Laricitrin suppresses increased benzo(a)pyrene-induced lung tumor-associated monocyte-derived dendritic cell cancer progression

Chang,Wei‑An; Hung,Jen‑Yu; Tsai,Ying‑Ming; Hsu,Ya‑Ling; Chiang,Hung‑Hsing; Chou,Shah‑Hwa; Huang,Ming‑Shyan; Kuo,Po‑Lin

doi:10.3892/ol.2016.4153

Laricitrin suppresses increased benzo(a)pyrene-induced lung tumor-associated monocyte-derived dendritic cell cancer progression

Authors:
- Wei‑An Chang
- Jen‑Yu Hung
- Ying‑Ming Tsai
- Ya‑Ling Hsu
- Hung‑Hsing Chiang
- Shah‑Hwa Chou
- Ming‑Shyan Huang
- Po‑Lin Kuo
View Affiliations

Affiliations: Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung 807, Taiwan, R.O.C., Division of Pulmonary and Critical Care Medicine, Kaohsiung Medical University Hospital, Kaohsiung 807, Taiwan, R.O.C., Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung 807, Taiwan, R.O.C., Division of Chest Surgery, Department of Surgery, Kaohsiung Medical University Hospital, Kaohsiung 807, Taiwan, R.O.C.
Published online on: January 26, 2016 https://doi.org/10.3892/ol.2016.4153
Pages: 1783-1790

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

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

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Benzo(a)pyrene (BaP) stimulates lung cancer cells, promoting monocyte-derived dendritic cells to secrete soluble factors, including heparin binding-epidermal growth factor and C-X-C motif chemokine 5. The secretions from monocyte‑derived dendritic cells stimulate the progression of lung cancer cells, including the migration and invasion of cells. To the best of our knowledge, these secretions remain unknown, and require additional study. The present study identified that treatment with BaP‑H1395‑tumor‑associated dendritic cell‑conditioned medium had the most marked effect on cell migration and invasion. This result may be associated with the female gender, stage 2 adenocarcinoma or mutation of the proto-oncogene B‑Raf (BRAF), according to the cell line background. Laricitrin, a dietary flavonoid derivative present in grapes and red wine, suppresses certain factors and decreases the progression of lung cancer cells that are promoted by BaP in the lung cancer tumor microenvironment. The results of the present study suggest that prolonged exposure to BaP exacerbates lung cancer, particularly in female lung cancer patients with the BRAF mutation, but that laricitrin may ameliorate this effect.

View Figures

View References

1	Jemal A, Siegel R, Ward E, Hao Y, Xu J and Thun MJ: Cancer statistics, 2009. CA Cancer J Clin. 59:225–249. 2009. View Article : Google Scholar : PubMed/NCBI
2	Tsai MJ, Chang WA, Huang MS and Kuo PL: Tumor microenvironment: A new treatment target for cancer. ISRN Biochem. 2014:3519592014. View Article : Google Scholar : PubMed/NCBI
3	Hsu YL, Huang MS, Cheng DE, Hung JY, Yang CJ, Chou SH and Kuo PL: Lung tumor-associated dendritic cell-derived amphiregulin increased cancer progression. J Immunol. 187:1733–1744. 2011. View Article : Google Scholar : PubMed/NCBI
4	Kuo CH, Chen KF, Chou SH, Huang YF, Wu CY, Cheng DE, Chen YW, Yang CJ, Hung JY and Huang MS: Lung tumor-associated dendritic cell-derived resistin promoted cancer progression by increasing Wolf-Hirschhorn syndrome candidate 1/Twist pathway. Carcinogenesis. 34:2600–2609. 2013. View Article : Google Scholar : PubMed/NCBI
5	Kuo PL, Huang MS, Hung JY, Chou SH, Chiang SY, Huang YF, Yang CJ, Tsai MJ, Chang WA and Hsu YL: Synergistic effect of lung tumor-associated dendritic cell-derived HB-EGF and CXCL5 on cancer progression. Int J Cancer. 135:96–108. 2014. View Article : Google Scholar : PubMed/NCBI
6	Alexandrov K, Rojas M and Satarug S: The critical DNA damage by benzo(a)pyrene in lung tissues of smokers and approaches to preventing its formation. Toxicol Lett. 198:63–68. 2010. View Article : Google Scholar : PubMed/NCBI
7	Zuo J, Brewer DS, Arlt VM, Cooper CS and Phillips DH: Benzo pyrene-induced DNA adducts and gene expression profiles in target and non-target organs for carcinogenesis in mice. BMC Genomics. 15:8802014. View Article : Google Scholar : PubMed/NCBI
8	Wang Y, Zhai W, Wang H, Xia X and Zhang C: Benzo(a)pyrene promotes A549 cell migration and invasion through up-regulating Twist. Arch Toxicol. 89:451–458. 2015. View Article : Google Scholar : PubMed/NCBI
9	Mattivi F, Guzzon R, Vrhovsek U, Stefanini M and Velasco R: Metabolite profiling of grape: Flavonols and anthocyanins. J Agric Food Chem. 54:7692–7702. 2006. View Article : Google Scholar : PubMed/NCBI
10	Kozłowska A and Szostak-Wegierek D: Flavonoids - food sources and health benefits. Rocz Panstw Zakl Hig. 65:79–85. 2014.PubMed/NCBI
11	Wang CZ, Calway TD, Wen XD, Smith J, Yu C, Wang Y, Mehendale SR and Yuan CS: Hydrophobic flavonoids from Scutellaria baicalensis induce colorectal cancer cell apoptosis through a mitochondrial-mediated pathway. Int J Oncol. 42:1018–1026. 2013.PubMed/NCBI
12	Tsui KC, Chiang TH, Wang JS, Lin LJ, Chao WC, Chen BH and Lu JF: Flavonoids from Gynostemma pentaphyllum exhibit differential induction of cell cycle arrest in H460 and A549 cancer cells. Molecules. 19:17663–17681. 2014. View Article : Google Scholar : PubMed/NCBI
13	Castillo-Muñoz N, Gómez-Alonso S, García-Romero E and Hermosín-Gutiérrez I: Flavonol profiles of Vitis vinifera red grapes and their single-cultivar wines. J Agric Food Chem. 55:992–1002. 2007. View Article : Google Scholar : PubMed/NCBI
14	NCI-Navy Medical Oncology Branch cell line supplement. J Cell Biochem. (Suppl)24:1–291. 1996.
15	Naoki K, Chen TH, Richards WG, Sugarbaker DJ and Meyerson M: Missense mutations of the BRAF gene in human lung adenocarcinoma. Cancer Res. 62:7001–7003. 2002.PubMed/NCBI
16	Koivunen JP, Kim J, Lee J, et al: Mutations in the LKB1 tumour suppressor are frequently detected in tumours from Caucasian but not Asian lung cancer patients. Br J Cancer. 99:245–252. 2008. View Article : Google Scholar : PubMed/NCBI
17	Jala VR, Radde BN, Haribabu B and Klinge CM: Enhanced expression of G-protein coupled estrogen receptor (GPER/GPR30) in lung cancer. BMC Cancer. 12:6242012. View Article : Google Scholar : PubMed/NCBI
18	Sunaga N, Kaira K, Imai H, et al: Oncogenic KRAS-induced epiregulin overexpression contributes to aggressive phenotype and is a promising therapeutic target in non-small-cell lung cancer. Oncogene. 32:4034–4042. 2013. View Article : Google Scholar : PubMed/NCBI
19	Zhou BB, Peyton M, He B, et al: Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell. 10:39–50. 2006. View Article : Google Scholar : PubMed/NCBI
20	Tomshine JC, Severson SR, Wigle DA, Sun Z, Beleford DA, Shridhar V and Horazdovsky BF: Cell proliferation and epidermal growth factor signaling in non-small cell lung adenocarcinoma cell lines are dependent on Rin1. J Biol Chem. 284:26331–26339. 2009. View Article : Google Scholar : PubMed/NCBI
21	Zito CR, Jilaveanu LB, Anagnostou V, et al: Multi-level targeting of the phosphatidylinositol-3-kinase pathway in non-small cell lung cancer cells. PLoS One. 7:e313312012. View Article : Google Scholar : PubMed/NCBI
22	Khode R, Larsen DA, Culbreath BC, et al: Comparative study of epidermal growth factor receptor mutation analysis on cytology smears and surgical pathology specimens from primary and metastatic lung carcinomas. Cancer Cytopathol. 121:361–369. 2013. View Article : Google Scholar : PubMed/NCBI
23	Uchiyama M, Usami N, Kondo M, et al: Loss of heterozygosity of chromosome 12p does not correlate with KRAS mutation in non-small cell lung cancer. Int J Cancer. 107:962–969. 2003. View Article : Google Scholar : PubMed/NCBI
24	Futreal PA, Wooster R and Stratton MR: Somatic mutations in human cancer: Insights from resequencing the protein kinase gene family. Cold Spring Harb Symp Quant Biol. 70:43–49. 2005. View Article : Google Scholar : PubMed/NCBI
25	Medina PP, Romero OA, Kohno T, et al: Frequent BRG1/SMARCA4-inactivating mutations in human lung cancer cell lines. Hum Mutat. 29:617–622. 2008. View Article : Google Scholar : PubMed/NCBI
26	Sordella R, Bell DW, Haber DA and Settleman J: Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science. 305:1163–1167. 2004. View Article : Google Scholar : PubMed/NCBI
27	Kobayashi S, Boggon TJ, Dayaram T, et al: EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 352:786–792. 2005. View Article : Google Scholar : PubMed/NCBI
28	Shibata T, Hanada S, Kokubu A, et al: Gene expression profiling of epidermal growth factor receptor/KRAS pathway activation in lung adenocarcinoma. Cancer Sci. 98:985–991. 2007. View Article : Google Scholar : PubMed/NCBI
29	Sharma R, Haque AK, Awasthi S, Singh SV, Piper JT and Awasthi YC: Differential carcinogenicity of benzo[a]pyrene in male and female CD-1 mouse lung. J Toxicol Environ Health. 52:45–62. 1997. View Article : Google Scholar : PubMed/NCBI
30	Paik PK, Arcila ME, Fara M, et al: Clinical characteristics of patients with lung adenocarcinomas harboring BRAF mutations. J Clin Oncol. 29:2046–2051. 2011. View Article : Google Scholar : PubMed/NCBI
31	Ji H, Wang Z, Perera SA, et al: Mutations in BRAF and KRAS converge on activation of the mitogen-activated protein kinase pathway in lung cancer mouse models. Cancer Res. 67:4933–4939. 2007. View Article : Google Scholar : PubMed/NCBI
32	Tang X, Shigematsu H, Bekele BN, Roth JA, Minna JD, Hong WK, Gazdar AF and Wistuba II: EGFR tyrosine kinase domain mutations are detected in histologically normal respiratory epithelium in lung cancer patients. Cancer Res. 65:7568–7572. 2005.PubMed/NCBI
33	Hu H, Pan Y, Li Y, Wang L, Wang R, Zhang Y, Li H, Ye T, Zhang Y, Luo X, et al: Oncogenic mutations are associated with histological subtypes but do not have an independent prognostic value in lung adenocarcinoma. Onco Targets Ther. 7:1423–1437. 2014. View Article : Google Scholar : PubMed/NCBI
34	Bonanno L, Schiavon M, Nardo G, Bertorelle R, Bonaldi L, Galligioni A, Indraccolo S, Pasello G, Rea F and Favaretto A: Prognostic and predictive implications of EGFR mutations, EGFR copy number and KRAS mutations in advanced stage lung adenocarcinoma. Anticancer Res. 30:5121–5128. 2010.PubMed/NCBI
35	Marchetti A, Felicioni L, Malatesta S, et al: Clinical features and outcome of patients with non-small-cell lung cancer harboring BRAF mutations. J Clin Oncol. 29:3574–3579. 2011. View Article : Google Scholar : PubMed/NCBI
36	Froudarakis ME: Pleural effusion in lung cancer: more questions than answers. Respiration. 83:367–376. 2012. View Article : Google Scholar : PubMed/NCBI