Open Access

Particulate matter 2.5 regulates lipid synthesis and inflammatory cytokine production in human SZ95 sebocytes

  • Authors:
    • Qin Liu
    • Jianbo Wu
    • Jiquan Song
    • Pin Liang
    • Kaiping Zheng
    • Guifeng Xiao
    • Lanting Liu
    • Christos C. Zouboulis
    • Tiechi Lei
  • View Affiliations

  • Published online on: August 25, 2017     https://doi.org/10.3892/ijmm.2017.3109
  • Pages: 1029-1036
  • Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

A large body of evidence indicates that particulate matter (PM)2.5 is associated with various negative effects on human health. However, the impact and molecular mechanism of PM2.5 on the skin have not been elucidated. Therefore, the present study aimed to investigate the effects of two types of PM2.5 [water-soluble extracts (W-PM2.5) and non-water-soluble extracts (NW-PM2.5)] on cell proliferation, cell cycle progression, lipid synthesis, and inflammatory cytokine production of human SZ95 sebocytes. The results demonstrated that NW-PM2.5 and W-PM2.5 exposure dose-dependently inhibited SZ95 sebocyte proliferation by inducing G1 cell arrest. Furthermore, NW-PM2.5 and W-PM2.5 significantly reduced sebaceous lipid synthesis and markedly promoted the production of inflammatory cytokines, including interleukin-1α (IL-1α), IL-6 and IL-8 in SZ95 sebocytes. Additionally, the expression of aryl hydrocarbon (Ah) receptor (AhR), AhR nuclear translocator protein (ARNT), as well as cytochrome P450 1A1 were significantly increased following PM2.5 exposure. Thus, these findings indicate that PM2.5 exerts inhibitory effects on cell proliferation and lipid synthesis, and stimulatory effects on inflammatory cytokine production and AhR signaling activation in human SZ95 sebocytes.

Introduction

Increasing evidence has demonstrated the association between air pollution and sebaceous gland-associated diseases (14). Recently, studies regarding environmental pollutants indicated that dioxins inhibit lipid synthesis and induce differentiation of human sebaceous cells into keratinocytes, leading to the development of clinical chlorine acne (5). Hu et al (6) also identified that cigarette smoke extract benzo(a)pyrene regulates the synthesis of lipids and induce pro-inflammatory effects in human sebocytes, as evidenced by promoting the release of pro-inflammatory cytokines [interleukin-1α (IL-1α), IL-6 and IL-8] (6). The above-mentioned studies demonstrate that environmental pollution is closely associated with the synthesis and secretion of sebaceous glands, and potentially involved in the development of sebaceous gland-associated diseases (7).

Particulate matter (PM)2.5, also termed fine particles, were identified as PM, which are <2.5 µm in diameter (8). Due to the small particle size and specific surface area, PM2.5 easily penetrate the alveoli or even the blood, which increases the risk of human health problems (9,10). A recent study demonstrated that ambient PM2.5 increases the risk of eczema and other skin diseases (11). However, to the best of our knowledge, the effects of PM2.5 on the function of human sebaceous glands have not yet been elucidated.

The key molecular signaling pathway involved in the response of skin cells against environment pollutants is the aromatic hydrocarbon receptor (AhR) pathway (12,13). AhR, also termed dioxin receptor, is a ligand-activated transcription factor expressed in all skin cells, including keratinocytes (14), fibroblasts (15) and SZ95 sebocytes cells (16) in vitro and in human skin in vivo (17). The formation of the AhR/AhR nuclear translocator (ARNT) heterodimer activates the cytoplasmic cytochrome P4501 A1 (CYP1A1) (18,19). Furthermore, increasing evidence has highlighted that AhR is significant in cell growth, proliferation, cell cycle progression (20), cell differentiation and inflammatory responses (21) in the absence of external ligands. Recently, Kakimoto et al (22) identified that PM2.5 has the highest AhR ligand activity among all of the particle sizes, which supports the possible involvement of AhR signaling in the mechanism of PM2.5-induced skin diseases. However, whether the PM2.5 effects on SZ95 sebocytes are associated with AhR/CYP1A1 signaling remains unclear.

Therefore, the present study aimed to investigate the influences of PM2.5 on human SZ95 sebocytes, and to investigate the relevant mechanisms. The effects of water-soluble extract (W-PM2.5) and non-water-soluble extract (NW-PM2.5) exposure on cell proliferation, cell cycle progression, lipid synthesis and the inflammatory response were investigated in human SZ95 sebocytes. Furthermore, whether the AhR/CYP1A1 signaling pathway is involved in these effects was investigated.

Materials and methods

Collection and extraction of PM2.5

PM2.5 was collected by TH-150C Medium flow air total suspended particulate sampler (Wuhan TianHong Environmental Protection Industry Co., Ltd., Wuhan, China) (100 1/min) in Wuhan urban air during July 2015. The sample was set on the rooftop of a building of the Institute of Atmospheric Research, School of Environmental Studies, China University of Geosciences (Wuhan, China), ~6 m above the ground. The filter was changed every 24 h using the air total particle sampler. Subsequent to sampling, the PM2.5 filter was placed under an ultraviolet lamp for 30 min and cut into two equal size pieces. The W-PM2.5 and NW-PM2.5 were isolated and prepared as previously described (23). The samples were collected and stored at −80°C until later use.

Cell culture and exposure

Immortalized human SZ95 sebaceous gland cells, (patented cell, gifted by Professor Christos C. Zouboulis, Department of Dermatology, Venereology, Allergology and Immunology, Dessau Medical Center, Theodore Fontane Medical University of Brandenburg, Germany) at passages 30–40 were cultured at 37°C in Sebomed® basal medium (Biochrom GmbH, Berlin, Germany) supplemented with 10% fetal calf serum, Gibco 5 ng/ml human epidermal growth factor (Thermo Fisher Scientific, Inc., Waltham, MA, USA), 100 U/ml penicillin and 100 g/ml streptomycin (Gibco; Thermo Fisher Scientific, Inc.). Various concentrations (1, 10, 100 and 250 µg/ml) of PM2.5 were prepared. For the exposure, cells were exposed to a W-PM2.5 or NW-PM2.5 for 48 h.

Cell counting kit-8 (CCK-8) assay

Following exposure for 48 h, cell viability was determined using CCK-8 assay kits (C0038; Shanghai Beyotime Biotechnology Co., Ltd., Shanghai, China) according to the manufacturer's instructions. CCK-8 solution (10 µl) was added to each well, followed by an incubation for 1–4 h. Absorbance was measured using a microplate reader at a wavelength of 450 nm. The cells treated with the solvent served as a control group and wells without cells served as the blank group. Cell viability was calculated according to the following formula: cell proliferation (%) = optical density (OD) of the experimental group/OD of the control group ×100.

Cellular toxicity

SZ95 sebocytes were seeded in 96-well plates. Subsequent to exposure for 48 h, lactate dehydrogenase (LDH) activity was detected using a Pierce LDH cytotoxicity assay kit (Thermo Fisher Scientific, Inc.) according to the manufacturer's protocol.

Cell cycle assay

SZ95 sebocytes were seeded into 6-well plates. Following exposure for 48 h with different concentrations of PM2.5 suspension, cells were collected using 0.25% trypsin and phosphate-buffered saline (PBS). Also, culture was centrifuged at 300 × g for 5 min at room temperature twice. After that precooled 90% ethanol was added. Then cells were resuspended at 4°C for 20 min and centrifuged at 300 × g for 5 min at room temperature. Cells were incubated with propidium iodide (PI) buffer [50 mg/ml containing ribonuclease A (50 ng/ml)] at room temperature and stained in the dark for 20 min at room temperature. Cell cycle distribution was analyzed using a BD Biosciences Flow Cytometer (BD Biosciences, San Jose, CA, USA).

Oil Red O staining

SZ95 sebocytes were seeded in 24-well plates (5×104 cells/well). After a 48-h exposure with different concentrations of PM2.5 suspension, cells were washed with PBS and fixed in 10% neutral formaldehyde for 30 min. The cells were then washed twice in distilled water for 2 min, stained with Oil Red O dye (AS1083; Wuhan Aspen Biotechnology Co., Ltd., Wuhan, China) (0.5% Oil Red dissolved in isopropanol, then diluted with distilled water at a ratio of 6:4) at room temperature in the dark for 10 min and washed in distilled water for 1 min. Subsequently, cells were counterstained with hematoxylin, and then sealed by glycerol gelatin for long-term preservation, and observed under an inverted Olympus microscope.

Enzyme-linked immunosorbent assay (ELISA)

SZ95 sebocytes were seeded in 24-well plates (1×105 cells/well). After 48-h exposure to different concentrations of PM2.5 suspension, the supernatant was collected at 4°C, centrifuged for 20 min at 1,000 × g at 4°C, and the supernatant was collected and stored at −20°C for subsequent assays. Concentrations of IL-1α, IL-6 and IL-8 were determined using commercial ELISA kits (E-EL-H0088c, E-EL-H0102c and E-EL-H0048c; ElabScience Biotechnology Co., Ltd., Wuhan, China) according to the manufacturer's instructions.

Immunofluorescent cytochemical analysis

Immunofluorescent cytochemical analysis was performed using anti-AhR (17840-1-AP), anti-ARNT (14105-1-AP), anti-CYP1A1 (13241-1-AP) (all from Proteintech Group, Inc., Wuhan, China) and Cy3-conjugated anti-rabbit IgG antibodies (AS-1109; Wuhan Aspen Biotechnology Co., Ltd.). SZ95 sebocytes were seeded into 6-well plates. Following exposure for 48 h to various concentrations of PM2.5 suspension, coverslips were added to the plates and incubated with 5% CO2 at 37°C until cells reached 80% confluence. Media was aspirated from the plates and washed 3 times with PBS. Cells were fixed with 4% paraformaldehyde for 30 min at room temperature. We then added Triton X-100 for 10 min and hydrogen peroxide solution at room temperature in the dark for 20 min; after each step, the cells were washed 3 times with PBS for 5 min. The cell culture was incubated with primary antibody overnight at 4°C and washed 3 times for 5 min with PBS. Stained with conjugated secondary antibody for 30 min at room temperature for 50 min and washed 3 times for 5 min with PBS. Nuclear staining was then performed with DAPI. Images of each slide were obtained using an optical microscope system (Axiomager; Carl Zeiss AG, Oberkochen, Germany). The protein expression levels of AhR, ARNT and CYP1A1 were quantified with an image analysis program (Q-imaging Pro-7; Olympus, Tokyo, Japan) from the microscope system.

Western blotting

Following exposure for 48 h to various concentrations of PM2.5 suspension, the adherent cells were washed with TBS buffer for 3 times. After drying the residual liquid, protease inhibitor was added for 3 min at room temperature. The cell total protein extraction reagent was then added for 5 min at room temperature. Cells were collected to 1.5 ml centrifuge tubes and centrifuged at 10,000 × g for 5 min at 4°C. The supernatant which was the total protein solution was collected at 4°C. The concentration of the proteins was determined using a BCA protein assay kit (AS1086; Wuhan Aspen Biotechnology Co., Ltd.). Total protein samples (ensure that the total protein amount of each sample was 40 µg) were separated with 10% sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE), then transferred onto polyvinylidene fluoride membrane (EMD Millipore, Bedford, MA, USA), blocked with skimmed milk and incubated overnight at 4°C with primary antibodies against anti-AhR (dilution, 1:1,000), anti-ARNT (dilution, 1:500), CYP1A1 (dilution, 1:500) and glyceraldehyde 3-phosphate dehydrogenase (GAPDH) (dilution, 1:1,000). The membranes were incubated with the secondary antibody (horseradish peroxidase goat anti rabbit; dilution, 1:10,000) for 30 min at room temperature, and the blots were detected using an enhanced chemiluminescence kit (Cell Signaling Technology, Inc., Danvers, MA, USA). GAPDH served as an internal control.

Statistical analysis

Results are expressed as the mean ± standard error of the mean. Statistical analysis was performed using two-way ANOVA and Dunnett's post hoc test. P<0.05 was considered to indicate a statistically significant difference.

Results

PM2.5 exposure inhibits the viability of SZ95 sebocytes

To evaluate the effects of PM2.5 exposure on the viability of SZ95 sebocytes, a CCK-8 assay was performed in the present study and the results are presented in Fig. 1. PM2.5 (NW-PM2.5 and W-PM2.5) exposure for 48 h significantly induced cell viability when compared with the control cells (P<0.01) (Fig. 1A and B). No significant difference was identified between the viability of NW-PM2.5- and W-PM2.5-exposed SZ95 sebocytes (P>0.05). In addition, the toxicity of NW-PM2.5 and W-PM2.5 exposure on SZ95 sebocytes was evaluated using a Pierce LDH cytotoxicity assay kit according to the manufacturer's instructions. Compared with the control cells, NW-PM2.5 exposure (10 µg/ml, P<0.05; 100 and 250 µg/ml, P<0.01) significantly increased LDH activity in a dose-dependent manner (Fig. 1C). W-PM2.5 exhibited similar effects on SZ95 sebocytes (Fig. 1D).

PM2.5 exposure arrested the cell cycle at the G1 phase in SZ95 sebocytes

The effects of PM2.5 on the cell cycle were investigated (Fig. 2). Flow cytometry demonstrated that compared with the unexposed control cells, the number of cells in the G1 phase were markedly increased in cells exposed to NW-PM2.5 (Fig. 2A). With increasing NW-PM2.5 concentrations, the cell rates in the G1 phase also significantly increased. As illustrated in Fig. 2B, compared with the control cells, W-PM2.5 exposure markedly increased the number of cells in the G1 phase in a dose-dependent manner.

PM2.5 exposure regulated lipid synthesis in SZ95 sebocytes

As lipids secreted by sebaceous gland cells are important in the process of skin physiology involving cell structure, cohesion and desquamation as well as formation and function of a permeability barrier, the effects of PM2.5 exposure on lipid synthesis were examined in SZ95 sebocytes. Oil Red O staining indicated that NW-PM2.5 (Fig. 3A) and W-PM2.5 (Fig. 3B) at low concentrations promoted lipid synthesis, while high concentrations of NW-PM2.5 and W-PM2.5 markedly inhibited lipid synthesis in SZ95 sebocytes.

PM2.5 exposure regulated pro-inflammatory cytokine secretion in SZ95 sebocytes

Whether PM2.5 exposure regulated pro-inflammatory cytokine secretion was investigated by ELISA of pro-inflammatory cytokines (IL-1α, IL-6 and IL-8). NW-PM2.5 (Fig. 4A, C and E) and W-PM2.5 (Fig. 4B, D and F) exposure dose-dependently elevated the levels of all the evaluated pro-inflammatory cytokines that were released by SZ95 sebocytes, when compared with the unexposed control cells.

PM2.5 exposure activated AhR/CYP1A1 signaling in SZ95 sebocytes

In addition, whether AhR/CYP1A1 signaling is involved in the effect of PM2.5 exposure on SZ95 sebocytes was evaluated. Western blot analysis revealed that compared with unexposed control cells, SZ95 sebocyte exposure to NW-PM2.5 dose-dependently induced the elevation of protein expression levels of AhR, ARNT and CYP1A1. Similarly, the AhR, ARNT and CYP1A1 expression levels were reduced in the unexposed control cells, whereas the AhR, ARNT and CYP1A1 expression levels in SZ95 sebocytes were markedly increased in a dose-dependent manner by W-PM2.5 (Fig. 5).

Furthermore, immunocytochemical analysis (Fig. 6) demonstrated the localization of AhR, ARNT and CYP1A1 in PM2.5-exposed SZ95 sebocytes. Compared with unexposed control cells, significant AhR induction was observed in NW-PM2.5- (Fig. 6A) and W-PM2.5-exposed (Fig. 6B) cells. Similar to AhR, the staining for ARNT and CYP1A1 was significantly and dose-dependently increased in NW-PM2.5-exposed [ARNT (Fig. 6C); CYP1A1 (Fig. 6E)] and W-PM2.5-exposed [ARNT (Fig. 6D); CYP1A1 (Fig. 6F)] SZ95 sebocytes.

Discussion

The adverse effects of PM2.5 on respiratory diseases have been widely documented (2426). However, the effects of PM2.5 on the function of human sebaceous glands have not been fully elucidated. To the best of our knowledge, this is the first study to investigate the influence of NW-PM2.5 and W-PM2.5 exposure on human sebocytes. The present study identified that PM2.5 exposure significantly inhibits the viability of SZ95 sebocytes, inducing cell toxicity. Furthermore, a high dose of NW-PM2.5 and W-PM2.5 exposure markedly reduced lipid synthesis in SZ95 sebocytes. In addition, pro-inflammatory cytokines, including IL-1α, IL-6 and IL-8, were demonstrated to be markedly elevated in PM2.5-exposed cells, and PM2.5 exposure induced G1 arrest in SZ95 sebocytes. Finally, the key AhR signaling pathway was activated following PM2.5 exposure in SZ95 sebocytes. A previous study demonstrated the cytotoxicity of PM2.5 on human HaCaT keratinocytes (11). Our study also identified that PM2.5 significantly inhibited cell viability, inducing toxicity on SZ95 sebocytes. The effects of PM2.5 exposure on cell cycle progression are controversial, as certain studies demonstrated that PM2.5 induced G1 delay (27), while other studies found that PM2.5 arrested the cell cycle at the G2/M phase (28). In the present study, flow cytometry indicated that SZ95 sebocytes exposed to PM2.5 were arrested at the G1 phase. As G1 is the preparation phase of DNA synthesis, arresting the cell cycle at the G1 phase directly inhibits cell growth. Therefore, cell proliferation suppression induced by PM2.5 is associated with G1 arrest, and is consistent with the detected LDH increase.

Reduced lipid synthesis is associated with various diseases of the sebaceous gland, including chloracne (29,30). In the present study, lipid synthesis markedly increased at a low PM2.5 concentration, while increased PM2.5 concentrations rapidly reduced the lipid synthesis in SZ95 sebocytes. In addition to activating lipid metabolism, SZ95 sebocytes were found to contribute to the inflammatory environment by stimulating the release of pro-inflammatory cytokines, such as IL-1α, IL-6 and IL-8. The results of the present study indicated that PM2.5 dose-dependently elevated the levels of IL-1α, IL-6 and IL-8, which are involved in the initiation of the pathogenesis of various types of sebaceous gland-associated disease (31,32).

Previous studies have reported that PM2.5 (33) and extractable organic matter from PM2.5 (34,35) may activate AhR in human cell lines. Consistent with these studies, the present study found that the protein expression level of AhR, ARNT and CYP1A1 was markedly enhanced in the PM2.5-exposed SZ95 sebocytes, indicating the activation of AhR signaling following PM2.5 exposure. Additionally, it has been demonstrated that AhR negatively regulates lipid synthesis in SZ95 sebocytes (16). Thus, the activated AhR signaling by PM2.5 exposure may lead to a reduction of lipid synthesis, which is consistent with the results of the present study. It is likely that PM2.5 exposure regulates the lipid synthesis in human SZ95 sebocytes by activating AhR/ARNT/CYP1A1 signaling. However, further studies are required to clarify the molecular mechanism involved.

In conclusion, the present study investigated the influences of PM2.5 exposure on the functions of human SZ95 sebocytes. PM2.5 exposure was shown to exhibit inhibitory effects on cell proliferation, lipid synthesis, and stimulatory effects on inflammatory cytokine production and AhR signaling activation in human SZ95 sebocytes. These findings indicate that PM2.5 may increase the risk for the occurrence of sebaceous gland-associated diseases, which are dependent on inflammatory responses and lipid synthesis. While further studies are necessary to fully elucidate the molecular mechanism, the present study provides a foundation to better understand the complex interactions involved in extrinsic triggering of sebaceous gland-associated diseases.

Acknowledgments

The authors would like to thank Professor Qiang Ju, Dr Tingting Hu (Renji Hospital of Shanghai Jiao Tong University, Shanghai, China) and Dr Li Meng (Shanghai Dermatology Hospital, Shanghai, China) for their help in developing this project. The present study was supported by grants from CMA-L'OREAL China Skin/Hair Grant Funds (grant no. S2016131419) and the youth funds of Zhongnan Hospital of Wuhan University (grant no. 2015A014; Wuhan, China).

References

1 

Kim KE, Cho D and Park HJ: Air pollution and skin diseases: Adverse effects of airborne particulate matter on various skin diseases. Life Sci. 152:126–134. 2016. View Article : Google Scholar : PubMed/NCBI

2 

Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G and Seite S: Pollution and skin: From epidemiological and mechanistic studies to clinical implications. J Dermatol Sci. 76:163–168. 2014. View Article : Google Scholar : PubMed/NCBI

3 

Ju Q, Zouboulis CC and Xia L: Environmental pollution and acne: Chloracne. Dermatoendocrinol. 1:125–128. 2009. View Article : Google Scholar

4 

Ju Q and Zouboulis CC: Endocrine-disrupting chemicals and skin manifestations. Rev Endocr Metab Disord. 17:449–457. 2016. View Article : Google Scholar : PubMed/NCBI

5 

Ju Q, Fimmel S, Hinz N, Stahlmann R, Xia L and Zouboulis CC: 2,3,7,8-Tetrachlorodibenzo-p-dioxin alters sebaceous gland cell differentiation in vitro. Exp Dermatol. 20:320–325. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Hu T, Pan Z, Yu Q, Mo X, Song N, Yan M, Zouboulis CC, Xia L and Ju Q: Benzo(a)pyrene induces interleukin (IL)-6 production and reduces lipid synthesis in human SZ95 sebocytes via the aryl hydrocarbon receptor signaling pathway. Environ Toxicol Pharmacol. 43:54–60. 2016. View Article : Google Scholar : PubMed/NCBI

7 

Ju Q, Yiang K, Zouboulis CC, Ring J and Chen W: Chloracne: From clinic to research. Zhonghua Pifuke Yixue Zazhi. 30:2–6. 2012.

8 

Díaz RV and Rosa Dominguez E: Health risk by inhalation of PM2.5 in the metropolitan zone of the City of Mexico. Ecotoxicol Environ Saf. 72:866–871. 2009. View Article : Google Scholar

9 

Dockery DW: Health effects of particulate air pollution. Ann Epidemiol. 19:257–263. 2009. View Article : Google Scholar : PubMed/NCBI

10 

Weichenthal SA, Godri-Pollitt K and Villeneuve PJ: PM2.5, oxidant defence and cardiorespiratory health: A review. Environ Health. 12:402013. View Article : Google Scholar : PubMed/NCBI

11 

Li Q, Kang Z, Jiang S, Zhao J, Yan S, Xu F and Xu J: Effects of ambient fine particles PM2.5 on human HaCaT cells. Int J Environ Res Public Health. 14:E722017. View Article : Google Scholar

12 

Sugihara K, Kitamura S, Yamada T, Ohta S, Yamashita K, Yasuda M and Fujii-Kuriyama Y: Aryl hydrocarbon receptor (AhR)-mediated induction of xanthine oxidase/xanthine dehydrogenase activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Biophys Res Commun. 281:1093–1099. 2001. View Article : Google Scholar : PubMed/NCBI

13 

Hong CH, Lee CH, Yu HS and Huang SK: Benzopyrene, a major polyaromatic hydrocarbon in smoke fume, mobilizes Langerhans cells and polarizes Th2/17 responses in epicutaneous protein sensitization through the aryl hydrocarbon receptor. Int Immunopharmacol. 36:111–117. 2016. View Article : Google Scholar : PubMed/NCBI

14 

Jux B, Kadow S and Esser C: Langerhans cell maturation and contact hypersensitivity are impaired in aryl hydrocarbon receptor-null mice. J Immunol. 182:6709–6717. 2009. View Article : Google Scholar : PubMed/NCBI

15 

Cho YC, Zheng W and Jefcoate CR: Disruption of cell-cell contact maximally but transiently activates AhR-mediated transcription in 10T1/2 fibroblasts. Toxicol Appl Pharmacol. 199:220–238. 2004. View Article : Google Scholar : PubMed/NCBI

16 

Hu T, Wang D, Yu Q, Li L, Mo X, Pan Z, Zouboulis CC, Peng L, Xia L and Ju Q: Aryl hydrocarbon receptor negatively regulates lipid synthesis and involves in cell differentiation of SZ95 sebocytes in vitro. Chem Biol Interact. 258:52–58. 2016. View Article : Google Scholar : PubMed/NCBI

17 

Ju Q, Yu Q, Song N, Tan Y, Xia L and Zouboulis CC: Expression of aryl hydrocarbon receptor in human epidermis, hair follicles and sebaceous glands and its significance. Zhonghua Pifuke Zazhi. 44:761–764. 2011.

18 

Esser C, Bargen I, Weighardt H, Haarmann-Stemmann T and Krutmann J: Functions of the aryl hydrocarbon receptor in the skin. Semin Immunopathol. 35:677–691. 2013. View Article : Google Scholar : PubMed/NCBI

19 

Yu Q, Hu T, Mo X, Zhang C, Xia L, Zouboulis CC and Ju Q: Effect of tetrachlorodibenzo-p-dioxin on the expression of cytochrome P4501A1 in human SZ95 sebocytes and its significance. Zhonghua Pifuke Zazhi. 46:557–560. 2013.

20 

Kalmes M, Hennen J, Clemens J and Blömeke B: Impact of aryl hydrocarbon receptor (AhR) knockdown on cell cycle progression in human HaCaT keratinocytes. Biol Chem. 392:643–651. 2011. View Article : Google Scholar : PubMed/NCBI

21 

Tauchi M, Hida A, Negishi T, Katsuoka F, Noda S, Mimura J, Hosoya T, Yanaka A, Aburatani H, Fujii-Kuriyama Y, et al: Constitutive expression of aryl hydrocarbon receptor in keratinocytes causes inflammatory skin lesions. Mol Cell Biol. 25:9360–9368. 2005. View Article : Google Scholar : PubMed/NCBI

22 

Kakimoto K, Nagayoshi H, Konishi Y, Kajimura K, Ohura T, Nakano T, Hata M, Furuuchi M, Tang N, Hayakawa K, et al: Size distribution of chlorinated polycyclic aromatic hydrocarbons in atmospheric particles. Arch Environ Contam Toxicol. 72:58–64. 2017. View Article : Google Scholar

23 

Jeong SC, Song MK, Cho Y, Lee E and Ryu JC: Integrative analysis of mRNA and microRNA expression of a human alveolar epithelial cell(A549) exposed to water and organic-soluble extract from particulate matter (PM)2.5. Environ Toxicol. 32:302–310. 2017. View Article : Google Scholar

24 

Yang B, Chen D, Zhao H and Xiao C: The effects for PM2.5 exposure on non-small-cell lung cancer induced motility and proliferation. Springerplus. 5:20592016. View Article : Google Scholar : PubMed/NCBI

25 

Zhou Z, Liu Y, Duan F, Qin M, Wu F, Sheng W, Yang L, Liu J and He K: Transcriptomic analyses of the biological effects of airborne PM2.5 exposure on human bronchial epithelial cells. PLoS One. 10:e01382672015. View Article : Google Scholar : PubMed/NCBI

26 

Huang Q, Zhang J, Peng S, Tian M, Chen J and Shen H: Effects of water soluble PM2.5 extracts exposure on human lung epithelial cells (A549): A proteomic study. J Appl Toxicol. 34:675–687. 2014. View Article : Google Scholar

27 

Zhang J, Ghio AJ, Gao M, Wei K, Rosen GD and Upadhyay D: Ambient particulate matter induces alveolar epithelial cell cycle arrest: Role of G cyclins. FEBS Lett. 581:5315–5320. 2007. View Article : Google Scholar : PubMed/NCBI

28 

Longhin E, Holme JA, Gutzkow KB, Arlt VM, Kucab JE, Camatini M and Gualtieri M: Cell cycle alterations induced by urban PM2.5 in bronchial epithelial cells: Characterization of the process and possible mechanisms involved. Part Fibre Toxicol. 10:632013. View Article : Google Scholar : PubMed/NCBI

29 

Chen W, Obermayer-Pietsch B, Hong J-B, Melnik BC, Yamasaki O, Dessinioti C, Ju Q, Liakou AI, Al-Khuzaei S, Katsambas A, et al: Acne-associated syndromes: Models for better understanding of acne pathogenesis. J Eur Acad Dermatol Venereol. 25:637–646. 2011. View Article : Google Scholar : PubMed/NCBI

30 

Zouboulis CC, Picardo M, Ju Q, Kurokawa I, Törőcsik D, Bíró T and Schneider MR: Beyond acne: Current aspects of sebaceous gland biology and function. Rev Endocr Metab Disord. 17:319–334. 2016. View Article : Google Scholar : PubMed/NCBI

31 

Zouboulis CC, Jourdan E and Picardo M: Acne is an inflammatory disease and alterations of sebum composition initiate acne lesions. J Eur Acad Dermatol Venereol. 28:527–532. 2014. View Article : Google Scholar

32 

Ganceviciene R, Graziene V, Fimmel S and Zouboulis CC: Involvement of the corticotropin-releasing hormone system in the pathogenesis of acne vulgaris. Br J Dermatol. 160:345–352. 2009. View Article : Google Scholar

33 

Zhang H, Yao Y, Chen Y, Yue C, Chen J, Tong J, Jiang Y and Chen T: Crosstalk between AhR and wnt/β-catenin signal pathways in the cardiac developmental toxicity of PM2.5 in zebrafish embryos. Toxicology. 355–356:31–38. 2016. View Article : Google Scholar

34 

Borgie M, Ledoux F, Verdin A, Cazier F, Greige H, Shirali P, Courcot D and Dagher Z: Genotoxic and epigenotoxic effects of fine particulate matter from rural and urban sites in Lebanon on human bronchial epithelial cells. Environ Res. 136:352–362. 2015. View Article : Google Scholar

35 

Líbalová H, Krčková S, Uhlířová K, Milcová A, Schmuczerová J, Ciganek M, Kléma J, Machala M, Šrám RJ and Topinka J: Genotoxicity but not the AhR-mediated activity of PAHs is inhibited by other components of complex mixtures of ambient air pollutants. Toxicol Lett. 225:350–357. 2014. View Article : Google Scholar : PubMed/NCBI

Related Articles

Journal Cover

October-2017
Volume 40 Issue 4

Print ISSN: 1107-3756
Online ISSN:1791-244X

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
x
Spandidos Publications style
Liu Q, Wu J, Song J, Liang P, Zheng K, Xiao G, Liu L, Zouboulis CC and Lei T: Particulate matter 2.5 regulates lipid synthesis and inflammatory cytokine production in human SZ95 sebocytes. Int J Mol Med 40: 1029-1036, 2017.
APA
Liu, Q., Wu, J., Song, J., Liang, P., Zheng, K., Xiao, G. ... Lei, T. (2017). Particulate matter 2.5 regulates lipid synthesis and inflammatory cytokine production in human SZ95 sebocytes. International Journal of Molecular Medicine, 40, 1029-1036. https://doi.org/10.3892/ijmm.2017.3109
MLA
Liu, Q., Wu, J., Song, J., Liang, P., Zheng, K., Xiao, G., Liu, L., Zouboulis, C. C., Lei, T."Particulate matter 2.5 regulates lipid synthesis and inflammatory cytokine production in human SZ95 sebocytes". International Journal of Molecular Medicine 40.4 (2017): 1029-1036.
Chicago
Liu, Q., Wu, J., Song, J., Liang, P., Zheng, K., Xiao, G., Liu, L., Zouboulis, C. C., Lei, T."Particulate matter 2.5 regulates lipid synthesis and inflammatory cytokine production in human SZ95 sebocytes". International Journal of Molecular Medicine 40, no. 4 (2017): 1029-1036. https://doi.org/10.3892/ijmm.2017.3109