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Poult Sci 2008. 87:2259-2265. doi:10.3382/ps.2007-00525
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METABOLISM AND NUTRITION

Effect of Intravenously Injected Manganese on the Gene Expression of Manganese-Containing Superoxide Dismutase in Broilers1

S. F. Li*,{dagger},{ddagger}, X. G. Luo*,{dagger},2, L. Lu*,{dagger}, B. Liu*,{dagger}, X. Kuang*, G. Z. Shao*,{dagger} and S. X. Yu*,{dagger}

* Mineral Nutrition Research Division, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, People’s Republic of China; {dagger} State Key Laboratory of Animal Nutrition, Beijing 100193, People’s Republic of China; and {ddagger} Department of Animal Science, Hebei Normal University of Science |and Technology, Qinhuangdao 066000, People’s Republic of China

2 Corresponding author: wlysz{at}263.net


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The goal of this study was to investigate the effect of intravenously injected Mn from different Mn sources on tissue Mn concentration, heart Mn-containing superoxide dismutase (MnSOD) activity and its gene expression in broilers, so as to detect differences in Mn metabolic utilization among Mn sources. On d 22 posthatching, a total of 180 chicks were randomly allotted by BW to 1 of 5 treatments in a completely randomized design. The 5 treatments included a 0.9% NaCl injection solution without Mn addition (the control), a 0.9% NaCl solution with Mn sulfate or one of 3 organic Mn sources with weak, moderate, or strong chelation strengths at a dosage calculated according to the dietary Mn requirement of 120 mg/kg, Mn absorbability of 1.5%, and daily feed intake. Heart and bone samples were collected from broilers on d 10 and 20 after Mn injections for analyses of tissue indices. The results showed that on both d 10 and 20 after Mn injections, the birds injected with Mn-containing solutions had greater (P < 0.01) Mn concentrations in both heart and bone, heart MnSOD activities, and MnSOD mRNA levels than those injected with the control NaCl solution; however, intravenously injected Mn always had a sensitive and consistent effect on heart MnSOD mRNA level of broilers, and the birds injected with a solution containing the organic Mn source with moderate chelation strength always had the greatest heart MnSOD mRNA level. The results indicated that intravenously injected Mn from the organic Mn source with moderate chelation strength was the most utilizable Mn source and functioned in the sensitive target tissue more effectively than Mn from Mn sulfate or other 2 organic Mn sources with weak or strong chelation strength.

Key Words: intravenous injection • gene expression • manganese source • broiler


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Several sources of organic Mn supplements have been produced and used in animal feeds during recent years. The mode in which the organic mineral complex or chelate is absorbed and utilized is still unclear. So far, there have been 2 hypotheses in explaining the exiting phenomena. One of them is that the organic mineral complex or chelate with the optimum chelation strength could resist interferences from dietary anti-nutritional factors in the digestive tract and directly reach the intestinal brush border, where it is hydrolyzed and absorbed as an ion into the blood, resulting in a greater availability of the chelated than the inorganic form of the metal (Ashmead, 1993). The other hypothesis is that the organic mineral complex or chelate could maintain their structural integrity in the digestive tract and arrive at absorptive sites in the small intestine as the original intact molecule, and then be absorbed and metabolized as such, rendering these supplements superior in bioavailability to inorganic sources (Ashmead, 1993; Guo et al., 2001). There has been no direct evidence supporting any of the above 2 hypotheses in the literature.

Previous experiments in our lab indicated that heart Mn-containing superoxide dismutase (MnSOD) mRNA level was a more sensitive criterion than MnSOD activity or commonly used bone Mn for the detection of differences in bioavailabilities of Mn sources for broilers (Li et al., 2004, 2005; Luo et al., 2007), and the bioavailabilities of Mn in organic Mn sources for broilers were closely related to their chelation strength measured by polarography when heart MnSOD mRNA level was used as the criterion for bioavailability assessment (Li et al., 2004, 2005). Relative to Mn sulfate (assigned 100%), the bioavailability of organic Mn source with weak, moderate, or strong chelation strength for broilers fed normal calcium diet was 99, 132, and 113%, respectively, in which the organic Mn source with moderate chelation strength was significantly more available than inorganic Mn sulfate or the organic Mn sources with weak or strong chelation strength (Li et al., 2004). However, the bioavailability of the same 3 organic Mn sources for broilers fed high calcium diet was 112, 145, and 148%, respectively, in which the bioavailabilities of both organic Mn source with moderate and strong chelation strength were significantly greater than inorganic Mn sulfate or the organic Mn sources with weak chelation strength, suggesting that organic Mn sources with moderate and strong chelation strength could partially or completely resist the antagonistic effect of high dietary calcium during digestion, rendering the high relative bioavailability (Li et al., 2005).

A series of experiments in our lab concerning the absorption of organic Mn sources were conducted. The results showed that when broilers were fed normal calcium diet for 9 d, the plasma Mn contents in hepatic portal vein for the organic Mn source with strong chelation strength were significantly greater than contents of inorganic Mn sulfate or organic Mn source with moderate chelation strength, and the absorption for organic Mn source with strong chelation strength was 25.8% greater than that of organic Mn source with moderate chelation strength (Ji et al., 2006a). Moreover, the results for the absorption of the same 3 organic Mn sources from our previous experiments in everted gut sac with high calcium media showed that the uptake of Mn in jejunal sacs for the 3 organic Mn sources was 35.9, 23.7, and 76.0% greater than that of inorganic Mn sulfate, respectively. There was no difference in the absorption between organic Mn source with moderate and weak chelation strength or between strong and weak chelation strength, but the uptake of Mn for organic Mn source with strong chelation strength was 42.3% greater than that for organic Mn source with moderate chelation strength (Ji et al., 2006b). On the one hand, these results supported our previous report that the high bioavailability of organic Mn source with strong chelation strength for broilers a fed high-calcium diet might be caused by its relatively high absorbability in the gastric tract. On the other hand, the paradox between the bioavailability and the absorption of organic Mn sources implied that there might be a difference in the metabolic availability of absorbed Mn in tissue between organic and inorganic Mn sources or among organic Mn sources. However, no evidence relating to the utility of organic Mn sources at a tissue level has been reported.

Direct injection of Mn sources into a vein might be the best way to study the Mn metabolic utilization at a tissue level in animals (Davidsson et al., 1989; Davis et al., 1993). The goal of this study was to investigate the effect of intravenously injected Mn from different Mn sources on tissue Mn concentration, heart MnSOD activity, and its gene expression in broilers, so as to detect differences in Mn metabolic utilization between organic and inorganic Mn sources or among organic Mn sources, which would be of the great importance to address whether organic Mn sources intact absorbable in the gut should be developed and applied to the poultry industry.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Mn Sources and Injection Dosage

All 3 organic Mn sources used in the present study and their formation quotient (Qf) values and Mn concentrations are all from the previous studies for characteristics of organic Mn sources (Li et al., 2004, 2005). They were obtained from independent distributors, rather than directly from manufacturers. They were Mn methionine E (Mn Met E) with weak chelation strength (Qf = 3.2, containing 82.7 g of Mn/kg), Mn amino acid B (Mn AA B) with moderate chelation strength (Qf = 45.3, containing 64.8 g of Mn/kg), or Mn amino acid C (Mn AA C) with strong chelation strength (Qf = 115.4, containing 78.6 g of Mn/kg), respectively. Reagent grade Mn sulfate monohydrate (MnSO4·H20) was set as inorganic Mn source.

The 5 treatments included a 0.9% NaCl injection solution without Mn addition (the control), a saline solution with Mn sulfate or 1 of the 3 organic Mn sources. The assumption was made that the amount of Mn injected should be close to the normal amount of Mn absorbed when chicks are fed on the normal Mn diet. The injected dosage of Mn was calculated according to the dietary Mn requirement, Mn absorbability, and average daily feed intake (kg/d). Broilers usually require 120 mg Mn/kg of diet (Luo et al., 1991). Manganese apparent absorption coefficients in chicks were reported to range from 1 to 3% (Scott et al., 1976), so the value of 1.5% was used. The average daily feed intake was adjusted every 7 d according to the corresponding feed intake at the same age in our previous study (Li et al., 2004). The Mn concentrations in the saline solution with Mn sulfate or 1 of the 3 organic Mn sources were 0.720 mg of Mn/mL during d 22 to 28 of age, 0.972 mg of Mn/mL during 29 to 35 d of age, and 1.224 mg of Mn/mL during 36 to 42 d of age, respectively. Individual birds injected with Mn-containing solution received 1.926 mg of injected Mn for the first 10 d and 4.734 mg of injected Mn for the whole 20 d.

Birds and Diets

The experiment started at 22 d of age because it was difficult to perform intravenous injections on broilers younger than 21 d. During 1 to 21 d of age, 250 day-old Arbor Acres commercial male broilers (Huadu Broiler Breeding Corp., Beijing, China) were fed the same Mn-unsupplemented corn-soybean meal basal diet with all nutrients, except Mn, meeting or exceeding the requirements of starting broilers (NRC, 1994; Table 1Go). At 22 d of age, 180 birds were selected according to BW and randomly allotted to 1 of 5 treatments with 6 replicate cages (6 birds per cage) for each. Treatments included the control injected with saline solution with no added Mn, and the experimental groups injected with saline solution with Mn sulfate or one of the organic Mn sources. All injected solutions for all treatments contained the same concentration of methionine or lysine. All birds were fed on the same Mn-unsupplemented corn-soybean meal basal diet with all nutrients, except Mn, meeting or exceeding the requirements for growing broilers (NRC, 1994; Table 2Go).


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  		Table 1. Composition of the basal diet for broilers in the starter phase (d 1 to 21)
 

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  		Table 2. Composition of the basal diet for broilers in the grower phase (d 22 to 42)
 
Chicks were housed in electrically heated, thermostatically controlled stainless cages coated with plastic and equipped with plastic feeders and waterers. They were maintained on a 24-h constant-light schedule and managed according to guidelines approved by Arbor Acres Farm in Beijing. During the experimental period, all chicks had ad libitum access to feed and tap water containing no detectable Mn. Individual bird was injected with 0.5 mL of either saline without Mn or with Mn addition through the vein of the wing at 0800 h every other day for 20 d. On d 10 or 20 after injections, feed consumption and BW were recorded per cage, and 2 birds from each cage were selected according to the average BW of birds in the cage and killed by cervical dislocation. The heart was excised, and one part of it was frozen in –20°C for analyses of Mn and MnSOD activity, and another part was frozen in liquid nitrogen for gene expression analysis of MnSOD. The left leg was excised and frozen in an individual heat-sealed polyethylene bag. Tibiotarsal bones were boiled for approximately 10 min in deionized water, and all soft tissue was removed, dried at 105°C for 12 h, and finally ashed in a muffle furnace at 550°C for 16 h. The samples of 2 individual chicks from each cage were pooled before analysis.

Mn Concentration

Manganese concentrations in Mn sources, diets and bone ashes 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 ultraviolet 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). Beta-actin was used as an internal control in all reactions. The MnSOD mRNA level was presented as the relative intensity ratio (R, arbitrary units) between band intensity of MnSOD mRNA and β-actin mRNA. Each PCR reaction was performed in duplicate on 2 individual preparations of reverse-transcribed cDNA.

Statistical Analysis

Data were analyzed by 1-way ANOVA using the general linear models (GLM) procedure of SAS software (Version 6.02; SAS Institute Inc., Cary, NC) with the main effect of injection treatment. The replicate cage served as the experimental unit. Significant differences among individual treatment means were determined with the LSD option of the GLM procedure. Actual probability levels are reported for the main effect. Significance was set at P < 0.10 (Luo and Dove, 1996).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Manganese source and dosage had no effect (P > 0.51) on average daily gain, feed intake, and feed conversion coefficient during 1 to 10 d or 11 to 20 d after Mn injections (Table 3Go). The chicks injected with Mn-containing solutions had greater (P < 0.01) bone Mn concentrations than those injected with saline on d 10 or 20 after injections (Table 4Go). On d 10 after injections, there were no differences (P > 0.24) in bone Mn concentration among injected Mn sources. However, on d 20 after injections, the birds injected with Mn AA C with strong chelation strength had a greater (P < 0.03) bone Mn concentration than those injected with Mn sulfate or Mn Met E with weak chelation strength. There was no difference (P > 0.36) between Mn AA B with moderate chelation strength and Mn AA C with strong chelation strength. The birds injected with Mn AA B with moderate chelation strength also had a greater (P < 0.02) bone Mn concentration than those injected Mn Met E with weak chelation strength, but no difference (P > 0.18) was observed between Mn Met E with weak chelation strength and Mn sulfate.


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  		Table 3. Effect of intravenously injected Mn on growth performance in broilers (n = 6)1
 

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  		Table 4. Effect of intravenously injected Mn on tissue Mn content, heart Mn-containing superoxide dismutase (MnSOD) activity, and MnSOD molecular RNA level in broilers (n = 6)1
 
The chicks injected with the control saline solution had a lower (P < 0.01) heart Mn concentration than those injected with Mn-containing solutions on d 10 or 20 after injections (Table 4Go). On d 10 after injections, the chicks injected with Mn AA B with moderate chelation strength and Mn Met E with weak chelation strength had greater (P < 0.05) heart Mn concentrations than those injected with Mn sulfate. No differences (P > 0.19) were observed in heart Mn concentration between organic Mn sources and Mn sulfate or among organic Mn sources on d 20 after injections.

There was a close correlation between heart Mn concentration and MnSOD activity (r = 0.956, P = 0.011 for d 10, and r = 0.955, P = 0.012 for d 20). The chicks injected with Mn sources had greater (P < 0.03) Mn-SOD activities in the heart than those injected with the control (Table 4Go), but there were no differences (P > 0.18) among injected Mn sources on d 10 or 20 after injections.

There was a strong correlation between heart Mn concentration and MnSOD mRNA (r = 0.970, P = 0.003 for d 10, and r = 0.976, P = 0.005 for d 20). The chicks injected with the control saline solution had a lower (P < 0.01) heart MnSOD mRNA level than those injected with Mn-containing solutions on d 10 or 20 after injections (Table 4Go). On d 10 after injections, the chicks injected with Mn AA B with moderate chelation strength had a greater heart MnSOD mRNA level than those injected with Mn sulfate (P < 0.01) or Mn AA C (P < 0.09) with strong chelation strength. The chicks injected with Mn Met E with weak chelation strength showed a greater value than those injected with Mn sulfate (P < 0.06). There was no difference (P > 0.13) between the chicks injected with Mn AA C with strong chelation strength and Mn sulfate. The same results as described above for d 10 were observed for d 20 after injections.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
A good way to study mineral metabolism and utilization in animals would result from the use of intrinsically labeled radioisotope methodologies. It has been reported that the transferrin was the major plasma carrier protein for Mn when rat was given Mn orally or intravenously (Davidsson et al., 1989), whereas albumin, or a protein that behaves like albumin, might be the Mn transport protein between the small intestine and the liver (Davis et al., 1993). The clearance of 54Mn2+ complexed to transferrin was much slower than that of free 54Mn2+ or 54Mn2+-{alpha}2 macroglobulin complex after injections into a jugular vein or a carotid artery (Davidsson et al., 1989). There were no differences in the tissue distribution of 54Mn in the animals receiving oral isotope and those injected intraportally with 54Mn complexed to albumin; however, animals injected with 54Mn complexed to transferrin had a significantly larger proportion of 54Mn in their muscle and heart than those given the isotope as carrier-free 54Mn or 54Mn complexed to albumin (Davis et al., 1993).

The isotope method was not adopted in this study because all the commercial organic Mn products used had not been manufactured with intrinsic radiotracers or stable isotopes of Mn. Therefore, in the current study, the Mn from different sources was introduced into birds through intravenous injections bypassing the gastrointestinal tract to detect differences in metabolic utilization of Mn in the sensitive target tissue between organic and inorganic Mn sources or among organic Mn sources. The results from this study indicated that on both d 10 and 20 after injections, neither bone Mn concentration nor heart Mn concentration was sensitive and consistent for detecting differences in Mn metabolic utilization of broilers between organic and inorganic Mn sources or among organic Mn sources, which is in agreement with our previous studies (Li et al., 2004, 2005) because both indices are not functional ones. Like all other essential trace elements, Mn functions either as an integral part of metalloenzymes or as an enzyme activator. Numerous investigators have noted that Mn is a crucial component of MnSOD, 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 (Zidenberg-Cherr et al., 1983; Davis et al., 1990). Therefore, the MnSOD is the most important Mn-containing enzyme in the animal body.

Researches concerning the role of Mn in the regulation of MnSOD showed that Mn was involved in not only transcription and translation but also insertion of the metal prosthetic group during maturation of the newly synthesized polypeptide in prokaryotic and eukaryotic organisms. Culotta et al. (2006) reported that Mn insertion into MnSOD could not occur posttranslationally in eukaryotes, but required new synthesis and mitochondrial import of the MnSOD polypeptide. Manganese-deficient mice had lower Mn concentration, lower MnSOD activity, and lower MnSOD mRNA in liver than those of the control. It is postulated that the lower MnSOD mRNA probably result from the down-regulation at the (pre)-transcriptional level (Borrello et al., 1992). The MnSOD gene in Escherichia 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) and also induced MnSOD expression (mRNA, immunoreactive protein, and enzyme activity) in human breast cancer Hs578T cells (Thongphasuk et al., 1999).

Because heart tissue has more mitochondria (Mela-Riker and Bukoski, 1985), more electron transport activity (potentially generating more superoxide; Sugiyama et al., 1993), and contain an unidentified super-oxide generator (Nohl, 1987), heart was more sensitive to Mn deficiency than other tissues as judged by MnSOD activity (Luo et al., 1992; Malecki and Greger, 1996) and MnSOD mRNA (Hurt et al., 1992). The experiment herein and our previous experiments in our lab have investigated the effect of dietary Mn level on Mn concentration, MnSOD activity, and MnSOD mRNA level in the heart of broilers. Our previous experiments showed that the heart Mn concentration, MnSOD activity, and MnSOD mRNA level of broilers at 21 d of age increased linearly as diet supplemented Mn increased from 0 to 180 mg/kg when chicks were fed in the same surroundings (Li et al., 2004, 2005). Chicks herein injected with Mn-containing solutions had greater heart MnSOD mRNA levels than those injected with the control saline, suggesting that available Mn at least participated in the regulation of heart MnSOD gene expression of chicks at the transcriptional level. Different Mn sources always had a sensitive and consistent effect on heart MnSOD mRNA level of broilers; however, the heart mitochondrial MnSOD activities of broilers did not increase to the same extent as MnSOD mRNA levels in the present study and our previous studies (Li et al., 2004, 2005; Luo et al., 2007). Several studies have shown that activities of MnSOD increased in response to a wide range of agents including nutrient constituents (Koch et al., 2000) or other factors (Warner et al., 1991), but the magnitude of the increases was less robust than that of 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 TNF-{alpha} at a level of 25 ng/mL. This could be the reason why Mn sources did not result in significant change in heart MnSOD activity of broilers. Further experiments are needed to investigate the exact mechanisms by which Mn regulates MnSOD activity and gene expression.

The results from the current study demonstrated that under intravenous injections of Mn sources, based on the heart MnSOD mRNA level of broilers, Mn sulfate was the least utilizable for heart tissue of broilers, and Mn AA B with moderate chelation strength was the most favorable for heart utilization and functioned more effectively, followed by Mn Met E with weak chelation strength, and lastly Mn AA C with strong chelation strength was less favorable for tissue utilization. Combination of the results from the present study and our previous researches (Li et al., 2004, 2005; Ji et al., 2006a,b) indicated that there were differences not only in the absorption of Mn in the digestive tract, but also in the metabolic utilization of Mn in the target tissue between inorganic Mn sulfate and organic Mn sources or among organic Mn sources with different chelation strengths. Compared with the organic Mn sources with moderate chelation strength, the lower bioavailability of the organic Mn sources with strong chelation strength possibly might be due to its strong chelation strength, which retarded Mn chelated to the organic Mn source to be mobilized for utilization even though it could be absorbed during digestion. Exact mechanisms of the absorption in the digestive tract and utilization of organic Mn sources at a tissue level in broilers remain to be addressed in future studies.

In conclusion, intravenously injected Mn has always sensitively and consistently affected heart MnSOD mRNA level of broilers. Based on the heart MnSOD mRNA level, intravenously injected Mn from organic Mn sources with moderate chelation strength was the most utilizable Mn source and functioned in the sensitive target tissue more effectively than Mn from Mn sulfate or other 2 organic Mn sources with weak or strong chelation strength. Understanding how the organic mineral sources are metabolically utilized at a tissue level would provide a promising strategy for the exploitation and utilization of new and highly bioavailable organic mineral additives in the poultry industry.


   FOOTNOTES
 
1 This study was supported by the Key Program of the National Natural Science Foundation of China (Project No. 30530570), Basic Science Research Program (Project No: ywf-td-4), National Natural Science Foundation of China (Project No. 30070560), and Hebei Normal University of Science and Technology Foundation for Doctors (B200301). Back

Received for publication December 27, 2007. Accepted for publication June 29, 2008.


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 DISCUSSION
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