Isolation and Characterization of an Avian Slow Myosin Heavy Chain Gene Expressed during Embryonic Skeletal Muscle Fiber Formation

Nikovits, William; Wang, Gangfeng; Feldman, Jeffrey L.; Miller, Jeffrey B.; Wade, Robert; Nelson, Lowry; Stockdale, Frank E.

doi:10.1074/jbc.271.29.17047

Cited by 28 publications

(30 citation statements)

References 61 publications

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“…During the time of heart chamberization, between ED3 and ED6, the levels of slow MyHC 3 mRNA in the ventricles rapidly declined to reach a barely detectable level by ED10. Therefore, slow MyHC 3 gene expression in the ED10 heart is atrial chamber specific, which is consistent with previous Northern blot and in situ hybridization analyses (43).…”

Section: Resultssupporting

confidence: 77%

“…Similar to the mammalian ␤-cardiac/slow MyHC gene, the slow MyHC 3 gene is expressed in both slow skeletal and cardiac muscle cells, and the two genes have a high level of sequence homology in their coding regions (43). However, whereas the slow MyHC 3 gene becomes atrial chamber restricted, the ␤-cardiac/slow MyHC 3 gene is a ventricular chamber-specific gene (31).…”

Section: Discussionmentioning

confidence: 99%

“…Distinct lineages of prospective atrial and ventricular cardiomyocytes emerge in the posterior and anterior regions of the heart tube, respectively. An early marker of the atrial cardiomyocyte cell lineage is expression of the AMHC1 or slow MyHC 3 contractile protein gene (43,60). We have used the identification of cis elements and transacting factors that regulate atrial chamber-specific expression of this gene as a means of investigating the mechanism(s) underlying diversification of early cardiogenic cells into atrial or ventricular cell lineages and as an approach to the analysis of cardiac morphogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…Various amounts of an empty expression vector were added such that each dish was transfected with an equal amount of total DNA. Forty-eight hours after transfection, the cells were harvested and CAT and ␤-galactosidase assays were performed as described previously (43). All experiments were repeated at least three times, and the CAT activities were normalized to the ␤-galactosidase activities in order to standardize the transfection efficiency.…”

Section: Methodsmentioning

confidence: 99%

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A Positive GATA Element and a Negative Vitamin D Receptor-Like Element Control Atrial Chamber-Specific Expression of a Slow Myosin Heavy-Chain Gene during Cardiac Morphogenesis

Wang

Nikovits

Schleinitz

et al. 1998

Molecular and Cellular Biology

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We have used the slow myosin heavy chain (MyHC) 3 gene to study the molecular mechanisms that control atrial chamber-specific gene expression. Initially, slow MyHC 3 is uniformly expressed throughout the tubular heart of the quail embryo. As cardiac development proceeds, an anterior-posterior gradient of slow MyHC 3 expression develops, culminating in atrial chamber-restricted expression of this gene following chamberization. Two cis elements within the slow MyHC 3 gene promoter, a GATA-binding motif and a vitamin D receptor (VDR)-like binding motif, control chamber-specific expression. The GATA element of the slow MyHC 3 is sufficient for expression of a heterologous reporter gene in both atrial and ventricular cardiomyocytes, and expression of GATA-4, but not Nkx2-5 or myocyte enhancer factor 2C, activates reporter gene expression in fibroblasts. Equivalent levels of GATA-binding activity were found in extracts of atrial and ventricular cardiomyocytes from embryonic chamberized hearts. These observations suggest that GATA factors positively regulate slow MyHC 3 gene expression throughout the tubular heart and subsequently in the atria. In contrast, an inhibitory activity, operating through the VDR-like element, increased in ventricular cardiomyocytes during the transition of the heart from a tubular to a chambered structure. Overexpression of the VDR, acting via the VDR-like element, duplicates the inhibitory activity in ventricular but not in atrial cardiomyocytes. These data suggest that atrial chamber-specific expression of the slow MyHC 3 gene is achieved through the VDR-like inhibitory element in ventricular cardiomyocytes at the time distinct atrial and ventricular chambers form.The vertebrate heart, which initially forms as a linear, tubular structure, undergoes a complex series of morphogenetic movements to form a multichambered organ. The low-pressure atrial and high-pressure ventricular chambers which are formed differ in morphology, electrophysiology, and the repertoire of muscle contractile protein genes which are expressed (8,30). The developmental and molecular mechanisms responsible for establishing and maintaining chamber-specific differences are largely unknown.In adult animals, several members of contractile protein gene families show chamber-restricted or strong chamber-preferential expression. The myosin heavy-chain (MyHC) AMHC1 and slow MyHC 3 genes (56, 60), the myosin light-chain 1a (MLC-1a) and MLC-2a genes (21,31), and the atrial natriuretic factor (ANF) gene (61) show atrial specificity. In small mammals, the ␣-MyHC gene exhibits an atrial chamber preference of expression before birth (31). Conversely, MLC-2v

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Section: Resultssupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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A Positive GATA Element and a Negative Vitamin D Receptor-Like Element Control Atrial Chamber-Specific Expression of a Slow Myosin Heavy-Chain Gene during Cardiac Morphogenesis

Wang

Nikovits

Schleinitz

et al. 1998

Molecular and Cellular Biology

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“…The quail slow myosin heavy chain 3 gene is expressed throughout the heart until embryonic day 7 when ventricular expression is repressed. Expression of quail slow MHC 3 is also detected in embryonic slow skeletal muscles (14,15). VMHC1 expression is detected throughout the developing chick heart until day 5 of development when its cardiac expression is restricted to the ventricle.…”

mentioning

confidence: 89%

Identification and Genomic Cloning of CMHC1

Croissant

Carpenter

Bader

2000

Journal of Biological Chemistry

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We report the identification and cloning of a unique chick myosin heavy chain (CMHC1) that is expressed exclusively in the heart during embryogenesis. Using primers specific to myosin heavy chains, we used reverse transcriptase-polymerase chain reaction to clone and isolate CMHC1 from embryonic day 10 chicken heart RNA. Sequence analysis indicated that CMHC1 was a novel member of the myosin heavy chain family. Expression of the CMHC1 transcripts was detected in Hamburger Hamilton stage 10 chick embryos in the fusing myocardium. Expression of CMHC1 was maintained at high levels throughout the tubular heart of later stage embryos. Reverse transcriptase-polymerase chain reaction and in situ hybridizations failed to detect CMHC1 transcripts in the developing somites, limb buds, or skeletal musculature at any stage of chick development. Genomic CMHC1 clones have been isolated that contain sequences approximately 5.2 kilobase upstream of the presumptive CMHC1 transcription start site. Portions of the upstream regulatory region induced a 21-fold increase in reporter gene expression in primary cardiomyocytes. Because of its unique cardiac-restricted expression, CMHC1 will provide an excellent model system to study the molecular mechanisms required for the early developmental regulation of heart-specific genes.

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Evolutionary significance of myosin heavy chain heterogeneity in birds

Bandman

Rosser

2000

Microsc. Res. Tech.

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Isolation and Characterization of an Avian Slow Myosin Heavy Chain Gene Expressed during Embryonic Skeletal Muscle Fiber Formation

Cited by 28 publications

References 61 publications

A Positive GATA Element and a Negative Vitamin D Receptor-Like Element Control Atrial Chamber-Specific Expression of a Slow Myosin Heavy-Chain Gene during Cardiac Morphogenesis

A Positive GATA Element and a Negative Vitamin D Receptor-Like Element Control Atrial Chamber-Specific Expression of a Slow Myosin Heavy-Chain Gene during Cardiac Morphogenesis

Identification and Genomic Cloning of CMHC1

Evolutionary significance of myosin heavy chain heterogeneity in birds

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