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Association between survivin -31G>C polymorphism and cancer risk: meta-analysis of 29 studies

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Abstract

Purpose

A growing body of evidence has shown the possible relevance of survivin -31G>C (rs9904341) promoter polymorphism to the genetic susceptibility of cancer. Because of the lack of available conclusive data, we performed a meta-analysis of all relevant available studies to derive a more precise estimation of the relationship.

Methods

A comprehensive literature search of Medline electronic database was conducted to collect relevant studies until August 18, 2013. References of the retrieved articles were also screened. The extracted data were statistically analyzed, and pooled odds ratios (ORs) with 95 % confidence intervals (CIs) were calculated to estimate the association strength using Stata version 11.2 software.

Results

A total of 29 studies with 7,473 cancer cases and 9,086 controls were included in the meta-analysis. Overall, the pooled analysis revealed that suvivin -31G>C polymorphism was significantly associated with increased cancer risk under multiple genetic models (CC vs. GG: OR = 1.37, 95 % CI 1.06–1.76; CC vs. CG: OR = 1.27, 95 % CI = 1.10–1.46; CC vs. CG + GG: OR = 1.31, 95 % CI = 1.10–1.57). In subgroup analysis with different cancer types, the -31G>C polymorphism significantly increased the risk of colorectal, gastric, and urothelial cancers, while this SNP remarkably decreased the susceptibility to hepatocellular carcinoma. Further stratification analysis by ethnicity showed an increasing cancer risk in the Asian population (CC vs. GG: OR = 1.61, 95 % CI 1.17–2.21; CC vs. CG: OR = 1.31, 95 % CI 1.12–1.53; CC vs. CG + GG: OR = 1.43, 95 % CI 1.16–1.77) but not in Europeans.

Conclusions

The survivin -31G>C polymorphism is associated with elevated cancer risk, especially among colorectal, gastric, and urothelial cancers and Asian populations.

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References

  • Altieri DC (2001) The molecular basis and potential role of survivin in cancer diagnosis and therapy. Trends Mol Med 7:542–547

    Article  CAS  PubMed  Google Scholar 

  • Andric M, Nikolic N, Boskovic M, Milicic B, Skodric S, Basta Jovanovic G, Milasin J (2012) Survivin gene promoter polymorphism -31G/C as a risk factor for keratocysticodontogenic tumor development. Eur J Oral Sci 120:9–13

    Article  CAS  PubMed  Google Scholar 

  • Antonacopoulou AG, Floratou K, Bravou V, Kottorou A, Dimitrakopoulos FI, Marousi S, Stavropoulos M, Koutras AK, Scopa CD, Kalofonos HP (2011) The survivin -31 snp in human colorectal cancer correlates with survivin splicevariant expression and improved overall survival. Cell Oncol (Dordr) 34:381–391

    Article  CAS  Google Scholar 

  • Aynaci E, Coskunpinar E, Eren A, Kum O, Oltulu YM, Akkaya N, Turna A, Yaylim I, Yildiz P (2013) Association between survivin gene promoter -31G/C and -644C/T polymorphisms and non-small cell lung cancer. Genet Mol Res: GMR 12 (AOP)

  • Bayram S, Akkiz H, Bekar A, Akgollu E (2011) The association between the survivin -31G/C promoter polymorphism and hepatocellular carcinoma risk in a Turkish population. Cancer Epidemiol 35:555–559

    Article  CAS  PubMed  Google Scholar 

  • Borbely AA, Murvai M, Szarka K, Konya J, Gergely L, Hernadi Z, Veress G (2007) Survivin promoter polymorphism and cervical carcinogenesis. J Clin Pathol 60:303–306

    Article  CAS  PubMed  Google Scholar 

  • Borges Bdo N, Burbano RR, Harada ML (2011) Survivin -31C/G polymorphism and gastric cancer risk in a Brazilian population. Clin Exp Med 11:189–193

    Article  PubMed  Google Scholar 

  • Cheng ZJ, Hu LH, Huang SJ (2008) Correlation of -31G/C polymorphisms of survivin promoter to tumorigenesis ofgastric carcinoma. Chin J Cancer 27:258–263

    CAS  Google Scholar 

  • Chen JW, Cui XH, Zhou H, Qin C, Cao Q, Ju XB, Li P, Cai HZ, Zhu J, Meng XX, Wang M, Zhang ZD, Shao PF, Li J, Yin CJ (2013) Functional promoter -31G/C variant of Survivin gene predict prostate cancer susceptibility among Chinese: a case control study. BMC Cancer 13:356

    Article  PubMed Central  PubMed  Google Scholar 

  • Eckelman BP, Salvesen GS, Scott FL (2006) Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7:988–994

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujisawa T, Ikegami H, Kawaguchi Y, Hamada Y, Ueda H, Shintani M, Fukuda M, Ogihara T (1998) Meta-analysis of association of insertion/deletion polymorphism of angiotensinI-converting enzyme gene with diabetic nephropathy and retinopathy. Diabetologia 41:47–53

    Article  CAS  PubMed  Google Scholar 

  • Gazouli M, Tzanakis N, Rallis G, Theodoropoulos G, Papaconstantinou I, Kostakis A, Anagnou NP, Nikiteas N (2009) Survivin -31G/C promoter polymorphism and sporadic colorectal cancer. Int J Colorectal Dis 24:145–150

    Article  PubMed  Google Scholar 

  • Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70

    Article  CAS  PubMed  Google Scholar 

  • Hattori M, Sakamoto H, Satoh K, Yamamoto T (2001) DNA demethylase is expressed in ovarian cancers and the expression correlates with demethylation of CpG sites in the promoter region of c-erbB-2 and survivingenes. Cancer Lett 169:155–164

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YS, Tsai CM, Yeh CB, Yang SF, Hsieh YH, Weng CJ (2012) Survivin T9809C, an SNP located in 3′-UTR, displays a correlation with the risk and clinicopathological development of hepatocellular carcinoma. Ann Surg Oncol 19(Suppl 3):S625–S633

    Article  PubMed  Google Scholar 

  • Huang J, Wang JP, Wang L, Liu HL, Wei YS, Huang MJ, Chen DK, Fu XH, Chen J (2010) Association between Survivin promoter-31C/G polymorphism and genetic susceptibility to sporadic colorectal cancer. Journal of Sun Yat-Sen University (Medical Science) 31:59–63

    Google Scholar 

  • Islam A, Kageyama H, Takada N, Kawamoto T, Takayasu H, Isogai E, Ohira M, Hashizume K, Kobayashi H, Kaneko Y, Nakagawara A (2000) High expression of Survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 19:617–623

    Article  CAS  PubMed  Google Scholar 

  • Jaiswal PK, Goel A, Mandhani A, Mittal RD (2012) Functional polymorphisms in promoter survivin gene and its association with susceptibility to bladder cancer in North Indian cohort. Mol Biol Rep 39:5615–5621

    Article  CAS  PubMed  Google Scholar 

  • Jang JS, Kim KM, Kang KH, Choi JE, Lee WK, Kim CH, Kang YM, Kam S, Kim IS, Jun JE, Jung TH, Park JY (2008) Polymorphisms in the survivin gene and the risk of lung cancer. Lung cancer (Amsterdam, Netherlands) 60:31–39

    Article  Google Scholar 

  • Kawata N, Tsuchiya N, Horikawa Y, Inoue T, Tsuruta H, Maita S, Satoh S, Mitobe Y, Narita S, Habuchi T (2011) Two survivin polymorphisms are cooperatively associated with bladder cancer susceptibility. Int J Cancer 129:1872–1880

    Article  CAS  PubMed  Google Scholar 

  • Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC (2003) Survivin and molecular pathogenesis of colorectal cancer. Lancet 362:205–209

    Article  CAS  PubMed  Google Scholar 

  • Li F, Altieri DC (1999) Transcriptional analysis of human survivin gene expression. Biochem J 344(Pt 2):305–311

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang J, Jiang F, Lin W, Meng W (2012) Association of polymorphisms in survivin gene with the risk of hepato cellular carcinoma in Chinese han population: a case control study. BMC Med Genet 13:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Li XB, Li SN, Yang ZH, Cao L, Duan FL, Sun XW (2013) Polymorphisms of survivin and its protein expression are associated with colorectal cancer susceptibility in Chinese population. DNA Cell Biol 32:236–242

    Article  CAS  PubMed  Google Scholar 

  • Liarmakopoulos E, Theodoropoulos G, Vaiopoulou A, Rizos S, Aravantinos G, Kouraklis G, Nikiteas N, Gazouli M (2013) Effects of stromal cell-derived factor-1 and survivin gene polymorphisms on gastric cancer risk. Mol Med Rep 7:887–892

    CAS  PubMed  Google Scholar 

  • Liu Y, Li L, Qi H, Gao Y, Liu S, Xu C (2013) Survivin -31G>C polymorphism and gastrointestinal tract cancer risk: a meta-analysis. PLoS ONE 8:e54081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liwei L, Chunyu L, Ruifa H (2009) Association between manganese superoxide dismutase gene polymorphism and risk of prostate cancer: a meta-analysis. Urology 74:884–888

    Article  PubMed  Google Scholar 

  • Ma F, Zhang H, Zhai Y, Huang W, Zhao C, Ou S, Zhou H, Yuan W, Wang Z, Wang H, Yue W, Yu L, Li P, Xia X, Cai M, Zhang Y, Cui Y, He F, Ma Y, Zhou G (2011) Functional polymorphism -31C/G in the promoter of BIRC5 gene and risk of nasopharyngeal carcinoma among chinese. PLoS ONE 6:e16748

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marques I, Teixeira AL, Ferreira M, Assis J, Lobo F, Mauricio J, Medeiros R (2013) Influence of survivin (BIRC5) and caspase-9 (CASP9) functional polymorphisms in renal cell carcinoma development: a study in a southern European population. Mol Biol Rep 40:4819–4826

    Article  CAS  PubMed  Google Scholar 

  • Mityaev MV, Kopantzev EP, Buzdin AA, Vinogradova TV, Sverdlov ED (2008) Functional significance of a putative sp1 transcription factor binding site in the survivin gene promoter. Biochemistry (Mosc) 73:1183–1191

    Article  CAS  Google Scholar 

  • Peng XH, Karna P, Cao Z, Jiang BH, Zhou M, Yang L (2006) Cross-talk between epidermal growth factor receptor and hypoxia-inducible factor-1alpha signal pathways increases resistance to apoptosis by up-regulating survivin gene expression. J Biol Chem 281:25903–25914

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qin C, Cao Q, Li P, Ju X, Wang M, Chen J, Wu Y, Meng X, Zhu J, Zhang Z, Lu Q, Yin C (2012) Functional promoter -31G>C variant in survivin gene is associated with risk and progression of renal cell cancer in a Chinese population. PLoS ONE 7:e28829

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Radojevic-Skodric S, Basta-Jovanovic G, Brasanac D, Nikolic N, Bogdanovic L, Milicic B, Milasin J (2012) Survivin gene promoter -31 G/C polymorphism is associated with Wilms tumor susceptibility in Serbian children. J Pediatr Hematol Oncol 34:e310–e314

    Article  CAS  PubMed  Google Scholar 

  • Rodel F, Hoffmann J, Distel L, Herrmann M, Noisternig T, Papadopoulos T, Sauer R, Rodel C (2005) Survivin as a radioresistance factor, and prognostic and therapeutic target for radiotherapy in rectal cancer. Cancer Res 65:4881–4887

    Article  PubMed  Google Scholar 

  • Salvesen GS, Duckett CS (2002) IAP proteins: blocking the road to death’s door. Nature reviews Mol Cell Biol 3:401–410. doi:10.1038/nrm830

    Article  CAS  Google Scholar 

  • Srivastava K, Srivastava A, Mittal B (2012) Survivin promoter -31G/C (rs9904341) polymorphism and cancer susceptibility: a meta-analysis. Mol Biol Rep 39:1509–1516

    Article  CAS  PubMed  Google Scholar 

  • Theodoropoulos GE, Michalopoulos NV, Panoussopoulos SG, Taka S, Gazouli M (2010) Effects of caspase-9 and survivin gene polymorphisms in pancreatic cancer risk and tumor characteristics. Pancreas 39:976–980

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay R, Khurana R, Kumar S, Ghoshal UC, Mittal B (2011) Role of survivin gene promoter polymorphism (-31G>C) in susceptibility and survival of esophageal cancer in northern India. Ann Surg Oncol 18:880–887

    Article  PubMed  Google Scholar 

  • Verdecia MA, Huang H, Dutil E, Kaiser DA, Hunter T, Noel JP (2000) Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat Struct Biol 7:602–608

    Article  CAS  PubMed  Google Scholar 

  • Wang YH, Chiou HY, Lin CT, Hsieh HY, Wu CC, Hsu CD, Shen CH (2009) Association between survivin gene promoter -31 C/G polymorphism and urothelial carcinoma risk in Taiwanese population. Urology 73:670–674

    Article  PubMed  Google Scholar 

  • Wang X, Huang L, Xu Y, Shi Z, Wang Y, Zhang J, Wang X, Cao L, Luo H, Chen J, Liu N, Yin Y, You Y (2012) Association between survivin -31G>C promoter polymorphism and cancer risk: a meta-analysis. Eur J Hum Genet 20:790–795

    Article  CAS  PubMed  Google Scholar 

  • Weng CJ, Hsieh YH, Chen MK, Tsai CM, Lin CW, Yang SF (2012) Survivin SNP-carcinogen interactions in oral cancer. J Dent Res 91:358–363

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto H, Ngan CY, Monden M (2008) Cancer cells survive with survivin. Cancer Sci 99:1709–1714

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Zhu H, Zhou B, Gu H, Yan H, Tang N, Dong H, Sun Q, Cong R, Chen G, Wang B (2009a) The association between the survivin C-31G polymorphism and gastric cancer risk in a Chinese population. Dig Dis Sci 54:1021–1028

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Xiong G, Chen X, Xu X, Wang K, Fu Y, Yang K, Bai Y (2009b) Polymorphisms of survivin promoter are associated with risk of esophageal squamous cell carcinoma. J Cancer Res Clin Oncol 135:1341–1349

    Article  CAS  PubMed  Google Scholar 

  • Yazdani N, Sayahpour FA, Haghpanah V, Amiri P, Shahrabi-Farahani M, Moradi M, Mirmiran A, Khorsandi MT, Larijani B, Mostaan LV, Amoli MM (2012) Survivin gene polymorphism association with papillary thyroid carcinoma. Pathol Res Pract 208:100–103

    Article  CAS  PubMed  Google Scholar 

  • Zahedi P, Aminimoghaddam S, Sayahpour FA, Haghpanah V, Amiri P, Fereidoni F, Mahrampour E, Larijani B, Tavakkoly-Bazzaz J, Amoli MM (2012) Association of survivin gene polymorphism with endometrial cancer. Int J Gynecol Cancer 22:35–37

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of China (Grant No. 81272504), the Innovation Team (No. LJ201123), Jiangsu Provincial Natural Science Fund (BK2011854), and “333” Project of Jiangsu Province (BRA2012210 (RS12)).

Conflict of interest

We declare that we have no conflict of interest.

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Correspondence to Xinchen Sun.

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Q. Qin and C. Zhang have contributed equally to this work.

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Qin, Q., Zhang, C., Zhu, H. et al. Association between survivin -31G>C polymorphism and cancer risk: meta-analysis of 29 studies. J Cancer Res Clin Oncol 140, 179–188 (2014). https://doi.org/10.1007/s00432-013-1524-z

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  • DOI: https://doi.org/10.1007/s00432-013-1524-z

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