Elsevier

Cellular Signalling

Volume 20, Issue 7, July 2008, Pages 1313-1319
Cellular Signalling

Caveolin-1 increases basal and TGF-β1-induced expression of type I procollagen through PI-3 kinase/Akt/mTOR pathway in human dermal fibroblasts

https://doi.org/10.1016/j.cellsig.2008.02.020Get rights and content

Abstract

Caveolin-1 (Cav-1) is a major structural protein of caveolae and plays an important role as a negative regulator of various signaling pathways such as the transforming growth factor-β (TGF-β)/smad pathway. In this study, we investigated the role of cav-1 on basal and TGF-β1-induced expression of type I procollagen in human dermal fibroblasts. Our results demonstrated that basal and TGF-β1-induced expression of type I procollagen were significantly increased by adenoviral cav-1 (Ad-cav-1) overexpression, while the basal level of type I procollagen was decreased by cav-1 siRNA. Overexpression of cav-1 inhibited TGF-β1-induced phosphorylation of smad3 and transcription of 3TP-Lux and SBE luciferase reporters, suggesting that cav-1 may inhibit the TGF-β1/smad signaling pathway. We observed that TGF-β1-induced type I procollagen expression was decreased by smad3 siRNA transfection. However, the reduction of TGF-β1-induced type I procollagen expression by smad3 siRNA was reversed by cav-1 overexpression. In addition, our results also showed that TGF-β1 treatment increased the phosphorylation of Akt, and Ad-cav-1 infection augmented this TGF-β1-induced phosphorylation of Akt. Ad-myr-Akt infection significantly increased the basal expression of type I procollagen. In contrast, TGF-β1-induced type I procollagen expression was decreased by Akt siRNA transfection and the PI3-kinase inhibitor, LY294002, inhibited the TGF-β1-induced type I procollagen expression and also inhibited the cav-1-induced expression of type I procollagen. In conclusion, our results suggest that cav-1 increases the basal and TGF-β1-induced expression of type I procollagen by regulating two opposite signaling pathways: inhibiting TGF-β1/smad signaling and activating a PI-3 kinase/Akt/mTOR-dependent pathway in human dermal fibroblasts, ultimately resulting in increased type I procollagen expression.

Introduction

Caveolae are 50- to 100-nm sized, omega-shaped plasma membrane invaginated pits [1] that contain numerous small lipid patches enriched with cholesterol and glycosphingolipids [2], [3], [4]. Caveolae are considered to serve as platforms for dynamic association of signaling proteins and for the initiation or modulation of signaling [5], [6], [7]. The inner surface of caveolae is coated with scaffolding protein formed by members of the caveolin family (caveolin-1, -2, and -3) [2], [8]. Caveolins are highly hydrophobic proteins with a characteristic hairpin shape; caveolins are located within the plasma membrane, with both ends facing the cytoplasm. The N-terminal domain of the protein mediates homo- and hetero-oligomerization of the caveolin monomers as well as its binding to different molecules [9], [10], [11], [12]. Caveolin-1 plays a regulatory role in signaling as a direct inhibitor of a variety of plasma membrane-initiated signaling cascades including those of TGF-β, EGFR, and PKC [3], [13].

Type I collagen, the major structural component of the extracellular matrix, is a heterotrimer composed of three alpha chains encoded by the COL1A1 and COL1A2 genes [14]. Type I collagen comprises approximately 84% of the collagen synthesized by fibroblasts, and large depositions of type I collagen lead to skin and internal organ fibrosis [15]. TGF-β is known to regulate extracellular matrix (ECM) metabolism and the genesis of tissue fibrosis through overproduction of type I collagen [16], [17], [18], [19]. Several signaling pathways, including smad and ERK pathways, have been implicated in mediating TGF-β-induced extracellular matrix production and fibrosis [20], [21], [22]. However, despite recent research to understand the regulation of collagen expression, the regulatory mechanism of collagen gene expression has not been fully elucidated in human dermal fibroblasts.

The aim of this study was to investigate the role of caveolin-1 in type I procollagen expression in human dermal fibroblasts. In this study, we found that basal and TGF-β1-induced expression of type I procollagen are regulated by caveolin-1, which inhibits TGF-β1/smad signaling and activates PI-3 Kinase/Akt/mTOR pathways in human dermal fibroblasts, ultimately resulting in increased type I procollagen expression.

Section snippets

Reagents

Dulbecco's modified Eagle's medium (DMEM) and antibiotics were purchased from Life Technologies, (Rockville, MA). Fetal bovine serum (FBS) was obtained from Hyclone (Logan, UT). Rabbit polyclonal anti-p-Akt and anti-p-smad3 were purchased from Cell Signaling Technology (Beverly, MA). The mouse monoclonal anti-type I procollagen antibody, SP1.D8, was used. LY294002 was purchased from Calbiochem (San Diego, CA). Rapamycin was obtained from Biomol (Plymouth Meeting, PA).

Cell cultures

Primary human dermal

Basal expression of type I procollagen is increased by cav-1 overexpression, but decreased by cav-1 siRNA in human dermal fibroblasts

To verify the role of cav-1 in type I procollagen expression, human dermal fibroblasts were infected with adenovirus expressing either GFP (Ad-GFP) only or human cav-1 cDNA (Ad-cav-1) for 24 h and further cultured in serum-free media for 72 h. Type I procollagen and cav-1 expression were measured by Western blotting of both culture media and whole cell lysates. Our results showed that type I procollagen expression was dose-dependently increased by Ad-cav-1 (Fig. 1A). Infection of 25 and 50 MOI

Discussion

In this study, we found that cav-1 significantly increased the basal and TGF-β1-induced type I procollagen expression, even though cav-1 overexpression inhibited TGF-β1/smad signaling. Previously, it was reported that cav-1 inhibited TGF-β/smad signaling through an interaction with the TGF-β type I receptor [13]. Our results also demonstrated that TGF-β1-induced smad3 phosphorylation and TGF-β1-induced transcriptional activities were significantly prevented by cav-1 overexpression. In addition

Acknowledgement

This research was supported by a grant (R11-2002-097-06001-0) through the Center for Aging and Apoptosis Research at Seoul National University from the Korean Science & Engineering Foundation (KOSEF) and by a research agreement with Amorepacific R&D Center.

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    Present address: Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-gu, Seoul 135-710.

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