J. Anim. Sci. 2004. 82:3162-3174
© 2004 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Cloning and expression of porcine adiponectin and adiponectin receptor 1 and 2 genes in pigs1
S. T. Ding2,
B. H. Liu and
Y. H. Ko
Department of Animal Science, National Taiwan University, Taipei 106, Taiwan
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Abstract
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In mice, adiponectin receptors (AdipoR) have been found to mediate the effect of adiponectin in muscle and liver in regulation of glucose and fatty acid metabolism. The purposes of this study were to clone these receptors from pig tissues by reverse transcription PCR using mRNA from skeletal muscle and adipose tissue and to investigate the expression of these genes in various pig tissues. Sequences of adiponectin, AdipoR1, and AdipoR2 were determined and found to be highly homologous to those of the human and mouse. The AA sequences predicted for the full-length cDNA of porcine adiponectin, AdipoR1, and AdipoR2 were similar to those of the human and mouse, ranging from 81 to 97% homology, suggesting similar functions of these genes in pigs as in other species. Transcripts for adiponectin were abundant in s.c. adipose tissue in Lee-Sung pigs and in crossbred pigs. Transcripts for AdipoR1 were abundant in heart and skeletal muscle and also detected to a lesser extent (P < 0.05) in adipose tissue, liver, and spleen of the Lee-Sung pigs. Transcripts for AdipoR2 were abundant in s.c. adipose tissue and present to a lesser extent (P < 0.05) in the liver, heart, skeletal muscle, and spleen. These results indicate that the effect of adiponectin may be mediated through these receptors in various porcine tissues. Fasting for 8 h did not have a significant effect on the expression of adiponectin and AdipoR1 mRNA, but it increased (P < 0.05) the AdipoR2 mRNA in the s.c. adipose tissue of crossbred pigs. These results indicate that the AdipoR2-mediated fatty acid oxidation may be responsible at least in part for the fasted state fatty acid oxidation in porcine adipose tissues. The successful cloning of pig adiponectin and adiponectin receptors will enhance the understanding of the involvement of these genes in regulating energy metabolism in pigs.
Key Words: Adiponectin • Adiponectin Receptor • Adipose Tissue • Pigs
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Introduction
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The major function of adipose tissue is to accumulate excess energy as fat in animals. Recent research indicates that adipose tissue is also an endocrine and paracrine tissue that secretes leptin, adiponectin, and other factors into the blood to regulate energy homeostasis (Mohamed-Ali et al., 1998
; Havel, 2002). Scherer et al. (1995) was the first to clone the adiponectin gene and found that the product of this gene was a 30-kDa protein. Wang et al. (2004) cloned a porcine adiponectin gene fragment and found that adiponectin mRNA is abundant in porcine adipose tissue and differentiating adipocytes.
Recent evidence showed that adiponectin has significant roles in inhibiting gluconeogenesis (Combs et al., 2001), increasing fatty acid oxidation (Fruebis et al., 2001), and increasing insulin sensitivity in mice (Yamauchi et al., 2002). Yamauchi et al. (2003) cloned the adiponectin receptors 1 and 2 (AdipoR1 and AdipoR2) from the human and mouse and demonstrated high expression of AdipoR1 in skeletal muscle and AdipoR2 in liver. Fasshauer et al. (2004) demonstrated that AdipoR2 was expressed in the adiponectin secreting 3T3-L1 clonal adipocytes, indicating that adiponectin has characteristics of an autocrine substance.
Although functions of adiponectin in humans and rodents have been revealed, porcine AdipoR has not been reported. We conducted this experiment to clone the full-length cDNA for porcine adiponectin and AdipoR genes and to study the tissue distribution of these genes in pigs. We also measured the effect of short-term feed restriction on the expression of porcine adiponectin, AdipoR1, and AdipoR2 genes.
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Materials and Methods
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Animals
For cloning of gene fragments, three 2-wk-old crossbred pigs (Sus domesticus; sows were predominantly Landrace-Yorkshire crossbreds mated to a Duroc boar) were killed by electrocution combined with exsanguination. Longissimus muscle and s.c. adipose tissues were taken for RNA extraction. For tissue distribution studies, three Lee-Sung pigs (10 mo old; 52 ± 5 kg) were used. Lee-Sung pigs, described by Lee et al. (1983) and Mason and Porter (2002), represent a breed selected for lower BW from pigs derived from crossing Lanyu pigs (sows, small-ear and small-size pigs, mature BW < 50 kg) with Landrace boars in Taiwan. Lee-Sung pigs have been widely used as a model for medical study in Taiwan. Heart, LM, liver, spleen, and s.c. adipose tissue were dissected, frozen quickly in liquid N, and then stored at –70°C until RNA extraction. Eight crossbred pigs (average BW = 30.32 ± 4.36 kg) were fed with commercial feed (CP = 20.3%; ME = 3,600 kcal/kg; as-fed basis). Three biopsy circles of back fat (2.54 cm diameter) were taken from each pig at 2 h after feeding (fed, four pigs) or 8 h after feeding (fasted, four pigs). The pigs injected i.m. with anesthetic (Zoletil containing zolazepam, Virbac Laboratories, Carros, France) at 10 mg/kg BW. The pigs were then maintained under constant anesthesia (2 to 3% halothane, 0.5% oxygen, and 1% nitrous oxide). The s.c. adipose tissue was dissected out and stored in liquid N immediately. The Experimental Animal Management and Use Committee at National Taiwan University approved all animal use protocols.
Extraction of RNA
Total RNA was extracted by the guanidinium-phenol-chloroform extraction method (Chomczynski and Sacchi, 1987), with modifications as described by Hsu and Ding (2003). The quality of the RNA was monitored by examination of the 18S and 28S ribosomal RNA bands after electrophoresis. The RNA was quantified by spectrophotometry at 260 nm and stored at –70°C.
Cloning of the Porcine Gene Fragments
Four microgams of tissue total RNA from a crossbred pig was reverse transcribed (RT) at 42°C with a SuperScript II First-Strand Synthesis System for RT-PCR (Invitrogen, Carsbad, CA). Total RNA from adipose tissue and skeletal muscle was used for RT-PCR to clone adiponectin and AdipoR2 from adipose tissue and AdipoR1 from muscle. The transcribed single strand DNA was amplified by PCR for 32 cycles, using pairs of sense and antisense primers (Table 1). AccuPrime Pfx DNA polymerase (Invitrogen), a high-fidelity DNA polymerase, was used to amplify cDNA. The conditions for PCR were denaturation at 94°C for 20 s (2 min in the first cycle), annealing for 30 s, and extension at 68°C for 2 min (5 min in the last cycle). The annealing temperatures for adiponectin, AdipoR1, and AdipoR2 were 56, 54, and 52°C, respectively. The PCR product for each gene was separated by gel electrophoresis, purified by gel extraction, and cloned into a pCR-Blunt II-TOPO vector (Invitrogen). Sequences of these PCR gene fragments were determined and homologies of these fragments with gene fragments from other species were compared.
Northern Analysis
Total RNA (20 µg of each sample) was electrophoresed and transferred to nylon membranes. The membrane was prehybridized at 42°C in UltraHyb (Ambion, Austin, TX) for 1 h, and then the denatured cDNA probe (95°C for 5 min) was added at a concentration of 1 pM of each cDNA, to hybridize with the targeted gene transcripts overnight at 42°C. The porcine 18S and adiponectin probe sequences were previously described (Wang et al., 2004), and the AdipoR1 (1 to 1,128 nucleotides) and AdipoR2 (331 to 946 nucleotides) probes were generated from sequences reported in this study. Hybridization results were quantified by phosphor-image analysis as previously described (Ding et al., 1999, 2002; Hsu et al., 2004). The densitometric value for an individual transcript in a sample lane was normalized to the densitometric value for the 18S ribosomal RNA in the same lane.
Statistical Analyses
The tissue distribution data were analyzed using an ANOVA procedure to determine the main effect of tissues, and Duncan’s new multiple-range test was used to evaluate differences among means (SAS Inst., Inc., Cary, NC). The fed and fasted data were analyzed by Student’s t-test for comparison of two means. A significant difference was indicated at a P 
0.05.
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Results and Discussion
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Porcine Gene Sequences
The RT-PCR products for porcine adiponectin, generated from porcine adipose tissue, covered the intact open reading frame with translation start codon (atg) and stop codon (tag; Figure 1). This full-length cDNA sequence for pig adiponectin was 732 bp long (GenBank AY589691), and sequence analysis showed that it contained the same sequence as the one published in Gen-Bank (AY135647). The sequences for pigs were highly homologous with those of the human (86%; GenBank NM 004797) and mouse (79%; Scherer et al., 1995). The AA sequence of porcine adiponectin was deduced from the cDNA sequence. It is a protein with 243 AA and a molecular weight of 26,369 g/mol, similar to that of the human (MW = 26,413; GenBank NM 004797) and mouse (MW = 26,409; Scherer et al., 1995) adiponectin. The predicted isoelectric point (pI) for the cloned porcine adiponectin (determined by Sequence Analyzer at http://www.proteinchemist.com) is 5.70, similar to that of human and mouse adiponectin, with a predicated pI of 5.42 for both, using the same software. The adiponectin AA sequence of pigs was very similar to those of the human (83%) and mouse (81%; Figure 2). The high homology of the porcine adiponectin compared with the sequences from human and mouse suggests a similar function of this protein in pigs compared with that in other mammalian species. Adiponectin has been found to decrease the basal blood glucose level by increasing insulin sensitivity (Combs et al., 2001; Yamauchi et al., 2001) and to increase use of plasma free fatty acids through increasing expression of genes involved in fatty acid oxidation in mice (Fruebis et al., 2001; Yamauchi et al., 2002).
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Figure 1. Full-length cDNA sequence for the pig adiponectin (ADN). This full-length open reading frame was obtained from reverse transcription PCR of mRNA from porcine adipose tissues. The dots indicate the same nucleotide. The homology between pig and human (GenBank NM 004797) was 86%, and between pig and mouse was 79% (Scherer et al., 1995).
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The full-length cDNA sequence for pig AdipoR1 cloned by RT-PCR from skeletal muscle mRNA was 1,128 bp long. Sequence analysis showed that this porcine AdipoR1 (GenBank AY578142) was identical to a partial porcine sequence in GenBank (1,044 bp, AY452710) and highly homologous with those of humans and mice (Yamauchi et al., 2003). The homology between pigs and humans or mice was 90 and 91%, respectively (Figure 3). The porcine sequence was homologous to 194 to 1,311 nucleotides in the human sequence (Yamauchi et al., 2003; Figure 3). The AA sequence of the porcine AdipoR1 was deduced from the cDNA sequence. It was a protein with 375 AA and calculated MW of 42,431 g/mol, similar to those of the human and mouse (Yamauchi et al., 2003). The predicted pI for the cloned porcine AdipoR1 (determined by Sequence Analyzer) is 6.39. The AdipoR1 AA sequence of pigs was very similar to those of the human (97%) and the mouse (97%; Figure 4). The high homology of the porcine AdipoR1 compared with the sequences from other species suggests a similar function of this protein in pigs as in other species. The AdipoR1 has been found to mediate the effect of adiponectin in muscle and liver to regulate energy homeostasis (Yamauchi et al., 2003). The hydrophobicity of AdipoR1 was analyzed by the Kyte-Doolittle hydrophobicity indices (Kyte and Doolittle, 1982) based on the software at http://bioinformatics-.weizmann.ac.il/hydroph/index.html. Porcine AdipoR1 contained seven highly hydrophobic areas from AA 119 to 356 (Figure 5), similar to that in human and mouse AdipoR1 (Yamauchi et al., 2003). It has been suggested that these regions are seven transmembrane domains that anchor AdipoR1 on cell membrane (Yamauchi et al., 2003).
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Figure 5. Hydrophobicity analysis of adiponectin receptor 1 (AdipoR1) protein domains. The hydrophobicity of AdipoR1 was analyzed by the Kyte-Doolittle hydrophobicity indices (Kyte and Doolittle, 1982) based on the software at http://bioinformatics.weizmann.ac.il/hydroph/index.html. The vertical axis indicates the hydrophilicity of the AA sequence (arbitrary units), whereas the horizontal axis indicates the AA sequence number started with the N terminal. Porcine AdipoR1 contained seven highly hydrophobic areas, as indicated in the figure.
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The full-length cDNA for porcine AdipoR2 cloned by RT-PCR from adipose tissue mRNA was 1,161 bp long (Figure 6). Sequence analysis showed that this porcine AdipoR2 (AY606803) was identical to a partial porcine sequence in GenBank (652 bp, AY452711) and highly homologous with those of human and mouse (Yamauchi et al., 2003). The homology between pig and human or mouse was 90 and 87%, respectively. The AA sequence of the porcine AdipoR2 was deduced from the cDNA sequence. It was a protein with 386 AA and a calculated molecular weight of 43,808 g/mol, similar to that of the human (43,883 g/mol) and mouse (43,980 g/mol; Yamauchi et al., 2003). The predicted pI for the cloned porcine AdipoR2 (determined by Sequence Analyzer at http://www.proteinchemist.com) is 6.12. The AdipoR2 amino acid sequence of pigs was very similar to those of the human (94%) and the mouse (91%; Figure 7). The high degree of homology between the porcine AdipoR2 compared with the sequences from other species indicates a similar function of this gene in pigs compared with other species. The AdipoR2 has been found to mediate the effect of adiponectin in liver (Yamauchi et al., 2003), 3T3-L1 clonal adipocyte (Fasshauer et al., 2004), and pancreatic ß-cell (Kharroubi et al., 2003) to regulate blood glucose level and the degree of fatty acid oxidation. The hydrophobicity of AdipoR2 was analyzed with the Kyte-Doolittle (Kyte and Doolittle, 1982) hydrophobicity indices based on the software at http://bioinformatics.weizmann.ac.il/hydroph/index.html. Porcine AdipoR2, similar to AdipoR1, contained seven highly hydrophobic areas from AA 150 to 364 (Figure 8), similar to that in human and mouse AdipoR2 (Yamauchi et al., 2003). It has been suggested that these regions are seven transmembrane domains that anchor AdipoR2 on cell membrane (Yamauchi et al., 2003).
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Figure 6. Full-length cDNA sequence for the pig adiponectin receptor 2 (AdipoR2). This full-length open reading frame was obtained from reverse transcription PCR of mRNA from porcine adipose tissue. The dots indicate the same nucleotide. The sequence of cloned porcine AdipoR2 cDNA was highly homologous compared with AdipoR2 gene of human (90%) and mouse (87%; Yamauchi et al., 2003).
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Figure 8. Hydrophobicity analysis of adiponectin receptor 2 (AdipoR2) protein domains. The hydrophobicity of AdipoR2 was analyzed by the Kyte-Doolittle hydrophobicity indices (Kyte and Doolittle, 1982) based on the software at http://bioinformatics.weizmann.ac.il/hydroph/index.html. The vertical axis indicates the hydrophilicity of the AA sequence (arbitrary units), whereas the horizontal axis indicates the AA sequence number started with the N terminal. Porcine AdipoR2 contained seven highly hydrophobic areas, as indicated in the figure.
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Tissue Distribution of Porcine Genes
The adiponectin transcript was abundant in the adipose tissue of Lee-Sung pigs (Figure 9). It was also detected in the LM in two out of three pigs tested, but was not detectable in the heart, liver, or spleen. Because the LM in mature Lee-Sung pigs contains a greater amount of i.m. fat than that of crossbred pigs (Wu et al., 2003), it is speculated that the adiponectin mRNA was actually extracted from the LM i.m. fat. Indeed, the two pigs with adiponectin mRNA in the LM had numerically greater fat content (2.55% measured by chloroform/methanol extraction) than the third pig (1.6%). In other species, it has been reported that adiponectin is only expressed in adipose tissue (Scherer et al., 1995; Fruebis et al., 2001; Yamauchi et al., 2002). Our result confirms that adiponectin is abundant in adipose tissue as previously observed in crossbred pigs (Wang et al., 2004) and in other species (Scherer et al., 1995). Adiponectin is generated by adipose tissue and secreted into the blood to assert its endocrine functions of regulating glucose use and fatty acid oxidation in mammals (Fruebis et al., 2001; Yamauchi et al., 2002).
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Figure 9. Tissue distribution of adiponectin (ADN) and adiponectin receptor 1 (AdipoR1) and 2 (AdipoR2) transcripts. Total RNA was isolated from heart (H), liver (L), longissimus muscle (M), spleen (S), and s.c. adipose tissue (AT), obtained from 8-mo-old Lee-Sung pigs (n = 3). Twenty micrograms of total RNA was electrophoresed and transferred to nylon membranes. The membranes were hybridized with porcine cDNA probes for various gene fragments. The top portion of the figure represents the typical expression and the bottom portion is the mean and SEM for each tissue. The size of the primary transcript detected in porcine total RNA samples by each gene fragment was 3.3 kb for ADN, 2.0 kb for AdipoR1, 4.0 kb for AdipoR2, and 1.9 kb for 18S. Within transcript, the asterisks indicate a difference (P < 0.05) compared with means without an asterisk.
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The AdipoR1 transcript was abundant in the heart and skeletal muscle and, to a lesser extent, in the adipose tissue, liver, and spleen of Lee-Sung pigs (Figure 9
). The AdipoR2 transcript was abundant in the adipose tissue and, to a much lesser extent, in the liver, it was barely detectable in the heart and skeletal muscle, and was not detectable in the spleen of Lee-Sung pigs. These results suggest that adiponectin may function through the AdipoR1 and AdipoR2 in the tissues expressed these receptors. The wide range of expression of adiponectin receptors also suggests that adiponectin affects the metabolism of many types of tissues. In mice, the AdipoR1 transcript is abundant in heart, kidney, lung, skeletal muscle, and spleen (Yamauchi et al., 2003). Physiologically, heart and skeletal muscle use a large quantity of fatty acids as an energy source. The high AdipoR1 expression provides receptors to mediate the function of adiponectin in increasing fatty acid oxidation by enhancing fatty acid transportation into the mitochondria of these tissues (Yamauchi et al., 2002). Although the AdipoR2 is widely expressed in many tissues in the mouse, the highest concentration was found in the liver (Yamauchi et al., 2003). We observed that the greatest AdipoR2 mRNA concentration was in the s.c. adipose tissue, with a much lower concentration in the liver. Therefore, there is a species difference regarding the expression of AdipoR2 mRNA. The adipose tissue in pigs is the major lipogenic tissue, with very high lipolytic activity (Mersmann, 1986). The greater AdipoR2 mRNA concentration in porcine adipose tissue vs. other tissues indicates that AdipoR2 plays a more significant role in enhancing glucose import for lipogenesis and fatty acid oxidation in the adipose tissue than other tissues. Fasshauer et al. (2004) found that AdipoR2 was expressed in 3T3-L1 adipocytes and the expression of AdipoR2 was stimulated by growth hormone. The discovery of adiponectin receptors in various mammalian tissues further demonstrates that the secreted adiponectin in the blood could assert its function through the tissues that express adiponectin receptors. These results also indicate that regulation of adiponectin function is tissue-dependent because receptor population differs between tissues. The regulation of the expression of these receptors awaits further investigation.
Gene Expression in Adipose Tissues from Fed or Fasted Pigs
Eight hours of fasting had no effect on the mRNA concentration of adiponectin in pig s.c. adipose tissue (Figure 10), suggesting that short-term fasting has a minimal effect on the expression of adiponectin gene in porcine adipose tissue. English et al. (2003) observed that the postprandial blood adiponectin concentration increased only in obese human subjects. Imbeault et al. (2004) also observed that fasting or postprandial condition did not affect blood adiponectin concentration in humans. These results suggest that adipose tissue adiponectin secretion was not affected by feeding status in lean humans. However, Gui et al. (2003) and Seo et al. (2004) reported that adiponectin gene expression in adipose tissue and adiponectin secretion was decreased by fasting in normal mice. Therefore, there might be species-specific responses for the expression of adiponectin under different feeding states. The AdipoR1 mRNA concentration was not affected by the short-term feed restriction, whereas AdipoR2 was increased in the adipose tissue of the fasted pigs (Figure 10). Because the AdipoR2 mRNA concentration is high in porcine adipose tissue, the data suggest that part of the adiponectin function in adipose tissue is enhanced by the short-term feed restriction. Both AdipoR1 and AdipoR2 mRNA concentrations are increased by 48-h fasting in both liver and muscle tissues in mice (Tsuchida et al., 2004). Tsuchida et al. (2004) further demonstrated that the expression of mouse AdipoR1 and AdipoR2 was inhibited by high insulin concentration. In pigs, we found that AdipoR2 mRNA concentration in adipose tissues was more sensitive to fasting (Figure 10). One of the functions of adiponectin is to increase fatty acid oxidation (Fruebis et al., 2001; Yamauchi et al., 2002), which is high in the fasted state. Therefore, the AdipoR2 mediated fatty acid oxidation is responsible at least in part for the fasted state fatty acid oxidation in porcine adipose tissues. We speculate that the roles of AdipoR1 and AdipoR2 may be different in porcine adipose tissue therefore the mRNA concentrations are influenced differently by feeding states for these two adiponectin receptors.
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Figure 10. Porcine gene expression in fed or fasted adipose tissue. Pig s.c. adipose tissues were taken at 2 h after feeding (fed) or 8 h after feeding (fasted). The total RNA from the adipose tissue of each pig (20 µg) was electrophoresed and transferred to a nylon membrane. The membranes were hybridized with cDNA probes for stearoyl coenzyme A desaturase (SCD), adiponectin (ADN), adiponectin receptor 1 (AdipoR1), adiponectin receptor 2 (AdipoR2), and 18S ribosomal RNA. The data represent the mean of four crossbred pigs per treatment. The error bar indicates SEM of each treatment. The asterisk indicates that fasting increased (P < 0.05) AdipoR2 mRNA abundance.
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Taken together, these tissue distribution data reveal that adiponectin receptors are widely expressed in various porcine tissues. Because there are different expression patterns for porcine AdipoR1 and AdipoR2 and the mRNA concentrations of these genes are affected differently by short-term fasting, functions of these two receptors may be different in pigs and await further investigation.
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Implications
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The successful cloning of porcine adiponectin and its receptors full-length cDNA provides new molecular tools to study the involvement of adiponectin in regulating energy metabolism in pigs. Functional expression of these genes can be used to further investigate the roles of these genes in different tissues and under various physiological and nutritional conditions. In current study, we demonstrated that adiponectin receptors, AdipoR1 and AdipoR2, expressed differently in various porcine tissues, suggesting a possible tissue-dependent regulation mechanism and possibly different functions of these receptors in different tissues. The differential effects of short-term fasting on the mRNA concentration of adiponectin receptors 1 and 2 in porcine adipose tissue suggest that the roles of these two receptors are different in adipose tissue. Understanding the functions and gene expression regulation of these genes will enhance our ability to take new approaches to modify energy metabolism in pigs.
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Footnotes
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1 This work was supported in part by National Science Council and Council of Agriculture in Taiwan. We thank W. M. Cheng for care and feeding of the animals. 
2 Correspondence: 50, Lane 155, Kee-Long Rd. Sec. 3 (phone: +886953610078; fax: +886227324070; e-mail: sding{at}ntu.edu.tw).
Received for publication April 28, 2004.
Accepted for publication July 14, 2004.
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Abstract
Introduction
