The proximal promoter of the aldolase A gene remains active during myogenesis in vitro and muscle development in vivo

Colbert, Melissa C.; Ciejek-Baez, Elena

doi:10.1016/0012-1606(92)90264-h

Cited by 13 publications

(17 citation statements)

References 46 publications

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“…This period is characterized by the appearance of adult fast-type myosin heavy chains IIA, IIX, and IIB (2,59). During muscle maturation, transgenic human pM becomes highly active in fast-type muscles, as does the mouse endogenous pM (8). The muscle fiber specificity of the human pM is not known in detail.…”

Section: Discussionmentioning

confidence: 99%

Fast-muscle-specific expression of human aldolase A transgenes.

Salminen¹,

Maire²,

Concordet³

et al. 1994

Mol. Cell. Biol.

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The expression of the human aldolase A gene is controlled by three alternative promoters. In transgenic mice, pN and pH are active in all tissues whereas pM is activated specifically in adult muscles composed mainly of fast, glycolytic fibers. To detect potential regulatory regions involved in the fast-muscle-specific activation of pM, we analyzed DNase I hypersensitivity in a 4.3-kbp fragment from the 5' end of the human aldolase A gene. Five hypersensitive sites were located near the transcription initiation site of each promoter in those transgenic-mouse tissues in which the corresponding promoter was active. Only one muscle-specific hypersensitive site was detected, mapping near pM. To functionally delimit the elements required for muscle-specific activity of pM, we performed a deletion analysis of the aldolase A 5' region in transgenic mice. Our results show that a 280-bp fragment containing 235 bp of pM proximal upstream sequences together with the noncoding M exon is sufficient for tissue-specific expression of pM. When a putative MEF-2-binding site residing in this proximal pM region is mutated, pM is still active and no change in its tissue specificity is detected.Furthermore, we observed a modulation of pM activity by elements lying further upstream and downstream from pM. Interestingly, pM was expressed in a tissue-specific way in all transgenic mice in which the 280-bp region was present (32 lines and six founder animals). This observation led us to suggest that the proximal pM region contains elements that are able to override to some extent the effects of the surrounding chromatin.The developmental basis for different skeletal muscle fiber types is not completely understood, but the discovery of distinct myoblast lineages in early stages of myogenesis indicates that intrinsic properties could determine the early fiber types. In later stages of myogenesis, innervation and hormones influence muscle fiber development and maturation (51, 53) (see references 36, 37, and 56 for recent reviews). In mature vertebrate muscles, four major types of myofibers are detected on the basis of their metabolic properties and expression of different myosin heavy-chain isoforms. Slow-twitch fibers (type I) use primarily oxidative respiration. Fast-twitch type IIA fibers use both oxidative and glycolytic pathways in energy metabolism, whereas fast-twitch type IIB fibers are purely glycolytic. The third fast-type, IIX, fibers are classified as intermediate fast fibers (reviewed in reference 45).The regulatory factors responsible for the establishment of the different fiber phenotypes are yet unknown. Nevertheless, the identification of a family of skeletal muscle-specific nuclear factors which can activate the myogenic program in nonmuscle cells has led to an increased understanding of muscle development. This MyoD family of factors includes MyoD, myogenin, Myf-5, and MRF4, which bind to a DNA consensus sequence referred to as the E box, found in the regulatory regions of many muscle genes (reviewed in references 14 and ...

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Section: Discussionmentioning

confidence: 99%

Fast-muscle-specific expression of human aldolase A transgenes.

Salminen¹,

Maire²,

Concordet³

et al. 1994

Mol. Cell. Biol.

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“…Northern blot analysis was done as described previously (14). The murine aldolase A pM-derived mRNAs (M-mRNA)-specific probe corresponds to the M-specific exon of the mouse aldolase A gene (18). The myoglobin probe was synthesized by reverse transcription-polymerase chain reaction and corresponds to the third exon of the gene (27).…”

Section: Methodsmentioning

confidence: 99%

“…This down-regulation of pM activity could result from muscle atrophy and/or improper fiber specialization caused by denervation. Because M-mRNAs are mostly expressed in 2B fibers (18) and thus coexpressed in adults with transcripts of the MyHC-2B gene, we checked by Northern blots ( Fig. 1) and immunohistochemistry (not shown) whether the formation of 2B fibers and concomitant accumulation of MyHC-2B transcripts is altered following denervation.…”

Section: Innervation Is Required For Pm Activation Duringmentioning

confidence: 99%

“…Aldolase A expression is achieved through the use of alternative promoters that have distinct tissue and developmental specificities (12)(13)(14)(15)(16)(17). The muscle-specific promoter, pM, is highly activated during postnatal muscle maturation, and in adults, pM-derived transcripts accumulate in fast twitch glycolytic muscles and to a much lower level in slow twitch muscles (14,18,19). We have previously shown that the proximal regulatory sequences (bp Ϫ310 to ϩ45 relative to the transcription start site) of the human aldolase A muscle-specific promoter are sufficient to target the expression of a chloramphenicol acetyltransferase reporter gene (pM310CAT transgene) to fast twitch muscles of transgenic mice, in a pattern mimicking its preferential expression in 2B fibers (20).…”

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confidence: 99%

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Proximal Sequences of the Aldolase A Fast Muscle-specific Promoter Direct Nerve- and Activity-dependent Expression in Transgenic Mice

Spitz¹,

Vasconcelos²,

Châtelet³

et al. 1998

Journal of Biological Chemistry

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Muscle activity is known to modulate the muscle fiber phenotype. Changes in muscle activity (normal or experimentally induced) lead to modifications of the expression status of several muscle-specific genes. However, the transcription regulatory elements involved in the adaptative response are mainly unknown. The aldolase A muscle-specific promoter, pM, is expressed in adult fast twitch muscle with a preferential expression in fast glycolytic-2B fibers. Its activity is induced during postnatal muscle maturation, suggesting a role of nerve and/or muscle activity. Indeed, denervation of gastrocnemius in newborn mice prevented the activation of the promoter in this muscle, despite the nerve-independent formation of 2B fibers. Although the nerve was necessary for pM onset during development, denervating the gastrocnemius in adults had only mild effects on pM activity. By contrast, a transgene including the pM proximal regulatory sequences that are sufficient to reproduce the 2B fiber-specific expression of the endogenous promoter was shown to be highly sensitive to both neonatal and adult denervation. Transgenes containing muscle-specific pM proximal promoter elements were used to delineate the regulatory elements involved in this response to innervation and changes in the contractile activity pattern. Nerve-and activity-dependent elements could be localized in the 130-base pair-long proximal promoter region of the human aldolase A gene.

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“…The distal promoter M functions only in adult skeletal muscle, and the proximal promoter AH is active in early muscle development and in most other tissues. The intragenic switching of the promoter from AH to M occurs in skeletal muscle mainly due to drastic induction of the M promoter (4). In a the transientexpression assay in chicken primary myoblasts, the region comprising bp 202 to 85 upstream from the transcription initiation site of the M promoter was found to be necessary for muscle-specific induction (14).…”

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confidence: 99%

The MEF-3 motif is required for MEF-2-mediated skeletal muscle-specific induction of the rat aldolase A gene.

Hidaka¹,

Yamamoto²,

Arai³

et al. 1993

Mol. Cell. Biol.

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The rat aldolase A gene contains two alternative promoters and two alternative first exons. The distal promoter M is expressed at a high level only in skeletal muscle. Previous in vitro transfection studies identified the region from -202 to -85 as an enhancer that is responsible for dramatic activation during the differentiation of chicken primary myoblasts. This enhancer contains an A/T-rich sequence resembling the MEF-2 motif, which is an important element of muscle enhancers and promoters. In this study, we demonstrate that the MEF-2 sequence is essential but not sufficient for the activity of the enhancer. Another region required for the activity was recognized by a nuclear factor, tentatively named MAF1. MAF1 was found in both muscle cells and nonmuscle cells, and MAF1 from both cell types was indistinguishable by gel retardation and DNase I footprint experiments. The sequence required for MAF1 binding is very similar to the MEF-3 motif, which is an element of the skeletal muscle-specific enhancer of the cardiac troponin C gene. Because MAF1 and MEF-3 are closely related in both recognition sequence and distribution, MAF1 and MEF-3 probably represent the same nuclear factor which may play an important role in muscle gene transcription. Thus, the muscle-specific induction of the aldolase A gene is governed by muscle-specific MEF-2 and existing MEF-3 (MAFi).Numerous studies have shown that the regulation of muscle-specific gene expression is governed by complex sets of both muscle-specific and ubiquitous nuclear factors. The best-characterized of these are the basic helix-loop-helix

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The proximal promoter of the aldolase A gene remains active during myogenesis in vitro and muscle development in vivo

Cited by 13 publications

References 46 publications

Fast-muscle-specific expression of human aldolase A transgenes.

Fast-muscle-specific expression of human aldolase A transgenes.

Proximal Sequences of the Aldolase A Fast Muscle-specific Promoter Direct Nerve- and Activity-dependent Expression in Transgenic Mice

The MEF-3 motif is required for MEF-2-mediated skeletal muscle-specific induction of the rat aldolase A gene.

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