J. Anim. Sci. 2003. 81:E94-E101
© 2003 American Society of Animal Science
Heterogeneity of protein expression within muscle fibers1
B. W. C. Rosser* and
E. Bandman2
* University of Saskatchewan, College of Medicine, Department of Anatomy and Cell Biology, Saskatoon, Saskatchewan, S7N 5E5, Canada and University of California, Department of Food Sciences and Technology, Davis 95616
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Abstract
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Skeletal muscle fibers are elongated multinucleated cells. Along its length, an individual fiber may contain thousands of myonuclei, each controlling protein synthesis within its surrounding cytoplasm. Therefore, a fiber can be considered to be a series of myonuclear domains, each responding to distinct localized signaling mechanisms that may result in differential gene expression within the fiber. This brief review examines phenomena that produce distinct subsets of proteins within different regions of a muscle fiber. These include changes in protein expression associated with activity-induced fiber-type transformation, muscle development, and denervation. Myosin heavy-chain (MyHC) proteins are fundamental structural and functional components of the muscle fiber. They are represented by different isoforms, each of which is the product of a separate gene that may be differentially expressed during the development of distinct muscle fiber types. We have found that in mature chicken and pigeon pectoralis muscle, the tapered ends of fibers contain the neonatal MyHC isoform in addition to the adult isoform found throughout the lengths of the fibers. Examination of serial sections along the length of muscle fibers of chicken pectoralis at different stages of development illustrates that repression of neonatal MyHC isoform expression proceeds as a gradient from the centrally located motor endplate toward the ends of a fiber. In denervated mature fibers, myonuclei furthest from the endplate are the first to reexpress neonatal myosin. We hypothesize that trophic factor(s) emanating from the vicinity of the motor endplate represent a potential localized signaling pathway that may differentially modulate MyHC gene expression along the length of the muscle fiber. Muscle fibers grow in length by the addition of new sarcomeres to their tapered tips, and growing fibers have smaller myonuclear domains (less cytoplasm per nucleus). Additional experiments using chicken pectoralis demonstrated that myonuclear domains are significantly smaller in those areas of the fibers expressing predominantly neonatal myosin. In maturing muscle, the volume of cytoplasm per nucleus is less within the ends of the fibers. Thus, when an increase in the expression of one or more gene products is required within a specific region of the muscle fiber, transcriptional output may be enhanced by the concentration of myonuclei within that region.
Key Words: Denervation • Development • Muscle • Muscle Fibers • Myosins
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Introduction
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Vertebrate skeletal muscle cells caudal to the brachial arches are derived from myotomes of the somites (Wigmore and Evans, 2002
). In early embryonic development, myogenic regulatory factors are responsible for transformation of these mesodermal cells into myoblasts (Perry and Rudnicki, 2000; Stockdale, 2000). Initially, each myoblast is a small spindle-shaped cell with a single central nucleus (Swatland, 1994). There are embryonic, fetal, and adult waves of myoblasts (Stockdale, 1997). Embryonic and fetal myoblasts divide repeatedly by mitosis and are highly mobile, aggregating into clusters. Subsequently, these myoblasts align with their long axes parallel to one another and fuse to form small, multinucleate cells called myotubes (Leiber, 1992). During growth and maturation, additional myoblasts are incorporated into each myotube. The resultant cells are elongate, fusiform-shaped multinucleate cells termed muscle fibers (McComas, 1996).
Muscle fibers, along with a few other select animal cell types, such as osteoclasts and cytotrophoblasts, are exceptional in that they are multinucleate (Allen et al., 1999). A typical fiber may contain hundreds or thousands of myonuclei (Cullen and Landon, 1994; Tseng et al., 1994). Each myonucleus regulates gene expression within the surrounding portion of the fiber (Hall and Ralston, 1989; Pavlath et al., 1989; Ono et al., 1994).
It has long been held that, with the exception of certain proteins associated with the motor endplate, expression of most proteins is relatively uniform along the lengths of skeletal muscle fibers. Certainly, this may be the case for some proteins (Pette et al., 1980). However, accruing evidence indicates that there is pronounced regional variation in the expression of many genes (Newlands et al., 1998; Apel et al., 2000; Rossi et al., 2000). It is the purpose of this review to highlight some of the research showing heterogeneity of gene/protein expression within individual muscle fibers.
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Protein Subsets within Specialized Regions of the Muscle Fiber
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The neuromuscular junction (NMJ) is the site at which a motor neuron communicates with a muscle fiber, and is comprised of highly specialized portions of three cells: motor neuron, Schwann cell, and muscle fiber. Due to its accessibility, the NMJ has been widely used by neurobiologists as a model for the study of synaptic development. Consequently, the NMJ has been one of the most studied regions of the muscle fiber. Numerous proteins involved in complex signaling pathways are localized at the NMJ. As a complete description of NMJ gene expression is well beyond the scope of this paper, for a comprehensive overview the reader is referred to review articles (Meier and Wallace, 1998; Sanes and Lichtman, 1999).
Acetylcholine receptors (AChR) are initially distributed evenly and at low densities within the plasmalemma along the length of developing muscle fibers. Two trophic factors, agrin and neuregulin, pass from the developing nerve terminal to the muscle fiber. Each of these factors act collectively to concentrate AChR beneath the nerve terminal. Agrin cooperates with muscle-specific tyrosine kinase to coordinate AChR clustering by the AChR-associated protein rapsyn. Neuregulin interacts with erbB kinases to stimulate selective expression of AChR subunit genes by synaptic myonuclei. Calcitonin gene-related peptide is another nerve-derived trophic factor that stimulates AChR synthesis, although gene knockout studies indicate that it is not as crucial as agrin and neuregulin (Meier and Wallace, 1998). The neurotransmitter acetylcholine indirectly represses AChR subunit gene expression by extrasynaptic myonuclei (Sanes and Lichtman, 1999). After development, although the NMJ comprises less than 0.1% of the muscle fiber surface, it contains over 95% of the AChR (Tsim and Barnard, 2001). Myonuclei at the NMJ are clustered and are larger and rounder than extrasynaptic myonuclei. Also, unlike extrasynaptic myonuclei, there is upregulation of synaptic genes (Apel et al., 2000).
The subsarcolemmal cytoskeleton of muscle fibers is organized into distinct compartments, including the NMJ, costameres (at each Z-line), and the myotendinous junction (MTJ). At these locations, multiple proteins form elaborate complexes that anchor actin filaments to the sarcolemma. Fibronectin, laminin, vinculin, talin, and other proteins are especially concentrated at the MTJ (Tidball, 1991; Berthier and Blaineau, 1997). Again, since a thorough explanation of these regions is beyond the scope of our paper, the reader is referred to a review (Berthier and Blaineau, 1997).
Fiber ends display localized expression of additional proteins. Acetylcholinesterase is concentrated at the tips of some fibers, although its purpose there is not fully understood (Trotter, 1993; Rosser et al., 1995; Paul and Rosenthal, 2002). Myostatin is a negative regulator of muscle growth. It is normally present at the ends of muscle fibers of the mature rat and is elevated by muscle unloading (Wehling et al., 2000). In addition, the expression of certain myogenic regulatory factors (MyoD and myogenin) have been reported to be greater at the ends of fibers in mature rat muscle. The expression of these factors along the lengths of the fibers is increased by stretch-induced hypertrophy (Zador et al., 1999).
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Heterogeneity of Myosin Heavy-Chain Expression within Fibers
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Myosin is a fundamental structural and functional component of all skeletal muscles. In skeletal muscle, the myosin molecule is a hexamer consisting of two heavy (MyHC) and four light chains (Lowey, 1994). A diverse multigene family encodes MyHC (Bandman et al., 1994; Weiss and Leinwand, 1996; Shrager et al., 2000). There are many biochemically distinct but related MyHC isoforms that are expressed during various stages of development (Tidyman et al., 1997; McKoy et al., 1998) and in a functional muscle fiber type-specific manner (Bottinelli et al., 1994; Reiser et al., 1996).
There is a sequential expression of MyHC isoforms within developing and maturing muscle fibers. This is true of both fast- and slow-contacting fibers (Bandman and Rosser, 2000). Because this differential expression is usually gradual, developing and maturing fibers normally coexpress more than one MyHC isoform (Gordon and Lowey, 1992; Gauthier and Orfanos, 1993; Baldwin and Haddad, 2001).
It was formerly held that each mature skeletal muscle fiber type expressed a characteristic MyHC isoform, and that those mature fibers observed expressing multiple isoforms were undergoing a fiber type transition in response to altered functional demands (Pette and Staron, 1997). Whereas increased neuromuscular activity, mechanic loading, or hypothyroidism induced a change from fast to slow MyHC isoforms, the opposite initiated a transition from slow to fast MyHC. This dynamic process yielded transitional fibers, each containing a mix of MyHC isoforms (Pette and Staron, 2000; Baldwin and Haddad, 2001).
It is now appreciated that large numbers of mature fibers in normal muscle may typically express more than a single MyHC isoform (Peuker and Pette, 1997; Wu et al., 2000; Lefaucheur, et al., 2002). It is thought that these fibers are stable hybrids and not transitional fiber types (Stephenson, 1999: Lutz and Lieber, 2000). However, it is not generally known that these fibers may exhibit pronounced heterogeneity of MyHC expression along their lengths.
We have shown that in addition to the mature (adult) MyHC isoform normally expressed throughout the length of a fiber, the ends or terminal tips of fast-contracting fibers of mature chicken (Gallus gallus; Rosser et al., 1995) and pigeon (Columba livia; Bartnik et al., 1999) pectoralis muscle express an isoform characteristic of earlier development. Heterogeneity of MyHC expression along the lengths of individual fast fibers was also observed in studies of adult rabbit hind-limb muscles (Peuker and Pette, 1997). Similarly, multiple myosin isoforms were found to be synthesized and localized differentially along the lengths of certain extraocular fiber types of mature mammals (Lucas and Hoh, 1997; Rubinstein and Hoh, 2000; Porter, 2002). Variation in MyHC isoform expression was also observed along the lengths of intrafusal muscle fibers of mature rat (Kucera et al., 1992), human (Liu et al., 2002), and chicken (Maier, 1994). MyHC composition was reported to vary significantly between consecutive 1-mm segments along the length of fibers from mature frog hind-limb muscles (Lutz et al., 2001). In experimentally injured leg muscles of chicken, a MyHC isoform characteristic of early development was reexpressed within the damaged parts of the muscle fibers (Zhang and Dhoot, 1998).
Speed or velocity of contraction has been directly correlated with MyHC isoform content in single fibers from chicken (Reiser et al., 1996) and mammals (Bottinelli et al., 1994; Hilber et al., 1999; Bottinelli and Reggiani, 2000). It has been postulated that variation of MyHC content along a fiber’s length should yield correspondingly different contractile properties within the fiber (Rubinstein and Hoh, 2000; Lutz et al., 2001). Similarly, it has been suggested that variation in myosin content along fiber lengths might be responsible for the differences observed in contractile properties of adjacent segments of single fibers from mature humans (Wilkins et al., 2001).
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Development and Influence of Innervation
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Each embryonic muscle fiber initially receives input from many motor neurons. In both birds and mammals, this polyneuronal innervation is lost from twitch fibers by the early postnatal stages (Navarette and Vrbova, 1993; Bennett, 1999). Subsequently, each twitch fiber is normally innervated by one motor neuron at a single motor endplate located on the central one-third of the fiber’s length (Trotter et al., 1992; Engel, 1994).
Innervation is essential for the typical myosin expression seen during development (Washabaugh et al., 1998; Pette and Staron, 2001). Innervation regulates MyHC isoform expression in both fast and slow fibers of developing quail (Coturnix coturnix; Lefeuvre et al., 1996). Not only is proper motor innervation required for normal maturation of a fiber, it also represses traits representative of earlier development (Grinnell, 1994).
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Myosin Heavy-Chain Expression at the Ends of Developing and Denervated Muscle Fibers
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The avian pectoralis muscle is, in most birds, substantially larger than any other muscle of the body. In chickens and other birds, this muscle consists of serially arranged fibers that overlap one another to a considerable extent (Gaunt and Gans, 1993; Sokoloff and Goslow, 1998). A transverse section through the belly of such a muscle reveals populations of very small diameter fiber profiles that are, in fact, the tapered ends of larger fiber profiles seen in more distant sections (Swatland, 1983; Rosser et al., 2000).
In the chicken, the pectoralis consists almost exclusively of fast-twitch glycolytic (type IIB) fibers (see Rosser et al., 1996; Rushbrook et al., 1998). Within most of these fibers, at least six MyHC are expressed during development: ventricular, embryonic 1, embryonic 2, embryonic 3, neonatal, and adult (Hofmann et al., 1988; Tidyman et al., 1997; Rushbrook et al., 1998). Embryonic MyHC protein isoforms are largely supplanted by the neonatal MyHC isoform approximately 10 to 20 d after hatching (Bandman, 1985). Whereas the neonatal isoform first appears around hatching, an adult MyHC isoform appears approximately 20 d after hatching. The adult isoform almost totally replaces the neonatal isoform approximately 90 d after hatching (Bandman and Rosser, 2000). Cell culture experiments with chicken pectoralis show uneven acquisition of neonatal isoform along the lengths of the fibers (Cerny and Bandman, 1987a). Innervation is necessary for the usual embryonic to neonatal to adult MyHC isoform transformations observed in developing chicken pectoralis, and denervation experiments demonstrate that innervation also represses neonatal and embryonic MyHC isoforms in the mature muscle (Bandman et al., 1990).
There is a centrifugal gradient in MyHC transition within developing muscle fibers. We revealed this by following profiles of individual fibers in numerous serial cross-sections of chicken pectoralis (Figure 1; Rosser et al., 2000). During posthatch maturation, neonatal myosin was first lost from the largest fiber profiles. By locating motor endplates, we deduced that the neonatal-to-adult MyHC isoform change was initiated near the centrally located motor endplate of each muscle fiber (Rosser et al., 2000). Thereafter, during development, this change progressed toward the fiber ends (Figure 2).
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Figure 1. Immunocytochemical labelling of neonatal MyHC by 2E9 antibody, in serial sections of pectoralis muscle from a 41-d-old chicken. The distance of each section, in microns, from that in panel A is 360 (B), 680 (C), 1,180 (D), 1,300 (E), 1,600 (F), 1,760 (G), 2,220 (H), 2,540 (I), 2,720 (J), 3,240 (K), 3,560 (L), 3,820 (M), 4,220 (N), 4,400 (O), and 4,900 (P). Bar = 20 µm. The large arrowhead throughout the series, panels A to P, identifies sections (or fiber profiles) along the length of the same single fiber. The small arrow in panels A to G identifies serial sections through another fiber. Initially, in panel A, these two fiber profiles are of comparable diameter and 2E9 labeling intensity. The fiber profile indicated by the arrow diminishes in diameter from panel A until it is lost in panel H. The fiber profile indicated by the arrowhead increases in diameter but decreases in staining intensity as one proceeds through the sections from panel A. Small, darkly labeled fiber profiles are the tapered ends of larger more lightly labeled fiber profiles. (Figure reprinted with the permission of Wiley-Liss Inc., a subsidiary of John Wiley & Sons Inc., from Rosser et al., 2000.)
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Figure 2. Schema of motor endplate and muscle fiber at different ages. The number indicates days after hatching. The darker the stippling, the greater the amount of neonatal myosin heavy-chain isoform. During development, repression of neonatal myosin heavy-chain isoform radiates from the motor endplate toward the fiber ends.
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Denervation of chicken pectoralis for 8 wk results in reexpression of some neonatal MyHC isoform within all fibers (Cerny and Bandman, 1987b). We severed the nerves to the left pectoralis of mature chickens for 3, 7, 15, and 21 d and demonstrated that this reexpression progressed from the tapered fiber ends toward the central regions of the fiber (Figure 3; Rosser et al., 2000). The right pectoralis served as the control.
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Figure 3. Schema of muscle fiber of chicken pectoralis, illustrating the effect of denervation on distribution of neonatal myosin. The number indicates days after surgical denervation. Stippled regions indicate the presence of neonatal myosin heavy chain isoform. Denervation for 2 and 3 wk resulted in an overall decrease in diameter and reexpression of neonatal myosin from the ends toward the central regions of the fibers.
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Our results are consistent with trophic factor(s) emanating from the motor endplate, which play a major role in modulating myosin expression. If membrane depolarization and/or twitch contractile activity were solely responsible for regulating myosin expression, one would expect uniform expression of any given myosin isoform throughout the length of the fiber. However, the regional distribution of neonatal myosin seen during both development and denervation indicates that an additional factor must be involved in regulating myosin expression.
Our data may also be consistent with a signal originating from the tapered ends of the fibers and dissipating near the center. This hypothesis has some support since a number of regulatory proteins are localized at fiber ends (see "Protein Subsets within Specialized Regions of the Muscle Fiber"). Nonetheless, our experiments do clearly show that denervation—which directly impacts the centrally located motor endplate—reverses the centrifugal gradient of neonatal MyHC repression normally seen during development.
Our observations have led others to propose that a centrifugal gradient in MyHC transition within developing muscle fibers may explain the presence of small fibers of different MyHC phenotype in mammalian muscles (Gojo et al., 2002). However, additional work is required to extend our observations and theories to mammalian muscle. There is no shortage of experimental models available for study since many muscles of large mammals (rabbit, goat, horse, cattle, pig), and certain muscles of small mammals (mouse, rat, cat) and humans, have muscle fibers arranged in series (Trotter et al., 1992; Paul and Rosenthal, 2002). Invariably, serial sectioning of these muscles should demonstrate that smaller fiber profiles seen in cross-section are the tapered ends of larger fiber profiles (see Swatland, 1994).
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Variation of Myonuclear Domains within Developing and Mature Muscle Fibers
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Each myonucleus is responsible for gene expression in its surrounding cytoplasm. The region of cytoplasm associated with an individual myonucleus is termed the "myonuclear domain" (Landing et al., 1974; Allen et al., 1999) or DNA unit (Cheek, et al., 1971; Mozdziak et al., 1997). Myonuclear domain size is correlated with muscle fiber type and MyHC expression. Cytoplasmic volume per myonucleus is smaller in fibers expressing slow as compared to fast MyHC (Allen et al., 1999; Schmalbruch and Lewis, 2000). It has been hypothesized that fibers highly active in protein synthesis have smaller domains (Edgerton and Roy, 1991). There was an inverse correlation between myonuclear domain size and rate of growth in chicken pectoralis (Knizetova et al., 1972). In developing turkey (Melleagris gallopavo) pectoralis, younger, smaller fibers were shown to have smaller myonuclear domains (Mozdziak et al., 1994). Similar results have been reported from a study of rat muscle (Ohira et al., 2001).
We have shown that in chicken pectoralis myonuclear domains expressing neonatal MyHC within the tapered end regions of maturing muscle fibers are smaller than domains in other regions of the fibers (Rosser et al., 2002). Myonuclei were counted and formulas used to calculate mean myonuclear domain sizes. Fiber profiles were classified as neonatal, transforming (between neonatal and adult in neonatal MyHC content), or adult. Volume of cytoplasm/myonucleus (Figure 4) was different for adult, transforming, and neonatal (mean = 16,132, 12,899, and 8,130 µm3/myonucleus, respectively). Transforming and adult profiles had significantly (P < 0.001) larger myonuclear domains than did neonatal profiles. Since neonatal MyHC is located at the ends of the fibers, our work demonstrated smaller domains at the terminal tips of maturing muscle fibers. Whereas there may have been a localized concentration of myonuclei in the immediate vicinity of the motor endplate of each fiber, as has been reported by researchers studying other experimental models (see "Protein Subsets within Specialized Regions of the Muscle Fiber"), we did not specifically quantify myonuclear numbers within this tiny region of the fiber.
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Figure 4. Myonuclear domain (volume of cytoplasm per myonucleus) in maturing chicken pectoralis. Values are expressed as mean ± SD. The overall pattern of myonuclear domain size is adult or transforming > neonatal. Those fiber profiles classified as neonatal from 21 d onward are predominately the ends of the muscle fibers. (Figure reprinted with permission of University of Basque Country Press, Rosser et al., 2002.)
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Increased transcriptional output in muscle fibers appears to be enhanced by regional concentration of myonuclei. The ends of muscle fibers are the sites of longitudinal growth (see Swatland, 1994), and myonuclear domains are thought to be smaller in growing muscle (Winchester and Gonyea, 1992). We integrated these earlier observations by showing that fiber ends contain smaller myonuclear domains. A number of other sources provide indirect support for the hypothesis that increased transcriptional output is enhanced by the regional concentration of myonuclei. Rossi et al. (2000), in studying acetylcholinesterase expression along the lengths of individual fibers, suggested that the regulation of transcription could be an on/off event at individual myonuclei. Newlands et al. (1998) studied the expression of a variety of genes within individual fibers and determined that myonuclei were independently regulated and that not all myonuclei were transcriptionally active. Newlands et al. (1998) proposed that the number of myonuclei simultaneously expressing the same gene is an important mechanism regulating transcriptional output of a fiber. Hypotheses pertaining to the effects of myonuclear recruitment and/or concentration on transcriptional activity currently wait further testing.
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Other Proteins
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Most research to date on protein heterogeneity within muscle fibers has been focused on MyHC. However, most other myofibrillar proteins in skeletal muscle also exist as a number of isoforms (Schiaffino and Reggiani, 1996). It is possible that other proteins, such as troponin, titin, and C protein, could also modulate the functional properties of a muscle fiber (Bottinelli, 2001) and exhibit variation in isoform expression along the fiber length. Certainly, myosin light-chain isoforms have been directly correlated with contractile properties (Reiser et al., 1996) and show regional variation in isoform expression (Lutz et al., 2001). Formerly, researchers correlated subtle variations in energy-generating enzyme activities with fine differences in contractile properties (Nemeth et al., 1991), although it was held that metabolic capacity did not vary along a fiber (Pette et al., 1980). The MyHC hegemony in studies of muscle fiber typing and function is being questioned (Botinnelli, 2001). It is probable that future studies will show a greater array of genes exhibiting regional expression within muscle fibers.
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Implications
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Earlier studies established that differences in contractile speeds among skeletal muscle fibers are correlated with myosin heavy-chain content. Thus, our work showing that fiber ends have a myosin heavy-chain content different from that found along the rest of the fiber length suggests that there are variations in intracellular contractile properties. Our findings show a centrifugal gradient in repression of developmental myosin heavy-chain proteins within developing fibers and the centripetal reexpression of this isoform in denervated fibers, indicating regulation by trophic factor(s) emanating from the motor endplate. However, the causative factors have yet to be determined. Previous work demonstrated that fiber ends are the site of longitudinal growth and that myonuclear domains are smaller in growing muscle. We integrated these findings by showing that fiber ends contain smaller domains. Thus, increased transcriptional output in muscle fibers seems to be enhanced by regional concentration of myonuclei.
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Footnotes
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1 This work was supported by equipment and operating grants awarded to B. W. C. Rosser by the Natural Sciences and Engineering Research Council of Canada, and by grants awarded to E. Bandman by the National Institutes of Health (AM08573) and the USDA (98-35206-6395). The authors also wish to thank J. Jones of the Department of Art and Art History, University of Saskatchewan, for providing the two original drawings used in this paper. 
2 Correspondence: phone: 530-752-2490; fax: 530-752-4759; E-mail: ebandman{at}ucdavis.edu.
Received for publication July 20, 2002.
Accepted for publication January 17, 2003.
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Abstract
Introduction
