, Shargal E, Choshniak I, Sharir B, Gutman M (2004) Energy balance of grazing beef cows in Mediterranean pasture, the effects of stocking rate and season: 2. Energy expenditure estimated from heart rate and oxygen consumption, and energy balance. Livest Prod Sci 90:101–115, doi:10.1016/j.livprodsci.2004.03.008
Buehring GC (1990) Culture of mammary epithelial cells from bovine milk. J Dairy Sci 73:956–963
Chouinard PY, Corneau L, Barbano DM, Metzger LE, Bauman DE (1999) Conjugated linoleic acids alter milk fatty acid composition and inhibit milk fat secretion in dairy cows. J Nutr 129:1579–1584
Christie WW (1982) A simple procedure of rapid trans-methylation of glycerolipids and cholesteryl esters. J Lipid Res 23:1072–1075
Craig EA, Lindquist S (1988) The heat shock proteins. Annu Rev Genet 22:631–677, doi:10.1146/annurev.ge.22.120188.000453
Crocker LM, DePeters EJ, Fadel JG, Perez-Monti H, Taylor SJ, Wyckoff JA, Zinn RA (1997) Influence of processed corn grain in diets of dairy cows on digestion of nutrients and milk composition. J Dairy Sci 81:2394–2407
de Roos APW, van den Bijgaart HJCM, Hørlyk J, de Jong G (2007) Screening for subclinical ketosis in dairy cattle by Fourier transform infrared spectrometry. J Dairy Sci 90:1761–1766, doi:10.3168/jds.2006-203
Dils RR (1983) Milk fat synthesis. In: Mepham TB (ed) Biochemistry of lactation. Elsevier, Amsterdam, pp 141–157
Duffy PH, Leakey JEA, Pipkin JL, Turturro A, Hart RW (1997) The physiologic, neurologic, and behavioral effects of caloric restriction related to aging, disease, and environmental factors. Environ Res 73:242–248, doi:10.1006/enrs.1997.3714
German T, Barash I (2002) Characterization of an epithelial cell line from bovine mammary gland. In Vitro Cell Dev Biol 38:282–292, doi:10.1290/1071-2690(2002)038<0282:COAECL>2.0.CO;2
Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90:420–426
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858, doi:10.1126/science.1068408
Hurtaud C, Rulquin H, Vérité R (1998) Effects of level and type of energy source (volatile fatty acids or glucose) on milk yield, composition and coagulating properties in dairy cows. Reprod Nutr Dev 38:315–330, doi:10.1051/rnd:19980312
Jenkins TG, Ferrell CL (1992) Lactation characteristics of nine breeds of cattle fed various quantities of dietary energy. J Anim Sci 70:1652–1660
Kehrli ME, Shuster DE (1994) Factors affecting milk somatic cells and their role in health of the bovine mammary gland. J Dairy Sci 77:619–627
Kovacs IA, Szalay MS, Csermely P (2005) Water and molecular chaperones act as weak links of protein folding networks: energy landscape and punctuated equilibrium changes point towards a game theory of proteins. FEBS Lett 579:2254–2260, doi:10.1016/j.febslet.2005.03.056
Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186
Loor JJ, Herbein JH (1998) Exogenous conjugated linoleic acid isomers reduce bovine milk fat concentration and yield by inhibiting de novo synthesis. J Nutr 128:2411–2419
Main AR (1986) Resilience on the level of individual animal. In: Dell B, Hopkins AJM, Lamont BB (eds) Resilience in mediterranean type ecosystems. Junk, Dordrecht, Netherlands, pp 83–94
Mallinckrodt CH, Bourdon RM, Golden BL, Schalles RR, Odde KG (1993) Relationship of maternal milk expected progeny differences to actual milk yield and calf weaning weight. J Anim Sci 71:355–362
Meyer K, Carrick MJ, Donnelly BJP (1994) Genetic parameters for milk production of Australian beef cows and weaning weight of their calves. J Anim Sci 72:1155–1165
Morrissey PA (1985) In: Fox PF (ed) Developments in dairy chemistry, vol 3. Elsevier, New York, pp 1–34
Nocek JE, Russell JB (1988) Protein and energy as an integrated system. Relationship of ruminal protein and carbohydrate availability to microbial synthesis and milk production. J Dairy Sci 71:2070–2107
NRC (1996) Nutrient requirements of beef cattle, 7th edn. National Academies, Washington, DC, USA
Palmquist DL, Beaulieu AD, Barbano DM (1993) Feed and animal factors influencing milk fat composition. J Dairy Sci 76:1753–1771
Patel NV, Finch CE (2002) The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiol Aging 23:707–717, doi:10.1016/S0197-4580(02)00017-9
Randel RD (1990) Nutrition and postpartum rebreeding in cattle. J Anim Sci 68:853–862
Roseler DK, Ferguson JD, Sniffen CJ, Herrema J (1993) Dietary protein degradability effects on plasma and milk urea nitrogen and milk nonprotein nitrogen in Holstein cows. J Dairy Sci 76:525–534
Simpson MA, LiCata VJ, Ribarik Coe N, Bernlohr DA (1999) Biochemical and biophysical analysis of the intracellular lipid binding proteins of adipocytes. Mol Cell Biochem 192:33–40, doi:10.1023/A:1006819715146
Sørensen ES, Møller L, Vinther M, Petersen TE, Rasmussen LK (2003) The phosphorylation pattern of human as1-casein is markedly different from the ruminant species. Eur J Biochem 270:3651–3655, doi:10.1046/j.1432–1033.2003.03755.x
SPSS Inc. (2005) SPSS 14.0 for Windows. SPSS, Chicago, IL
Sternberg M, Gutman M, Perevolotsky A, Ungar ED, Kigel J (2000) Vegetation response to grazing management in a Mediterranean herbaceous community: a functional group approach. J Appl Ecol 37:224–237, doi:10.1046/j.1365-2664.2000.00491.x
Sutton JD (1988) Altering milk composition by feeding. J Dairy Sci 72:2801–2814
Ungar ED, Karlibach Y, Yehuda Y, Baram H, Gutman M (2005) Multi-year analysis of production in free grazing beef cattle herd in the Golan height. Yediot Labokrim 113:13–19, In Hebrew
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 Laboratory, New York, pp 223–278
Whetstone HD, Hurley WL, Davis CL (1986) Identification and Characterization of a fatty acid binding protein in bovine mammary gland. Comp Biochem Physiol B 85:687–692, doi:10.1016/0305-0491(86)90068-4
Yu BP, Chung HY (2001) Stress resistance by caloric restriction for longevity. Ann N Y Acad Sci 928(1):39–47
Acknowledgements
We thank Professor Zeev Arad for critically reviewing this manuscript. This research was supported by funds of the Israeli Milk Marketing Board. Contribution No. 525/08 from the ARO, The Volcani Center, Bet Dagan, Israel.
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Eitam, H., Brosh, A., Orlov, A. et al. Caloric stress alters fat characteristics and Hsp70 expression in milk somatic cells of lactating beef cows. Cell Stress and Chaperones 14, 173–182 (2009). https://doi.org/10.1007/s12192-008-0070-0
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DOI: https://doi.org/10.1007/s12192-008-0070-0