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VASCULAR BIOLOGY
1Department of Anatomy and Cell Biology, 2Department of Physiology, and 3The Cardiovascular Center for Research, Temple University Medical School, Philadelphia, Pennsylvania
Submitted 4 April 2006 ; accepted in final form 7 November 2006
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ABSTRACT |
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 TOP ABSTRACT METHODS AND MATERIALSRESULTSDISCUSSIONREFERENCES |
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migration; proliferation
Periostin-like factor (PLF) is related to periostin (osf2), 
ig-H3, Fasciclin I, MBP70, and Algal CAM (9, 10, 20, 25, 29, 30, 34). A recent review presents details on each protein (19). Differences between these proteins reside in the COOH-terminal region (19, 20). Evidence in other systems suggests that PLF expression is associated with tissue remodeling, such as in the failing heart (18). PLF expression in the context of any other vascular pathology has not been previously reported. However, because extensive remodeling is one consequence of vascular injury, we hypothesized that PLF expression may be modulated in models of vascular injury and in activated smooth muscle cells. We also asked whether PLF itself played an active role in VSMC activation. In this study, we report that PLF is not expressed in normal human, rat, and swine arteries, but is rapidly induced in all upon both inflammatory and mechanical injury. PLF expression in primary human vascular smooth muscle cells was increased following treatment with mitogenic compounds, suggesting that this isoform plays a role in VSMC activation. Changes in the level of PLF resulted in changes in VSMC migration and proliferation. We suggest that PLF acts in vascular proliferative diseases such as restenosis by regulating VSMC proliferation and migration, possibly by an autocrine mechanism. Its conserved species expression suggests that it plays a fundamental role in vascular proliferative disorders.
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METHODS AND MATERIALS |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONREFERENCES |
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(IFN-), 20 ng/ml platelet-derived growth factor (PDGF-AB), 2 ng/ml transforming growth factor (TGF-1) or T-cell-conditioned medium for 48 h, at which time treated cells were harvested for RNA or protein isolation. In addition, 1 ml of medium was collected from cells exposed to 1.0% FBS, PDGF-AB, and TGF-1. Proteins in the media were concentrated by TCA precipitation, for further analysis by Western blot. PDGF-AB, IFN-, and TGF-1 were purchased from Invitrogen and T-cell-conditioned media was purchased from Fisher Scientific (Biotechnology). All animal care and use, as well as the maintenance of the rats are under direct supervision of the Temple University's veterinarian. The animals are housed in an AAALAC-accredited facility and all animal care and use strictly followed the guidelines established by NIH and Temple University's IACUC. Swine coronary artery balloon angioplasty. Domestic swine (20–30 kg) were sedated, and general anesthesia administered (see Ref. 4). An 8-Fogarty introducer sheath with a hockey stick curve was introduced into the femoral artery and a bolus of heparin (200 U/kg) and bretylium (2.5 mg/kg) was administered. A guiding catheter was advanced to the aortic root, intracoronary nitroglycerine (200 µg) was injected, and baseline angiograms of the left and right coronaries were obtained. Coronary injury was induced by deliberate stretching of the vessel wall with an oversized angioplasty balloon inflated to a pressure of 8–10 atm for 30 s, with a 1-min rest period, for a total of three times. After withdrawal of the catheter, the femoral sheath was removed, and the cut-down site was repaired. At various times after angioplasty the animals were euthanized, the left main coronary artery was cannulated, and injured segments were identified by examination. These sections were dissected, fixed in 10% formalin, and embedded in paraffin for sectioning.
Rat coronary artery balloon angioplasty. Left common carotid artery balloon angioplasty was performed under aseptic surgery conditions for rodents (autoclaved instruments and sterile draping) on male Sprague-Dawley rats (350 g; Charles River Breeding Laboratory, Wilmington, MA) under pentobarbital sodium anesthesia (65 mg/kg ip) as described previously (6). The left external carotid artery was identified, cleared of adherent tissue, and the segment to be injured, transiently isolated from the internal carotid artery by temporary ligatures allowing the insertion of a 2-F Fogarty arterial embolectomy catheter (model 12-060-2F; Baxter Healthcare). The catheter was guided a fixed distance down the common carotid artery to the aortic arch, inflated with a fixed volume of fluid and withdrawn to the site of insertion three times.
Human coronary arteries. Human coronary arteries were removed from failed transplanted hearts with severe cardiac allograft vasculopathy (CAV; 3). All tissue procurement protocols were approved by the Institutional Review Board for Human Studies at Temple University.
Immunostaining. Cultured cells were rinsed in PBS and fixed in 4% paraformaldelyde, blocked in 5% goat serum, incubated with anti-PLF (rabbit anti-mouse) and anti-actin (mouse anti-human) antibodies, washed in PBS, followed by incubation with secondary antibody conjugated to cy3 (red) or fluoroscein (green).
Human as well as rat and swine arteries were fixed in 10% buffered formalin, embedded in paraffin, sectioned at 7 µm, and placed on microscope slides. Sections were then deparaffinized, washed in PBS, blocked in 5% goat serum, incubated with anti-PLF (1:1,000) or anti-smooth muscle 
-actin antibodies (1:200), washed in PBS, followed by incubation with goat-anti-rabbit biotinylated secondary antibody (1:2,000). This was washed and incubated with an avidin-biotin enzyme complex and 3,3'-diaminobenzidene chromogenic substrate, as described by the manufacturer (Vector), which develops a brown color. Sections were counterstained with hematoxylin and eosin. Endogenous peroxidase activity was blocked with 1.5% hydrogen peroxide in methanol for 15 min. As controls, sections were incubated with nonimmune isotype antibodies instead of primary antibody. Tissue from at least three animals and three sections per vessel were evaluated.
RNA isolation and Northern blot analysis. Cultured cells were rinsed in phosphate-buffered saline (PBS) and total RNA extracted in TRIzol reagent (Invitrogen) as suggested by the manufacturer. Ten micrograms of total RNA was separated on a 1% formaldehyde-denatured agarose gel, electrotransferred to a nylon membrane (NYTRAN), and probed with the [32P]-labeled PLF cDNA. The blot was stripped and reprobed with a [32P]-labeled 18S ribosomal cDNA as a loading control. The blots were exposed to X-ray films, and the films were analyzed by densitometry. Three separate Northern blots were performed on RNAs obtained from cells treated in three separate experiments. For each Northern blot, the data was expressed as a ratio of PLF/18S mRNA. The average and standard deviation for the values obtained by densitometry were calculated for each treatment and fold increase over control (1% FBS) was calculated.
Western blot analysis. Cultured cells were rinsed in PBS, and proteins were extracted in RIPA buffer (50 mM HEPES, pH 7.5, 150 mmol NaCl, and 0.1% Triton X-100) containing protease inhibitors (Sigma). Lysates were incubated on ice for 20 min, passed through an 18-gauge needle twice, and centrifuged at 3,000 rpm for 10 min at 4°C. Protein concentration was determined using the BCA kit (Pierce Biochemicals). Equal protein from each sample (100 µg/lane) was separated by PAGE and the proteins transferred to nitrocellulose. The blots were probed with anti-PLF-specific antibody (18), stripped, and reprobed with anti-GAPDH as a loading control. Western blots were performed on proteins obtained from cells treated as described above in three separate experiments. Each blot was analyzed by densitometry and the data expressed as a ratio of PLF/GAPDH. The average and standard deviation of the values obtained by densitometry were calculated for each treatment and fold increase over control (1% FBS) was calculated.
Infection and proliferation assay. Human coronary artery VSMCs were grown in T-75 flasks and infected with 100 multiplicity of infection adenovirus for 4 h. Twenty-four hours later, the VSMCs were trypsinized, and equal numbers (7,500) of cells were seeded in 12-well dishes. Forty-eight hours after infection, a subset of the cultures was treated with anti-PLF antibody (5 µg/ml). Four and ten days later, respectively, the cells were trypsinized and counted on a hemocytometer. Each condition was done in triplicate and the experiment was repeated three times.
Migration and chemotaxis.
Transwell Boyden chamber plates (6.5 mm in diameter) with a 8 µm polycarbonate membrane pore were seeded with human VSMCs (20,000 cells per membrane) infected with adenovirus-expressing -galactosidase or PLF and grown in medium containing 0.5% FBS (see Ref. 2). In some cases, 40 ng of PDGF-Ab was placed in the lower chamber, and cells were incubated for 3 h at 37°C, at which time cells were fixed and stained in Dif-Quick Cell Stain (American Hospital Supply). The upper layer was scraped free of cells. VSMCs that had migrated to the lower surface of the membrane were quantitated by counting six fields per membrane under high magnification. Treatments were performed in triplicate in each of three experiments.
For directional migration, equal numbers of cells infected with adenovirus expressing -galactosidase or PLF were grown on glass slides in growth media to confluence. The monolayers were scraped with a cell scraper to create a 3 mm track devoid of cells in the center of the chamber. The wound tracks were washed to remove detached cells and fresh media was added. Cells were fixed at 24 h after wounding and stained with hematoxylin.
Statistical analysis. Data were expressed as means ± SD. The statistical significance regarding multigroup comparison was determined by two-way ANOVA with Bonferroni correction. A value of P < 0.05 was considered significant.
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RESULTS |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONREFERENCES |
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1, and IFN. Northern blot analysis indicated that PLF was expressed at low levels in unstimulated VSMCs, but was reproducibly highly upregulated by PDGF-AB and TGF-1 and to a lesser level by the inflammatory response-related cytokines (see Fig. 1, A and B). Statistical analysis demonstrated a significant fold increase over control (1% FBS) of PLF mRNA by soluble growth factors (Fig. 1C).
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1 and to a lesser extent by T-cell conditioned media, IFN and 10% FBS, which suggests that PLF expression is regulated by soluble, stimulatory factors (Fig. 1, D and E). Statistical analysis demonstrated a significant fold increase over control (1% FBS) of PLF protein by soluble stimulatory factors (Fig. 1E). Since PLF protein was highly induced by PDGF-AB and TGF-1 we investigated whether PLF was secreted from VSMCs when stimulated. Data presented in Fig. 1F demonstrates that PLF was secreted from cells induced with PDGF-AB and TGF-1 (Fig. 1F), suggesting that PLF is secreted from VSMCs induced by cytokines. PDGF-AB, a growth factor that induces high levels of PLF expression was used to stimulate cells to determine localization of PLF protein by immunostaining with anti-PLF antibody. PLF was not detected in unstimulated cells (Fig. 1G,b); whereas it was present at a markedly higher level in cells stimulated with PDGF-AB (Fig. 1G,a). PLF has molecular signatures of a matrix protein and sequence analysis indicates the presence of a signal peptide (19, 20). To investigate whether PLF was secreted, VSMCs were infected with either adenovirus to overexpress PLF (AdPLFS) or control adenovirus (AdLacZ). Proteins were extracted from infected cells, and from infected cell-conditioned-serum-free media, and equal amount of protein was analyzed by Western blot. Data shown in Fig. 1H confirm that PLF is secreted from VSMCs. Together, these findings indicate that PLF expression is cytokine inducible in cultured VSMCs, and is secreted from VSMCs.
PLF protein is induced in swine and rat coronary arteries by balloon angioplasty.
Given that the vascular response to injury and development of neointimal hyperplasia is initiated and driven by multiple cytokines, we hypothesized that PLF would be expressed in models of mechanically induced vascular injury. Vascular injury in swine results in VSMC activation and formation of a neointima. PLF expression was examined at 3 and 14 days after oversized balloon angioplasty surgery in swine coronary arteries and these data were compared with PLF expression in uninjured swine coronaries. PLF was not detected in uninjured arteries (Fig. 2A) but was rapidly upregulated post-injury on day 3 (Fig. 2, B and E) and day 14 (Fig. 2, C and F). At day 3, PLF expression was detected in VSMCs in the media and neointima (Fig. 2, B and E). Positively stained medial cells were identified based on their morphological appearance and co-expression of SMC -actin (4). At day 14, PLF expression was not only detected in SMCs in the media and neointima, but was also seen in endothelial cells (Fig. 2, C and F). Similar results were detected in the rat model of balloon angioplasty. PLF was not detected in uninjured rat coronaries (Fig. 3A) and was markedly increased by day 15 after injury (Fig. 3B). Expression was detected in SMCs in the media and neointima and in endothelial cells. This data corroborates the in vitro data in which PLF expression, though detected at low levels in unstimulated VSMCs, was markedly upregulated by cytokine stimulation. This data also suggests a role for PLF in the vascular response to injury.
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-galactosidase (data not shown), and we were unable to detect PLF by immunohistochemistry in these cells (Fig. 5A,b). In addition, we showed that >90% of cells infected with AdPLFS expressed PLF protein detected by immunoreaction with anti-PLF antibody (Fig. 5A,c). To examine the effects of PLF over expression on proliferation, equal numbers of cells were infected with adenovirus to over express PLF or with adenovirus expressing -galactosidase (control) and counted on days 4 and 10. Since PLF is a secreted protein, in some experiments its effects were blocked with an anti-PLF-specific neutralizing antibody. Overexpression of PLF resulted in a significant increase in cell proliferation compared with cells infected with control virus (23 ± 1.38 control vs. 29 ± 1.44 PLF on day 4 and 80 ± 3.07 control vs. 120 ± 7.91 PLF on day 10; see Fig. 5). PLF is a secreted protein, and we hypothesized a role in autocrine growth regulation. Therefore, its effects were blocked with an anti-PLF-specific neutralizing antibody. VSMC proliferation was significantly reduced when cells were treated with the PLF neutralizing antibody, suggesting a PLF-specific autocrine-mediated induction of proliferation in VSMCs (23 ± 1.38 control-Ab vs. 5.75 ± 0.59 PLF-Ab day 4 and 75.91 ± 2.66 control-Ab vs. 9.16 ± 0.89 PLF-Ab on day 10). At day 10, this represents a 393% decrease in cell numbers, and strongly associates PLF expression with VSMC proliferation.
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DISCUSSION |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONREFERENCES |
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Periostin was first identified in bone, but since has been implicated in heart development (12, 13, 22) and oncogenesis (33). It is expressed in developing and mature heart valves (12, 22), under pressure or volume overload in the adult heart (11, 27), in developing teeth (14, 28) and it regulates adhesion and migration of ovarian epithelial cells via its binding to the v3 and v5 integrins (8). PLF and periostin are generated by alternative splicing with differences located in their COOH-terminal region (20). The PLF-specific antibody is directed against a peptide in exon 17, in the COOH-terminal end and is not present in periostin. Both proteins contain a signal peptide and are secreted proteins. In addition, PLF contains a putative nuclear localization signal (20). A pronounced increase in periostin mRNA and protein was observed in rat carotid arteries after balloon injury (17). Periostin mRNA was detected in smooth muscle cells in the neointima and adventitia (17) and the protein was associated with SMC differentiation and migration in vitro. In response to the stress of hypoxia, periostin was increased in pulmonary arterial smooth muscle cells and the response was mediated through the P13K/p70Sk6, Ras/MEK1/2, and Ras/p38MAPK signaling pathways (15). In general, it appears that periostin is upregulated in adult tissues under adverse conditions such as damage, overload, and/or stress. Its function under these conditions is not known. Low levels of periostin are reported in uninjured rat carotid arteries, whereas levels increase after injury (17). Eight days after injury periostin expression was detected in adventitial fibroblasts and 2 wk after injury in cells in the neointima. Neointimal VSMCs assume a myofibroid appearance (24). Because markers for smooth muscle cells and fibroblasts were not utilized, it is unclear whether expression was detected in smooth muscle cells and/or fibroblasts in the neointima (17). Since in other tissues periostin is expressed in fibroblasts and mesenchymal cells, it is likely that periostin is also expressed in vessel fibroblasts or possibly in smooth muscle cells that dedifferentiate to a fibroblast-like phenotype as they migrate to the neointima. Differences between periostin and PLF lie in their temporal and spatial pattern of expression reflecting possibly different functions for each.
Expression of PLF, a splice variant of periostin, is inducible in activated VSMCs. In cultured primary human coronary artery VSMC, PLF is detectible at very low levels in unstimulated cells, but was markedly upregulated at both the mRNA and protein levels in VSMC treated with growth factors and cytokines (Fig. 1). Similarly PLF is not expressed in uninjured arteries, but was strongly induced by balloon angioplasty injury in vivo. PLF expression in human coronary arteries with clinical CAV is localized to neointimal VSMC, which phenotypically are a synthetic, fibroproliferative smooth muscle cell. These data strongly associate PLF expression with vascular pathophysiology, in a species conserved fashion, suggesting PLF expression as a central component of the VSMC response to injury. PLF was detected in the supernatant of cultured VSMC, and over expression of PLF led to an increase in VSMC proliferation and migration suggesting that PLF is an important molecule involved in VSMC activation. Importantly, neutralizing anti-PLF antibody significantly suppressed PLF-driven VSMC proliferation, suggesting that its growth promoting effects is via an autocrine mechanism. While at present an association between PLF and activation of signal transduction pathways is not known, we do not expect that PLF functions exclusively as an extracellular protein. It has a putative nuclear localization signal and because reports by Yoshioka et al. (33) suggest an intracellular function for periostin, we propose that this family of protein may have an important intracellular function as well as one in the extracellular milieu.
The common features between periostin and PLF are their shared homologies as isoforms generated from a single gene. One difference between the isoforms lies in their temporal and spatial pattern of expression reflecting possibly different functions for each. Upregulation during development and/or in response to damage and their role in cell adhesion possibly through integrins suggests a function in tissue remodeling (20). The biological significance of alternative splicing in the heart has recently become apparent (7, 31). The data presented in this study is the first to report an association between PLF expression and vascular pathophysiology. There are four novel findings presented in this study: 1) PLF expression is associated with vascular proliferative diseases, 2) PLF expression is induced in cultured VSMC by cytokines and secreted into culture media, 3) PLF expression induces VSMC migration, and 4) PLF expression induces VSMC proliferation. When taken together, this report suggests a central role for PLF in regulation of vascular proliferative diseases.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONREFERENCES |
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