Upregulation of BIRC5 plays essential role in esophageal squamous cell carcinoma

Zu-Xuan Chen; Guo-Sheng Li; Li-Hua Yang; He-Chuan Liu; Guang-Mei Qin; Lang Shen; Wei-Ying He; Ting-Qing Gan; Jian-Jun Li; Zu-Xuan Chen; Guo-Sheng Li; Li-Hua Yang; He-Chuan Liu; Guang-Mei Qin; Lang Shen; Wei-Ying He; Ting-Qing Gan; Jian-Jun Li

doi:10.3934/mbe.2021345

Mathematical Biosciences and Engineering

2021, Volume 18, Issue 5: 6941-6960. doi: 10.3934/mbe.2021345

Previous Article Next Article

Research article

Upregulation of BIRC5 plays essential role in esophageal squamous cell carcinoma

1.
Department of Medical Oncology, Second Affiliated Hospital of Guangxi Medical University, 166 DaxueXi Road, Nanning, Guangxi Zhuang Autonomous Region, 530021, P. R. China
2.
Department of Medical Oncology, First Affiliated Hospital of Guangxi Medical University, 6 Shuangyong Road, Nanning, Guangxi Zhuang Autonomous Region, 530021, P. R. China
3.
Department of General Surgery, Second Affiliated Hospital of Guangxi Medical University, 166 DaxueXi Road, Nanning, Guangxi Zhuang Autonomous Region, 530021, P. R. China
^#Contributed equally as co-first authors; ^*Contributed equally as co-corresponding authors

Received: 14 June 2021 Accepted: 30 July 2021 Published: 20 August 2021

Background
Esophageal squamous cell carcinoma (ESCC) is one of the most common cancers in the world, the detection and prognosis of which are still unsatisfactory. Thus, it is essential to explore the factors that may identify ESCC and evaluate the prognosis of ESCC patients.
Results
Both protein and mRNA expression levels of BIRC5 are upregulated in ESCC group rather than non-ESCC group (standardized mean difference > 0). BIRC5 mRNA expression is related to the age, tumor location, lymph node stage and clinical stage of ESCC patients (p < 0.05). BIRC5 expression makes it feasible to distinguish ESCC from non-ESCC (area under the curve > 0.9), and its high expression is related to poor prognosis of ESCC patients (restrictive survival time difference = -0.036, p < 0.05). BIRC5 may play an important role in ESCC by influencing the cell cycle pathway, and CDK1, MAD2L and CDC20 may be the hub genes of this pathway. The transcription factors-MAZ and TFPD1 -are likely to regulate the transcription of BIRC5, which may be one of the factors for the high expression of BIRC5 in ESCC.
Conclusions
The current study shows that upregulation of BIRC5 may have essential clinical value in ESCC, and contributes to the understanding of the pathogenesis of ESCC.
- esophageal squamous cell carcinoma,
- baculoviral inhibitor of apoptosis repeat containing 5,
- microarray,
- RNA sequencing,
- prognosis
Citation: Zu-Xuan Chen, Guo-Sheng Li, Li-Hua Yang, He-Chuan Liu, Guang-Mei Qin, Lang Shen, Wei-Ying He, Ting-Qing Gan, Jian-Jun Li. Upregulation of BIRC5 plays essential role in esophageal squamous cell carcinoma[J]. Mathematical Biosciences and Engineering, 2021, 18(5): 6941-6960. doi: 10.3934/mbe.2021345

Related Papers:

Abstract

Background

Esophageal squamous cell carcinoma (ESCC) is one of the most common cancers in the world, the detection and prognosis of which are still unsatisfactory. Thus, it is essential to explore the factors that may identify ESCC and evaluate the prognosis of ESCC patients.

Results

Both protein and mRNA expression levels of BIRC5 are upregulated in ESCC group rather than non-ESCC group (standardized mean difference > 0). BIRC5 mRNA expression is related to the age, tumor location, lymph node stage and clinical stage of ESCC patients (p < 0.05). BIRC5 expression makes it feasible to distinguish ESCC from non-ESCC (area under the curve > 0.9), and its high expression is related to poor prognosis of ESCC patients (restrictive survival time difference = -0.036, p < 0.05). BIRC5 may play an important role in ESCC by influencing the cell cycle pathway, and CDK1, MAD2L and CDC20 may be the hub genes of this pathway. The transcription factors-MAZ and TFPD1 -are likely to regulate the transcription of BIRC5, which may be one of the factors for the high expression of BIRC5 in ESCC.

Conclusions

The current study shows that upregulation of BIRC5 may have essential clinical value in ESCC, and contributes to the understanding of the pathogenesis of ESCC.

References

[1]	M. J. Domper Arnal, A. Ferrandez Arenas, A. Lanas Arbeloa, Esophageal cancer: Risk factors, screening and endoscopic treatment in Western and Eastern countries, World J. Gastroenterol., 21 (2015), 7933-7943. doi: 10.3748/wjg.v21.i26.7933
[2]	F. Kamangar, G. M. Dores, W. F. Anderson, Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world, J. Clin. Onco.l, 24 (2006), 2137-2150. doi: 10.1200/JCO.2005.05.2308
[3]	J. Ferlay, I. Soerjomataram, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, et al., Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012, Int. J. Cancer, 136 (2015), E359-386. doi: 10.1002/ijc.29210
[4]	P. C. Enzinger, R. J. Mayer, Esophageal cancer, N Engl. J. Med., 349 (2003), 2241-2252. doi: 10.1056/NEJMra035010
[5]	A. Hesari, M. Azizian, A. Sheikhi, A. Nesaei, S. Sanaei, N. Mahinparvar, et al., Chemopreventive and therapeutic potential of curcumin in esophageal cancer: Current and future status, Int. J. Cancer, 144 (2019), 1215-1226. doi: 10.1002/ijc.31947
[6]	M. Watanabe, Y. Tachimori, T. Oyama, Y. Toh, H. Matsubara, M. Ueno, et al., Comprehensive registry of esophageal cancer in Japan, 2013, Esophagus, 18 (2021), 1-24. doi: 10.1007/s10388-020-00785-y
[7]	M. di Pietro, M. I. Canto, R. C. Fitzgerald, Endoscopic management of early adenocarcinoma and squamous cell carcinoma of the esophagus: Screening, diagnosis, and therapy, Gastroenterology, 154 (2018), 421-436. doi: 10.1053/j.gastro.2017.07.041
[8]	S. W. Chen, H. F. Zhou, H. J. Zhang, R. Q. He, Z. G. Huang, Y. W. Dang, et al., The clinical significance and potential molecular mechanism of PTTG1 in esophageal squamous cell carcinoma, Front. Genet., 11 (2020), 583085.
[9]	E. O. Then, M. Lopez, S. Saleem, V. Gayam, T. Sunkara, A. Culliford, et al., Esophageal cancer: An updated surveillance epidemiology and end results database analysis, World J. Oncol., 11 (2020), 55-64. doi: 10.14740/wjon1254
[10]	C. C. Abnet, M. Arnold, W. Q. Wei, Epidemiology of esophageal squamous cell carcinoma, Gastroenterology, 154 (2018), 360-373. doi: 10.1053/j.gastro.2017.08.023
[11]	M. Recalde, V. Davila-Batista, Y. Diaz, M. Leitzmann, I. Romieu, H. Freisling, et al., Body mass index and waist circumference in relation to the risk of 26 types of cancer: A prospective cohort study of 3.5 million adults in Spain, BMC Med., 19 (2021), 10. doi: 10.1186/s12916-020-01877-3
[12]	Z. W. Reichenbach, M. G. Murray, R. Saxena, D. Farkas, E. G. Karassik, A. Klochkova, et al., Clinical and translational advances in esophageal squamous cell carcinoma, Adv. Cancer Res., 144 (2019), 95-135. doi: 10.1016/bs.acr.2019.05.004
[13]	W. Cao, H. Lee, W. Wu, A. Zaman, S. McCorkle, M. Yan, et al., Multi-faceted epigenetic dysregulation of gene expression promotes esophageal squamous cell carcinoma, Nat. Commun., 11 (2020), 3675. doi: 10.1038/s41467-020-17227-z
[14]	Z. C. Xie, H. Y. Wu, F. C. Ma, Y. W. Dang, Z. G. Peng, H. F. Zhou, et al., Prognostic alternative splicing signatures and underlying regulatory network in esophageal carcinoma, Am. J. Transl. Res., 11 (2019), 4010-4028.
[15]	Y. Bi, S. Guo, X. Xu, P. Kong, H. Cui, T. Yan, et al., Decreased ZNF750 promotes angiogenesis in a paracrine manner via activating DANCR/miR-4707-3p/FOXC2 axis in esophageal squamous cell carcinoma, Cell Death Dis., 11 (2020), 296. doi: 10.1038/s41419-020-2492-2
[16]	K. Ghaffari, M. Hashemi, E. Ebrahimi, R. Shirkoohi, BIRC5 genomic copy number variation in early-onset breast cancer, Iran Biomed. J., 20 (2016), 241-245.
[17]	C. Li, Z. Li, M. Zhu, T. Zhao, L. Chen, W. Ji, et al., Clinicopathological and prognostic significance of survivin over-expression in patients with esophageal squamous cell carcinoma: a meta-analysis, PLoS One, 7 (2012), e44764. doi: 10.1371/journal.pone.0044764
[18]	H. Xia, S. Chen, H. Huang, H. Ma, Survivin over-expression is correlated with a poor prognosis in esophageal cancer patients, Clin. Chim. Acta, 446 (2015), 82-85. doi: 10.1016/j.cca.2015.04.009
[19]	X. Shang, G. Liu, Y. Zhang, P. Tang, H. Zhang, H. Jiang, et al., Downregulation of BIRC5 inhibits the migration and invasion of esophageal cancer cells by interacting with the PI3K/Akt signaling pathway, Oncol. Lett., 16 (2018), 3373-3379.
[20]	J. T. Leek, W. E. Johnson, H. S. Parker, A. E. Jaffe, J. D. Storey, The sva package for removing batch effects and other unwanted variation in high-throughput experiments, Bioinformatics, 28 (2012), 882-883. doi: 10.1093/bioinformatics/bts034
[21]	M. E. Ritchie, B. Phipson, D. Wu, Y. Hu, C. W. Law, W. Shi, et al., limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43 (2015), e47. doi: 10.1093/nar/gkv007
[22]	M. D. Robinson, D. J. McCarthy, G. K. Smyth, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26 (2010), 139-140. doi: 10.1093/bioinformatics/btp616
[23]	S. Balduzzi, G. Rucker, G. Schwarzer, How to perform a meta-analysis with R: A practical tutorial, Evid. Based Ment. Health, 22 (2019), 153-160. doi: 10.1136/ebmental-2019-300117
[24]	H. Hu, Y. R. Miao, L. H. Jia, Q. Y. Yu, Q. Zhang, A. Y. Guo, AnimalTFDB 3.0: A comprehensive resource for annotation and prediction of animal transcription factors, Nucleic Acids Res., 47 (2019), D33-D38. doi: 10.1093/nar/gky822
[25]	R. Zheng, C. Wan, S. Mei, Q. Qin, Q. Wu, H. Sun, et al., Cistrome Data Browser: Expanded datasets and new tools for gene regulatory analysis, Nucleic Acids Res., 47 (2019), D729-D735. doi: 10.1093/nar/gky1094
[26]	G. D. Stormo, Modeling the specificity of protein-DNA interactions, Quant. Biol., 1 (2013), 115-130. doi: 10.1007/s40484-013-0012-4
[27]	W. W. Wasserman, A. Sandelin, Applied bioinformatics for the identification of regulatory elements, Nat. Rev. Genet., 5 (2004), 276-287. doi: 10.1038/nrg1315
[28]	C. E. Grant, T. L. Bailey, W. S. Noble, FIMO: Scanning for occurrences of a given motif, Bioinformatics, 27 (2011), 1017-1018. doi: 10.1093/bioinformatics/btr064
[29]	L. Zhao, B. Claggett, L. Tian, H. Uno, M. A. Pfeffer, S. D. Solomon, et al., On the restricted mean survival time curve in survival analysis, Biometrics, 72 (2016), 215-221. doi: 10.1111/biom.12384
[30]	S. Tian, L. Zhang, Y. Li, D. Cao, S. Quan, Y. Guo, et al., Human papillomavirus E7 oncoprotein promotes proliferation and migration through the transcription factor E2F1 in cervical cancer cells, Anticancer Agents Med. Chem., (2020).
[31]	M. Arnold, I. Soerjomataram, J. Ferlay, D. Forman, Global incidence of oesophageal cancer by histological subtype in 2012, Gut, 64 (2015), 381-387. doi: 10.1136/gutjnl-2014-308124
[32]	L. Jamali, R. Tofigh, S. Tutunchi, G. Panahi, F. Borhani, S. Akhavan, et al., Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers, J. Cell Physiol., 233 (2018), 8538-8550. doi: 10.1002/jcp.26850
[33]	U. Malhotra, A. H. Zaidi, J. E. Kosovec, P. M. Kasi, Y. Komatsu, C. L. Rotoloni, et al., Prognostic value and targeted inhibition of survivin expression in esophageal adenocarcinoma and cancer-adjacent squamous epithelium, PLoS One, 8 (2013), e78343. doi: 10.1371/journal.pone.0078343
[34]	U. Warnecke-Eberz, S. Hokita, H. Xi, H. Higashi, S. E. Baldus, R. Metzger, et al., Overexpression of survivin mRNA is associated with a favorable prognosis following neoadjuvant radiochemotherapy in esophageal cancer, Oncol. Rep., 13 (2005), 1241-1246.
[35]	Y. X. Zhou, Q. Liu, H. Wang, F. Ding, Y. Q. Ma, The expression and prognostic value of SOX2, beta-catenin and survivin in esophageal squamous cell carcinoma, Future Oncol., 15 (2019), 4181-4195. doi: 10.2217/fon-2018-0884
[36]	V. A. Beardmore, L. J. Ahonen, G. J. Gorbsky, M. J. Kallio, Survivin dynamics increases at centromeres during G2/M phase transition and is regulated by microtubule-attachment and Aurora B kinase activity, J. Cell Sci., 117 (2004), 4033-4042. doi: 10.1242/jcs.01242
[37]	S. P. Wheatley, D. C. Altieri, Survivin at a glance, J. Cell Sci., 132 (2019).
[38]	L. Sisinni, F. Maddalena, V. Condelli, G. Pannone, V. Simeon, V. Li Bergolis, et al., TRAP1 controls cell cycle G2-M transition through the regulation of CDK1 and MAD2 expression/ubiquitination, J. Pathol., 243 (2017), 123-134. doi: 10.1002/path.4936
[39]	L. Wang, J. Zhang, L. Wan, X. Zhou, Z. Wang, W. Wei, Targeting Cdc20 as a novel cancer therapeutic strategy, Pharmacol. Ther., 151 (2015), 141-151. doi: 10.1016/j.pharmthera.2015.04.002
[40]	H. Karra, H. Repo, I. Ahonen, E. Loyttyniemi, R. Pitkanen, M. Lintunen, et al., CDC20 and securin overexpression predict short-term breast cancer survival, B.r J. Cancer, 110 (2014), 2905-2913. doi: 10.1038/bjc.2014.252
[41]	W. J. Wu, K. S. Hu, D. S. Wang, Z. L. Zeng, D. S. Zhang, D. L. Chen, et al., CDC20 overexpression predicts a poor prognosis for patients with colorectal cancer, J. Transl. Med., 11 (2013), 142. doi: 10.1186/1479-5876-11-142
[42]	Z. Wang, C. Dang, R. Yan, H. Zhang, D. Yuan, K. Li, Screening of cell cycle-related genes regulated by KIAA0101 in gastric cancer, Nan Fang Yi Ke Da Xue Xue Bao, 38 (2018), 1151-1158.
[43]	Q. Yang, C. Lang, Z. Wu, Y. Dai, S. He, W. Guo, et al., MAZ promotes prostate cancer bone metastasis through transcriptionally activating the KRas-dependent RalGEFs pathway, J. Exp. Clin. Cancer Res., 38 (2019), 391. doi: 10.1186/s13046-019-1374-x
[44]	S. D. Castillo, B. Angulo, A. Suarez-Gauthier, L. Melchor, P. P. Medina, L. Sanchez-Verde, et al., Gene amplification of the transcription factor DP1 and CTNND1 in human lung cancer, J. Pathol., 222 (2010), 89-98. doi: 10.1002/path.2732
[45]	K. Yasui, S. Arii, C. Zhao, I. Imoto, M. Ueda, H. Nagai, et al., TFDP1, CUL4A, and CDC16 identified as targets for amplification at 13q34 in hepatocellular carcinomas, Hepatology, 35 (2002), 1476-1484. doi: 10.1053/jhep.2002.33683

Reader Comments

Your name:*

Email:*
© 2021 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)