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METABOLISM AND NUTRITION |
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* Mineral Nutrition Research Division, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100094, PR China; State Key Laboratory of Animal Nutrition, Beijing 100094, PR China; and Department of Animal Science, Hebei Normal University of Science and Technology, Changli 066600, PR China
2 Corresponding author: wlysz{at}263.net
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: gene expression • biomarker • manganese source • bioavailability • broiler
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Because of the low availability and high requirement of Mn in broilers, Mn additive is routinely supplemented into diets for the optimum growth. Organic Mn supplements have been increasingly used in the feed industry during the last 10 yr. However, there are conflicting results reported regarding bioavailability of these products relative to traditional inorganic form of the element (Ammerman, 1995). Different approaches have been used to search for the sensitive criteria in assessing the bioavailability of organic Mn souces. Most experiments conducted to evaluate the bioavailabilty of Mn from organic Mn sources were based on bone Mn concentration of birds at 21 d when Mn was supplemented at 1,000 to 4,000 mg/kg of diet (Baker and Halpin, 1987; Henry et al., 1989; Scheideler, 1991). It is reported that bioavailability values of inorganic Mn estimated from diets with added Mn at 20 to 120 mg/kg of diet were 20 and 40% higher than estimates derived from diets with added Mn at 1,000 to 4,000 mg/kg of diet (Luo, 1994).
Manganese is a crucial component of the metalloenzyme Mn superoxide dismutase (MnSOD). It has been determined that MnSOD functioning as a free radical scavenger is by far the most important Mn-containing enzyme (Luo et al., 1992). Some experiments have elicited that animals fed a Mn-deficient diet developed Mn-responsive abnormalities in mitochondrial ultrastructure, accompanied by a reduction in MnSOD activity, and suggested that MnSOD activity was a specific index for assessing Mn status and requirements for mice (De Rosa et al., 1980), rats (Paynter, 1980), and chicks (Luo et al., 1991). In a previous experiment supplementing organic Mn sources with 60 to 180 mg of Mn/kg of diet up to 21 d in a duration, we found that MnSOD activity and its gene expression in heart were positively related to dietary Mn concentration when chicks were fed in the same surroundings; however, MnSOD mRNA level in heart was more sensitive than MnSOD activity or commonly used bone Mn in the discrimination of the difference among the bioavailability of Mn from organic Mn sources (Li et al., 2004). Therefore, MnSOD mRNA level could potentially be used as an index for evaluating Mn bioavailability in a short-time trial of Mn supplementation.
The aim of this study was to investigate whether heart MnSOD gene expression could detect the differences among bioavailabilities of Mn sources earlier than other indices, so as to elicit a quicker and more sensitive criterion for the detection of differences in bioavailabilities of Mn sources as early as possible.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and tap water, which contained no detectable Mn. Birds were managed according to guidelines approved by Arbor Acres Farm in Beijing.
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). Dietary treatments included the basal diet with no added Mn (the control) or the control supplemented with 120 mg of Mn/ kg of diet supplied as reagent grade Mn sulfate (MnSO4·H2O) or Mn methionine E (Mn Met E) with weak chelation strength [formation quotient (Qf) = 3.2, 8.27% Mn], Mn amino acid B (Mn AA B) with moderate chelation strength (Qf = 45.3, 6.48% Mn), or Mn amino acid C (Mn AA C) with strong chelation strength (Qf = 115.4, 7.86% Mn). All 3 organic Mn sources used in the present study and their Qf values and Mn concentrations are as same as those used in the previous study for 21 d (Li et al., 2004, 2005), and the 3 organic Mn sources were obtained from independent distributors, rather than directly from manufacturers of the products. Birds were weighed, and feed intake was recorded at 7, 14, or 21 d of age. Incidence of leg abnormalities was calculated as a percentage of chicks within each cage with visual swelling at the tibiotarsus joint (Luo et al., 1991).
At 7 or 14 d of age, 3 chicks from each cage, which were selected according to average BW of the cage, and at 21 d of age, the remaining chicks in each cage were weighed individually and immediately killed by cervical dislocation after they were fully bled. The heart was excised, a subsample was frozen (–20°C) for Mn and MnSOD activity analysis, and a second subsample was frozen in liquid nitrogen for assays of MnSOD gene expression. The left leg was excised and frozen in individual heat-sealed polyethylene bag. Tibotarsal bones were boiled for approximately 10 min in deionized water, and all soft tissue was removed, dried for 12 h at 105°C, and finally charred in a muffle furnace at 550°C for 16 h. The samples of 3 individual chicks from each cage were pooled prior to analysis.
Manganese Concentration
Manganese concentrations in Mn sources, diets, and charred bones were determined by inductively coupled argon plasma spectroscopy (Model 9000, Thermal Jarrell Ash, Waltham, MA) as described by Li et al. (2004). Validation of the mineral analysis was conducted using bovine liver powder [GBW (E) 080193, National Institute of Standards and Technology, Beijing, China] as a standard reference material.
MnSOD Activity
The MnSOD activity was measured by the nitrite method as described by Li et al. (2004). The MnSOD activity in heart was expressed as nitrite units (NU) per gram of fresh weight (NU/g of fresh weight), and 1 NU was defined as the amount of enzyme needed to obtain 50% inhibition of nitrite formation.
RNA Extraction and Analysis
Total RNA in heart tissue was isolated using Trizol reagent (15596-026, Invitrogen Life Technologies, Carlsbad, CA) according to the manufacturer’s instructions. The RNA concentration was estimated by measuring UV light absorbance at 260 nm (Ultrospec III, Perkin Elmer Cetus, Norwalk, CT). The MnSOD mRNA level was determined from samples using a semiquantitative reverse transcription-PCR method as described by Li et al. (2004). ß-Actin was used as an internal control in all reactions. The MnSOD mRNA level was presented as the relative intensity ratio (R, arbitrary unit) between band intensity of MnSOD mRNA and ß-actin mRNA. Each PCR reaction was performed in duplicate on 2 individual preparations of reverse-transcribed cDNA.
Statistical Analysis
Data were analyzed by 2-way ANOVA using the GLM procedure with a model that included dietary treatment and chick age (d) as main effects, and their interaction. The replicate cage served as an experimental unit. Because there were no interactions between dietary treatment and chick age, data were then analyzed by 1-way ANOVA for the effect of dietary treatment at each age. An arc sin transformation was applied to the data on the incidence of leg abnormalities before statistical analysis. Significant differences among individual group means were determined by least significant difference test. All analyses were conducted using SAS (version 6.02; SAS Institute Inc., Cary, NC) software. Actual probability levels were reported for all main effects.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Birds fed the control diet had a higher (P < 0.09) incidence of leg abnormality than those fed the supplemental Mn diet except for the chicks fed the diet supplemented with 120 mg of Mn/kg of diet as Mn sulfate during 8 to 14 d of age (Table 2). There were no differences (P > 0.14) among supplemented Mn treatments.
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). The results herein implied that neither bone Mn concentration nor MnSOD activity in the heart could detect the differences among supplemental Mn sources.
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) was affected by age (P = 0.001) with the highest value at 14 d. Chicks fed the control diet had the lowest (P < 0.02) heart Mn concentration at each stage. Chicks fed the diet supplemented with Mn AA B showed higher (P < 0.05) heart Mn concentration than those fed the diet supplemented with Mn sulfate. There were no differences (P > 0.15) among organic Mn sources except that chicks fed diet supplemented with Mn AA B had the higher (P = 0.041) heart Mn concentration than chicks in Mn Met E groups at 14 d.
Heart MnSOD mRNA level (Table 3) was not affected (P = 0.121) by age. Chicks fed the control diet had lower (P < 0.01) heart MnSOD mRNA level than those fed diets supplemented with 120 mg of Mn/kg from Mn sources. On d 7, chicks fed the diet supplemented with Mn AA B had higher MnSOD mRNA level than those fed the diet supplemented with Mn sulfate (P = 0.018) and Mn Met E (P = 0.019), and the same tendency was observed on d 14 or 21 (P < 0.05). Chicks fed the diet supplemented with Mn AA B had a higher (P = 0.046) MnSOD mRNA level than those fed the diet supplemented with Mn AA C on d 21, and chicks fed the diet supplemented with Mn AA B showed a numerically and uniformly high MnSOD mRNA level compared with those fed the diet supplemented with Mn AA C on d 7 or 14 (P > 0.23).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Tissue accumulation of a mineral was considered to be a sensitive criterion for mineral utilization. Bone Mn has been used as the criterion for bioavailability assays of Mn sources. Henry et al. (1989) reported that the estimated bioavailability based on bone Mn accumulation was 108 for Mn Met relative to Mn sulfate for chicks fed a corn-soybean meal diet (93 mg of Mn/kg of diet) supplemented with 700 to 2,100 mg of Mn/kg of diet, indicating that Mn from Mn Met was significantly more available than that from Mn sulfate. The present experiment, however, along with Scheideler (1991) and Li et al. (2004) found no differences in bone Mn concentration among chicks fed diets with added organic Mn sources relative to those fed diet supplemented with Mn sulfate at any age, demonstrating that bone Mn concentration is not sensitive enough to determine the difference among organic Mn sources.
Heart Mn was found to be a useful indicator for Mn deficiency of lambs (Black et al., 1985) and rats (Paynter, 1980). Because heart Mn showed a linear relationship with dietary Mn when diets were supplemented with 500 to 4,000 mg of Mn/kg of diet, it was used as a biomarker for the bioavailability assay in lambs (Black et al., 1985). Heart Mn concentration in the present studies showed a close relationship with MnSOD activity or MnSOD mRNA, which could be related with the function of Mn in heart tissue. However, Mn concentration in heart of chicks fed the diet supplemented with Mn AA B was higher by 5.47% at 7 d and 3.37% at 21 d than those fed the diet supplemented with Mn Met E. As the result, heart Mn concentration failed to detect the differences among organic Mn sources at 7 or 21 d, implying that heart Mn concentration was not essentially stable, and lacked the sufficient sensitivity required to detect differences among organic Mn sources as early as possible.
The MnSOD is the primary antioxidant enzyme in the mitochondria that plays a key role in the detoxification of superoxide free radicals and protects cells from oxidative stress. It has been implicated in various cellular functions such as growth, senescence, death, immortalization, and tumorigenesis (Kong et al., 2003). Accumulating studies have shown that cellular levels of MnSOD increased in a dose- and time-dependent manner when cells were exposed to oxidative stress (Del Maestro and McDonald, 1989), inflammatory responses (Wispe et al., 1992), tumor necrosis factor-
(Wong and Goeddel, 1988; Wong et al., 1989), interleukin-1ß (Visner et al., 1990), ionizing radiation (Eastgate et al., 1993; Akashi et al., 1995), and neuro-toxins (Manganaro et al., 1995; Baker et al., 1998). Previous studies showed that MnSOD activity increased as dietary Mn increased at 21 d when chicks fed diets supplemented with 60 to 180 mg of Mn/kg of diet (Li et al., 2004, 2005). However, even though chicks fed Mn-supplemented diets had higher MnSOD activity than the control group at any age in the present experiment, there were no differences among Mn sources, indicating that MnSOD activity in heart lacked the sensitivity required to detect differences among Mn sources. The sophisticated control in MnSOD synthesis process could help to explain the change of cellular MnSOD level.
The MnSOD is a nuclear encoded mitochondrial protein, which is encoded by a nuclear gene in the long arm of chromosome 6. It is synthesized in the cytosol and posttranscriptionally modified for transport into the mitochondrion (Wispe et al., 1989; Shimoda-Matsubayashi et al., 1996). The prepro-MnSOD taken into the mitochondria is cleaved by a proteolytic process to a mature 198-amino-acid molecule (Shimoda-Matsubayashi et al., 1996). The biosynthesis of MnSOD in most biological systems is complicated and under rigorous controls, not only at the transcriptional level but also at the posttranscriptional, translational, and posttranslational levels (Cyrne et al., 2003).
The mRNA level of MnSOD has been demonstrated to elicit dramatic elevations in time- and dose-dependent manner by a wide variety of factors: cellular redox state (Cyrne et al., 2003), hyperoxia (Fridovich, 1995), irradiation (Akashi et al., 1995), and various inflammatory mediators (tumor necrosis factor-, interleukin-1ß, interleukin-6, and lipolysaccharide; Dougall and Nick, 1991; Visner et al., 1991, 1992; Valentine and Nick, 1992). Transcriptional run-on analysis showed that irradiation increased the rate of MnSOD transcription 2-fold in human fibroblasts. Stability studies of MnSOD mRNA in these cells showed that the half-life increased from <1.5 h in nonirradiated cells to >4 h in irradiated cells. The increase in MnSOD mRNA observed after irradiation occurs through transcriptional and posttranscriptional mechanisms (Akashi et al., 1995). A good correlation between transcript level and protein level or enzyme activity was observed in multiple tissues. However, mitochondrial MnSOD protein level and activity did not increase to the same extent as antioxidant protein mRNA level (Warner et al., 1991; Kim et al., 2005). Activities of MnSOD increased in response to the oxidative challenges in mouse skeletal muscle, but the magnitudes of the increases were less robust than the increases of the respective transcript levels (Franco et al., 1999). Warner et al. (1991) showed that MnSOD activity and mRNA in human pulmonary adenocarcinoma cells increased significantly in a dose-and time-dependent manner. Activity of MnSOD was increased 3-fold and mRNA 20-fold after a 48-h incubation with tumor necrosis factor- reached a level of 25 ng/mL. The tight regulation of mitochondrial protein levels seems to be necessary for optimal cellular function (Kim et al., 2005).
Several studies showed that Mn was involved in not only transcription and translation of MnSOD gene, but also insertion of the metal prosthetic group during maturation of the newly synthesized polypeptide in prokaryotic and eukaryotic organisms. The Mn-deficient mice had a lower Mn concentration, MnSOD activity, and MnSOD mRNA in liver than those on the control, and the lower MnSOD mRNA probably resulted from the downregulation at the (pre)transcriptional level (Borrello et al., 1992). The MnSOD gene in E. coli was regulated transcriptionally (Touati, 1988) and posttranslationally (Privalle and Fridovich, 1992) in a Mn-dependent fashion. Addition of MnCl2 to the growth medium for Pseudomonas putida induced MnSOD gene (sodA) transcripts from the sodA operon (Kim et al., 1999). Supplementation of MnCl2 could also induce MnSOD expression (mRNA, immuno-reactive protein, and enzyme activity) in human breast cancer Hs578T cells (Thongphasuk et al., 1999).
No evidence has been reported in the literature relevant to the mechanism of MnSOD regulation in chickens. Our previous study showed that heart MnSOD mRNA levels increased as dietary Mn levels increased when chicks fed diets supplemented with 60 to 180 mg of Mn/kg of diet for 21 d (Li et al., 2004, 2005). The present experiment indicated that MnSOD mRNA levels in heart tissue of chicks fed the diet supplemented with 120 mg of Mn/kg of diet were significantly higher than the control chicks at 7, 14, or 21 d when chicks were fed in the same surroundings, and the MnSOD mRNA level in heart tissue of chicks fed the diet supplemented with Mn from Mn AAB with moderate chelation strength was increased by 11.5% over those fed the diet supplemented with Mn from Mn Met E at 7 d, suggesting that dietary Mn could significantly upregulate heart MnSOD gene transcription, and this functionally responsive criterion detected differences among organic Mn sources as early as at 7 d.
In the present experiment, heart MnSOD mRNA level was not affected significantly as age increased from d 7 to d 21, whereas the activity of MnSOD herein increased as the age increased no matter which diet was fed to chicks. The above disparity between MnSOD mRNA level and MnSOD activity at different ages might reflect the necessary function in the chick heart. The significant age-related increases in MnSOD activities occurred probably in response to increased mitochondrial production of superoxide (Judge et al., 2005). Kurokawa et al. (2001) supposed that MnSOD protein was posttranslationally modified by age to carry out an optimal cellular function.
In conclusion, MnSOD mRNA in heart significantly increased as dietary Mn level increased, suggesting that dietary Mn could regulate heart MnSOD gene expression at a transcriptional level. Heart MnSOD mRNA level could detect the differences of Mn bioavailabilities between organic Mn sources and Mn sulfate or among organic Mn sources as early as 7 d, implying that changes in MnSOD mRNA might occur before significant differences in the amount of excess Mn deposited in tissue or activity of enzyme are detectable. The shorter time required to conduct the feeding portion of a bioavailability trial, as well as the smaller number of samples needed to find significant differences among supplemental sources using heart MnSOD mRNA expression as a criterion, might provide cost and time savings in bioassays for Mn sources. Understanding how MnSOD can be regulated by dietary intake of Mn could provide a novel strategy for evaluating the function of this element. Further experiments are needed to evaluate more fully and exploit the cellular functions of Mn as an index of bioavailability.
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FOOTNOTES |
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Received for publication October 7, 2006. Accepted for publication December 30, 2006.
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REFERENCES |
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Ammerman, C. B. 1995. Methods for estimation of mineral bio-availability. Pages 83–92 in Bioavailability of Nutrients for Animals: Amino Acids, Minerals, and Vitamins. C. B. Ammerman, D. H. Baker, and A. J. Lewis, ed. Academic Press, San Diego, CA.
Baker, D. H., and K. M. Halpin. 1987. Research note: Efficacy of a manganese-protein chelate compared with that of manganese sulfate for chicks. Poult. Sci. 66:1561–1563.[ISI][Medline]
Baker, K., C. B. Marcus, K. Huffman, H. Kruk, B. Malfroy, and S. R. Doctrow. 1998. Synthetic combined superoxide dismutase/catalase mimetics are protective as a delayed treatment in a rat stroke model: A key role for reactive oxygen species in ischemic brain injury. J. Pharmacol. Exp. Ther. 284:215–221.
Black, J. R., C. B. Ammerman, and P. R. Henry. 1985. Effects of high dietary manganese as manganese oxide or manganese carbonate in sheep. J. Anim. Sci. 60:861–866.
Borrello, S., M. E. Deleo, and T. Galeotti. 1992. Transcriptional regulation of Mn-SOD by manganese in the liver of manganese-deficient mice and during rat development. Biochem. Int. 28:595–601.[ISI][Medline]
Cyrne, L., L. Martins, L. Fernandes, and S. H. Marinho. 2003. Regulation of antioxidant enzymes gene expression in the yeast Saccharomyces cerevisiae during stationary phase. Free Radic. Biol. Med. 34:385–393.[ISI][Medline]
De Rosa, G., C. L. Keen, R. M. Leach, and L. S. Hurley. 1980. Regulation of superoxide dismutase activity by dietary manganese. J. Nutr. 110:795–804.
Del Maestro, R., and W. McDonald. 1989. Subcellular localization of superoxide dismutases, glutathione peroxidase and catalase in developing rat cerebral cortex. Mech. Aging Dev. 48:15–31.[Medline]
Dougall, W. C., and H. S. Nick. 1991. Manganese superoxide dismutase: A hepatic acute phase protein regulated by interleukin-6 and glucocorticoids. Endocrinology 129:2376–2384.[Abstract]
Eastgate, J., J. Moreb, H. S. Nick, K. Suzuki, N. Taniguchi, and J. R. Zucali. 1993. A role for manganese superoxide dismutase in radioprotection of hematopoietic stem cells by interleukin-1. Blood 81:639–646.
Franco, A. A., R. S. Odom, and T. A. Rando. 1999. Regulation of antioxidant enzyme gene expression in response to oxidative stress and during differentiation of mouse skeletal muscle. Free Radic. Biol. Med. 27:1122–1132.[ISI][Medline]
Fridovich, I. 1995. Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64:97–112.[ISI][Medline]
Halpin, K. M., and D. H. Baker. 1987. Mechanism of the tissue manganese-lowering effect of corn, soybean meal, fish meal, wheat bran and rice bran. Poult. Sci. 66:332–340.[ISI][Medline]
Henry, P. R., C. B. Ammerman, and R. D. Miles. 1989. Relative bioavailability of manganese in a manganese-methionine complex for broiler chicks. Poult. Sci. 68:107–112.[ISI][Medline]
Judge, S., Y. M. Jang, A. Smith, T. Hagen, and C. Leeuwenburgh. 2005. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: Implications for the mitochondrial theory of aging. FASEB J. 19:419–421.
Kies, C. 1994. Bioavailability of manganese. Pages 39–58 in Manganese in Health and Disease. D. L. Klimis-Tavantzis, ed. CRC Press Inc., Boca Raton, FL.
Kim, Y. C., C. D. Miller, and A. J. Anderson. 1999. Transcriptional regulation by iron of genes encoding iron- and manganese-superoxide dismutases from Pseudomonas putida. Gene 239:129–135.[ISI][Medline]
Kim, A., M. P. Murphy, and T. D. Oberley. 2005. Mitochondrial redox state regulates transcription of the nuclear-encoded mitochondrial protein manganese superoxide dismutase: A proposed adaptive response to mitochondrial redox imbalance. Free Radic. Biol. Med. 38:644–654.[ISI][Medline]
Kong, B. W., H. Kim, and D. N. Foster. 2003. Expression analysis and mitochondrial targeting properties of the chicken manganese-containing superoxide dismutase. Biochim. Biophys. Acta 1625:98–108.[Medline]
Kurokawa, T., S. Asada, S. Nishitani, and O. Hazeki. 2001. Age-related changes in manganese superoxide dismutase activity in the cerebral cortex of senescence-accelerated prone and resistant mouse. Neurosci. Lett. 298:135–138.[ISI][Medline]
Li, S., X. Luo, B. Liu, T. D. Crenshaw, X. Kuang, and G. Shao. 2004. Use of chemical characteristics to predict relative bio-availability of supplemental organic manganese sources for broilers. J. Anim. Sci. 82:2352–2363.
Li, S. F., X. Luo, L. Lu, B. Liu, X. Kuang, and G. Shao. 2005. Bioavailability of organic manganese sources in broilers fed high dietary calcium. Anim. Feed Sci. Technol. 123-124:703–715.
Luo, X. G. 1994. Studies of bioavailability of different inorganic manganese sources for broilers. Pages 92–94 in Proc. First Natl. Symp. Anim. Sci. Chin. Agric. Sci. Press, Beijing, China.
Luo, X. G., Q. Su, J. C. Huang, and J. X. Liu. 1991. A study on the optimal manganese (Mn) level in a practical diet of broiler chicks. Chin. J. Anim. Vet. Sci. 22:313–317.
Luo, X. G., Q. Su, J. C. Huang, and J. X. Liu. 1992. Effects of manganese (Mn) deficiency on tissue Mn-containing superoxide dismutase (MnSOD) activity and its mitochondrial ultrastructures of broiler chicks fed a practical diet. Chin. J. Anim. Vet. Sci. 23:97–101.
Manganaro, F., V. S. Chopra, M. B. Mydlarski, G. Bernatchez, and H. M. Schipper. 1995. Redox perturbations in cysteamine-stressed astroglia: Implications for inclusion formation and gliosis in the aging brain. Free Radic. Biol. Med. 19:823–835.[ISI][Medline]
National Research Council. 1994. Nutrient Requirements of Poultry. 9th ed. Natl. Acad. Press, Washington, DC.
Nielsen, F. H. 1999. Ultratrace minerals. Pages 283–303 in Nutrition in Health and Disease. 9th ed. M. Shils, J. A. Olson, M. Shike, and A. C. Ross, ed. Williams & Wilkins, Baltimore, MD.
Paynter, D. I. 1980. Changes in activity of the manganese superoxide dismutase enzyme in tissues of the rat with changes in dietary manganese. J. Nutr. 110:437–447.
Privalle, C. T., and I. Fridovich. 1992. Transcriptional and maturational effects of manganese and iron on the biosynthesis of manganese-superoxide dismutase in Escherichia coli. J. Biol. Chem. 267:9140–9145.
Scheideler, S. E. 1991. Interaction of dietary calcium, manganese and manganese source (manganese oxide or manganese methionine chelate) on chick performance and manganese utilization. Biol. Trace Elem. Res. 29:217–223.[ISI][Medline]
Shimoda-Matsubayashi, S., H. Matsumine, T. Kobayashi, Y. Nakagawa-Hattori, Y. Shimizu, and Y. Mizuno. 1996. Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene. A predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson’s disease. Biochem. Biophys. Res. Commun. 226:561–565.[ISI][Medline]
Smith, O. B., and E. Kabaija. 1985. Effect of high dietary calcium and wide calcium-phosphorus ratio in broiler chicks. Poult. Sci. 64:1713–1720.[ISI]
Thongphasuk, J., L. W. Oberley, and T. D. Oberley. 1999. Induction of superoxide dismutase and cytotoxicity by manganese in human breast cancer cells. Arch. Biochem. Biophys. 365:317–327.[ISI][Medline]
Touati, D. 1988. Transcriptional and posttranscriptional regulation of manganese superoxide dismutase biosynthesis in Escherichia coli, studied with operon and protein fusions. J. Bacteriol. 170:2511–2520.
Valentine, J. F., and H. S. Nick. 1992. Acute-phase induction of manganese superoxide dismutase in intestinal epithelial cell lines. Gastroenterology 103:905–912.[ISI][Medline]
Visner, G. A., E. R. Block, I. M. Burr, and H. S. Nick. 1991. Regulation of manganese superoxide dismutase in porcine pulmonary artery endothelial cells. Am. J. Physiol. 260:L444–L449.[ISI][Medline]
Visner, G. A., S. E. Chesrown, J. Monnier, U. S. Ryan, and H. S. Nick. 1992. Regulation of manganese superoxide dismutase: IL-1 and TNF induction in pulmonary artery and microvascular endothelial cells. Biochem. Biophys. Res. Commun. 188:453–462.[ISI][Medline]
Visner, G. A., W. C. Dougall, J. M. Wilson, I. M. Burr, and H. S. Nick. 1990. Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor. Role in the acute inflammatory response. J. Biol. Chem. 256:2856–2864.
Warner, B. B., M. S. Barhans, J. C. Clark, and J. R. Wispe. 1991. Tumor necrosis factor- increase MnSOD expression: Protection against oxidant injury. J. Physiol. 260:L296–L301.
Wispe, J. R., J. C. Clark, M. S. Burhans, K. E. Kropp, T. R. Korfhagen, and J. A. Whitsett. 1989. Synthesis and processing of the precursor for human mangano-superoxide dismutase. Biochim. Biophys. Acta 994:30–36.[Medline]
Wispe, J. R., B. B. Warner, J. C. Clark, C. R. Dey, J. Neuman, S. W. Glasser, J. D. Crapo, L. Chang, and J. A. Whitselt. 1992. Human Mn-superoxide dismutase in pulmonary epithelial cells of transgenic mice confers protection from oxygen injury. J. Biol. Chem. 267:23937–23941.
Wong, G. H., J. Elwell, L. Overly, and D. V. Goeddel. 1989. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58:923–931.[ISI][Medline]
Wong, G. H., and D. V. Goeddel. 1988. Induction of manganous superoxide dismutase by tumor necrosis factor: Possible protective mechanism. Science 242:941–944.
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