© 1996 American Heart Association, Inc.
Articles |
SM22
, a Marker of Adult Smooth Muscle, Is Expressed in Multiple Myogenic Lineages During Embryogenesis
From the Department of Biochemistry and Molecular Biology, The University of Texas M.D. Anderson Cancer Center, Houston.
Correspondence to Dr Eric N. Olson, Hamon Center for Basic Cancer Research, The University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd, Dallas, TX 75235-9148.
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Abstract |
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Abstract SM22
is a calponin-related protein that is
expressed specifically in adult smooth muscle. To begin to define the
mechanisms that regulate the establishment of the smooth muscle
lineage, we analyzed the expression pattern of the SM22 gene
during mouse embryogenesis. In situ hybridization demonstrated that
SM22 transcripts were first expressed in vascular smooth muscle
cells at about embryonic day (E) 9.5 and thereafter continued to be
expressed in all smooth muscle cells into adulthood. In contrast to its
smooth muscle specificity in adult tissues, SM22 was expressed
transiently in the heart between E8.0 and E12.5 and in skeletal muscle
cells in the myotomal compartment of the somites between E9.5 and
E12.5. The expression of SM22 in smooth muscle cells, as well as
early cardiac and skeletal muscle cells, suggests that there may be
commonalities between the regulatory programs that direct
muscle-specific gene expression in these three myogenic cell types.
Key Words: SM22 • cardiovascular development • smooth muscle cells • myogenic lineages
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Introduction |
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TopAbstractIntroductionMaterials and Methods Results Discussion References |
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Smooth muscle cells are important for the functions of the circulatory, genitourinary, respiratory, and digestive systems. Unlike skeletal and cardiac muscle cells, where cell differentiation is accompanied by the stable expression of muscle-specific genes,1 2 SMCs display remarkable phenotypic plasticity and retain the capacity to reenter the cell cycle.3 This unique property of SMC phenotypic modulation is often associated with the loss of many SMC-specific markers.4 5 Such alterations in SMC proliferation and differentiation are associated with a variety of vascular diseases, including atherosclerosis, restenosis following angioplasty, and hypertension.3 4 However, our understanding of the molecular mechanisms that control the SMC myogenic program is limited, and no SMC-specific transcription factors that regulate the expression of SMC-specific genes have been identified. Thus, an understanding of the molecular mechanisms governing SMC differentiation may be important for developing therapeutic strategies for the treatment of human vascular diseases.
The three muscle cell types, skeletal, cardiac, and smooth, are all derived from distinct populations of myogenic precursor cells during embryogenesis.6 7 Skeletal muscle arises from the somites, which form adjacent to the neural tube beginning at about E8.0 in the mouse. Subsequent compartmentalization of the somites gives rise to the myotome, from which the axial musculature is derived.8 Cells from the ventrolateral edge of the dermamyotome of the somite also migrate into the limb buds to form the limb muscles.8 Cardiac muscle is derived from the anterior lateral plate mesoderm, which forms a primitive heart tube at about E8.0 and subsequently undergoes looping and chamber specification to form the mature multichambered heart.9 The embryonic origins of SMCs are less clear, in part because they arise in multiple regions of the embryo from different precursor populations. For example, studies in chick/quail chimeras have shown that SMCs in the great vessels are derived from a subpopulation of mesenchymal neural crest cells, whereas SMCs in the coronary arteries are of non–neural crest origin.10 11 12 13 In addition to vascular SMCs, there exist several seemingly distinct populations of SMCs in most visceral organs. The latter SMCs are thought to originate from local mesenchyme, apparently through inductive processes.14 From this discussion, it is clear that smooth muscle shows unique properties in terms of both differentiation control and ontogeny when compared with sarcomeric muscle.
Only a few genes that are expressed specifically in adult SMCs have
been studied extensively with respect to transcriptional regulation.
Among these are SM -actin15 16 and
SM-MHC.17 One marker,
SM22,18 19 20 has been
less characterized. SM22 is considered to be an SMC-specific protein
structurally related to calponin, which is an actin- and
tropomyosin-binding protein.21 SM22 also shows
homology to the Drosophila protein mp20, which is expressed
specifically in synchronous oscillatory flight muscles but not in
asynchronous flight muscles,22 and protein NP25, which is
expressed specifically in a subpopulation of neuronal
cells.23 There are three isoforms of SM22, but the
alpha isoform is the most abundant one.20 24
SM22 has been shown to be expressed in all smooth muscle tissues of
birds and mammals. However, SM22 mRNA expression during
embryogenesis has not been examined. To begin to define the mechanisms
that control muscle gene expression during SMC differentiation and to
further characterize the embryonic origins of SMC lineages, we cloned
the mouse SM22 gene and examined its mRNA expression pattern during
mouse embryogenesis. SM22 transcripts were expressed in SMCs within
the dorsal aorta at E9.5 and thereafter in all SMCs throughout prenatal
and postnatal life. In contrast to the smooth muscle specificity of
SM22 expression in adult tissues, SM22 mRNA was expressed
transiently in the heart and in skeletal muscle cells within the somite
myotome during embryogenesis. The expression of SM22 in multiple
myogenic lineages suggests that aspects of the smooth muscle gene
regulatory program may be shared by skeletal and cardiac muscle
cells.
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Materials and Methods |
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TopAbstractIntroductionMaterials and Methods Results Discussion References |
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Isolation of Mouse SM22
cDNA A 275-bp mouse SM22
PCR fragment was initially obtained from
a mouse uterus cDNA library25 using the following primers
to the published rat SM22 sequence19 :
5'-ATGGCCAACAAGGGTCCATCC-3' (nucleotides 1 to 21 of rat
sequence) and 5'-TCCATCTGCTTGAAGACCATG-3' (reverse complement to
nucleotides 255 to 275 of rat SM22). The resulting
275-nucleotide PCR fragment was subcloned into the
EcoRI/HindIII sites of pBluescript SK+plasmid
(Stratagene) and used for in situ hybridizations, RNase protections,
and further library screening, as described below. Using this 275-bp
DNA fragment as a probe, several overlapping cDNA clones were isolated
from the same uterus library under high stringency. One clone
containing a 1078-bp insert was sequenced on both strands by dideoxy
sequencing with Sequenase (United States Biochemical) according to the
manufacturer's instructions. Sequence analysis was carried out
using the GCG sequence analysis software package (Department of
Biomathematics, The University of Texas M.D. Anderson Cancer
Center).
RNase Protection Analysis
Total RNA from adult mouse tissues
was isolated by the acid
phenol protocol.26 SM22 transcripts were detected by
RNase protection by using the Maxi-Script and RPA kits (Ambion).
Approximately 15 µg of total RNA was hybridized to an in vitro
transcribed SM22 riboprobe (
1x105 cpm) corresponding
to the 275-bp PCR product described above. Hybridizations were
carried out at 45°C for 16 hours. After hybridization, samples were
treated with RNase A+T for 40 minutes at 37°C, precipitated, and
resolved in a denaturing 5% polyacrylamide/7% urea gel. After
soaking in 10% acetic acid/10% methanol, the gel was vacuum dried and
exposed to autoradiographic film. In some experiments,
hybridizations included a 108-bp 18S rRNA riboprobe (Ambion) or a
156-bp riboprobe corresponding to the 3' untranslated region of mouse
SM -actin.27
In Situ Hybridization
The same 275-bp mouse antisense
SM22 probe used for RNase
protection assays was used for in situ hybridization. In addition, a
157-bp mouse SM -actin riboprobe was labeled and used as a
comparative marker for muscle gene expression. Both sense and antisense
probes were labeled by 35S-UTP and hybridized to paraffin
sections (8 µm) from staged embryos (7.5 dpc to 17.5 dpc). Detailed
in situ protocols were described previously.25
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Results |
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TopAbstractIntroductionMaterials and Methods Results Discussion References |
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Cloning of Mouse SM22
To study the regulation of SM22
gene expression during mouse
development, we isolated an SM22 cDNA that was 1078 bp in length,
using sequences derived from the rat cDNA (see "Materials and
Methods"). Sequence analysis showed that the mouse SM22
protein contains 204 amino acids and shares 98%, 97%, and 84%
identity with the rat, human, and chicken proteins, respectively (Fig
1
). The deduced amino acid sequence of SM22 agrees
with the sequence recently reported by Solway et al.28
Within the 5' and 3' untranslated regions, the mouse SM22
sequence
showed extensive homology to the rat and human sequences, but it
diverged from the chicken sequence (not shown).
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SM22 Transcript Distribution in Adult Mouse
Tissues
The pattern of SM22 mRNA expression in adult mouse
tissues was
determined by RNase protection. SM22 transcripts were present at
the highest levels in aorta, intestine, stomach, and uterus, which
contain a large smooth muscle component (Fig 2A).
SM22 transcripts were detected at a lower level in lung, kidney,
spleen, brain, heart, and skeletal muscle. We believe the expression of
SM22 in these tissues reflects the presence of vascular smooth
muscle (see below). We were unable to detect SM22 transcripts in
liver and testes. A probe for 18S RNA was included in each RNase
protection assay to ensure equivalent loading of RNA.
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To determine
whether the expression of SM22 in adult skeletal and
cardiac muscle was due to the presence of blood vessels in these
tissues, sections of heart and skeletal muscle from young mice were
examined by in situ hybridization with an SM22 antisense riboprobe.
SM22 mRNA was not detected in the myocardium or in
skeletal muscles but instead was localized to the blood vessels
present in these sections (Fig 2B
and 2C).
Within the uterus,
SM22 was highly expressed in the myometrial layer, with little or no
expression in the glandular endometrial layer (Fig 2D). We
conclude
that SM22 mRNA expression is highly restricted to adult smooth
muscle, making it an excellent marker for studying the regulation of
SMC differentiation.
Temporal and Spatial Expression Pattern of SM22 mRNA During
Mouse Embryogenesis
To determine whether SM22 expression marks
the smooth muscle
lineage during embryogenesis, we examined the expression of SM22
transcripts by in situ hybridization of mouse embryos beginning at
E7.5. Surprisingly, SM22 transcripts were first detected at E8.0 in
the premyocardial tissue of the primitive heart tube (Fig 3A
and 3B). No expression was detected elsewhere in the embryo
at this stage, including the dorsal aorta. At E8.5, the heart is
asymmetrical and contains a common atrium and ventricle in direct
continuity with the aortic sac. At this stage, SM22 expression was
observed throughout the bulbus cordis (the future right ventricle) and
the newly formed common ventricle (Fig 3C and
3D). Between E9.5 and
E10.5, the volume of the heart increases dramatically, the outflow
tract begins to differentiate, and the aortic arches are fully formed.
SM22 continued to be expressed at high levels throughout the entire
developing heart and the outflow tract until E10.5 (Fig 3G and
3H).
SM22 expression gradually diminished in the heart after E10.5. By
E12.5, expression was restricted to the right ventricle, and it became
undetectable in the heart by E13.5 (Fig 4A through
4C).
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SM22 expression was also observed in the myotomal compartment
of the
somites beginning at E9.5 (Fig 3G). Expression proceeded
caudally in
parallel with somite maturation and disappeared in the somites after 2
to 3 days. We did not detect SM22 expression in differentiating
skeletal muscles in the limb buds or elsewhere in the embryo,
indicating that it specifically marks early myotomal muscles.
The
expression of SM22 in SMCs was detected in the developing dorsal
aorta at E9.5 (Fig 3G). At E10.5, SM22 expression was
observed in
the umbilical vessels and other forming vessels in the head region (Fig
3H). At E12.5, SM22 expression in the basilar artery was
very high
(Fig 4A and 4B). The expression of SM22 in
visceral SMCs within the
gut and bladder, as well as in the bronchi of the lung, which contain a
smooth muscle component, became apparent at E13.5 (Fig 4C).
Expression
in the cranial vessels and intersomitic arteries was also observed at
this stage.
At E14.5, SM22 transcripts were clearly seen in all
major vessels,
bronchi of the lungs, and gut (Fig 4D). There was no signal
observed in
skeletal muscles or heart. However, expression was detected in the
ventral body wall at this stage (Fig 4D). By E17.5, SM22
mRNA was
observed in all structures containing SMCs, including the major
vessels, and the gut (Fig 4F). The signal in the bladder was
very
intense in all three layers of smooth muscle and was not present in
the epithelial layer (Fig 4F). Together, these results
demonstrate that
SM22 mRNA is expressed in all three muscle types during mouse
embryogenesis.
Expression of SM -Actin During Embryogenesis
The
expression pattern of SM22 was clearly distinct from that
of SM-MHC, which is not expressed in SMCs until about E10.5 and is
never detected in cardiac or skeletal muscle cells.25 To
determine whether SM22 might be expressed in a pattern similar to
other smooth muscle genes, we compared its expression pattern with that
of SM -actin. Similar to SM22, SM -actin transcripts
were first detected in the heart at E8.0 (Fig 5A). At
E8.5, expression was also observed in the aortic sac (Fig 5B).
Moreover, SM -actin transcripts were detected in the dorsal
aorta, cranial vessels, and myotomes of the somites between E9.5 and
E10.5 (Fig 5C and 5D). The expression of SM
-actin in the heart
gradually decreased after E10.5 and became restricted to the bulbus
cordis at E12.5 (Fig 6A), and at E13.5 it was no longer
detectable in the heart (Fig 6B). In contrast to SM22, SM
-actin expression increased continuously in the myotomes and
skeletal muscles after E12.5 (Fig 6B through 6D). At E15.5, the
signal
was quite intense throughout the head and neck muscles, diaphragm, and
intercostal muscles (Fig 6D). Thus, the expression patterns of
SM22
and SM -actin overlap extensively during the early stages of
differentiation, with one notable exception: SM -actin mRNA
persists in skeletal muscle at a time when SM22 is no longer
present.
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Discussion |
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TopAbstractIntroductionMaterials and Methods Results Discussion References |
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In contrast to skeletal and cardiac muscle cells, in which the molecular mechanisms governing muscle-specific gene expression are beginning to be understood,29 relatively little is known about the mechanisms controlling muscle gene expression in SMCs. On the basis of reports that SM22
was a specific marker for adult
SMCs,20 30 we chose to use this gene as a potential
marker
to study the genesis of SMCs during embryogenesis. Indeed, we found
that SM22 was expressed in all SMCs throughout embryogenesis,
irrespective of their embryonic origin. However, an unanticipated
result of our studies was the finding that SM22 was also expressed
transiently in the early cardiac and skeletal muscle lineages. This
gene will therefore provide an opportunity to define the mechanisms
that regulate muscle gene expression in all three myogenic lineages as
well as to understand how SM22 expression becomes restricted to the
SMC lineage during ontogeny.
Expression of SM22 in Different Muscle Cell Types
The
primitive heart originates from the anterior portions of
paired tubes derived from the splanchnic mesoderm.31 The
first site of SM22 expression during mouse embryogenesis was in the
primitive heart tube at E8.0. SM22 expression was maintained
throughout the heart until E10.5, when it became restricted to the
bulbus cordis. By E13.5, SM22 expression was extinguished in the
heart. Consistent with previous studies in chick and rat
embryos,32 33 we found that SM -actin was also
expressed in the early heart. It is intriguing that SM22 and SM
-actin, which have previously been considered SMC-specific
genes, are expressed in the tubular heart. Perhaps SMC genes are
important for maintaining the contractility of
embryonic cardiomyocytes. Consistent with this
speculation, another SMC-specific contractile gene, calponin, has also
been detected in the early embryonic heart (Miano and Olson,
unpublished observations).
The expression of SM -actin, SM22,
and calponin in the early
developing mouse heart should be contrasted with SM-MHC, which is never
detected in the heart by in situ hybridization.25 Why
several SMC contractile genes are expressed during cardiogenesis while
another is not is unclear. One possibility is that the transcription
factors directing SM-MHC expression are distinct from those governing
SM -actin, SM22, and calponin expression. The expression of
at least three SMC genes in the early embryonic heart suggests that
cardiac muscle in early embryogenesis may functionally and structurally
resemble smooth muscle. In this regard, it is interesting to point out
that SM -actin mRNA has been demonstrated in adult rat hearts
subjected to pressure overload.34 Moreover, several
cardiac fetal markers are coordinately upregulated in response to
pressure overload.35 This raises the question of whether
the contractile properties of such perturbed adult
cardiomyocytes are functionally comparable to embryonic
cardiomyocytes.
SM22 expression was also detected in the myotomal
compartment of the
somites beginning at E9.5, but expression was maintained for only 3
days in each somite as somitogenesis progressed rostrocaudally.
Expression of SM22 was not observed in the skeletal muscle lineage
at any other developmental stage. Whereas the temporospatial expression
pattern of SM22 in the smooth and cardiac muscle lineages is similar
to that of SM -actin, within the skeletal muscle lineage the
expression patterns of these genes are notably different. In contrast
to the transient expression of SM22 in the myotome, SM -actin
is expressed at high levels throughout later stages of skeletal muscle
development.
SM22 mRNA expression was first detected at E9.5 in
SMCs within the
developing dorsal aorta. Later, SM22 was expressed in SMCs
throughout the vascular system, as well as within the respiratory,
urinary, and digestive tracts. The temporospatial expression pattern of
SM -actin in the SMC lineage paralleled that of SM22.
Both markers, however, appeared in SMCs of the dorsal aorta (E9.5)
before SM-MHC, which is not expressed until E10.5.25 This
and the fact that SM-MHC is never expressed in sarcomeric muscle
suggest that SM-MHC expression is governed by transcription factor(s)
different from those that control SM22 and SM -actin.
Transcriptional Control of Muscle Gene Expression
The
expression of SM22 in smooth, cardiac, and skeletal muscle
cells raises the possibility that these different muscle cell types may
share a common myogenic regulatory program early in development and
that the mechanisms that direct muscle gene expression in these
different lineages subsequently diverge. Alternatively, the SM22
gene could contain separate regulatory elements that direct its
expression in the three myogenic lineages.
The only transcription
factors identified to date that control muscle
gene expression in multiple muscle cell types are SRF and MEF2, which
belong to the MADS-box family of transcription factors.36
SRF binds an A/T-rich DNA sequence, referred to as the serum response
element, or CArG box. CArG boxes have been shown to play an important
role in the control of several skeletal and cardiac muscle genes, such
as skeletal -actin, skeletal MLC1/3, cardiac -actin, and
cardiac
-MHC.37 38 39 40 41
The promoter of the SM -actin
gene, which is expressed in a pattern similar to SM22 during
development, also contains two CArG elements, which are required for
transcriptional activity in cultured
SMCs.16 42 43
Intriguingly, there are two CArG boxes in the proximal SM22
promoter28 44 that may participate in its regulation
in
myogenic lineages. Indeed, this proximal SM22 promoter is sufficient
to direct transcription of a linked reporter gene in all three muscle
lineages in transgenic mice.44
MEF2 binding sites are
present in the control regions of the
majority of muscle-specific genes.45 Four
mef2 genes (mef2A through mef2D) are
expressed in the skeletal, cardiac, and smooth muscle lineages during
mouse embryogenesis.46 The pattern of MEF2 expression is
consistent with these factors playing a role in the regulation
of SM22 expression. The functions of MEF2 have been analyzed
in Drosophila, which contains a single mef2 gene,
called D-mef2.47 48 During
embryogenesis, D-mef2 is expressed in precursors
of the skeletal, cardiac, and visceral muscle lineages and their
descendants. Loss-of-function mutations of
D-mef2 prevent expression of muscle structural
genes in all three myogenic
lineages.49 50 51 It remains to
be determined whether the MEF2 family is involved in regulating SMC
gene expression, although all four members are clearly expressed in
this muscle type.52
Analysis of the cis-acting
sequences that regulate
SM22 transcription during embryogenesis will provide insights into
the molecular mechanisms that control early
cardiovascular development and SMC lineage
determination and differentiation.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This work was supported by grants from the National Institutes of Health, the Muscular Dystrophy Association, and The Robert A. Welch Foundation (to Dr Olson); by the Kimberly-Clark Scientific Achievement fund (to Dr Li); and by a National Research Service Award (to Dr Miano). We are grateful to K. Tucker for editorial assistance and A. Tizenor for graphic assistance. We also thank Art Strauch for the murine SM
-actin cDNA. Received August 23, 1995; accepted November 7, 1995.
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Q Lin, J Lu, H Yanagisawa, R Webb, G. Lyons, J. Richardson, and E. Olson Requirement of the MADS-box transcription factor MEF2C for vascular development Development, January 11, 1998; 125(22): 4565 - 4574. [Abstract] [PDF]
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Y Yang, K. Palmer, N Relan, C Diglio, and L Schuger Role of laminin polymerization at the epithelial mesenchymal interface in bronchial myogenesis Development, January 7, 1998; 125(14): 2621 - 2629. [Abstract] [PDF]
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M.C. DeRuiter, R.E. Poelmann, J.C. VanMunsteren, V. Mironov, R.R. Markwald, and A.C. Gittenberger-de Groot Embryonic Endothelial Cells Transdifferentiate Into Mesenchymal Cells Expressing Smooth Muscle Actins In Vivo and In Vitro Circ. Res., April 19, 1997; 80(4): 444 - 451. [Abstract] [Full Text]
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M. B. Hautmann, C. S. Madsen, and G. K. Owens A Transforming Growth Factor beta (TGFbeta ) Control Element Drives TGFbeta -induced Stimulation of Smooth Muscle alpha -Actin Gene Expression in Concert with Two CArG Elements J. Biol. Chem., April 18, 1997; 272(16): 10948 - 10956. [Abstract] [Full Text] [PDF]
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C. Biben, S. Palmer, D.A. Elliott, and R.P. Harvey Homeobox Genes and Heart Development Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 395 - 403. [Abstract] [PDF]
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J. M. Miano and E. N. Olson Expression of the Smooth Muscle Cell Calponin Gene Marks the Early Cardiac and Smooth Muscle Cell Lineages during Mouse Embryogenesis J. Biol. Chem., March 22, 1996; 271(12): 7095 - 7103. [Abstract] [Full Text] [PDF]
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H Moessler, M Mericskay, Z Li, S Nagl, D Paulin, and J. Small The SM 22 promoter directs tissue-specific expression in arterial but not in venous or visceral smooth muscle cells in transgenic mice Development, January 8, 1996; 122(8): 2415 - 2425. [Abstract] [PDF]
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P. J. Adam, C. P. Regan, M. B. Hautmann, and G. K. Owens Positive- and Negative-acting Kruppel-like Transcription Factors Bind a Transforming Growth Factor beta Control Element Required for Expression of the Smooth Muscle Cell Differentiation Marker SM22alpha in Vivo J. Biol. Chem., November 22, 2000; 275(48): 37798 - 37806. [Abstract] [Full Text] [PDF]
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P. S. Chang, L. Li, J. McAnally, and E. N. Olson Muscle Specificity Encoded by Specific Serum Response Factor-binding Sites J. Biol. Chem., May 11, 2001; 276(20): 17206 - 17212. [Abstract] [Full Text] [PDF]
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M. Strobeck, S. Kim, J. C. L. Zhang, C. Clendenin, K. L. Du, and M. S. Parmacek Binding of Serum Response Factor to CArG Box Sequences Is Necessary but Not Sufficient to Restrict Gene Expression to Arterial Smooth Muscle Cells J. Biol. Chem., May 4, 2001; 276(19): 16418 - 16424. [Abstract] [Full Text] [PDF]
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S. Beqaj, S. Jakkaraju, R. R. Mattingly, D. Pan, and L. Schuger High RhoA activity maintains the undifferentiated mesenchymal cell phenotype, whereas RhoA down-regulation by laminin-2 induces smooth muscle myogenesis J. Cell Biol., March 4, 2002; 156(5): 893 - 903. [Abstract] [Full Text] [PDF]
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J. M. Miano, C. M. Kitchen, J. Chen, K. M. Maltby, L. A. Kelly, H. Weiler, R. Krahe, L. K. Ashworth, and E. Garcia Expression of human smooth muscle calponin in transgenic mice revealed with a bacterial artificial chromosome Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1793 - H1803. [Abstract] [Full Text] [PDF]
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T. Imai, T. Morita, T. Shindo, R. Nagai, Y. Yazaki, H. Kurihara, M. Suematsu, and S. Katayama Vascular Smooth Muscle Cell-Directed Overexpression of Heme Oxygenase-1 Elevates Blood Pressure Through Attenuation of Nitric Oxide-Induced Vasodilation in Mice Circ. Res., July 6, 2001; 89(1): 55 - 62. [Abstract] [Full Text] [PDF]
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P. Qiu and L. Li Histone Acetylation and Recruitment of Serum Responsive Factor and CREB-Binding Protein Onto SM22 Promoter During SM22 Gene Expression Circ. Res., May 3, 2002; 90(8): 858 - 865. [Abstract] [Full Text] [PDF]
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