Proteomic analysis of serum deprivation in tongue squamous cell carcinoma

Zhang,Junfeng; Dong,Wei; Meng,Yufen; Jiang,Miao; Zhan,Zhen

doi:10.3892/mmr.2017.7807

Proteomic analysis of serum deprivation in tongue squamous cell carcinoma

Authors:
- Junfeng Zhang
- Wei Dong
- Yufen Meng
- Miao Jiang
- Zhen Zhan
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Affiliations: Discipline of Chinese and Western Integrative Medicine, School of Medicine and Life Sciences, Nanjing University of Chinese Medicine, Nanjing, Jiangsu 210023, P.R. China, College of Chinese Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu 210023, P.R. China
Published online on: October 17, 2017 https://doi.org/10.3892/mmr.2017.7807
Pages: 9323-9330
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The occurrence of tongue squamous cell carcinoma (TSCC) is closely correlated with serum components; however, the detailed mechanism remains to be fully elucidated. Proteomic analysis contributed to the discovery of potential biomarkers and provided an insight into TSCC at a molecular level. The present study investigated the effect of serum deprivation on the Tca‑8113 TSCC cell line through protein profiling using two‑dimensional gel electrophoresis and mass spectrometry, with the aim of improving TSCC diagnosis. The results showed that the Tca‑8113 cells maintained proliferative capacity and resisted apoptosis following serum deprivation. A total of 43 proteins were upregulated and 45 were downregulated following serum deprivation for 24 h, compared with untreated controls (0 h). The upregulated caspase-7, heat shock protein 27 and Annexin A1, and the downregulated peroxiredoxin‑6 and heat shock protein 70, were selected for verification using reverse transcription‑polymerase chain reaction analysis following serum deprivation for 16 h. The results indicated that reactive oxygen species may be important in serum deprivation‑induced oxidative stress.

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1	Ching CT, Sun TP, Huang SH, Hsiao CS, Chang CH, Huang SY, Chen YJ, Cheng CS, Shieh HL and Chen CY: A preliminary study of the use of bioimpedance in the screening of squamous tongue cancer. Int J Nanomed. 5:213–220. 2010. View Article : Google Scholar
2	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
3	Layland MK, Sessions DG and Lenox J: The influence of lymph node metastasis in the treatment of squamous cell carcinoma of the oral cavity, oropharynx, larynx, and hypopharynx: N0 versus N+. Laryngoscope. 115:629–639. 2005. View Article : Google Scholar : PubMed/NCBI
4	Korostoff A, Reder L, Masood R and Sinha UK: The role of salivary cytokine biomarkers in tongue cancer invasion and mortality. Oral Oncol. 4:282–287. 2011. View Article : Google Scholar
5	Faratzis G, Tsiambas E, Rapidis AD, Machaira A, Xiromeritis K and Patsouris E: VEGF and ki 67 expression in squamous cell carcinoma of the tongue: An immunohistochemical and computerized image analysis study. Oral Oncol. 45:584–588. 2009. View Article : Google Scholar : PubMed/NCBI
6	Patel RS, Clark JR, Dirven R, Wyten R, Gao K and O'Brien CJ: Prognostic factors in the surgical treatment of patients with oral carcinoma. Anz J Surg. 79:19–22. 2009. View Article : Google Scholar : PubMed/NCBI
7	Lee SB, Kim JJ, Kim TW, Kim BS, Lee MS and Yoo YD: Serum deprivation-induced reactive oxygen species production is mediated by Romo1. Apoptosis. 15:204–218. 2010. View Article : Google Scholar : PubMed/NCBI
8	Grossman N, Binyamin LA and Bodner L: Effect of rat salivary glands extracts on the proliferation of cultured skin cells-a wound healing model. Cell Tissue Bank. 4:205–212. 2004. View Article : Google Scholar
9	De Giuseppe R, Cossellu G, Vigna L, Dicorato F, De Vita C, Venturelli G, Bamonti F, Maiavacca R and Farronato G: Correlation between salivary and serum oxidized LDL levels: A pilot study on overweight/obese subjects. J Oral Pathol Med. 44:884–887. 2015. View Article : Google Scholar : PubMed/NCBI
10	Hayes LD, Sculthorpe N, Herbert P, Baker JS, Hullin DA, Kilduff LP and Grace FM: Poor levels of agreement between serum and saliva testosterone measurement following exercise training in aging men. Aging Male. 18:67–70. 2015. View Article : Google Scholar : PubMed/NCBI
11	Seethalakshmi C, Koteeswaran D and Chiranjeevi V: Correlation of serum and salivary biochemical parameters in end stage renal disease patients undergoing hemodialysis in pre and post-dialysis state. J Clin Diagn Res. 12:CC12–CC14. 2014.
12	Boraldi F, Annovi G, Paolinelli-Devincenzi C, Tiozzo R and Quaglino D: The effect of serum withdrawal on the protein profile of quiescent human dermal fibroblasts in primary cell culture. Proteomics. 8:66–82. 2008. View Article : Google Scholar : PubMed/NCBI
13	Li WZ, Wang XY, Li ZG, Zhang JH and Ding YQ: Celecoxib enhances the inhibitory effect of cisplatin on Tca8113 cells in human tongue squamous cell carcinoma in vivo and in vitro. J Oral Pathol Med. 7:579–584. 2010.
14	Wu J, Wang F, Gong Y, Li D, Sha J, Huang X and Han X: Proteomic analysis of changes induced by nonylphenol in Sprague-Dawley rat Sertoli cells. Chem Res Toxicol. 22:668–675. 2009. View Article : Google Scholar : PubMed/NCBI
15	Cheuk BL and Cheng SW: Annexin A1 expression in atherosclerotic carotid plaques and its relationship with plaque characteristics. Eur J Vasc Endovasc Surg. 41:364–371. 2011. View Article : Google Scholar : PubMed/NCBI
16	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
17	Yuan F, Cheng Q, Li G and Tong T: Nucleostemin knockdown sensitizes hepatocellular carcinoma cells to ultraviolet and serum starvation-induced apoptosis. PLoS One. 10:e01416782015. View Article : Google Scholar : PubMed/NCBI
18	Takeda K, Akagi S, Takahashi S, Onishi A, Hanada H and Pinkert CA: Mitochondrial activity in response to serum starvation in bovine (Bos taurus) cell culture. Cloning Stem Cells. 4:223–229. 2002. View Article : Google Scholar : PubMed/NCBI
19	Liu J and Du L: PERK pathway is involved in oxygen-glucose-serum deprivation-induced NF-kB activation via ROS generation in spinal cord astrocytes. Biochem Biophys Res Commun. 467:197–203. 2015. View Article : Google Scholar : PubMed/NCBI
20	Gerrits EG, Alkhalaf A, Landman GW, van Hateren KJ, Groenier KH, Struck J, Schulte J, Gans RO, Bakker SJ, Kleefstra N and Bilo HJ: Serum peroxiredoxin 4: A marker of oxidative stress associated with mortality in type 2 diabetes (ZODIAC-28). PLoS One. 2:e897192014. View Article : Google Scholar
21	Ding Y, Yamada S, Wang KY, Shimajiri S, Guo X, Tanimoto A, Murata Y, Kitajima S, Watanabe T, Izumi H, et al: Overexpression of peroxiredoxin 4 protects against high-dose streptozotocin-induced diabetes by suppressing oxidative stress and cytokines in transgenic mice. Antioxid Redox Signal. 13:1477–1490. 2010. View Article : Google Scholar : PubMed/NCBI
22	Manta B, Hugo M, Ortiz C, Ferrer-Sueta G, Trujillo M and Denicola A: The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch Biochem Biophys. 484:146–154. 2009. View Article : Google Scholar : PubMed/NCBI
23	Martinez A, Peluffo G, Petruk AA, Hugo M, Piñeyro D, Demicheli V, Moreno DM, Lima A, Batthyány C, Durán R, et al: Structural and molecular basis of the peroxynitrite-mediated nitration and inactivation of trypanosoma cruzi iron-superoxide dismutases (Fe-SODs) A and B: Disparate susceptibilities due to the repair of Tyr35 radical by Cys83 in Fe-SODB through intramolecular electron transfer. J Biol Chem. 289:12760–12778. 2014. View Article : Google Scholar : PubMed/NCBI
24	Cerda MB, Lloyd R, Batalla M, Giannoni F, Casal M and Policastro L: Silencing peroxiredoxin-2 sensitizes human colorectal cancer cells to ionizing radiation and oxaliplatin. Cancer Lett. 388:312–319. 2017. View Article : Google Scholar : PubMed/NCBI
25	Rostila A, Puustinen A, Toljamo T, Vuopala K, Lindström I, Nyman TA, Oksa P, Vehmas T and Anttila SL: Peroxiredoxins and tropomyosins as plasma biomarkers for lung cancer and asbestos exposure. Lung Cancer. 77:450–459. 2012. View Article : Google Scholar : PubMed/NCBI
26	Shiota M, Yokomizo A, Kashiwagi E, Takeuchi A, Fujimoto N, Uchiumi T and Naito S: Peroxiredoxin 2 in the nucleus and cytoplasm distinctly regulates androgen receptor activity in prostate cancer cells. Free Radic Biol Med. 51:78–87. 2011. View Article : Google Scholar : PubMed/NCBI
27	Zhang B, Wang Y and Su Y: Peroxiredoxins, a novel target in cancer radiotherapy. Cancer Lett. 286:154–160. 2009. View Article : Google Scholar : PubMed/NCBI
28	Kwon T, Jin KR, Lee JC, Park YH, Shin HJ, Cho S, Kang YK, Kim BY, Yoon DY and Yu DY: An important role for peroxiredoxin II in survival of A549 lung cancer cells resistant to gefitinib. Exp Mol Med. 47:e1652015. View Article : Google Scholar : PubMed/NCBI
29	Sobral-Leite M, Wesseling J, Smit VT, Nevanlinna H, van Miltenburg MH, Sanders J, Hofland I, Blows FM, Coulson P and Patrycja G: Annexin A1 expression in a pooled breast cancer series: association with tumor subtypes and prognosis. BMC Med. 13:1562015. View Article : Google Scholar : PubMed/NCBI
30	Lin CY, Jeng YM, Chou HY, Hsu HC, Yuan RH, Chiang CP and Kuo MY: Nuclear localization of annexin A1 is a prognostic factor in oral squamous cell carcinoma. J Surg Oncol. 97:544–550. 2008. View Article : Google Scholar : PubMed/NCBI
31	Faria PC, Sena AA, Nascimento R, Carvalho WJ, Loyola AM, Silva SJ, Durighetto AF, Oliveira AD, Oliani SM and Goulart LR: Expression of annexin A1 mRNA in peripheral blood from oral squamous cell carcinoma patients. Oral Oncol. 46:25–30. 2010. View Article : Google Scholar : PubMed/NCBI
32	Vago JP, Nogueira CR, Tavares LP, Soriani FM, Lopes F, Russo RC, Pinho V, Teixeira MM and Sousa LP: Annexin A1 modulates natural and glucocorticoid-induced resolution of inflammation by enhancing neutrophil apoptosis. J Leukoc Biol. 92:249–258. 2012. View Article : Google Scholar : PubMed/NCBI
33	Kang JH, Li M, Chen X and Yin XM: Proteomics analysis of starved cells revealed Annexin A1 as an important regulator of autophagic degradation. Biochem Biophys Res Commun. 407:581–586. 2011. View Article : Google Scholar : PubMed/NCBI
34	Yi B, Jing Z, Wang G, Qian G and Lu K: Annexin A1 protein regulates the expression of PMVEC cytoskeletal proteins in CBDL rat serum-induced pulmonary microvascular remodeling. J Transl Med. 11:982013. View Article : Google Scholar : PubMed/NCBI
35	Thorburn A: Apoptosis and autophagy: Regulatory connections between two supposedly different processes. Apoptosis. 1:1–9. 2008. View Article : Google Scholar
36	Levine B and Kroemer G: Autophagy in the pathogenesis of disease. Cell. 132:27–42. 2008. View Article : Google Scholar : PubMed/NCBI
37	PLOS ONE Staff, . Correction: Association of genetic markers in the BCL-2 family of apoptosis-related genes with endometrial cancer risk in a Chinese population. PLoS One. 10:e01176322015. View Article : Google Scholar : PubMed/NCBI
38	Coutinho-Camillo CM and Soares FA: CASP7 (caspase 7, apoptosis-related cysteine peptidase). Atlas Genetics Cytogenetics Oncology Haematology. 3:160–163. 2015.
39	Brentnall M, Rodriguez-Menocal L, Guevara RL, Cepero E and Boise LH: Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol. 14:322013. View Article : Google Scholar : PubMed/NCBI
40	Multhoff G, Pockley AG, Schmid TE and Schilling D: The role of heat shock protein 70 (Hsp70) in radiation-induced immunomodulation. Cancer Lett. 368:179–184. 2015. View Article : Google Scholar : PubMed/NCBI
41	Yang G, Ziesch A, Hocke S, Kampmann E, Ochs S, De Toni EN, Göke B and Gallmeier E: Overexpression of heat shock protein 27 (HSP27) increases gemcitabine sensitivity in pancreatic cancer cells through S-phase arrest and apoptosis. J Cell Mol Med. 2:340–350. 2015.
42	Zhang NN, Sheng SH, Chen D, et al: Expression and significance of HSP27 in tongue squamous cell carcinoma. Beijing J Stomatol. 3:146–148. 2010.