Advertisement

Tumor Biology

, Volume 35, Issue 4, pp 3765–3770 | Cite as

Differential association of RANTES-403 and IL-1B-1464 polymorphisms on histological subtypes in male Korean patients with gastric cancer

  • Juwon Kim
  • Jong-Won Kim
  • Yoonjung Kim
  • Kyung-A Lee
Research Article

Abstract

The aims of this study were to elucidate the association between RANTES-403 and an increased risk of gastric cancer in Korean males and to investigate the gene–gene interaction between IL-1B and RANTES. In total, 218 male patients with gastric cancer (114 diffuse types, 97 intestinal types, and 7 mixed types) and 377 male controls were included. RANTES-403 was genotyped, and age-adjusted odds ratios (ORs) with 95 % confidence intervals (CIs) were estimated by logistic regression. A multifactor dimensionality reduction (MDR) test with three-way split interval validation confirmed by likelihood ratio and permutation analysis was carried out. A significant increase in the risk of gastric cancer for the intestinal-type group was observed for IL-1B-1464G carriers (OR = 2.535; 95 % CI = 1.121–5.732; P = 0.02) as well as for those with IL-1B-1464 CG (OR = 2.342; 95 % CI = 0.998–5.500; P = 0.05) or IL-1B-1464 GG (OR = 2.819; 95 % CI = 1.170–6.793; P = 0.02). For the RANTES-403 genotype, there was no significant difference in the risk of gastric cancer between the overall gastric cancer and the control groups. When further stratified according to histological types, RANTES-403A carriers (OR = 1.743; 95 % CI = 1.086–2.798; P = 0.021) or heterozygotes (OR = 1.791; 95 % CI = 1.092–2.935; P = 0.021) showed increased risk for developing diffuse-type gastric cancer. MDR revealed a three-way locus–locus interaction between RANTES-403AA, IL-1B-1464GG, and IL-1B-511CT for diffuse-type gastric cancer in Korean males. We demonstrated that RANTES-403 was significantly associated with the risk of developing diffuse-type gastric cancer in men and found a possible gene–gene interaction between RANTES and IL-1B polymorphisms in gastric cancer carcinogenesis.

Keywords

Gastric cancer IL-1B RANTES Diffuse type 

Notes

Acknowledgements

This work was supported by a research grant from Yonsei University School of Medicine in 2012.

Conflicts of interest

None

References

  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRefGoogle Scholar
  2. 2.
    Guggenheim DE, Shah MA. Gastric cancer epidemiology and risk factors. J Surg Oncol. 2013;107:230–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.PubMedCrossRefGoogle Scholar
  4. 4.
    Peek Jr RM, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2:28–37.PubMedCrossRefGoogle Scholar
  5. 5.
    Dinarello CA. Biologic basis for interleukin-1 in disease. Blood. 1996;87:2095–147.PubMedGoogle Scholar
  6. 6.
    Wallace JL, Cucala M, Mugridge K, Parente L. Secretagogue-specific effects of interleukin-1 on gastric acid secretion. Am J Physiol. 1991;261:G559–564.PubMedGoogle Scholar
  7. 7.
    El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000;404:398–402.PubMedCrossRefGoogle Scholar
  8. 8.
    Lu W, Pan K, Zhang L, Lin D, Miao X, You W. Genetic polymorphisms of interleukin (IL)-1B, IL-1RN, IL-8, IL-10 and tumor necrosis factor alpha and risk of gastric cancer in a Chinese population. Carcinogenesis. 2005;26:631–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Shin WG, Jang JS, Kim HS, Kim SJ, Kim KH, Jang MK, et al. Polymorphisms of interleukin-1 and interleukin-2 genes in patients with gastric cancer in Korea. J Gastroenterol Hepatol. 2008;23:1567–73.PubMedCrossRefGoogle Scholar
  10. 10.
    Chang YW, Jang JY, Kim NH, Lee JW, Lee HJ, Jung WW, et al. Interleukin-1b (IL-1B) polymorphisms and gastric mucosal levels of IL-1beta cytokine in Korean patients with gastric cancer. Int J Cancer. 2005;114:465–71.PubMedCrossRefGoogle Scholar
  11. 11.
    He BS, Pan YQ, Xu YF, Zhu C, Qu LL, Wang SK. Polymorphisms in interleukin-1B (IL-1B) and interleukin 1 receptor antagonist (IL-1RN) genes associate with gastric cancer risk in the Chinese population. Dig Dis Sci. 2011;56:2017–23.PubMedCrossRefGoogle Scholar
  12. 12.
    Lee KA, Ki CS, Kim HJ, Sohn KM, Kim JW, Kang WK, et al. Novel interleukin 1beta polymorphism increased the risk of gastric cancer in a Korean population. J Gastroenterol. 2004;39:429–33.PubMedCrossRefGoogle Scholar
  13. 13.
    Schall TJ, Jongstra J, Dyer BJ, Jorgensen J, Clayberger C, Davis MM, et al. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988;141:1018–25.PubMedGoogle Scholar
  14. 14.
    Kim HK, Song KS, Park YS, Kang YH, Lee YJ, Lee KR, et al. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer. 2003;39:184–91.PubMedCrossRefGoogle Scholar
  15. 15.
    Mrowietz U, Schwenk U, Maune S, Bartels J, Kupper M, Fichtner I, et al. The chemokine RANTES is secreted by human melanoma cells and is associated with enhanced tumour formation in nude mice. Br J Cancer. 1999;79:1025–31.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Negus RP, Stamp GW, Hadley J, Balkwill FR. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am J Pathol. 1997;150:1723–34.PubMedCentralPubMedGoogle Scholar
  17. 17.
    Vaday GG, Peehl DM, Kadam PA, Lawrence DM. Expression of CCL5 (RANTES) and CCR5 in prostate cancer. Prostate. 2006;66:124–34.PubMedCrossRefGoogle Scholar
  18. 18.
    Sugasawa H, Ichikura T, Tsujimoto H, Kinoshita M, Morita D, Ono S, et al. Prognostic significance of expression of CCL5/RANTES receptors in patients with gastric cancer. J Surg Oncol. 2008;97:445–50.PubMedCrossRefGoogle Scholar
  19. 19.
    Al-Qahtani A, Alarifi S, Al-Okail M, Hussain Z, Abdo A, Sanai F, et al. RANTES gene polymorphisms (-403G > A And -28c > G) associated with hepatitis B virus infection in a Saudi population. Genet Mol Res. 2012;11:855–62.PubMedCrossRefGoogle Scholar
  20. 20.
    Liu H, Chao D, Nakayama EE, Taguchi H, Goto M, Xin X, et al. Polymorphism in RANTES chemokine promoter affects HIV-1 disease progression. Proc Natl Acad Sci U S A. 1999;96:4581–5.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Nickel RG, Casolaro V, Wahn U, Beyer K, Barnes KC, Plunkett BS, et al. Atopic dermatitis is associated with a functional mutation in the promoter of the C-C chemokine RANTES. J Immunol. 2000;164:1612–6.PubMedGoogle Scholar
  22. 22.
    Liou JM, Lin JT, Huang SP, Wu CY, Wang HP, Lee YC, et al. RANTES-403 polymorphism is associated with reduced risk of gastric cancer in women. J Gastroenterol. 2008;43:115–23.PubMedCrossRefGoogle Scholar
  23. 23.
    Tahara T, Shibata T, Nakamura M, Yamashita H, Yoshioka D, Hirata I, et al. RANTES promoter genotype and gastric cancer risk in a Japanese population. Anticancer Res. 2009;29:4265–9.PubMedGoogle Scholar
  24. 24.
    Ahn HS, Shin YS, Park PJ, Kang KN, Kim Y, Lee HJ, et al. Serum biomarker panels for the diagnosis of gastric adenocarcinoma. Br J Cancer. 2012;106:733–9.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Winham SJ, Motsinger-Reif AA. An R package implementation of multifactor dimensionality reduction. BioData Min. 2011;4:24.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Gory JJ, Sweeney HC, Reif DM, Motsinger-Reif AA. A comparison of internal model validation methods for multifactor dimensionality reduction in the case of genetic heterogeneity. BMC Res Notes. 2012;5:623.PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Ritchie MD, Hahn LW, Roodi N, Bailey LR, Dupont WD, Parl FF, et al. Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Hum Genet. 2001;69:138–47.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Sugasawa H, Ichikura T, Kinoshita M, Ono S, Majima T, Tsujimoto H, et al. Gastric cancer cells exploit CD4+ cell-derived CCL5 for their growth and prevention of CD8+ cell-involved tumor elimination. Int J Cancer. 2008;122:2535–41.PubMedCrossRefGoogle Scholar
  29. 29.
    Tan IB, Ng I, Tai WM, Tan P. Understanding the genetic basis of gastric cancer: recent advances. Expert Rev Gastroenterol Hepatol. 2012;6:335–41.PubMedCrossRefGoogle Scholar
  30. 30.
    Hamilton JP, Meltzer SJ. A review of the genomics of gastric cancer. Clin Gastroenterol Hepatol. 2006;4:416–25.PubMedCrossRefGoogle Scholar
  31. 31.
    Saeki N, Saito A, Choi IJ, Matsuo K, Ohnami S, Totsuka H, et al. A functional single nucleotide polymorphism in mucin 1, at chromosome 1q22, determines susceptibility to diffuse-type gastric cancer. Gastroenterology. 2011;140:892–902.PubMedCrossRefGoogle Scholar
  32. 32.
    Sakamoto H, Yoshimura K, Saeki N, Katai H, Shimoda T, Matsuno Y, et al. Genetic variation in PSCA is associated with susceptibility to diffuse-type gastric cancer. Nat Genet. 2008;40:730–40.PubMedCrossRefGoogle Scholar
  33. 33.
    Gianfagna F, De Feo E, van Duijn CM, Ricciardi G, Boccia S. A systematic review of meta-analyses on gene polymorphisms and gastric cancer risk. Curr Genomics. 2008;9:361–74.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Lao-Sirieix P, Caldas C, Fitzgerald RC. Genetic predisposition to gastro-oesophageal cancer. Curr Opin Genet Dev. 2010;20:210–7.PubMedCrossRefGoogle Scholar
  35. 35.
    Pohjanen VM, Koivurova OP, Mäkinen JM, Karhukorpi JM, Joensuu T, Koistinen PO, Valtonen JM, Niemelä SE, Karttunen RA, Karttunen TJ. Interleukin 6 gene polymorphism-174 is associated with the diffuse type gastric carcinoma. Genes, Chromosomes & Cancer. 2013;52:976–82.Google Scholar
  36. 36.
    Frise S, Kreiger N, Gallinger S, Tomlinson G, Cotterchio M. Menstrual and reproductive risk factors and risk for gastric adenocarcinoma in women: Findings from the Canadian national enhanced cancer surveillance system. Ann Epidemiol. 2006;16:908–16.PubMedCrossRefGoogle Scholar
  37. 37.
    Qin X, He Z, Zhao D, Li L, Yuan L. The RANTES gene promoter polymorphisms are associated with the risk of atherothrombotic cerebral infarction in northern Han Chinese. Clin Chim Acta. 2011;412:1112–5.PubMedCrossRefGoogle Scholar
  38. 38.
    Akoum A, Lemay A, Maheux R. Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J Clin Endocrinol Metab. 2002;87:5785–92.PubMedCrossRefGoogle Scholar
  39. 39.
    Lee KA, Park JH, Sohn TS, Kim S, Rhee JC, Kim JW. Interaction of polymorphisms in the interleukin 1B-31 and general transcription factor 2A1 genes on the susceptibility to gastric cancer. Cytokine. 2007;38:96–100.PubMedCrossRefGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2013

Authors and Affiliations

  • Juwon Kim
    • 1
  • Jong-Won Kim
    • 2
  • Yoonjung Kim
    • 3
  • Kyung-A Lee
    • 3
  1. 1.Department of Laboratory Wonju Severance Christian HospitalYonsei University Wonju College of MedicineWonjuKorea
  2. 2.Department of Laboratory Medicine and Genetics, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulKorea
  3. 3.Department of Laboratory Medicine, Gangnam Severance HospitalYonsei University College of MedicineSeoulKorea

Personalised recommendations