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      Cecropia obtusa extract and chlorogenic acid exhibit anti aging effect in human fibroblasts and keratinocytes cells exposed to UV radiation

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          Abstract

          Cecropia obtusa is popularly used in the Amazonian region and exhibits antioxidant activity. Cosmetic formulations containing C. obtusa extract are commercially available for purchase; however, the chemical composition and the effects of the topical application of the extract are not described in the literature. Therefore, this study aimed to identify the main components of C. obtusa for the first time and to assess the anti aging effect in human fibroblasts and keratinocytes exposed to UVR. The main components in C. obtusa extract were identified by LC-DAD-MS/MS as chlorogenic acid (CGA), luteolin-C-hexoside, luteolin-C-hexose-O-deoxy-hexose, and apigenin-C-hexose-O-deoxy-hexose. C. obtusa extract and CGA decreased the metalloproteinase-1 and protein carbonyl levels and increased the collagen and hyaluronic acid contents. Overall, the extract exhibited better activity than CGA, and we demonstrated the ability of the extract to protect against the UV-induced increase in the pro inflammatory cytokines IL-1β and IL-6, which are potential pathways of the antioxidant and anti aging effect. The chemical characterization added important data to broaden the knowledge related to C. obtusa, and the results suggest that the extract is a promising candidate to be incorporated in topical photochemoprotective formulations.

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          Most cited references28

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          Distribution and Biological Activities of the Flavonoid Luteolin

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            Mechanisms of Photoaging and Cutaneous Photocarcinogenesis, and Photoprotective Strategies with Phytochemicals

            Photoaging and photocarcinogenesis are primarily due to solar ultraviolet (UV) radiation, which alters DNA, cellular antioxidant balance, signal transduction pathways, immunology, and the extracellular matrix (ECM). The DNA alterations include UV radiation induced thymine-thymine dimers and loss of tumor suppressor gene p53. UV radiation reduces cellular antioxidant status by generating reactive oxygen species (ROS), and the resultant oxidative stress alters signal transduction pathways such as the mitogen-activated protein kinase (MAPK), the nuclear factor-kappa beta (NF-κB)/p65, the janus kinase (JAK), signal transduction and activation of transcription (STAT) and the nuclear factor erythroid 2-related factor 2 (Nrf2). UV radiation induces pro-inflammatory genes and causes immunosuppression by depleting the number and activity of the epidermal Langerhans cells. Further, UV radiation remodels the ECM by increasing matrixmetalloproteinases (MMP) and reducing structural collagen and elastin. The photoprotective strategies to prevent/treat photoaging and photocarcinogenesis include oral or topical agents that act as sunscreens or counteract the effects of UV radiation on DNA, cellular antioxidant balance, signal transduction pathways, immunology and the ECM. Many of these agents are phytochemical derivatives and include polyphenols and non-polyphenols. The flavonoids are polyphenols and include catechins, isoflavones, proanthocyanidins, and anthocyanins, whereas the non-flavonoids comprise mono phenolic acids and stilbenes. The natural sources of polyphenols include tea, cocoa, grape/wine, soy, pomegranate, and Polypodium leucotomos. The non-phenolic phytochemicals include carotenoids, caffeine and sulphoraphance (SFN). In addition, there are other phytochemical derivatives or whole extracts such as baicalin, flavangenol, raspberry extract, and Photomorphe umbellata with photoprotective activity against UVB radiation, and thereby carcinogenesis.
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              Inhibition of activator protein-1, NF-kappaB, and MAPKs and induction of phase 2 detoxifying enzyme activity by chlorogenic acid.

              Chlorogenic acid, the ester of caffeic acid with quinic acid, is one of the most abundant polyphenols in the human diet. The antioxidant and anticarcinogenic properties of chlorogenic acid have been established in animal studies. However, little is known about the molecular mechanisms through which chlorogenic acid inhibits carcinogenesis. In this study, we found that chlorogenic acid inhibited the proliferation of A549 human cancer cells in vitro. The results of the soft agar assay indicated that chlorogenic acid suppressed 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced neoplastic transformation of JB6 P+ cells in a dose-dependent manner. Pretreatment of JB6 cells with chlorogenic acid blocked UVB- or TPA-induced transactivation of AP-1 and NF-kappaB over the same dose range. At low concentrations, chlorogenic acid decreased the phosphorylation of c-Jun NH2-terminal kinases, p38 kinase, and MAPK kinase 4 induced by UVB/12-O-tetradecanoylphorbol-13-acetate, yet higher doses were required to inhibit extracellular signal-regulated kinases. Chlorogenic acid also increased the enzymatic activities of glutathione S-transferases (GST) and NAD(P)H: quinone oxidoreductase. Further studies indicated that chlorogenic acid could stimulate the nuclear translocation of Nrf2 (NF-E2-related factor) as well as subsequent induction of GSTA1 antioxidant response element (ARE)-mediated GST activity. The phosphatidylinositol 3-kinase pathway might be involved in the activation of Nrf2 translocation. These results provide the first evidence that chlorogenic acid could protect against environmental carcinogen-induced carcinogenesis and suggest that the chemopreventive effects of chlorogenic acid may be through its up-regulation of cellular antioxidant enzymes and suppression of ROS-mediated NF-kappaB, AP-1, and MAPK activation.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Methodology
                Role: MethodologyRole: Writing – review & editing
                Role: Supervision
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 May 2019
                2019
                : 14
                : 5
                : e0216501
                Affiliations
                [1 ] Department of Pharmaceutical Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo, Brazil
                [2 ] Centre for Valorization of Amazonian Bioactive Compounds (CVACBA), Federal University of Pará, Belém, Pará, Brazil
                [3 ] Tokyo University of Technology, Tokyo, Japan
                National Institutes of Health, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-6735-8184
                Article
                PONE-D-19-03466
                10.1371/journal.pone.0216501
                6505949
                31067277
                faac5670-54e6-4915-bb11-db02b55dfa9b
                © 2019 Alves et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 February 2019
                : 22 April 2019
                Page count
                Figures: 4, Tables: 1, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 140091/2013-0
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Funded by: Fundo Amazônia (BNDS)
                Funded by: Brazilian Genetic Heritage Management Council
                Award ID: CGEN- License 010526/2015-3
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award ID: 001
                Award Recipient :
                This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award Number: 140091/2013-0 Recipient: Geórgia de Assis Dias Alves), Fundação de Amparo à Pesquisa do Estado de São Paulo Fundo Amazônia (BNDS), Brazilian Genetic Heritage Management Council (Award number: CGEN License 010526/2015-3), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Award Number: 001, Recipient: Geórgia de Assis Dias Alves, Ph.D). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Proteins
                Collagens
                Biology and Life Sciences
                Biochemistry
                Antioxidants
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Connective Tissue Cells
                Fibroblasts
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Connective Tissue Cells
                Fibroblasts
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Connective Tissue Cells
                Fibroblasts
                Medicine and Health Sciences
                Dermatology
                Photodermatology and Skin Aging
                Research and Analysis Methods
                Extraction Techniques
                Protein Extraction
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Epithelial Cells
                Keratinocytes
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Epithelium
                Epithelial Cells
                Keratinocytes
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Epithelium
                Epithelial Cells
                Keratinocytes
                Biology and Life Sciences
                Immunology
                Immune Response
                Inflammation
                Medicine and Health Sciences
                Immunology
                Immune Response
                Inflammation
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Inflammation
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Inflammation
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Light
                Ultraviolet Radiation
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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