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Gene expression profiling: Insights into skeletal muscle growth and development¹

Iowa State University, Department of Animal Science, Ames 50011-3150

	Abstract

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
Microarray technology is now available for many livestock species, and animal scientists are beginning to utilize the technology to address issues of importance to animal agriculture. This review discusses how microarray technology has been applied to study global gene expression changes in skeletal muscle. For example, microarrays have been used to elucidate gene function in knockout mice, evaluate breed differences, evaluate the effects of hormone administration, and evaluate the effects of diet. Data generated from these global gene expression studies are providing new insights to stimulate future hypothesis-driven research.

Key Words: development • gene expression • growth • microarray • skeletal muscle

	INTRODUCTION

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
As animal agriculture has become highly competitive with narrow profit margins, research has focused on improving the efficiency of animal production. For the meat-producing industries, emphasis has been on increasing understanding of physiological processes and molecular pathways associated with skeletal muscle growth and development. To date, the majority of the progress made in the field of muscle biology has been accomplished by examining single genes, proteins, or pathways. However, the availability of microarray technology for most production animal species provides new opportunities for researchers to generate global gene expression profiles. Initial microarray experiments have generated new information regarding the molecular consequences of gene expression changes associated with genetic, pharmacological, and nutritional models. These preliminary "whole genome" assessments of gene expression have provided new insights concerning changes in gene expression associated with skeletal muscle growth and development, and have identified novel candidate genes and physiological pathways to target in future hypothesis-based testing. These and future microarray studies are anticipated to open new avenues of research that will aid in the development of novel strategies to enhance the efficiency of lean tissue deposition in livestock species.

In the past decade, a tremendous number of gene expression profiling experiments has been completed using a wide range of experimental models. We have limited our discussion here to three areas of investigation with respect to the growth and development of skeletal muscle in which microarrays have been used to evaluate 1) the impact of genotype, 2) the effect of pharmacological stimulation, and 3) the impact of nutrition. There is a large body of literature describing the influence of physical activity level on skeletal muscle gene expression. However, the vast majority of this research is focused on skeletal muscle atrophy in response to a lack of physical activity, and as such will not be covered.

	GENOTYPE EFFECTS ON GENE EXPRESSION

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
A number of studies have been completed to investigate the effects of genotype on gene expression. Changes in gene expression profiles in response to gene inactivation, gene overexpression, and breed type have been studied to gain insight into the functional role of a gene or genotype. For example, Castro-Chavez et al. (2003) investigated changes in gene expression in several tissues (white adipose, kidney, liver, heart, and skeletal muscle) in response to the inactivation of perilipin, a protein that coats the surface of intracellular neutral lipid storage droplets. Perilipin-null mice are characterized by constitutive lipolysis, normal body weight, increased feed intake, and decreased fat deposition, and are resistant to diet-induced and genetic obesity. Interestingly, perilipin-null mice exhibited a coordinated increased expression of genes involved in ß-oxidation, the Krebs cycle, and electron transport chain, with a decreased expression of lipid biosynthesis genes in all of the tissues studied. For example, SCD-1 expression was reduced 5-fold in skeletal muscle of perilipin-null mice. These results demonstrate how a single gene primarily expressed in white adipose tissue can have profound effects on other tissues including skeletal muscle.

Alteration of the expression level of proteins with no known ties to regulation of gene expression can have dramatic effects on the mRNA transcript profile of skeletal muscle. For example, Janssen et al. (2003) reported that inactivation of adenylate kinase 1 in mice resulted in fiber-type specific changes in the expression level of genes involved in glycolysis, mitochondrial metabolism, cell structure, and myogenic events. Their observations indicate there is a widespread remodeling in adenylate kinase 1-deficient muscle such that communication between ATP-producing and utilizing sites is maintained to some extent. Similarly, Zimmerman et al. (2004) reported that inactivation of carbonic anhydrase III in mice can alter skeletal muscle gene expression. When the studies of Castro-Chavez et al. (2003), Janssen et al. (2003), and Zimmerman et al. (2004) are taken together, they indicate that there are nutrient-sensing mechanisms within the cell that regulate gene expression in skeletal muscle. It is likely that metabolic intermediates act as ligands, cofactors, or coactivators for proteins involved in the regulation of gene expression.

Other studies have evaluated the function of transcription factors. Kamei et al. (2004) described the changes in gene expression in transgenic mice overexpressing FOXO1, a forkhead-type transcription factor, which is expressed in skeletal muscle. In general, overexpression of FOXO1 altered the expression level of genes involved in cell/cytoskeletal structure, cell signaling, cell defense, metabolism, and protein turnover. These researchers were able to categorize each of the changes in gene expression with respect to the phenotypes observed in FOXO1 transgenic mice. This provides them with insight into the molecular adaptations that have taken place, as well as starting points from which to further define the phenotype. Similarly, Glenmark et al. (2004) reported the difference in gene expression in male and female mice in response to the inactivation of estrogen receptor-ß. Interestingly, it was observed that, in general, inactivation of estrogen receptor-ß decreased gene expression in female and conversely increased the expression of those same genes in male mice. These results are important because they point out the profound effect that the sex of the animal can have on gene expression in skeletal muscle, and demonstrate that the sex of an animal has to be considered when interpreting microarray results.

Recently in livestock, microarrays have been used to evaluate the effect of breed-type in skeletal muscle of boars and steers (Lin and Hsu, 2005; Wang et al., 2005). Not surprisingly, Japanese Black cattle expressed lipid metabolism genes at a higher level, whereas Holstein cattle had higher levels of skeletal muscle contractile genes (Wang et al., 2005). Similarly, Lin and Hsu (2005) observed that Duroc pigs had higher levels of contractile gene expression compared with Taoyan pigs. In addition, there were a number of membrane receptor/transport, protein catabolism, transcription-related, metabolism, and stress genes that were expressed at higher levels in skeletal muscle of Duroc vs. Taoyan pigs.

Working within a single breed of cattle, Sudre et al. (2005) demonstrated that transcription profiling could detect differential gene expression between Charolais bulls of high and low growth potential. Importantly, these livestock studies demonstrate the utility of gene expression profiling as a tool for the discovery of genes contributing to quantitative variation among breeds with respect to the trait analyzed. Differentially expressed genes could be directly responsible for the observed breed differences.

	PHARMACOLOGICAL EFFECTS ON GENE EXPRESSION

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
A number of pharmacological compounds are known to alter skeletal muscle metabolism, resulting in a variety of physiological changes including muscle hypertrophy or atrophy, altered energy expenditure, and insulin resistance. Changes in gene expression profiles in response to some of these compounds have been studied to gain insight into the mechanisms by which they influence muscle metabolism and protein turnover. For example, Viguerie et al. (2004) investigated changes in skeletal muscle gene expression profiles before and during a 6-h infusion of epinephrine in young men. Although epinephrine is a hormone typically associated with the fight-or-flight stress response, it also influences a number of important metabolic processes, including energy and protein metabolism in skeletal muscle. Viguerie et al. (2004) described changes in expression of genes involved with cyclic AMP (cAMP)-dependent signal transduction pathways and cAMP-responsive genes, consistent with prior knowledge that epinephrine acts on skeletal muscle through the ß2-adrenergic receptor and stimulation of cAMP production. A number of genes associated with energy metabolism were also identified as differentially expressed in response to epinephrine infusion. In general, these genes had important roles in glucose and lipid metabolism.

Thyroid hormone is another important regulator of energy metabolism in skeletal muscle. Clement et al. (2002) described a microarray experiment that investigated gene expression changes in skeletal muscle of men treated with thyroid hormone for 14 d. These authors also reported changes in the expression of genes associated with energy metabolism. However, gene expression profiles associated with thyroid hormone administration suggested that changes in energy metabolism occurred through alterations in mitochondrial activity. This result is in contrast to the work of Viguerie et al. (2004) that indicated gene expression alters in response to epinephrine function to modify substrate availability to the mitochondria, but has little impact on genes associated with mitochondrial function. Thus, these results suggest that even though epinephrine and thyroid hormone both stimulate energy expenditure by skeletal muscle, this effect is brought about by different mechanisms.

Insulin is another hormone that influences energy metabolism, as well as many other functions, of skeletal muscle. Rome et al. (2003) investigated the impact of insulin on human skeletal muscle using a 3-h hyperin-sulinemic euglycemic clamp to study transcriptional changes produced directly by insulin. These authors observed a clear influence of insulin on genes related to energy balance, and reported changes in expression of genes that regulated substrate availability as well as mitochondrial activity.

In addition to influencing energy expenditure, epinephrine, thyroid hormone, and insulin affect protein turnover in skeletal muscle; epinephrine and insulin stimulate a net gain, and thyroid hormone stimulates a net loss in muscle protein. Interestingly, each of these hormones significantly altered the expression of multiple genes involved in the ubiquitin/proteasomal system. Thyroid hormone and epinephrine stimulated and inhibited, respectively, genes associated with the ubiquitin/proteasomal system (Clement et al., 2002; Viguerie et al., 2004). This result is consistent with a general increase and decrease in protein degradation normally associated with thyroid hormone and epinephrine, respectively, in skeletal muscle. Insulin increased the expression of multiple genes that promote protein degradation via the ubiquitin/proteasomal system (Rome et al., 2003), even though insulin is known to stimulate net skeletal muscle protein accretion in part through reduced protein degradation. One potential explanation for this result is that insulin stimulates an increase in controlled degradation of specific proteins that function in important biological processes, such as signal transduction, that contribute to an overall net protein gain. Overall, these microarray experiments have revealed that a common mechanism for regulating protein turnover is shared by three compounds that generate very different physiological responses from skeletal muscle.

The use of microarrays to study changes in skeletal muscle in response to pharmacological compounds has contributed to the identification of novel genes and physiological pathways of importance to skeletal muscle growth and metabolism. For example, McDaneld et al. (2004), using differential display technology, reported the downregulation of a novel gene, Asb15, in response to administration of a ß-adrenergic receptor agonist. The down regulation of additional members of the Asb gene family has since been observed by microarray analysis in skeletal muscle of mice following administration of the ß-adrenergic receptor agonist clenbuterol (our unpublished data). Members of the Asb gene family may be important regulators of signal transduction via the ubiquitin/proteasomal pathway (Chung et al., 2005; Heuze et al., 2005), and have been implicated in the regulation of insulin signaling (Wilcox et al., 2004). Because the ubiquitin/proteasomal system has a critical role in the regulation of protein turnover, the Asb family may prove to be an important regulator of muscle growth.

Additionally, microarray experiments have linked important functions relative to immunoregulatory and inflammatory processes to skeletal muscle. Expression of multiple genes important to the immune response was altered in skeletal muscle following epinephrine (Viguerie et al., 2004) and insulin (Rome et al., 2003) administration. This finding is important because it suggests a novel link between energy metabolism and the immune system that may be regulated by skeletal muscle. Such a role may have important implications for livestock production in the context of animals meeting their genetic potential for growth under suboptimal environmental conditions.

	NUTRITIONAL EFFECTS ON GENE EXPRESSION

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
Although gene expression profiling technologies such as microarrays are becoming increasingly available to animal scientists, little research has utilized these technologies to understand the influence of nutrition on the genetic basis of economically important traits of muscle. The majority of microarray studies examining the impact of nutrients on gene expression in skeletal muscle to date have focused on the effects of nutrient restriction and its potential to reduce changes seen during the aging process (Weindruch et al., 2001; Sreekumar et al., 2002). An argument could be made that these studies are relevant to animal production, particularly to breeding stock longevity; however, we will not discuss them further. Three additional areas in which gene expression profiling of skeletal muscle in nutritional studies could impact livestock production are in improving the efficiency of production, the quality of products, and the health and well-being of animals.

Da Costa et al. (2004) examined the impact of both protein and energy restriction on gene expression in skeletal muscle of growing pigs. The restricted diets used in that experiment also induced an increase in intramuscular fat and phospholipids, suggesting that some of the differentially expressed genes may be of importance to meat quality as well as nutrient use. Nutrient deficiency in this experiment increased the expression of genes that facilitate a potential for increased breakdown of substrates, increased generation of ATP, increased translation, and increased growth modulation or differentiation. A similar study was conducted in steers by Reverter et al. (2003), but this work focused more on the statistical analysis of the microarray experiment and less on the possible roles of the differentially expressed genes. Subsequently, Byrne et al. (2005) found that many of the genes that were differentially expressed in response to nutrient restriction were involved in protein turnover and cytoskeletal metabolism.

One potential benefit of microarray technology will be to aid in establishing more accurate nutrient requirements specific to animals’ genetic background. With increasing concerns and regulations over the environmental impact of animal agriculture, more precisely defining nitrogen and phosphorus needs of animals is of profound importance. In our laboratory, we have begun to look at the impact of genetic background and dietary phosphorus deficiency on gene expression in growing porcine muscle using microarray analysis (our unpublished observations). We anticipate that this work will contribute to genotype-specific phosphorus requirements for pig production. This work is desperately needed to maximize our ability to produce animal products in an "environmentally friendly" manner.

Additionally, combining gene expression profiling with nutritional studies of animals from different genetic backgrounds may reveal new opportunities for developing genotype-specific diets to enhance product quality or animal well-being. For example, product traits such as fatty acid profiles or mineral content may be enhanced, or dietary interventions may be developed to optimize the animals’ response to immune challenges by impacting the expression of genes important to these traits.

	LIMITATIONS

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
Microarray technology, like all experimental approaches, has important limitations that must be recognized as experiments are designed and interpreted. Unique issues relevant to the design, statistical analysis, and management of data from microarray experiments have been reviewed elsewhere (for example, Anderle et al., 2003; Blalock, 2003; Simon, 2003). Of particular importance to microarray experiments involving skeletal muscle is the recognition that muscle tissue is not a homogeneous cell population. In particular, differences between fiber types may alter gene expression profiles. Several researchers have reported differences in gene expression between white and red skeletal muscles (Bai et al., 2003; Kim et al., 2004). Recognizing these differences, as well as the variation contributed by nonmuscle cells and other physiological factors such as sex of the animal, will be essential for accurate and meaningful interpretation of microarray data.

	CONCLUSIONS

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 
With the development of microarray technology, researchers have been able to obtain broad and accurate estimates of global gene expression levels. These experiments have provided insights into the molecular consequences of a treatment, including genetic, pharmacological, nutritional, or other effects. Although we have discussed a few applications of microarrays here, it is easy to envision that this technology can be beneficial to all disciplines within the animal sciences. Armed with "global" assessments of gene expression, researchers could then develop hypothesis-driven experiments to further define gene function within the context of their experimental model of interest. These experiments are anticipated to open new avenues of research and aid in the development of strategies to enhance the efficiency of lean tissue deposition in livestock species.

	Footnotes

 
¹ Invited review. Presented at the "Meat Science and Muscle Biology" symposium held at the American Society of Animal Science Annual Meeting, Cincinnati, OH, July 24–28, 2005.

² Corresponding author: jreecy{at}iastate.edu

Received for publication August 10, 2005. Accepted for publication September 2, 2005.

	LITERATURE CITED

Top Abstract INTRODUCTION GENOTYPE EFFECTS ON GENE... PHARMACOLOGICAL EFFECTS ON GENE... NUTRITIONAL EFFECTS ON GENE... LIMITATIONS CONCLUSIONS LITERATURE CITED

 


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