Departments of 1 Pediatrics and 2 Cell Biology and Neuroscience, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75235-9063
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ABSTRACT |
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Caveolae are specialized plasmalemmal microdomains originally studied in numerous cell types for their involvement in the transcytosis of macromolecules. They are enriched in glycosphingolipids, cholesterol, sphingomyelin, and lipid-anchored membrane proteins, and they are characterized by a light buoyant density and resistance to solubilization by Triton X-100 at 4°C. Once the identification of the marker protein caveolin made it possible to purify this specialized membrane domain, it was discovered that caveolae also contain a variety of signal transduction molecules. This includes G protein-coupled receptors, G proteins and adenylyl cyclase, molecules involved in the regulation of intracellular calcium homeostasis, and their effectors including the endothelial isoform of nitric oxide synthase, multiple components of the tyrosine kinase-mitogen-activated protein kinase pathway, and numerous lipid signaling molecules. More recent work has indicated that caveolae further serve to compartmentalize, modulate, and integrate signaling events at the cell surface. This specialized plasmalemmal domain warrants direct consideration in future investigations of both normal and pathological signal transduction in pulmonary cell types.
adenylyl cyclase; caveolin; cholesterol; endothelial nitric oxide synthase; mitogen-activated protein kinase
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INTRODUCTION |
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THE TERM CAVEOLAE (little caves) was coined by Yamada in 1955 (108) to describe "a small pocket, vesicle, cave or recess communicating with the outside of the cell" in gallbladder epithelium. Two years earlier, Palade (66) had described morphologically similar invaginations on the plasma membrane of endothelial cells that Bruns and Palade (5) later named plasmalemmal vesicles because they appeared to shuttle molecules into and out of the cell. The term caveolae then became synonymous with the terms "flask-shaped" or "omega-shaped" membrane because of their appearance in endothelial and smooth muscle cells.
Investigations that followed supported the hypothesis raised by Palade that caveolae are endocytic structures involved in the transcellular movement of molecules (85). This included the landmark observation of receptor-mediated uptake of folate by caveolae (1). After the first marker protein for caveolae, caveolin, was discovered (75), it was then possible to purify this specialized membrane domain, and it was found that caveolae contain a variety of signal transduction molecules. Recent research in the field (49, 83) has further indicated that caveolae serve to compartmentalize and integrate numerous signaling events at the cell surface. As such, caveolae are likely to be critically involved in both physiological and pathological events in numerous cell types in complex organs such as the lung.
In an effort to reveal the potential functions of caveolae in pulmonary health and disease, this review focuses on the role of caveolae in signal transduction as elucidated in a variety of cell types. After a discussion of the definition, structural composition, and purification of caveolae, the processes regulating caveolae function are examined. The important signaling molecules known to be enriched in this domain and the mechanisms underlying their targeting to caveolae are then addressed. Finally, examples of signal compartmentalization, modulation, and integration in caveolae are presented. It is anticipated that this specialized plasmalemmal domain will warrant direct consideration in future investigations of both normal and pathological signal transduction in pulmonary cell types.
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DEFINITION AND STRUCTURAL COMPOSITION OF CAVEOLAE |
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Definition. As mentioned in the introduction, the working definition of caveolae includes both morphological and biochemical parameters. Although the term caveolae was intended to refer to membrane invaginations at the cell surface (Fig. 1A), membranes with such classic morphological features are not found in all cells. With the use of the caveolae marker protein caveolin, purification techniques established new biochemical criteria for identifying this specialized membrane. These include a light buoyant density (92), resistance to solubilization by Triton X-100 at 4°C (77), and enrichment in glycosphingolipids (GSLs), cholesterol, sphingomyelin (SPH), and lipid-anchored membrane proteins including glycosylphosphatidylinositol (GPI)-anchored proteins. Membrane fractions with these properties can be isolated from the plasma membranes of essentially all cells. Thus it is likely that all cells have plasma membrane domains with the biochemical characteristics of caveolae, but only a portion of these membranes display flask-shaped morphology. Caveolae can assume a variety of shapes, including flat, vesicular, and tubular, and they can be either open or closed at the cell surface to yield endocytic or exocytic compartments. As such, the term caveolae is not limited to plasma membrane domains with a specific shape but should alternatively be considered to represent a dynamic cell surface-membrane system.
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Composition. Caveolae in endothelial
cells and fibroblasts have a striated coat on their cytoplasmic surface
(69, 75). Rapid-freeze, deep-etch electron micrographs reveal that the
coat decorates plasma membrane domains with variable amounts of
curvature (Fig. 1B), suggesting that
the coat may be involved in determining the shape of the membrane. The
striated coat is composed of integral membrane proteins including the
protein caveolin (75). There are at least four caveolin isoforms in
mammals, and the known isoforms are referred to as
caveolin-1 and -1
, caveolin-2, and caveolin-3 (29,
39, 40, 78, 100, 106). The amino and carboxy domains of each isoform
reside free in the cytoplasm, being separated by a 33-amino acid
hydrophobic domain that is believed to anchor caveolin in the membrane
(39). Caveolin-1 and -3 have cysteine residues at positions 134, 144, and 157, and these cysteines are acylated in caveolin-1 (13).
Caveolin-1 and caveolin-2 are ubiquitously expressed, whereas
caveolin-3 is primarily found in muscle cells (78, 100, 106). Most
studies to date have evaluated the presence and function of caveolin-1, and the potential role of caveolin-2 has often not been checked. The
expression of caveolin-1 in cells is correlated with the appearance of
invaginated caveolae and the presence of the striated coat (21, 91).
Although caveolin-1 forms homotypic oligomers (46, 58), it most likely
does not serve a mechanical function in shaping the membrane because
invaginated caveolae can lack the molecule (10, 90). The depletion of
intracellular cholesterol and the sequestration of membrane cholesterol
with agents such as filipin cause the striated coat to disassemble and
the invaginated caveolae to disappear (6, 75). Because caveolin appears
to be a cholesterol-binding protein and cholesterol stabilizes caveolin oligomers (44, 58, 62), it is likely that cholesterol and caveolin work
in concert to form the striated coat.
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PURIFICATION OF CAVEOLAE |
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The isolation of caveolae by cell subfractionation most frequently relies on the use of caveolin-1 as the marker protein. To date, six methods have been reported for the purification of caveolae from tissues or cultured cells. These methods can be generally divided into four categories: 1) flotation of a detergent-insoluble membrane on sucrose gradients (77), 2) flotation of sonicated plasma membranes on OptiPrep gradients (92), 3) differential centrifugation of tissue homogenates (7), and 4) recovery by either immunoadsorption or centrifugation from endothelial cell plasma membranes purified by adsorption to cationized silica (80, 95). The caveolae obtained by these procedures are most often not directly comparable, primarily because there is no morphological standard with which to judge the purity of the caveolae fraction. Coatlike material is visible in some preparations but is generally difficult to recognize. Caveolin-1 content is also not an optimal means to assess purity because the concentration in caveolae can be variable. As importantly, the physical interventions employed in purification, such as sonication, Triton X-100, immunoadsorption, and cationized silica, can alter the molecular composition of caveolae. Furthermore, detergents solubilize resident proteins (7), yielding extracted preparations of caveolae. As such, it may be difficult to make direct comparisons between results reported by different laboratories. As a result of these variables, investigators are obliged whenever possible to confirm any findings obtained by cell subfractionation with independent methods such as immunofluorescence or immunoelectron microscopy.
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MECHANISMS REGULATING CAVEOLAE FUNCTION |
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Biogenesis of caveolae. The initial assembly of caveolae first involves the formation of the detergent-insoluble, GSL-SPH-cholesterol lipid core of the caveolae membrane in the transitional region of the Golgi apparatus (4, 46). GPI proteins and caveolin arriving from the endoplasmic reticulum (ER) after synthesis (46) are then incorporated to complete the initial assembly step. Anticaveolin immunoprecipitation and chemical cross-linking experiments indicate that other proteins associate with the caveolin-enriched membrane at this point (46). Caveolae are then transported to the cell surface embedded in the membranes of exocytic vesicles (15). This overall process contrasts with that of other membrane domains coated with peripheral proteins such as clathrin. Whereas caveolae are assembled in the Golgi apparatus and are then transported to other locations, clathrin-coated membranes are assembled de novo at sites of vesicle formation (79). Caveolae-like domains may exist in all membranes that traffic to and from the cell surface.
Maintenance of caveolae. SPH and cholesterol are the major components of the lipid core of caveolae. Cholesterol, however, is constantly fluxing out of the cell (65). As stated in Composition, if caveolae cholesterol levels were to get excessively low, GPI proteins would no longer cluster properly in caveolae (6), the striated coat would disassemble (75) and the number of invaginated caveolae would decline (6). Pharmacological agents that block cholesterol transport to the cell surface have exactly these effects (91), suggesting that the maintenance of caveolae is dependent on the continuous transport of cholesterol to caveolae. A novel transport system has been identified that appears to be necessary for maintaining the proper level of cholesterol in caveolae. There is bidirectional movement of cholesterol between the ER and the plasma membrane, and caveolin appears to play a critical role in this process. Caveolin binds cholesterol (62), preferentially incorporates into cholesterol-containing membranes in vitro (44, 62), and moves between caveolae and internal membranes. There is evidence that a heat shock protein-caveolin chaperone complex may transport cholesterol through the cytoplasm (101). Furthermore, increasing the cellular cholesterol level also causes an increase in caveolin mRNA expression (20, 32). Thus caveolin appears to be an integral part of an intracellular lipid transport system that is required for the maintenance of caveolae.
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SIGNAL TRANSDUCTION MOLECULES ENRICHED IN CAVEOLAE |
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Biochemical and morphological techniques have identified a number of signal transduction molecules that appear to be concentrated in caveolae relative to the surrounding membrane (Table 1). Approximately 40% have been localized by both morphological and biochemical methods (see Table 1). Four major groups of signal transduction molecules can be considered.
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G protein-mediated signaling
molecules. There has previously been considerable
debate whether G protein-coupled receptors, G proteins, and their
effectors are organized or randomly distributed at the cell surface
(63). However, studies employing both cell subfractionation and
immunocytochemistry have revealed that all three components are
concentrated in caveolae. Receptors for endothelin, cholecystokinin,
acetylcholine, and bradykinin are associated with caveolae (8, 12, 18,
74), and G proteins are found in most caveolae preparations (Table 1).
In addition, there is evidence that the receptors are functionally
interactive with their effectors in caveolae. Isolated caveolae
fractions contain a significant proportion of total cellular adenylyl
cyclase activity (34), and isoproterenol-stimulated adenylyl cyclase
activity has been histochemically localized to membrane organelles
resembling caveolae (71, 86, 105). Moreover, the agonist bradykinin activates the movement of Gq
and Gi
to caveolae (12). There is evidence that caveolin plays a role in the recruitment of G proteins
to caveolae and in the modulation of their activity (42, 43, 78).
Calcium-mediated signaling molecules. Several studies have indicated that caveolae are sites of calcium storage and entry. In smooth muscle cells, pyroantimonate precipitates of calcium are present in caveolae under quiescent conditions, and the stimulation of contraction yields a diffuse distribution of the precipitate in the mycoplasm (98), suggesting that there is a movement of calcium into the cell. A morphological study (68) indicated that smooth muscle cell caveolae interact with smooth ER, similar to the interaction between sarcoplasmic reticulum and T tubules in skeletal muscle. In addition, there is evidence that critical molecules involved in calcium transport, including inositol 1,4,5-trisphosphate [Ins(1,4,5)P3] receptors, calcium ATPase, and calmodulin, are concentrated in caveolae (22, 23, 80, 83). It has been demonstrated that ATP-induced calcium waves in endothelial cells, which are at least partially mediated by Ins(1,4,5)P3 receptors, originate at specific discrete loci in caveolin-rich cell edges (36). Furthermore, endothelial nitric oxide (NO) synthase (eNOS), one of the key signaling molecules in endothelial cells that is acutely regulated by changes in calcium influx, is concentrated in caveolae. In a study (83) of cell fractions of quiescent cultured endothelial cells, 51-86% of total NOS enzymatic activity in the postnuclear supernatant was recovered in the plasma membrane, and 57-100% of the activity in the plasma membrane was recovered in caveolae. Thus caveolae appear to be critically involved in the regulation of calcium-mediated signaling at the cell surface.
Tyrosine kinase-mitogen-activated protein kinase pathway components. Both receptor and nonreceptor tyrosine kinases have been found to be enriched in caveolae in studies employing immunoblotting, determinations of enzymatic activity, and immunocytochemistry. The immunoprecipitation of multiple GPI-anchored proteins coprecipitates tyrosine kinases (96). A major substrate for tyrosine kinases is caveolin (27, 28, 30), and tyrosine phosphorylation of caveolin occurs in response to a variety of stimuli including insulin (52), oxidants (104), sulfonylurea (61), and cell transformation (28). In addition, a peptide sequence in caveolin known as the scaffolding domain (amino acids 82-101) interacts with c-Src and may modulate the activity of tyrosine kinase (42). Furthermore, more distal components of the tyrosine kinase-mitogen-activated protein (MAP) kinase signaling pathway including Ras, Raf-1, and MAP kinases have been localized to caveolae (Table 1).
Lipid signaling molecules. Besides
being critically important to the establishment and maintenance of the
molecular environment that is unique to caveolae, certain lipid
moieties and lipid-anchored proteins in the lipid core are substrates
for enzymes that release lipid signals. SPH, phosphatidylinositol
4,5-bisphosphate, and GPI-anchored proteins yield ceramide,
Ins(1,4,5)P3, and
inositolphosphoglycans (IPGs), respectively (2, 9, 33, 48,
70). Each is produced in caveolae in response to specific stimuli.
Ceramide increases in response to neurotrophin or interleukin-1
(2, 48),
Ins(1,4,5)P3 is
produced on stimulation with either bradykinin or epidermal growth
factor (EGF) (33), and IPGs are produced in response to insulin (67,
97), and the respective lipid signals elicit specific cellular
processes. There is evidence that these responses are unique to
caveolae because neither ceramide nor
Ins(1,4,5)P3 is
generated in noncaveolae subcellular fractions, and the IPG released
extracellularly is internalized, presumably by caveolae. Thus both the
receptors and the transducers of lipid signaling are concentrated in
the same, unique plasmalemmal domain.
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MECHANISMS UNDERLYING TARGETING TO CAVEOLAE |
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The association of certain signaling proteins with the plasma membrane is quite predictable based on the presence of moieties such as transmembrane spanning domains. However, another important mechanism underlying targeting of signaling proteins to caveolae is lipid modification. Proteins modified with either GPI or fatty acids are found to be enriched in caveolae fractions obtained by most methods of purification (77, 92). Mutations that abolish either the GPI anchor addition (38, 72) or the fatty acylation (73, 83, 84) shift the protein to other fractions, suggesting that the lipid moiety is necessary for targeting to caveolae. For example, in studies of caveolae-containing COS-7 cells transfected with wild-type eNOS cDNA, NOS activity is enriched 27-fold in caveolae compared with noncaveolae plasma membrane (Fig. 2). In contrast, transfection with a myristoylation-deficient mutant eNOS that is incapable of either myristoylation or palmitoylation results in a complete lack of targeting of eNOS to the caveolae fraction. However, transfection with a palmitoylation-deficient mutant eNOS that can be myristoylated yields modest enrichment of eNOS in the caveolae fraction, which exhibits threefold more NOS activity than noncaveolae membranes. Such studies have revealed that both myristoylation and palmitoylation are required to target eNOS to caveolae and that each acylation process enhances targeting 10-fold (83). These two different covalent modifications, GPI anchoring and fatty acylation, are responsible for targeting proteins with a broad range of biochemical activities to opposing surfaces of the same membrane domain. Because the acyl chains on these proteins intercalate in the lipid bilayer, they probably collect in caveolae as a result of a slowed lateral mobility on encountering the GSL-SPH-cholesterol lipid core. Altering the lipid core with cholesterol-sequestering agents such as filipin disperses GPI proteins in the plane of the membrane (76, 88). In addition, protein-protein and protein-lipid interactions within caveolae influence how long the molecules remain at that site (19, 109). Thus the properties of the lipid core play a key role in the maintenance of the complex molecular environment found in caveolae that enables many signaling proteins to be targeted there.
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SIGNAL COMPARTMENTALIZATION, MODULATION, AND INTEGRATION IN CAVEOLAE |
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Inspection of the long list of signal transduction molecules that have
been demonstrated to be enriched in caveolae (Table 1) suggests that
there may be close association of multiple interacting molecules
involved in the cellular responses to a specific external stimulus.
This is perhaps best illustrated by a recent study (49) of MAP kinase
activation by platelet-derived growth factor (PDGF) in human
fibroblasts. The various cellular responses to PDGF-receptor activation, which include effects on mitogenesis, cell differentiation, apoptosis, and calcium mobilization, appear to occur through multiple phosphorylation cascades that are all initiated by phosphorylation of
the receptor itself. This suggests the existence of a signaling module
associated with PDGF receptors at the cell surface, consisting of
components of the tyrosine kinase-MAP kinase pathway. Immunoblotting reveals that caveolae fractions from unstimulated fibroblasts contain
PDGF receptor, Ras, Raf-1, MAP kinase kinase-1, and extracellular signal-related kinase (ERK) 2, and immunoelectron
microscopy confirms colocalization of PDGF receptors and ERK2 in
caveolae. In addition, a 2-min exposure of intact fibroblasts to PDGF
activates MAP kinase in the caveolae fraction, indicating that these
components are functional in vivo. Activated MAP kinase was not
detected in noncaveolae plasma membrane fractions, which also do not
contain ERK2, suggesting that caveolae are a cell-surface domain where
MAP kinase is functionally linked to the PDGF receptor. Furthermore,
PDGF can stimulate tyrosine kinase activity and also MAP kinase
activity in isolated caveolae, and these effects are blocked by both
suramine, which prevents PDGF binding to its receptor, and genistein,
which inhibits tyrosine kinase (Fig.
3). Thus the entire pathway required
for this receptor tyrosine kinase to stimulate the activation of MAP
kinase, which may involve as many as 11 different molecules (35, 51),
is functional in isolated caveolae. These data complement previous demonstrations of signaling events originating specifically in caveolae, which include isoproterenol-stimulated adenylyl cyclase activation (71, 86, 105), EGF-stimulated Raf-1 recruitment (57),
interleukin-1-stimulated ceramide production (48), and histamine
regulation of caveolae internalization (89). In addition, it has
recently been demonstrated that the cationic amino acid transporter-1
protein, which is responsible for the majority of endothelial cell
uptake of the eNOS substrate arginine, is colocalized with eNOS in
caveolae (53). This is the first example of a functional complex
between a plasma membrane transport protein and an enzyme. When
considered collectively, these observations indicate that caveolae play
an important role in the compartmentalization of specific signaling
events at the cell surface.
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There is also evidence that the structural protein caveolin may
modulate the function of resident signaling molecules in caveolae. This
has been evaluated particularly in investigations of eNOS interaction
with caveolin. First, it was demonstrated in studies of endothelial and
cardiac myocyte cell lysates that eNOS coimmunoprecipitates with
caveolin-1 and caveolin-3, respectively (16, 24). Then, in vitro
studies and experiments with eNOS and caveolin-1 overexpression in
COS-7 cells revealed that both
NH2- and COOH-terminal domains of
caveolin interact directly with the eNOS oxygenase domain and inhibit
eNOS catalytic activity (25, 37, 54, 55). Interestingly, the neuronal
isoform of NOS and caveolin-3 have also been coimmunoprecipitated from
rat skeletal muscle (103). In vitro manipulations further indicated
that calcium-calmodulin may disrupt the interaction between eNOS and
caveolin, leading to enhanced enzymatic activity (54). Experiments
using particulate and soluble cellular fractions suggest that this may
be a cyclic phenomenon, with dissociation of eNOS and caveolin and
mobilization of eNOS from the particulate fraction on agonist
stimulation, followed later by reassociation of eNOS and caveolin in
the particulate fraction (17). Further work (11, 55, 64) indicates that
it is the 20-amino acid scaffolding domain of caveolin mentioned
earlier that binds and modifies the activity of eNOS as well as that of
other resident signaling molecules including protein kinase C and G
protein -subunits. However, a degree of caution is warranted in the
interpretation of these findings because it has not yet been determined
whether these processes lead to modifications in eNOS enzymatic
activity in vivo under physiological conditions. In addition, because
both caveolin and eNOS may be found in large abundance in the Golgi apparatus and other internal membranes (44, 62, 81), experiments have
yet to be performed to demonstrate whether these interactions take
place and have functional relevance within caveolae per se.
Along with involvement in the compartmentalization of specific signaling cascades and the potential modulation of the function of resident signaling molecules, it is likely that caveolae also serve as a site for feedback interplay between different signaling processes or signal integration. For example, GPI-anchored proteins can activate tyrosine kinases and lead to calcium influx (59, 102). Tyrosine kinases also phosphorylate eNOS, causing enzyme inhibition and enhancing its interaction with caveolin (24). However, the calcium entering the cell will bind calmodulin and thereby activate eNOS. The NO generated can stimulate the MAP kinase pathway via Ras (41). In this manner, the physical proximity of the different signaling pathways can lead to cross talk between them, resulting in higher levels of control of the cellular responses to external stimuli.
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FUTURE DIRECTIONS |
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Recent studies (49, 83) have demonstrated that caveolae are critically involved in multiple signal transduction events at the surface of a variety of cell types. Investigations indicating that numerous individual signal transduction molecules are housed in caveolae have been complemented by demonstrations of signal pathway compartmentalization, modulation, and integration in caveolae. In the process, our understanding of normal signaling events has been considerably advanced. The challenge is to determine the role of caveolae in pathological disorders, including those involving pulmonary epithelial, endothelial, and smooth muscle cells. Future progress in this field may lead to novel therapies for a variety of lung diseases.
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ACKNOWLEDGEMENTS |
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We thank Marilyn Dixon for secretarial assistance.
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FOOTNOTES |
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This work was supported by National Heart, Lung, and Blood Institute (NHLBI) Grant HL-58888 and National Institute of Child Health and Human Development Grant HD-30276 (to P. W. Shaul); NHLBI Grant HL-20948 and National Institute of General Medical Sciences Grant GM-43169 (to R. G. W. Anderson); the American Heart Association (P. W. Shaul); and the Perot Family Foundation (R. G. W. Anderson).
Address for reprint requests: P. W. Shaul, Dept. of Pediatrics, Univ. of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9063.
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