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      Value of caveolin-1 in cancer progression and prognosis: Emphasis on cancer-associated fibroblasts, human cancer cells and mechanism of caveolin-1 expression (Review)

      research-article
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      Oncology Letters
      D.A. Spandidos
      caveolin-1, cancer-associated fibroblasts, mechanisms, human cancer cells, cancer progression

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          Abstract

          Caveolin-1 (Cav-1) is found predominately in terminally differentiated cells, such as adipocytes, endothelia and smooth muscle cells, as well as type I pneumocytes. As a main structural component of caveolae, Cav-1 is important in modulating cellular signaling. In the present study, the expression and clinical role of Cav-1 were analyzed in tumor stromal and human cancer cells, respectively. The results of previous studies have shown that the downregulation of tumor stromal Cav-1 promotes tumor survival and predicts a poor tumor prognosis, predominantly concentrating on the mechanism of the metabolism of the cancer microenvironment (according to the autophagic tumor stroma model of cancer metabolism and the reverse Warburg effect). However, contradictory results concerning the expression, clinical roles and associated mechanisms of Cav-1 have been reported. An improved understanding of Cav-1 expression in tumor stromal and cancer cells will increase knowledge with regard to the clinical value of Cav-1 and its detailed mechanisms. This review summarizes the novel data concerning the clinical values and probable mechanisms of Cav-1 expression in tumor stromal (predominantly in cancer-associated fibroblasts) and cancer cells, respectively.

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          Most cited references125

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          Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing.

          Multicellular organisms initiate adaptive responses when oxygen (O(2)) availability decreases, but the underlying mechanism of O(2) sensing remains elusive. We find that functionality of complex III of the mitochondrial electron transport chain (ETC) is required for the hypoxic stabilization of HIF-1 alpha and HIF-2 alpha and that an increase in reactive oxygen species (ROS) links this complex to HIF-alpha stabilization. Using RNAi to suppress expression of the Rieske iron-sulfur protein of complex III, hypoxia-induced HIF-1 alpha stabilization is attenuated, and ROS production, measured using a novel ROS-sensitive FRET probe, is decreased. These results demonstrate that mitochondria function as O(2) sensors and signal hypoxic HIF-1 alpha and HIF-2 alpha stabilization by releasing ROS to the cytosol.
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            Caveolin, a protein component of caveolae membrane coats.

            Caveolae have been implicated in the transcytosis of macromolecules across endothelial cells and in the receptor-mediated uptake of 5-methyltetrahydrofolate. Structural studies indicate that caveolae are decorated on their cytoplasmic surface by a unique array of filaments or strands that form striated coatings. To understand how these nonclathrin-coated pits function, we performed structural analysis of the striated coat and searched for the molecular component(s) of the coat material. The coat cannot be removed by washing with high salt; however, exposure of membranes to cholesterol-binding drugs caused invaginated caveolae to flatten and the striated coat to disassemble. Antibodies directed against a 22 kd substrate for v-src tyrosine kinase in virus-transformed chick embryo fibroblasts decorated the filaments, suggesting that this molecule is a component of the coat. We have named the molecule caveolin. Caveolae represent a third type of coated membrane specialization that is involved in molecular transport.
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              Identification of fibroblast heterogeneity in the tumor microenvironment.

              Tumors are unorganized organs that contain many different cell types. In the recent years, many studies have reported that primary tumors contain fibroblasts/myofibroblasts (carcinoma-associated fibroblasts), mesenchymal cells such as pericytes/mural cells and other vascular smooth muscle cells. Several different markers are used routinely to identify carcinoma-associated fibroblasts (CAFs) such as alpha-smooth muscle actin (alpha-SMA), vimentin, S100A4 protein/fibroblast specific protein-1 (FSP1) and type I collagen. Likewise markers such as platelet derived growth factor receptor-beta (PDGFRbeta) and NG2 chondroitin sulfate proteoglycan (NG2) are used to identify mesenchymal cells such as pericytes and other vasculature associated smooth muscle cells. It is still unknown whether these markers overlap with each other or identify a unique population of cells within the tumor microenvironment. Therefore in the present study we utilized two different mouse models of cancer, the Rip1Tag2 mice that develop progressive pancreatic cancer and an orthotopic 4T1 breast cancer model, to study the overlap between six different mesenchymal markers commonly used in mouse cancer research. Our study demonstrates that among all the markers, S100A4/FSP1 identifies a unique population of fibroblasts with minimal overlap with markers for alphaSMA, PDGFRbeta and NG2. Vimentin and type I collagen are not specific markers for fibroblasts in these tumors. alphaSMA, PDGFRbeta and NG2 significantly overlap with each other in identifying a mixed population of fibroblasts (activated or resting), myofibroblasts, pericytes and vascular smooth muscle cells. Collectively, this study demonstrates that tumor microenvironment associated fibroblasts are a heterogeneous population and thus, the use of alphaSMA or vimentin as the only markers will not identify all the CAFs.
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                Author and article information

                Journal
                Oncol Lett
                Oncol Lett
                OL
                Oncology Letters
                D.A. Spandidos
                1792-1074
                1792-1082
                October 2014
                28 July 2014
                28 July 2014
                : 8
                : 4
                : 1409-1421
                Affiliations
                Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P.R. China
                Author notes
                Correspondence to: Professor Guowei Che, Department of Thoracic Surgery, West China Hospital, Sichuan University, 37 Guoxuexiang, Chengdu, Sichuan 610041, P.R. China, E-mail: guowei_che@ 123456yahoo.com
                Article
                ol-08-04-1409
                10.3892/ol.2014.2385
                4156192
                25202343
                1393ee4b-2230-40bc-96ff-99afa4b2309b
                Copyright © 2014, Spandidos Publications

                This is an open-access article licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License. The article may be redistributed, reproduced, and reused for non-commercial purposes, provided the original source is properly cited.

                History
                : 17 October 2013
                : 07 May 2014
                Categories
                Articles

                Oncology & Radiotherapy
                caveolin-1,cancer-associated fibroblasts,mechanisms,human cancer cells,cancer progression

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