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1 Research Institute for the Biology of Farm Animals Dummerstorf, Germany
2 Landesforschungsanstalt Mecklenburg-Vorpommern, Germany
3 University of Rostock, Institute of Cell Biology, Germany
Corresponding author: B. Löhrke; e-mail: viergutz{at}fbn-dummerstorf.de.
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ABSTRACT |
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Key Words: lipohydroperoxide • oxidative stress • superoxide formation
Abbreviation key: LDL = low-density lipoprotein, LHP = lipohydroperoxides, PAF = platelet-activating factor, PL = phospholipids
Milk energy output has been demonstrated in dairy cows to be a linear function of metabolizable energy intake (Schiemann et al., 1974). This intake correlates with heat production, a measure for oxidative metabolism, which is closely related to the oxygen consumption of the whole body in cattle (Löhrke et al., 1997). An increase in oxygen consumption does not necessarily mean oxidant stress, i.e., an imbalance between formation and detoxification of reactive oxygen metabolites (Behrman et al., 2001). In turn, an increase in oxidative metabolism corresponds to a higher production of reactive oxygen metabolites at least regarding the activity of the mitochondrial respiratory chain, the main oxygen consumer (Ainscow and Brand, 1999). Some of these metabolites generally escape from endogenous defense mechanisms and may serve both important physiologic and damaging roles (Behrman et al., 2001). Insufficient detoxification is indicated by oxidative modifications, including peroxidation of lipids (Porter et al., 1995). This study was conducted to investigate the potential for increased oxidative stress of high- vs. average-producing dairy cows.
German Holstein cows (experiment 1, n = 11; experiment 2, n = 13) from the Dummerstorf dairy cattle farm were used at postpartum d 53 ± 2, a lactation stage that corresponds to a period of reaching positive energy balance in high-performance cows (Selberg et al., 2004). In experiments 1 and 2, the number of cows in first, second, and third parity was n = 4 and 5, 3 and 4, 4 and 4, respectively. Cows were offered twice daily ad libitum amounts of TMR (containing a mineral and vitamin mixture) to allow for 10% orts. In terms of net energy retention (Beyer et al., 2003), the TMR offered 201 MJ/d (roughages, 58 MJ/d; concentrate, 143 MJ/d). Cows were milked 3 times daily, and milk performance records were accomplished by the governmental milk performance control association. The milk productivity results presented refer to an average of 2 consecutive milk performance data from records by the month. Milk energy output was calculated on the basis of daily milk yield and fat percentage using 2.92 MJ/kg of milk (3.5% fat) and 0.22 MJ/kg for increases in fat of 0.5% (Beyer et al., 2003). Twelve (±2) days following milk performance recording, blood was collected after morning milking before feeding via coccygeal arterio-venipuncture using glass tubes (10 mL). This procedure was approved by the governmental Animal Care Committee (Mecklenburg-Vorpommern). Blood was placed on ice and transported to our laboratory within 30 min. Serum prepared by centrifugation (3000 x g, 15 min, 4°C) was treated with butylated hydroxytoluene (to 20 µM), an antioxidant, and Pefabloc (to 0.2 mM) to inhibit deacylation of phospholipids; low-density lipoprotein (LDL) was isolated by ultracentrifugation and further purified by precipitation on the analogy of an established technique (Nauck et al., 1995). Lipohydroperoxides (LHP) were determined in serum lipids (experiment 1) or LDL (experiment 2) via reaction of LHP with ferrous ions to produce ferric ions, which were detected by thiocyanate as the chromogen in a deoxygenated organic phase (Mihaljevic et al., 1996) using a kit (Cayman, Alexis Biochemicals, Grünberg, Germany). In experiment 1, polar phospholipids (PL) were isolated by amberlite XAD-2 resin chromatography (Salari, 1986). Phosphorus was measured by a microassay (Ames and Dubin, 1960). Bioactivity of PL was assayed by responses of Mono-Mac-6 cells (not primed by cytokines), a monocytic cell line (Weber et al., 1993) possessing receptors for the platelet-activating factor (PAF). Formation of superoxide anions was detected through chemiluminescence of lucigenin. Luminescence was calibrated using a xanthine oxidase system (Ohara et al., 1993). Comparisons between 2 groups of animals were performed by unpaired t-test. The accepted level of significance was P < 0.05. Data are reported as the means (±SEM) when not otherwise stated. Tests and analysis of linear regression was accomplished by statistical software package (SAS Inst., Inc., Cary, NC and Sigma Stat, Jandel Scientific, Erkrath, Germany).
The results of experiment 1, shown in Table 1
, indicate presence of LHP in circulative lipids of dairy cows. These data demonstrate for the first time to our knowledge that cows with lower levels of LHP showed lower milk yield and milk energy output. This relationship was quantified in experiment 2 by an analysis of regression using lipids from LDL, a major oxidative target (Navab et al., 2001). The analysis resulted in the equation: LHP (µM) = –1.95 (±0.88) + 0.078 (±0.022) milk yield (kg/d), r = 0.77, P = 0.0048, regarding the slope of the regression line.
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; group I) did not significantly evoke superoxide production above basal level (data not shown). However, monocytes responded to PL of group II with a marked transient increase in superoxide formation (Figure 1). The response was similar to superoxide induction through PAF, a proinflammatory PL (Marathe et al., 1999). Responses of both PL and PAF were inhibited by 3-[4-(2-chlorophenyl)-9-methyl-6H-thienol[3,2-f](1,2,4)triazolo-[4,3-a][1,4]-diazepin-2yl]-1-(4-morpholinyl)-1-propanon, a PAF receptor blocker, indicating receptor-mediated (specific) responses. Ligand binding has been reported to cause a rapid down-regulation of these cell surface receptors of monocytes not primed by cytokines (Weber et al., 1993). Metabolic responses that are not mediated by PAF receptors include time-dependent fluctuations of basal superoxide formation (Figure 1). In conclusion, the current study demonstrates the presence of LHP in serum from average and high producing cows during an early lactation stage. However, the mechanism involved in changing LHP level remains to be identified. Phospholipids from high-performance cows contain pro-inflammatory PAF-like lipids. If the responses to those lipids observed in vitro apply to situations in vivo, the results may have implications for animal health and reproduction.
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Received for publication September 24, 2004. Accepted for publication January 11, 2005.
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