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The -765G>C Polymorphism in the Cyclooxygenase-2 Gene and Digestive System Cancer: a Meta-analysis

  • Zhao, Fen (Department of Pathophysiology, West China School of Preclinical and Forensic Medicine, Sichuan University) ;
  • Cao, Yue (Department of Physiology and Pathology, Basic Medicine College, Chengdu University of Traditional Chinese Medicine) ;
  • Zhu, Hong (Department of Abdominal Cancer, West China Hospital, Sichuan University) ;
  • Huang, Min (Department of Pathophysiology, West China School of Preclinical and Forensic Medicine, Sichuan University) ;
  • Yi, Cheng (Department of Abdominal Cancer, West China Hospital, Sichuan University) ;
  • Huang, Ying (Department of Pathophysiology, West China School of Preclinical and Forensic Medicine, Sichuan University)
  • Published : 2014.10.23

Abstract

Background: Published data regarding associations between the -765G>C polymorphism in cyclooxygenase-2 (COX-2) gene and digestive system cancer risk have been inconclusive. The aim of this study was to comprehensively evaluate the genetic risk of the -765G>C polymorphism in the COX-2 gene for digestive system cancer. Materials and Methods: A search was performed in Pubmed, Medline (Ovid), Embase, CNKI, Weipu, Wanfang and CBM databases, covering all studies until Feb 10, 2014. Statistical analysis was performed using Revman5.2. Results: A total of 10,814 cases and 16,174 controls in 38 case-control studies were included in this meta-analysis. The results indicated that C allele carriers (GC+CC) had a 20% increased risk of digestive system cancer when compared with the homozygote GG (odds ratio (OR)=1.20, 95% confidence interval (CI), 1.00-1.44 for GC+CC vs GG). In the subgroup analysis by ethnicity, significant elevated risks were associated with C allele carriers (GC+CC) in Asians (OR = 1.46, 95% CI=1.07-2.01, and p=0.02) and Africans (OR=2.12, 95% CI=1.57-2.87, and p< 0.00001), but not among Caucasians, Americans and mixed groups. For subgroup analysis by cancer type (GC+CC vs GG), significant associations were found between the -765G>C polymorphism and higher risk for gastric cancer (OR=1.64, 95% CI=1.03-2.61, and p=0.04), but not for colorectal cancer, oral cancer, esophageal cancer, and others. Regarding study design (GC+CC vs GG), no significant associations were found in then population-based case-control (PCC), hospital-based case-control (HCC) and family-based case-control (FCC) studies. Conclusions: This meta-analysis suggested that the -765G>C polymorphism of the COX-2 gene is a potential risk factor for digestive system cancer in Asians and Africans and gastric cancer overall.

Keywords

References

  1. Akkiz H, Bayram S, Bekar A, et al (2011). Functional polymorphisms of cyclooxygenase-2 gene and risk for hepatocellular carcinoma. Mol Cell Biochem, 347, 201-8. https://doi.org/10.1007/s11010-010-0629-9
  2. Andersen V, Ostergaard M, Christensen J, et al (2009). Polymorphisms in the xenobiotic transporter Multidrug Resistance 1 (MDR1) and interaction with meat intake in relation to risk of colorectal cancer in a Danish prospective case-cohort study. BMC Cancer, 9, 407. https://doi.org/10.1186/1471-2407-9-407
  3. Bakhle YS (2001). COX-2 and cancer: a new approach to an old problem. Br J Pharmacol, 134, 1137-50. https://doi.org/10.1038/sj.bjp.0704365
  4. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50, 1088-101. https://doi.org/10.2307/2533446
  5. Berlau J, Glei M, Pool-Zobel BL (2004). Colon cancer risk factors from nutrition. Anal Bioanal Chem, 378, 737-43. https://doi.org/10.1007/s00216-003-2284-4
  6. Bye H, Prescott NJ, Matejcic M, et al (2011). Populationspecific genetic associations with oesophageal squamous cell carcinoma in South Africa. Carcinogenesis, 32, 1855-61. https://doi.org/10.1093/carcin/bgr211
  7. Cao H, Xu Z, Long H, Li XQ (2010). The -765C allele of the cyclooxygenase-2 gene as a potential risk factor of colorectal cancer: a meta-analysis. Tohoku J Exp Med, 222, 15-21. https://doi.org/10.1620/tjem.222.15
  8. Cao Y, Prescott SM (2002). Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J Cell Physiol, 190, 279-86. https://doi.org/10.1002/jcp.10068
  9. Chang WS, Yang MD, Tsai CW, et al (2012). Association of cyclooxygenase 2 single-nucleotide polymorphisms and hepatocellular carcinoma in Taiwan. Chin J Physiol, 55, 1-7. https://doi.org/10.4077/CJP.2012.AMM056
  10. Chiang SL, Chen PH, Lee CH, et al (2008). Up-regulation of inflammatory signalings by areca nut extract and role of cyclooxygenase-2 -1195G>a polymorphism reveal risk of oral cancer. Cancer Res, 68, 8489-98. https://doi.org/10.1158/0008-5472.CAN-08-0823
  11. Cook MB, Kamangar F, Whiteman DC, et al (2010). Cigarette smoking and adenocarcinomas of the esophagus and esophagogastric junction: a pooled analysis from the international BEACON consortium. J Natl Cancer Inst, 102, 1344-53. https://doi.org/10.1093/jnci/djq289
  12. Cox DG, Pontes C, Guino E, et al (2004). Polymorphisms in prostaglandin synthase 2/cyclooxygenase 2 (PTGS2/COX2) and risk of colorectal cancer. Br J Cancer, 91, 339-43.
  13. Daraei A, Salehi R, Mohamadhashem F (2012). PTGS2 (COX2)-765G>C gene polymorphism and risk of sporadic colorectal cancer in Iranian population. Mol Biol Rep, 39, 5219-24. https://doi.org/10.1007/s11033-011-1319-8
  14. Dong J, Dai J, Zhang M, et al (2010). Potentially functional COX-2-1195G>A polymorphism increases the risk of digestive system cancers: a meta-analysis. J Gastroenterol Hepatol, 25, 1042-50. https://doi.org/10.1111/j.1440-1746.2010.06293.x
  15. Dubois RN, Abramson SB, Crofford L, et al (1998). Cyclooxygenase in biology and disease. FASEB J, 12, 1063-73.
  16. Egger M, Davey Smith G, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315, 629-34. https://doi.org/10.1136/bmj.315.7109.629
  17. Gong Z, Bostick RM, Xie D, et al (2009). Genetic polymorphisms in the cyclooxygenase-1 and cyclooxygenase-2 genes and risk of colorectal adenoma. Int J Colorectal Dis, 24, 647-54. https://doi.org/10.1007/s00384-009-0656-8
  18. Gu KS, Chen Y (2012). Mechanism of P-glycoprotein expression in the SGC7901 human gastric adenocarcinoma cell line induced by cyclooxygenase-2. Asian Pac J Cancer Prev, 13, 2379-83. https://doi.org/10.7314/APJCP.2012.13.5.2379
  19. Gunter MJ, Canzian F, Landi S, et al (2006). Inflammationrelated gene polymorphisms and colorectal adenoma. Cancer Epidemiol Biomarkers Prev, 15, 1126-31. https://doi.org/10.1158/1055-9965.EPI-06-0042
  20. Guo Y, Zhang X, Tan W, et al (2007). Platelet 12-lipoxygenase Arg261Gln polymorphism: functional characterization and association with risk of esophageal squamous cell carcinoma in combination with COX-2 polymorphisms. Pharmacogenet Genomics, 17, 197-205. https://doi.org/10.1097/FPC.0b013e328010bda1
  21. Hamajima N, Takezaki T, Matsuo K, et al (2001). Genotype Frequencies of cyclooxygenease 2 (COX2) rare polymorphisms for Japanese with and without colorectal cancer. Asian Pac J Cancer Prev, 2, 57-62.
  22. Harrison JR, Lorenzo JA, Kawaguchi H, et al (1994). Stimulation of prostaglandin E2 production by interleukin-1 alpha and transforming growth factor alpha in osteoblastic MC3T3-E1 cells. J Bone Miner Res, 9, 817-23.
  23. He JH, Li YM, Zhang QB (2011). Cyclooxygenase-2 promoter polymorphism -899G/C is associated with hepatitis B-related liver cancer in a Chinese population of Gansu province. Chinese Med J, 124, 4193-7.
  24. Hoff JH, te Morsche RH, Roelofs HM, et al (2009). COX-2 polymorphisms -765G-->C and -1195A-->G and colorectal cancer risk. World J Gastroenterol, 15, 4561-5. https://doi.org/10.3748/wjg.15.4561
  25. Hou L, Grillo P, Zhu ZZ, et al (2007). COX1 and COX2 polymorphisms and gastric cancer risk in a Polish population. Anticancer Res, 27, 4243-7.
  26. Huang F, Lin C, Shi YH, et al (2013). MicroRNA-101 inhibits cell proliferation, invasion, and promotes apoptosis by regulating cyclooxygenase-2 in Hela cervical carcinoma cells. Asian Pac J Cancer Prev, 14, 5915-20. https://doi.org/10.7314/APJCP.2013.14.10.5915
  27. Iglesias D, Nejda N, Azcoita MM, et al (2009). Effect of COX2-765G>C and c.3618A>G polymorphisms on the risk and survival of sporadic colorectal cancer. Cancer Causes Control, 20, 1421-9. https://doi.org/10.1007/s10552-009-9368-1
  28. Jongthawin J, Techasen A, Loilome W, et al (2012). Antiinflammatory agents suppress the prostaglandin E2 production and migration ability of cholangiocarcinoma cell lines. Asian Pac J Cancer Prev, 13, 47-51.
  29. Kamal MM, Youssef OZ, Lotfy AN, et al (2012). Association of folate intake, dietary habits, smoking and COX-2 promotor-765G>C polymorphism with K-ras mutation in patients with colorectal cancer. J Egypt Natl Canc Inst, 24, 115-22. https://doi.org/10.1016/j.jnci.2012.05.002
  30. Koh WP, Yuan JM, van den Berg D, et al (2004). Interaction between cyclooxygenase-2 gene polymorphism and dietary n-6 polyunsaturated fatty acids on colon cancer risk: the Singapore Chinese health study. Br J Cancer, 90, 1760-4.
  31. Kristinsson JO, van Westerveld P, te Morsche RH, et al (2009). Cyclooxygenase-2 polymorphisms and the risk of esophageal adeno- or squamous cell carcinoma. World J Gastroenterol, 15, 3493-7. https://doi.org/10.3748/wjg.15.3493
  32. KX Z, YM L, X L (2008). Association of COX-2 genetic polymorphisms and Hpylori infection with gastric cancer in high-incidence Hexi area of Gansu Province in China. Shijie Huaren Xiaohua Zazhi, 16, 2364-70.
  33. Leahy KM, Koki AT, Masferrer JL (2000). Role of cyclooxygenases in angiogenesis. Curr Med Chem, 7, 1163-70. https://doi.org/10.2174/0929867003374336
  34. Li Y, Dai L, Zhang J, et al (2012). Cyclooxygenase-2 polymorphisms and the risk of gastric cancer in various degrees of relationship in the Chinese Han population. Oncol Lett, 3, 107-12.
  35. Liang Y, Liu JL, Wu Y, et al (2011). Cyclooxygenase-2 polymorphisms and susceptibility to esophageal cancer: a meta-analysis. Tohoku J Exp Med, 223, 137-44. https://doi.org/10.1620/tjem.223.137
  36. Lin YC, Huang HI, Wang LH, et al (2008). Polymorphisms of COX-2 -765G>C and p53 codon 72 and risks of oral squamous cell carcinoma in a Taiwan population. Oral Oncol, 44, 798-804. https://doi.org/10.1016/j.oraloncology.2007.10.006
  37. Liu F, Pan K, Zhang X, et al (2006). Genetic variants in cyclooxygenase-2: Expression and risk of gastric cancer and its precursors in a Chinese population. Gastroenterology, 130, 1975-84. https://doi.org/10.1053/j.gastro.2006.03.021
  38. Liu JL, Liang Y, Wang ZN (2010). Cyclooxygenase-2 polymorphisms and susceptibility to gastric carcinoma: a meta-analysis. World J Gastroenterol, 16, 5510-7. https://doi.org/10.3748/wjg.v16.i43.5510
  39. Mittal M, Kapoor V, Mohanti BK, Das SN (2010). Functional variants of COX-2 and risk of tobacco-related oral squamous cell carcinoma in high-risk Asian Indians. Oral Oncol, 46, 622-6. https://doi.org/10.1016/j.oraloncology.2010.06.002
  40. Moons LM, Kuipers EJ, Rygiel AM, Groothuismink AZ (2007). COX-2 CA-haplotype is a risk factor for the development of esophageal adenocarcinoma. Am J Gastroenterol, 102, 2373-9. https://doi.org/10.1111/j.1572-0241.2007.01373.x
  41. Papafili A, Hill MR, Brull DJ, et al (2002). Common promoter variant in cyclooxygenase-2 represses gene expression: evidence of role in acute-phase inflammatory response. Arterioscler Thromb Vasc Biol, 22, 1631-6. https://doi.org/10.1161/01.ATV.0000030340.80207.C5
  42. Pereira C, Pimentel-Nunes P, Brandao C, et al (2010). COX-2 polymorphisms and colorectal cancer risk: a strategy for chemoprevention. Eur J Gastroenterol Hepatol, 22, 607-13. https://doi.org/10.1097/MEG.0b013e3283352cbb
  43. Pereira C, Sousa H, Ferreira P (2006). -765G>C COX-2 polymorphism may be a susceptibility marker for gastric adenocarcinoma in patients with atrophy or intestinal metaplasia. World J Gastroenterol, 12, 5473-8.
  44. Pharoah PD, Dunning AM, Ponder BA, Easton DF (2004). Association studies for finding cancer-susceptibility genetic variants. Nat Rev Cancer, 4, 850-60. https://doi.org/10.1038/nrc1476
  45. Saad N, Esa NM, Ithnin H (2013). Suppression of beta-catenin and cyclooxygenase-2 expression and cell proliferation in azoxymethane-induced colonic cancer in rats by rice bran phytic acid (PA). Asian Pac J Cancer Prev, 14, 3093-9. https://doi.org/10.7314/APJCP.2013.14.5.3093
  46. Saxena A, Prasad KN, Ghoshal UC (2008). Polymorphism of 765G C COX-2 is a risk factor for gastric adenocarcinoma and peptic ulcer disease in addition to H pylori infection A study from northern India. World J Gastroenterol, 14, 1498-503. https://doi.org/10.3748/wjg.14.1498
  47. Seibert K, Zhang Y, Leahy K, et al (1994). Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc Natl Acad Sci USA, 91, 12013-7. https://doi.org/10.1073/pnas.91.25.12013
  48. Shin WG, Kim HJ, Cho SJ (2012). The COX-2-1195AA genotype is associated with diffuse-type gastric cancer in Korea. Gut Liver, 6, 321-7. https://doi.org/10.5009/gnl.2012.6.3.321
  49. Sitarz R, Leguit RJ, de Leng WW, et al (2008). The COX-2 promoter polymorphism -765 G>C is associated with earlyonset, conventional and stump gastric cancers. Modern Pathology, 21, 685-90. https://doi.org/10.1038/modpathol.2008.36
  50. Szczeklik W, Sanak M, Szczeklik A (2004). Functional effects and gender association of COX-2 gene polymorphism G-765C in bronchial asthma. J Allergy Clin Immunol, 114, 248-53. https://doi.org/10.1016/j.jaci.2004.05.030
  51. Talar-Wojnarowska R, Gasiorowska A, Olakowski M, et al (2011). Role of cyclooxygenase-2 gene polymorphisms in pancreatic carcinogenesis. World J Gastroenterol, 17, 4113-7. https://doi.org/10.3748/wjg.v17.i36.4113
  52. Tan W, Wu J, Zhang X, et al (2007). Associations of functional polymorphisms in cyclooxygenase-2 and platelet 12-lipoxygenase with risk of occurrence and advanced disease status of colorectal cancer. Carcinogenesis, 28, 1197-201. https://doi.org/10.1093/carcin/bgl242
  53. Tang XF, Li YM, Li SX ( 2009). Correlation between the nucleotide polymorphisms of COX-2 and the susceptibility to gastric cancer in Hui ethnic group. Shijie Huaren Xiaohua Zazhi, 17, 1772-6.
  54. Tatsuguchi A, Matsui K, Shinji Y, et al (2004). Cyclooxygenase-2 expression correlates with angiogenesis and apoptosis in gastric cancer tissue. Hum Pathol, 35, 488-95. https://doi.org/10.1016/j.humpath.2003.10.025
  55. Tazawa R, Xu XM, Wu KK, Wang LH (1994). Characterization of the genomic structure, chromosomal location and promoter of human prostaglandin H synthase-2 gene. Biochem Biophys Res Commun, 203, 190-9. https://doi.org/10.1006/bbrc.1994.2167
  56. Thompson CL, PLummer SJ, Merkulova A (2009). No association between cyclooxygenase-2 and uridine diphosphate glucuronosyltransferase 1A6 genetic polymorphisms and colon cancer risk. World J Gastroenterology, 15, 2240. https://doi.org/10.3748/wjg.15.2240
  57. Ueda N, Maehara Y, Tajima O, et al (2008). Genetic polymorphisms of cyclooxygenase-2 and colorectal adenoma risk: the Self Defense Forces Health Study. Cancer Sci, 99, 576-81. https://doi.org/10.1111/j.1349-7006.2007.00711.x
  58. Ulrich CM, Whitton J, Yu JH, et al (2005). PTGS2 (COX-2) -765G>C promoter variant reduces risk of colorectal adenoma among nonusers of nonsteroidal anti-inflammatory drugs. Cancer Epidemiol Biomarkers Prev, 14, 616-9. https://doi.org/10.1158/1055-9965.EPI-04-0510
  59. Upadhyay R, Jain M, Kumar S, et al (2009). Functional polymorphisms of cyclooxygenase-2 (COX-2) gene and risk for esophageal squmaous cell carcinoma. Mutat Res, 663, 52-9. https://doi.org/10.1016/j.mrfmmm.2009.01.007
  60. Wang J, Joshi AD, Corral R, et al (2012). Carcinogen metabolism genes, red meat and poultry intake, and colorectal cancer risk. Int J Cancer, 130, 1898-907. https://doi.org/10.1002/ijc.26199
  61. Wang MT, Honn KV, Nie D (2007). Cyclooxygenases, prostanoids, and tumor progression. Cancer Metastasis Rev, 26, 525-34. https://doi.org/10.1007/s10555-007-9096-5
  62. Wang XF, Huang MZ, Zhang XW, et al (2013). COX-2-765G>C polymorphism increases the risk of cancer: a meta-analysis. PLoS One, 8, 73213. https://doi.org/10.1371/journal.pone.0073213
  63. Wu KK (1996). Cyclooxygenase 2 induction: molecular mechanism and pathophysiologic roles. J Lab Clin Med, 128, 242-5. https://doi.org/10.1016/S0022-2143(96)90023-2
  64. Xing LL, Wang ZN, Jiang L, et al (2008). Cyclooxygenase 2 polymorphism and colorectal cancer: -765G>C variant modifies risk associated with smoking and body mass index. World J Gastroenterol, 14, 1785-9. https://doi.org/10.3748/wjg.14.1785
  65. Xu D, ZHANG XM, Zhao P (2008). Association between single nucleotide polymorphisms in the promoter of cyclooxygenase COX-2 gene and hereditary susceptibility to pancreatic cancer. National Medical J China, 88, 1961-5.
  66. Yaghoobi M, Rakhshani N, Sadr F, et al (2004). Hereditary risk factors for the development of gastric cancer in younger patients. BMC Gastroenterol, 4, 28. https://doi.org/10.1186/1471-230X-4-28
  67. Yan WF, Sun PC, Nie CF (2013). Cyclooxygenase-2 polymorphisms were associated with the risk of gastric cancer: evidence from a meta-analysis based on case-control studies. Tumour Biol, 34, 3323-30. https://doi.org/10.1007/s13277-013-0901-1
  68. Zhang X, Miao X, Tan W, et al (2005). Identification of functional genetic variants in cyclooxygenase-2 and their association with risk of esophageal cancer. Gastroenterology, 129, 565-76.
  69. Zhang X, Zhong R, Zhang Z, et al (2011). Interaction of cyclooxygenase-2 promoter polymorphisms with Helicobacter pylori infection and risk of gastric cancer. Molecular Carcinogenesis, 50, 876-83. https://doi.org/10.1002/mc.20784
  70. Zhang XM, Miao XP, Tan W (2006). Genetic polymorphisms in the promoter region of cyclooxygenase-2 and their association with risk of gastric cancer. Zhongguo Yi Xue Ke Xue Yuan Xue Bao, 28, 119-23.
  71. Zhang XM, Zhong R, Liu L (2011). Smoking and COX-2 functional polymorphisms interact to increase the risk of gastric cardia adenocarcinoma in Chinese population. PLoS One, 6, 21894. https://doi.org/10.1371/journal.pone.0021894
  72. Zhang YG, Huang J, Zhang J, et al (2010). RANTES gene polymorphisms and asthma risk: A meta-analysis. Arch Med Res, 41, 50-8. https://doi.org/10.1016/j.arcmed.2010.01.002
  73. Zhao D, Xu D, Zhang X, et al (2009). Interaction of cyclooxygenase-2 variants and smoking in pancreatic cancer: a possible role of nucleophosmin. Gastroenterology, 136, 1659-68. https://doi.org/10.1053/j.gastro.2009.01.071

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