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Calpain-10 SNP43 and SNP19 Polymorphisms and Colorectal Cancer: a Matched Case-control Study

  • Hu, Xiao-Qin (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Yuan, Ping (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Luan, Rong-Sheng (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Li, Xiao-Ling (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Liu, Wen-Hui (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Feng, Fei (Department of Epidemiology, West China School of Public Health, Sichuan University) ;
  • Yan, Jin (Department of Intestinal Surgery, Sichuan Cancer Hospital) ;
  • Yang, Yan-Fang (Department of Epidemiology, West China School of Public Health, Sichuan University)
  • Published : 2013.11.30

Abstract

Objective: Insulin resistance (IR) is an established risk factor for colorectal cancer (CRC). Given that CRC and IR physiologically overlap and the calpain-10 gene (CAPN10) is a candidate for IR, we explored the association between CAPN10 and CRC risk. Methods: Blood samples of 400 case-control pairs were genotyped, and the lifestyle and dietary habits of these pairs were recorded and collected. Unconditional logistic regression (LR) was used to assess the effects of CAPN10 SNP43 and SNP19, and environmental factors. Both generalized multifactor dimensionality reduction (GMDR) and the classification and regression tree (CART) were used to test gene-environment interactions for CRC risk. Results: The GA+AA genotype of SNP43 and the Del/Ins+Ins/Ins genotype of SNP19 were marginally related to CRC risk (GA+AA: OR = 1.35, 95% CI = 0.92-1.99; Del/Ins+Ins/Ins: OR = 1.31, 95% CI = 0.84-2.04). Notably, a high-order interaction was consistently identified by GMDR and CART analyses. In GMDR, the four-factor interaction model of SNP43, SNP19, red meat consumption, and smoked meat consumption was the best model, with a maximum cross-validation consistency of 10/10 and testing balance accuracy of 0.61 (P < 0.01). In LR, subjects with high red and smoked meat consumption and two risk genotypes had a 6.17-fold CRC risk (95% CI = 2.44-15.6) relative to that of subjects with low red and smoked meat consumption and null risk genotypes. In CART, individuals with high smoked and red meat consumption, SNP19 Del/Ins+Ins/Ins, and SNP43 GA+AA had higher CRC risk (OR = 4.56, 95%CI = 1.94-10.75) than those with low smoked and red meat consumption. Conclusions: Though the single loci of CAPN10 SNP43 and SNP19 are not enough to significantly increase the CRC susceptibility, the combination of SNP43, SNP19, red meat consumption, and smoked meat consumption is associated with elevated risk.

Keywords

Calpain-10 gene;genetic polymorphism;interaction;colorectal cancer

References

  1. Barnea M, Shamay A, Stark AH, Madar Z (2006). A high-fat diet has a tissue-specific effect on adiponectin and related enzyme expression. Obesity (Silver Spring), 14, 2145-53. https://doi.org/10.1038/oby.2006.251
  2. Basen-Engquist K, Chang M (2011). Obesity and cancer risk: recent review and evidence. Curr Oncol Rep, 13, 71-6. https://doi.org/10.1007/s11912-010-0139-7
  3. Bastide NM, Pierre FH, Corpet DE (2011). Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Phila), 4, 177-84. https://doi.org/10.1158/1940-6207.CAPR-10-0113
  4. Bingham SA (1999). High-meat diets and cancer risk. Proc Nutr Soc, 58, 243-8. https://doi.org/10.1017/S0029665199000336
  5. Chaolu H, Asakawa A, Ushikai M, et al (2011). Effect of exercise and high-fat diet on plasma adiponectin and nesfatin levels in mice. Exp Ther Med, 2, 369-73. https://doi.org/10.3892/etm.2011.199
  6. Cowey SL, Quast M, Belalcazar LM, et al (2005). Abdominal obesity, insulin resistance, and colon carcinogenesis are increased in mutant mice lacking gastrin gene expression. Cancer, 103, 2643-53. https://doi.org/10.1002/cncr.21094
  7. Dasgupta S, Sirisha PV, Neelaveni K, et al (2012). Association of CAPN10 SNPs and haplotypes with polycystic ovary syndrome among South Indian Women. PLoS One, 7, e32192. https://doi.org/10.1371/journal.pone.0032192
  8. de Oliveira Otto MC, Alonso A, Lee DH, et al (2012). Dietary intakes of zinc and heme iron from red meat, but not from other sources, are associated with greater risk of metabolic syndrome and cardiovascular disease. J Nutr, 142, 526-33. https://doi.org/10.3945/jn.111.149781
  9. Derbel S, Doumaguet C, Hubert D, et al (2006). Calpain 10 and development of diabetes mellitus in cystic fibrosis. J Cyst Fibros, 5, 47-51. https://doi.org/10.1016/j.jcf.2005.09.011
  10. Djiogue S, Nwabo Kamdje AH, et al (2013). Insulin resistance and cancer: the role of insulin and IGFs. Endocr Relat Cancer, 20, R1-R17. https://doi.org/10.1530/ERC-12-0324
  11. Ferlay J, Shin HR, Bray F, et al (2010). GLOBOCAN 2008 v1.2, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]. Lyon, France: International Agency for Research on Cancer; Available from: http://globocan.iarc.fr, accessed on 8/9/2012.
  12. Fong PY, Fesinmeyer MD, White E, et al (2010). Association of diabetes susceptibility gene calpain-10 with pancreatic cancer among smokers. J Gastrointest Cancer, 41, 203-8. https://doi.org/10.1007/s12029-010-9130-7
  13. Frances CP, Conde MC, Saez ME, et al (2007). Identification of a protective haplogenotype within CAPN10 gene influencing colorectal cancer susceptibility. J Gastroenterol Hepatol, 22, 2298-302. https://doi.org/10.1111/j.1440-1746.2007.04843.x
  14. Gingras D, Beliveau R (2011). Colorectal cancer prevention through dietary and lifestyle modifications. Cancer Microenviron, 4, 133-9. https://doi.org/10.1007/s12307-010-0060-5
  15. Giovannucci E (1995). Insulin and colon cancer. Cancer Causes Control, 6, 164-79. https://doi.org/10.1007/BF00052777
  16. Goll DE, Thompson VF, Li H, et al (2003). The calpain system. Physiol Rev, 83, 731-801. https://doi.org/10.1152/physrev.00029.2002
  17. Hanis CL, Boerwinkle E, Chakraborty R, et al (1996). A genome-wide search for human non-insulin-dependent (type 2) diabetes genes reveals a major susceptibility locus on chromosome 2. Nat Genet, 13, 161-6. https://doi.org/10.1038/ng0696-161
  18. Horikawa Y, Oda N, Cox NJ, et al (2000). Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat Genet, 26, 163-75. https://doi.org/10.1038/79876
  19. Hu X, Yuan P, Yan J, et al (2013). Gene Polymorphisms of ADIPOQ +45T>G, UCP2 -866G>A, and FABP2 Ala54Thr on the Risk of Colorectal Cancer: A Matched Case-Control Study. PLoS One, 8, e67275. https://doi.org/10.1371/journal.pone.0067275
  20. J Sorimachi H, Ishiura S, Suzuki K (1993). A novel tissue-specific calpain species expressed predominantly in the stomachcomprises two alternative splicing products with and without Ca(2+)-binding domain. Biol Chem, 268, 19476-82.
  21. Jing C, Xueyao H, Linong J (2012). Meta-analysis of association studies between five candidate genes and type 2 diabetes in Chinese Han population. Endocrine, 42, 307-20. https://doi.org/10.1007/s12020-012-9643-x
  22. Johnson JD, Han Z, Otani K, et al (2004). RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J Biol Chem, 279, 24794-802. https://doi.org/10.1074/jbc.M401216200
  23. Knize MG, Salmon CP, Pais P, Felton JS (1999). Food heating and the formation of heterocyclic aromatic amine and polycyclic aromatichydrocarbon mutagens/carcinogens. Adv Exp Med Biol, 459, 179-93. https://doi.org/10.1007/978-1-4615-4853-9_12
  24. Komninou D, Ayonote A, Richie JP Jr, Rigas B (2003). Insulin resistance and its contribution to colon carcinogenesis. Exp Biol Med (Maywood), 228, 396-405. https://doi.org/10.1177/153537020322800410
  25. Kotnis A, Sarin R, Mulherkar R (2005). Genotype, phenotype and cancer: Role of low penetrance genes and environment in tumour susceptibility. J Biosci, 30, 93-102. https://doi.org/10.1007/BF02705154
  26. Kuhajda FP (2008). AMP-activated protein kinase and human cancer: cancer metabolism revisited. Int J Obes (Lond), 32, S36-41.
  27. Lajous M, Tondeur L, Fagherazzi G, et al (2012). Processed and unprocessed red meat consumption and incident type 2 diabetes among French women. Diabetes Care, 35, 128-30. https://doi.org/10.2337/dc11-1518
  28. Leng SL, Leeding KS, Gibson PR, Bach LA (2001). Insulin-like growth factor-II renders LIM 2405 human colon cancer cells resistant to butyrate-induced apoptosis: a potential mechanism for colon cancer cell survival in vivo. Carcinogenesis, 22, 1625-31. https://doi.org/10.1093/carcin/22.10.1625
  29. Li Y, Yang H, Cao J (2011). Association between alcohol consumption and cancers in the Chinese population--a systematic review and meta-analysis. PLoS One, 6, e18776. https://doi.org/10.1371/journal.pone.0018776
  30. Liu X, Van Vleet T, Schnellmann RG (2004). The role of calpain in oncotic cell death. Annu Rev Pharmacol Toxicol, 44, 349-70. https://doi.org/10.1146/annurev.pharmtox.44.101802.121804
  31. Lou XY, Chen GB, Yan L, et al (2007). A generalized combinatorial approach for detecting gene-by-gene and gene-by-environment interactions with application to nicotine dependence. Am J Hum Genet, 80, 1125-37. https://doi.org/10.1086/518312
  32. Macrae FA (1993). Fat and calories in colon and breast cancer: from animal studies to controlled clinical trials. Prev Med, 22, 750-66. https://doi.org/10.1006/pmed.1993.1069
  33. McKeown-Eyssen G (1994). Epidemiology of colorectal cancer revisited: are serum triglycerides and/or plasma glucose associated with risk? Cancer Epidemiol Biomarkers Prev, 3, 687-95.
  34. Meyer TE, Boerwinkle E, Morrison AC, et al (2010). Diabetes genes and prostate cancer in the Atherosclerosis Risk in Communities study. Cancer Epidemiol Biomarkers Prev, 19, 558-65. https://doi.org/10.1158/1055-9965.EPI-09-0902
  35. Moreno-Luna R, Abrante A, Esteban F, et al (2011). Calpain 10 gene and laryngeal cancer: a survival analysis. Head Neck, 33, 72-6. https://doi.org/10.1002/hed.21404
  36. Noto H, Tsujimoto T, Sasazuki T, Noda M (2011). Significantly increased risk of cancer in patients with diabetes mellitus: a systematic review and meta-analysis. Endocr Pract, 17, 616-28. https://doi.org/10.4158/EP10357.RA
  37. Ortiz AP, Thompson CL, Chak A, et al (2012). Insulin resistance, central obesity, and risk of colorectal adenomas. Cancer, 118, 1774-81. https://doi.org/10.1002/cncr.26454
  38. Permutt MA, Bernal-Mizrachi E, Inoue H (2000). Calpain 10: the first positional cloning of a gene for type 2 diabetes? J Clin Invest, 106, 819-21. https://doi.org/10.1172/JCI11228
  39. Pollak M (2000). Insulin and insulin-like growth factor signalling in neoplasia. Nature Reviews Cancer, 8, 915-28.
  40. Saez ME, Gonzalez-Sanchez JL, Ramirez-Lorca R, et al (2008). The CAPN10 gene is associated with insulin resistance phenotypes in the Spanishpopulation. PLoS One, 3, e2953. https://doi.org/10.1371/journal.pone.0002953
  41. Santarelli RL, Naud N, Tache S, et al (2013). Calcium inhibits promotion by hot dog of 1,2-dimethylhydrazine-induced mucin-depleted foci in rat colon. Int J Cancer, 133, 2533-41.
  42. Santarelli RL, Vendeuvre JL, Naud N, et al (2010). Meat processing and colon carcinogenesis: cooked, nitrite-treated, and oxidized high-heme smoked meat promotes mucin-depleted foci in rats. Cancer Prev Res (Phila), 3, 852-64. https://doi.org/10.1158/1940-6207.CAPR-09-0160
  43. Shima Y, Nakanishi K, Odawara M, et al (2003). Association of the SNP-19 genotype 22 in the calpain-10 gene with elevated body mass index and hemoglobin A1c levels in Japanese. Clin Chim Acta, 336, 89-96. https://doi.org/10.1016/S0009-8981(03)00320-6
  44. Simcox JA, McClain DA (2013). Iron and diabetes risk. Cell Metab, 17, 329-41. https://doi.org/10.1016/j.cmet.2013.02.007
  45. Tanaka T (2012). Development of an inflammation-associated colorectal cancer model and its application for research on carcinogenesis and chemoprevention. Int J Inflam, 2012, 658786.
  46. Tang FY, Pai MH, Chiang EP (2012). Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model. J Nutr Biochem, 23, 1302-13. https://doi.org/10.1016/j.jnutbio.2011.07.011
  47. Tuncman G, Hirosumi J, Solinas G, et al. (2006). Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA, 103, 10741-6. https://doi.org/10.1073/pnas.0603509103
  48. Turner MD, Cassell PG, Hitman GA (2005). Calpain-10: from genome search to function. Diabetes Metab Res Rev, 21, 505-14. https://doi.org/10.1002/dmrr.578
  49. Wang W, Guan KL (2009). AMP-activated protein kinase and cancer. Acta Physiol (Oxf), 196, 55-63. https://doi.org/10.1111/j.1748-1716.2009.01980.x
  50. WCRF (2007). Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. World Cancer Research Fund & American Institute for Cancer Research, Washington, DC.
  51. Wilkin TJ (2009). The accelerator hypothesis: a review of the evidence for insulin resistance as the basis for type I as well as type II diabetes. Int J Obes (Lond), 33, 716-26. https://doi.org/10.1038/ijo.2009.97
  52. Zeyda M, Stulnig TM (2009). Obesity, inflammation, and insulin resistance-a mini-review. Gerontology, 55, 379-86. https://doi.org/10.1159/000212758
  53. Zhao P, Zhang WQ (2011). Chinese tumor registration report in 2010. Beijing, China: Military medical science press.
  54. Zhong R, Liu L, Zou L, et al (2013). Genetic variations in the TGF$\beta$ signaling pathway, smoking and risk of colorectal cancer in a Chinese population. Carcinogenesis, 34, 936-42. https://doi.org/10.1093/carcin/bgs395

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