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Original Article Effects of Aspirin on Non-Small Cell Lung Cancer Cells Via Regulation of Angiogenesis Factors

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Original Article Effects of Aspirin on Non-Small Cell Lung Cancer Cells Via Regulation of Angiogenesis Factors Int J Clin Exp Med 2016;9(7):12729-12736 www.ijcem.com /ISSN:1940-5901/IJCEM0022044 Original Article Effects of aspirin on non-small cell lung cancer cells via regulation of angiogenesis factors Jian Zhang1, Taisheng Chi1, Pingping Yao2, Yanan Long3, Xingguang Wang4, Linben Gao5, Xianwen Gu6 Departments of 1Gastroenterology, 3Urology, 5Respiration Medicine, Haiyang Renmin Hospital, Affiliated Hospital of Qingdao University Medical College, Haiyang 265100, Shandong Province, China; 2General Medicine, Central Hosipital of Heze Development Zone, Heze 274000, Shandong Province, China; 4Department of Respiration Medi- cine, Shangdong Provincial Hospital, Jinan 250021, Shandong Province, China; 6Department of Thoracic Surgery, Linyi Tumor Hospital, Linyi 276000, Shandong Province, China Received December 16, 2015; Accepted June 8, 2016; Epub July 15, 2016; Published July 30, 2016 Abstract: Aspirin is a non-steroidal anti-inflammatory drug with many pharmacological properties. We aim to inves- tigate the effects of aspirin on the viability, migration and angiogenesis process of non-small cell lung cancer cells. MTT assay was employed to measure the viability of human non-small cell lung cancer cell line A549 cells treated with different concentrations of aspirin. The scratch wound experiment was applied for the migration of A549 cells. The anticancer activity of aspirin was then evaluated in a mouse model of A549 xenografts, to evaluate the role of antiangiogenesis of aspirin in A549 xenograft tissues, CD34 immunohistochemical staining was employed to analyze the mean vascular density. The in vivo anti-tumor effect of aspirin was compared with carboplatin, and the combination effect of aspirin and carboplatin in vivo was also detected. Western blot was used to analyze expres- sion of related protein levels. After A549 cells were treated with aspirin, the viability and migration of the cells were inhibited significantly. The levels of angiogenic factors including vascular endothelial growth factor, vascular endo- thelial growth factor receptor 2, and matrix metalloproteinase-2 were also decreased. We concluded that aspirin might be associated with tumor angiogenesis and growth in non-small cell lung cancer, and could be considered as a potential combination regimen choice for cancer chemotherapy. Keywords: Aspirin, non-small cell lung cancer, angiogenesis, carboplatin Introduction sis is suggested by animal models, in which aspirin and other NSAIDs inhibited the forma- Lung cancer is one of the leading cause of can- tion of chemically-induced lung tumors [4-7]. cer-related death worldwide characterized by Cyclooxygenase 2 (COX-2) has been implicated uncontrolled cell growth in tissues of the lung to involve in several process of carcinogenesis with approximately 1.4 million deaths world- including apoptosis resistance, angiogenesis, wide annually [1, 2]. Most primary lung cancers decreased host immunity, and enhanced inva- started in the lung are carcinomas that derive sion and metastasis, and thus COX-2 is become from epithelial cells. There are two main prima- one of the critical novel targets being studied ry types of lung cancer known as non-small cell for lung cancer therapy and chemoprevention lung cancer (NSCLC) (representing 80-85% of [8]. cases) and small cell lung cancer (SCLC) (repre- senting 15-20%) [3]. If left untreated the pri- Although the tumor-suppressive effects of mary lung carcinomas can spread beyond the NSAIDs were attributed to their ability to act as lung focal by process of metastasis and inva- COX-2 inhibitors, some effects of these agents sion into nearby tissues/organs or other parts cannot be explained by inhibition of COX-2 [9]. of the body. Acetylsalicylic acid (aspirin), with characteristic of NSAIDs, has been considered to prevent The role for nonsteroidal anti-inflammatory colorectal adenocarcinoma growth through the drugs (NSAIDs) in preventing lung carcinogene- mechanism of anti-inflammation, e.g. the inhibi- Effects of aspirin on NSCLC cells College and the Institutional Animal Care and Use Committee specifically approved this study. Cell proliferation assay A549 cells (5 × 103 per well) seeded in 96-well plates were exposed to increasing concentra- tions of aspirin (0.1-160 mM) for the indicated Figure 1. Aspirin induced cell death of A549 cells. time. The medium was then removed and the The cells were treated with different concentrations wells were washed with PBS. The 3-(4,5-dimeth- of aspirin for 48 h, and then percentage of cell sur- vival was determined using the MTT assay and de- ylthiazol-2-yl)-2,5-diphenyltetrazolium bromide noted as a percentage of untreated controls at the (MTT) assay was performed by adding 20 μl of concurrent time point. The bars indicate mean ± S.D. MTT (5 mg/ml, Sigma, USA) for 4 h. Then 150 (n=3). μL DMSO was added to dissolve the formazan precipitate before absorbance was measured at 570 nm using a THERMOmax microplate read- tion of COX-2 and NF-kappaB, and it was report- er (Molecular Devices, USA). Triplicate experi- ed that regular aspirin use may be inversely ments were performed. associated with lung cancer in women, although regular aspirin use in men is not previously Wound scratch assay proved to associate with the decreased risk of lung cancer [4, 10-12]. And there is also limiting Cells were seeded into 6-well culture dishes at factor for aspirin use characterized as gastroin- 3.0 × 105 cells/well. After cells attaching on the testinal toxicity, particularly gastrointestinal dishes and reaching about 80% confluence, a bleeding [13]. However, considering both its scratch about 1 mm width was made through benefits and risks of COX-2 inhibition, there is the culture dish with a sterile plastic 200 μl still great concern regarding the potential use micropipette tip to generate one homogeneous of aspirin and other COX-2-specific inhibitors in wound, then the peeled off cells were washed combination with other anti-cancer therapeu- twice with PBS. Cells were further incubated tics. In this study, we examined the effects of without or with 20 mM, 40 mM and 80 mM aspirin on the growth of A549 human non-small aspirin for 12 and 24 h. The wound widths were cell lung cancer cells, and the combination measured under microscope using an ocular effects of aspirin with carboplatin were also grid at each time point. Images were taken detected. using a microscope at 100 magnification (Olympus IX51, Japan). Cell migration = initial Materials and methods wound width (1 mm) -12 or 24 h wound width. Cell lines and animals The migration was represented as percentage of untreated control as 100%. The experiments The human non-small cell lung cancer cell line were repeated at least three times. A549 was purchased from American Type Culture Collection (Manassas, Virginia, USA) Western blot and cultured in RPMI-1640 medium (Gibco) 5 supplemented with 10% heat-inactivated fetal Cells (3.0 × 10 ) seeded in 6-well plates we- bovine serum (Gemini Bio-Products, USA), pen- re treated with with 20 mM, 40 mM and 80 icillin-streptomycin (100 IU/ml-100 μg/ml) and mM aspirin for 48 h. Then cells were harve- 10 mM Hepes buffer at 37°C in a humid atmo- sted and cell lysates (30 μg of protein per lane) sphere (5% CO -95% air). were fractionated by 10% SDS-PAGE. After 2 electrophoresis, proteins were electro-trans- Balb/c-nu mice (female, 6 weeks of age) were ferred onto PVDF membranes and then detect- purchased from the Animal Centre of China ed using dilutions of primary antibodies includ- Academy of Medical Sciences (Beijing, China) ing anti-VEGF (sc-152, Santa Cruz, USA), and kept under pathogen-free conditions. The anti-phospho-VEGF receptor 2 (19A10, Cell research protocol was in accordance with the Signaling Technology, USA), anti-MMP-2 (sc- institutional guidelines of Animal Care and Use 10736, Santa Cruz, USA) and anti-β-actin Committee at Qingdao University Medical (#ab6276, Abcam, Cambridge, MA, USA) which 12730 Int J Clin Exp Med 2016;9(7):12729-12736 Effects of aspirin on NSCLC cells group. Both drugs and veh- icle were given for 3 weeks totally. Immunohistochemical stain- ing for micro vessel density (MVD) CD34 is considered to be a marker of capillary endothe- lial cells, the inhibitory effe- ct of aspirin on angiogenesis in A549 xenograft tissues was evaluated by detection of CD34 immunohistochemical staining. Specifically, the for- malin-fixed paraffin-embed- ded tumor tissues were cut into slices of 4 µm thick, then deparaffinized, and dehydrat- ed by decreasing concentra- Figure 2. Inhibition of A549 cell migration by different concentrations of aspi- rin. Scratch assay was performed by plating cells in 6-well culture dish. After tions of ethanol solutions. The cells were allowed to attach and reach 80% confluence, a scratch (1 mm) sections were microwaved was made through culture dish with a sterile plastic 200 μl micropipette tip twice for 15 min at 600 W in to generate one homogeneous wound. Cells were further incubated without 10 mM citrate buffer for anti- or with aspirin for 12 h and 24 h, respectively. The wound widths were mea- gen retrieval, then endoge- sured under microscope using an ocular grid (magnification, × 100). nous peroxidase activity was blocked by incubation with 3% was used as loading control. The primary an- hydrogen peroxide in methanol for 5-10 min. tibodies were washed in 0.05% Tween-20/PBS Non-specific binding was blocked by incubating and then incubated with appropriate horserad- with 5% bovine serum albumin (BSA) at room ish peroxidase-conjugated secondary antibod- temperature for 20 min. After incubation with ies. The bound antibodies were visualized us- anti-CD34 antibody (BA0532, Boster, China) at ing an enhanced chemiluminescence reagent 4°C, the sections were washed and treated (Millipore, USA), and quantified by densitome- with biotinylated anti-immunoglobulin, washed, try using a ChemiDoc XRS + image analyzer reacted with avidin-conjugated horseradish (Bio-Rad, USA).
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