Skip to main content

Advertisement

Log in

Vascular endothelial growth factor (VEGF) gene polymorphisms and breast cancer risk in Punjabi population from North West India

  • Research Article
  • Published:
Tumor Biology

Abstract

The purpose of this study was to evaluate the association of seven VEGF promoter polymorphisms with breast cancer risk in Punjabi population from North West India. We screened DNA samples of 102 sporadic breast cancer patients and 102 unrelated healthy, gender, and age-matched individuals for seven VEGF promoter polymorphisms [−417C/T (rs833062), −172C/A (rs59260042), −165C/T (rs79469752), −160C/T, −152G/A (rs13207351), −141A/C (rs28357093) and −116G/A (rs1570360)] by direct sequencing. The frequency of GG, GA, and AA genotype of −152G/A polymorphism was 26.47 vs 38.34 %, 46.08 vs 51.96 %, and 27.45 vs 9.80 %, in patients and controls, respectively. VEGF −152 AA genotype was significantly associated with increased risk for breast cancer (OR = 4.04, 95 %CI, 1.69–9.68, p = 0.001; recessive model OR = 3.48, 95 %CI, 1.59–7.63, p = 0.001). For VEGF −116G/A polymorphism, G and A allele frequencies were 65.2 vs 76.47 % and 34.8 vs 23.53 % in patients and controls, respectively. Individuals having −116AA genotype (OR = 3.40; 95 %CI, 1.24–9.37; p = 0.014) and A allele (OR = 1.73; 95 %CI, 1.12–2.67; p = 0.012) were associated with increased risk for breast cancer. VEGF −165C/T and −141A/C polymorphisms were associated with reduced risk for breast cancer. There was significantly decreased frequency of CT genotype (4.90 vs 18.63 %; p = 0.002) and T allele (2.45 vs 9.31 %; p = 0.003) of −165C/T polymorphism among breast cancer patients as compared to controls. VEGF −141A and C allele frequency were 96.57 vs 91.18 % and 3.43 vs 8.82 % in patients and controls, respectively. Significant reduced risk for breast cancer was observed with AC genotype (OR = 0.34, 95 %CI, 0.14–0.86; p = 0.019) and C allele (OR = 0.37; 95 %CI, 0.15–0.89; p = 0.023) of −141A/C polymorphism. We did not observe association of VEGF −417T/C, −172C/A, −160C/T polymorphisms with breast cancer risk in the studied subjects (p > 0.05). The VEGF −152G/A and −116G/A polymorphisms were found to be significantly associated with increased risk for breast cancer while −165C/T and −141A/C polymorphisms were found to be associated with decreased risk for breast cancer in Punjabi population from North West India.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

VEGF :

Vascular endothelial growth factor

UTR:

Untranslated region

SNP:

Single nucleotide polymorphism

PCR:

Polymerase chain reaction

RFLP:

Restriction fragment length polymorphism

SD:

Standard deviation

HWE:

Hardy-Weinberg Equilibrium

OR:

Odds ratio

CI:

Confidence interval

BMI:

Body mass index

WHR:

Waist to hip ratio

WSR:

Waist to stature ratio

References

  1. Glatt CE, DeYoung JA, Delgado S, Service SK, Giacomini KM, Edwards RH, et al. Screening a large reference sample to identify very low frequency sequence variants: comparisons between two genes. Nat Genet. 2001;27(4):435–8.

    Article  CAS  PubMed  Google Scholar 

  2. Pritchard JK. Are rare variants responsible for susceptibility to complex diseases? Am J Hum Genet. 2001;69(1):124–37.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Taylor JG, Choi EH, Foster CB, Chanock SJ. Using genetic variation to study human disease. Trends Mol Med. 2001;7(11):507–12.

    Article  CAS  PubMed  Google Scholar 

  4. Eaves IA, Merriman TR, Barber RA, Nutland S, Tuomilehto-Wolf E, Tuomilehto J, et al. The genetically isolated populations of Finland and sardinia may not be a panacea for linkage disequilibrium mapping of common disease genes. Nat Genet. 2000;25(3):320–3.

    Article  CAS  PubMed  Google Scholar 

  5. Fullerton SM, Clark AG, Weiss KM, Nickerson DA, Taylor SL, Stengard JH, et al. Apolipoprotein E variation at the sequence haplotype level: implications for the origin and maintenance of a major human polymorphism. Am J Hum Genet. 2000;67(4):881–900.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Rieder MJ, Taylor SL, Clark AG, Nickerson DA. Sequence variation in the human angiotensin converting enzyme. Nat Genet. 1999;22(1):59–62.

    Article  CAS  PubMed  Google Scholar 

  7. Taillon-Miller P, Bauer-Sardina I, Saccone NL, Putzel J, Laitinen T, Cao A, et al. Juxtaposed regions of extensive and minimal linkage disequilibrium in human Xq25 and Xq28. Nat Genet. 2000;25(3):324–8.

    Article  CAS  PubMed  Google Scholar 

  8. Templeton AR, Weiss KM, Nickerson DA, Boerwinkle E, Sing CF. Cladistic structure within the human lipoprotein lipase gene and its implications for phenotypic association studies. Genetics. 2000;156(3):1259–75.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Pooley KA, Healey CS, Smith PL, Pharoah PD, Thompson D, Tee L, et al. Association of the progesterone receptor gene with breast cancer risk: a single-nucleotide polymorphism tagging approach. Cancer Epidemiol Biomarkers Prev. 2006;15(4):675–82.

    Article  CAS  PubMed  Google Scholar 

  10. Zhao Z, Fu YX, Hewett-Emmett D, Boerwinkle E. Investigating single nucleotide polymorphism (SNP) density in the human genome and its implications for molecular evolution. Gene. 2003;312:207–13.

    Article  CAS  PubMed  Google Scholar 

  11. Oshika Y, Nakamura M, Tokunaga T, Ozeki Y, Fukushima Y, Hatanaka H, et al. Expression of cell-associated isoform of vascular endothelial growth factor 189 and its prognostic relevance in non-small cell lung cancer. Int J Oncol. 1998;12(3):541–4.

    CAS  PubMed  Google Scholar 

  12. Yuan A, Yu CJ, Chen WJ, Lin FY, Kuo SH, Luh KT, et al. Correlation of total VEGF mRNA and protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. Int J Cancer. 2000;89(6):475–83.

    Article  CAS  PubMed  Google Scholar 

  13. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23(5):1011–27.

    Article  CAS  PubMed  Google Scholar 

  14. Belinsky GS, Claffey KP, Nambiar PR, Guda K, Rosenberg DW. Vascular endothelial growth factor and enhanced angiogenesis do not promote metastatic conversion of a newly established azoxymethane-induced colon cancer cell line. Mol Carcinog. 2005;43(2):65–74.

    Article  CAS  PubMed  Google Scholar 

  15. Roy H, Bhardwaj S, Yla-Herttuala. Biology of vascular endothelial growth factors. FEBS Lett. 2006;580(12):2879–87.

    Article  CAS  PubMed  Google Scholar 

  16. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer. 2002;2(10):795–803.

    Article  CAS  PubMed  Google Scholar 

  17. Vincenti V, Cassano C, Rocchi M, Persico G. Assignment of the vascular endothelial growth factor gene to human chromosome 6p21.3. Circulation. 1996;93(8):1493–5.

    Article  CAS  PubMed  Google Scholar 

  18. Akiri G, Nahari D, Finkelstein Y, Le SY, Elroy-Stein O, Levi BZ. Regulation of vascular endothelial growth factor (VEGF) expression is mediated by internal initiation of translation and alternative initiation of transcription. Oncogene. 1998;17(2):227–36.

    Article  CAS  PubMed  Google Scholar 

  19. Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol. 1998;18(6):3112–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Jacobs EJ, Feigelson HS, Bain EB, Brady KA, Rodriguez C, Stevens VL, et al. Polymorphisms in the vascular endothelial growth factor gene and breast cancer in the Cancer Prevention Study II cohort. Breast Cancer Res. 2006;8(2):R22.

    Article  PubMed Central  PubMed  Google Scholar 

  21. Pasqualetti G, Danesi R, Del Tacca M, Bocci G. Vascular endothelial growth factor pharmacogenetics: a new perspective for anti-angiogenic therapy. Pharmacogenomics. 2007;8(1):49–66.

    Article  CAS  PubMed  Google Scholar 

  22. Renner W, Kotschan S, Hoffmann C, Obermayer-Pietsch B, Pilger E. A common 936 C/T mutation in the gene for vascular endothelial growth factor is associated with vascular endothelial growth factor plasma levels. J Vasc Res. 2000;37(6):443–8.

    Article  CAS  PubMed  Google Scholar 

  23. Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE. Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine. 2000;12(8):1232–5.

    Article  CAS  PubMed  Google Scholar 

  24. Stevens A, Soden J, Brenchley PE, Ralph S, Ray DW. Haplotype analysis of the polymorphic human vascular endothelial growth factor gene promoter. Cancer Res. 2003;63(4):812–6.

    CAS  PubMed  Google Scholar 

  25. Del Bo R, Scarlato M, Ghezzi S, Martinelli Boneschi F, Fenoglio C, Galbiati S, et al. Vascular endothelial growth factor gene variability is associated with increased risk for AD. Ann Neurol. 2005;57(3):373–80.

    Article  PubMed  Google Scholar 

  26. Lambrechts D, Storkebaum E, Morimoto M, Del-Favero J, Desmet F, Marklund SL, et al. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat Genet. 2003;34(4):383–94.

    Article  CAS  PubMed  Google Scholar 

  27. Jin Q, Hemminki K, Enquist K, Lenner P, Grzybowska E, Klaes R, et al. Vascular endothelial growth factor polymorphisms in relation to breast cancer development and prognosis. Clin Cancer Res. 2005;11(10):3647–53.

    Article  CAS  PubMed  Google Scholar 

  28. Sa-Nguanraksa D, Chuangsuwanich T, Pongpruttipan T, Kummalue T, Rojananin S, Ratanawichhitrasin A, et al. Vascular endothelial growth factor 634G/C polymorphism is associated with increased breast cancer risk and aggressiveness. Mol Med Rep. 2013;8(4):1242–50.

    CAS  PubMed  Google Scholar 

  29. McCarron SL, Edwards S, Evans PR, Gibbs R, Dearnaley DP, Dowe A, et al. Influence of cytokine gene polymorphisms on the development of prostate cancer. Cancer Res. 2002;62(12):3369–72.

    CAS  PubMed  Google Scholar 

  30. Howell WM, Bateman AC, Turner SJ, Collins A, Theaker JM. Influence of vascular endothelial growth factor single nucleotide polymorphisms on tumour development in cutaneous malignant melanoma. Genes Immun. 2002;3(4):229–32.

    Article  CAS  PubMed  Google Scholar 

  31. Tzanakis N, Gazouli M, Rallis G, Giannopoulos G, Papaconstantinou I, Theodoropoulos G, et al. Vascular endothelial growth factor polymorphisms in gastric cancer development, prognosis, and survival. J Surg Oncol. 2006;94(7):624–30.

    Article  CAS  PubMed  Google Scholar 

  32. Cacev T, Loncar B, Seiwerth S, Spaventi S, Kapitanovic S. Vascular endothelial growth factor polymorphisms −1154 G/A and −460 C/T are not associated with VEGF mRNA expression and susceptibility to sporadic colon cancer. DNA Cell Biol. 2008;27(10):569–74.

    Article  CAS  PubMed  Google Scholar 

  33. Ungerback J, Elander N, Dimberg J, Soderkvist P. Analysis of VEGF polymorphisms, tumor expression of VEGF mRNA and colorectal cancer susceptibility in a Swedish population. Mol Med Rep. 2009;2(3):435–9.

    PubMed  Google Scholar 

  34. Li Y, Wang Y, Kang S, Wang N, Zhou RM, Duan YN, et al. Association of vascular endothelial growth factor gene polymorphisms with susceptibility to epithelial ovarian cancer. Int J Gynecol Cancer. 2010;20(5):717–23.

    Article  PubMed  Google Scholar 

  35. Salajegheh A, Smith RA, Kasem K, Gopalan V, Nassiri MR, William R, et al. Single nucleotide polymorphisms and mRNA expression of VEGF-A in papillary thyroid carcinoma: potential markers for aggressive phenotypes. Eur J Surg Oncol. 2011;37(1):93–9.

    Article  CAS  PubMed  Google Scholar 

  36. Holt RC, Ralph SA, Webb NJ, Watson CJ, Clark AG, Mathieson PW, et al. Steroid-sensitive nephrotic syndrome and vascular endothelial growth factor gene polymorphisms. Eur J Immunogenet. 2003;30(1):1–3.

    Article  CAS  PubMed  Google Scholar 

  37. Churchill AJ, Carter JG, Ramsden C, Turner SJ, Yeung A, Brenchley PE, et al. VEGF polymorphisms are associated with severity of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2008;49(8):3611–6.

    Article  PubMed  Google Scholar 

  38. Del Bo R, Scarlato M, Ghezzi S, Maestroni A, Sjolind L, Forsblom C, et al. VEGF gene variability and type 1 diabetes: evidence for a protective role. Immunogenetics. 2006;58(2–3):107–12.

    CAS  PubMed  Google Scholar 

  39. Palmirotta R, Ferroni P, Ludovici G, Martini F, Savonarola A, D’Alessandro R, et al. VEGF-A gene promoter polymorphisms and microvascular complications in patients with essential hypertension. Clin Biochem. 2010;43(13–14):1090–5.

    Article  CAS  PubMed  Google Scholar 

  40. Schoppmann SF, Horvat R, Birner P. Lymphatic vessels and lymphangiogenesis in female cancer: mechanisms, clinical impact and possible implications for anti-lymphangiogenic therapies (review). Oncol Rep. 2002;9(3):455–60.

    PubMed  Google Scholar 

  41. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98(19):10869–74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Schneider BP, Miller KD. Angiogenesis of breast cancer. J Clin Oncol. 2005;23(8):1782–90.

    Article  CAS  PubMed  Google Scholar 

  43. Schneider BP, Sledge Jr GW. Drug insight: VEGF as a therapeutic target for breast cancer. Nat Clin Pract Oncol. 2007;4(3):181–9.

    Article  CAS  PubMed  Google Scholar 

  44. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438(7070):932–6.

    Article  CAS  PubMed  Google Scholar 

  45. Adeli K, Ogbonna G. Rapid purification of human DNA from whole blood for potential application in clinical chemistry laboratories. Clin Chem. 1990;36(2):261–4.

    CAS  PubMed  Google Scholar 

  46. Churchill AJ, Carter JG, Lovell HC, Ramsden C, Turner SJ, Yeung A, et al. VEGF polymorphisms are associated with neovascular age-related macular degeneration. Hum Mol Genet. 2006;15(19):2955–61.

    Article  CAS  PubMed  Google Scholar 

  47. Akiyama Y. Transcription factor search version 1.3. 1995. Available from: http://www.cbrc.jp/research/db/TFSEARCH.html, accessed on 31/05/2014.

  48. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21(2):263–5.

    Article  CAS  PubMed  Google Scholar 

  49. WHO expert consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157–63.

  50. Brogan IJ, Khan N, Isaac K, Hutchinson JA, Hutchinson IV PV. Novel polymorphisms in the promoter and 5′ UTR regions of the human vascular endothelial growth factor gene. Hum Immunol. 1999;60(12):1245–9.

    Article  CAS  PubMed  Google Scholar 

  51. Shahbazi M, Fryer AA, Pravica V, Brogan IJ, Ramsay HM, Hutchinson IV, et al. Vascular endothelial growth factor gene polymorphisms are associated with acute renal allograft rejection. J Am Soc Nephrol. 2002;13(1):260–4.

    CAS  PubMed  Google Scholar 

  52. Smith KC, Bateman AC, Fussell HM, Howell WM. Cytokine gene polymorphisms and breast cancer susceptibility and prognosis. Eur J Immunogenet. 2004;31(4):167–73.

    Article  CAS  PubMed  Google Scholar 

  53. Koukourakis MI, Papazoglou D, Giatromanolaki A, Bougioukas G, Maltezos E, Sivridis E. VEGF gene sequence variation defines VEGF gene expression status and angiogenic activity in non-small cell lung cancer. Lung Cancer. 2004;46(3):293–8.

    Article  PubMed  Google Scholar 

  54. Coulam CB, Jeyendran RS. Vascular endothelial growth factor gene polymorphisms and recurrent pregnancy loss. Am J Reprod Immunol. 2008;59(4):301–5.

    Article  CAS  PubMed  Google Scholar 

  55. Samli H, Demir BC, Ozgoz A, Atalay MA, Uncu G. Vascular endothelial growth factor gene 1154 G/A, 2578 C/A, 460 C/T, 936 C/T polymorphisms and association with recurrent pregnancy losses. Genet Mol Res. 2012;11(4):4739–45.

    Article  CAS  PubMed  Google Scholar 

  56. Aggarwal S, Parveen F, Faridi RM, Phadke S, Borkar M, Agrawal S. Vascular endothelial growth factor gene polymorphisms in North Indian patients with recurrent miscarriages. Reprod Biomed Online. 2011;22(1):59–64.

    Article  CAS  PubMed  Google Scholar 

  57. Magdoud K, Dendana M, Herbepin V, Hizem S, Ben Jazia K, Messaoudi S, et al. Identification of specific vascular endothelial growth factor susceptible and protective haplotypes associated with recurrent spontaneous miscarriages. Hum Reprod. 2012;27(5):1536–41.

    Article  CAS  PubMed  Google Scholar 

  58. Yang JW, Hutchinson IV, Shah T, Fang J, Min DI. Gene polymorphism of vascular endothelial growth factor −1154 G>A is associated with hypertensive nephropathy in a Hispanic population. Mol Biol Rep. 2011;38(4):2417–25.

    Article  CAS  PubMed  Google Scholar 

  59. Prakash S, Prasad N, Sharma RK, Faridi RM, Agrawal S. Vascular endothelial growth factor gene polymorphisms in North Indian patients with end stage renal disease. Cytokine. 2012;58(2):261–6.

    Article  CAS  PubMed  Google Scholar 

  60. Papazoglou D, Galazios G, Papatheodorou K, Liberis V, Papanas N, Maltezos E, et al. Vascular endothelial growth factor gene polymorphisms and idiopathic recurrent pregnancy loss. Fertil Steril. 2005;83(4):959–63.

    Article  CAS  PubMed  Google Scholar 

  61. Goodman C, Jeyendran RS, Coulam CB. Vascular endothelial growth factor gene polymorphism and implantation failure. Reprod Biomed Online. 2008;16(5):720–3.

    Article  CAS  PubMed  Google Scholar 

  62. Kim OJ, Hong SH, Oh SH, Kim TG, Min KT, Oh D, et al. Association between VEGF polymorphisms and homocysteine levels in patients with ischemic stroke and silent brain infarction. Stroke. 2011;42(9):2393–402.

    Article  CAS  PubMed  Google Scholar 

  63. Yuan Q, Zuo X, Jia J. Association between promoter polymorphisms of vascular endothelial growth factor gene and sporadic Alzheimer’s disease among Northern Chinese Han. Neurosci Lett. 2009;457(3):133–6.

    Article  CAS  PubMed  Google Scholar 

  64. Zablotna M, Sobjanek M, Nedoszytko B, Lange M, Kozicka D, Glen J, et al. Association of psoriasis with the VEGF gene polymorphism in the northern Polish population. J Eur Acad Dermatol Venereol. 2013;27(3):319–23.

    Article  CAS  PubMed  Google Scholar 

  65. Yang X, Deng Y, Gu H, Lim A, Altankhuyag A, Jia W, et al. Polymorphisms in the vascular endothelial growth factor gene and the risk of diabetic retinopathy in Chinese patients with type 2 diabetes. Mol Vis. 2011;17:3088–96.

    CAS  PubMed Central  PubMed  Google Scholar 

  66. Bluher M. The distinction of metabolically ‘healthy’ from ‘unhealthy’ obese individuals. Curr Opin Lipidol. 2010;21(1):38–43.

    Article  PubMed  Google Scholar 

  67. Trentham-Dietz A, Newcomb PA, Egan KM, Titus-Ernstoff L, Baron JA, Storer BE, et al. Weight change and risk of postmenopausal breast cancer (United States). Cancer Causes Control. 2000;11(6):533–42.

    Article  CAS  PubMed  Google Scholar 

  68. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004;4(8):579–91.

    Article  CAS  PubMed  Google Scholar 

  69. Carmichael AR, Bates T. Obesity and breast cancer: a review of the literature. Breast. 2004;13(2):85–92.

    Article  CAS  PubMed  Google Scholar 

  70. Mannisto S, Pietinen P, Pyy M, Palmgren J, Eskelinen M, Uusitupa M. Body-size indicators and risk of breast cancer according to menopause and estrogen-receptor status. Int J Cancer. 1996;68(1):8–13.

    Article  CAS  PubMed  Google Scholar 

  71. Huang Z, Willett WC, Colditz GA, Hunter DJ, Manson JE, Rosner B, et al. Waist circumference, waist:hip ratio, and risk of breast cancer in the Nurses’ Health Study. Am J Epidemiol. 1999;150(12):1316–24.

    Article  CAS  PubMed  Google Scholar 

  72. Busby S, Ebright RH. Transcription activation by catabolite activator protein (CAP). J Mol Biol. 1999;293(2):199–213.

    Article  CAS  PubMed  Google Scholar 

  73. Lawson CL, Swigon D, Murakami KS, Darst SA, Berman HM, Ebright RH. Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol. 2004;14(1):10–20.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Ronco AL, De Stefani E, Deneo-Pellegrini H. Risk factors for premenopausal breast cancer: a case–control study in Uruguay. Asian Pac J Cancer Prev. 2012;13(6):2879–86.

    Article  PubMed  Google Scholar 

  75. Ronco AL, De Stefani E, Deneo-Pellegrini H, Quarneti A. Diabetes, overweight and risk of postmenopausal breast cancer: a case–control study in Uruguay. Asian Pac J Cancer Prev. 2012;13(1):139–46.

    Article  PubMed  Google Scholar 

  76. Shamsi U, Khan S, Usman S, Soomro S, Azam I. A multicenter matched case control study of breast cancer risk factors among women in Karachi, Pakistan. Asian Pac J Cancer Prev. 2013;14(1):183–8.

    Article  PubMed  Google Scholar 

  77. Sun JW, Li XR, Gao HY, Yin JY, Qin Q, Nie SF, et al. Electromagnetic field exposure and male breast cancer risk: a meta-analysis of 18 studies. Asian Pac J Cancer Prev. 2013;14(1):523–8.

    Article  PubMed  Google Scholar 

  78. Zhang YF, Kang HB, Li BL, Zhang RM. Positive effects of soy isoflavone food on survival of breast cancer patients in China. Asian Pac J Cancer Prev. 2012;13(2):479–82.

    Article  PubMed  Google Scholar 

  79. Zhou LP, Luan H, Dong XH, Jin GJ, Man DL, Shang H. Association between XRCC5, 6 and 7 gene polymorphisms and the risk of breast cancer: a HuGE review and meta-analysis. Asian Pac J Cancer Prev. 2012;13(8):3637–43.

    Article  PubMed  Google Scholar 

  80. Zhou P, Huang W, Chu X, Du LF, Li JP, Zhang C. The lymphotoxin-α 252A>G polymorphism and breast cancer: a meta-analysis. Asian Pac J Cancer Prev. 2012;13(5):1949–52.

    Article  PubMed  Google Scholar 

  81. Colditz GA, Kaphingst KA, Hankinson SE, Rosner B. Family history and risk of breast cancer: nurses’ health study. Breast Cancer Res Treat. 2012;133(3):1097–104.

    Article  PubMed Central  PubMed  Google Scholar 

  82. Llanos AA, Dumitrescu RG, Marian C, Makambi KH, Spear SL, Kallakury BV, et al. Adipokines in plasma and breast tissues: associations with breast cancer risk factors. Cancer Epidemiol Biomarkers Prev. 2012;21(10):1745–55.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C. et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer; 2013. Available from: http://globocan.iarc.fr, accessed on 31/05/2014.

  84. Wolin KY, Carson K, Colditz GA. Obesity and cancer. Oncologist. 2010;15(6):556–65.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The present study was supported by the DBT grant BT/PR 13252/GBD/27/236/2009 sanctioned to KG and VS. Research fellowship (No.3/1/3/JRF-2012/HRD) to RK from ICMR is duly acknowledged. We are thankful to Dr. Geeta Sharma, Principal, Sri Guru Ram Das Institute of Medical Sciences and Research, Vallah, Amritsar, Punjab for their help in providing access to patients and facilities for execution of research work.

Conflicts of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kamlesh Guleria.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kapahi, R., Guleria, K., Sambyal, V. et al. Vascular endothelial growth factor (VEGF) gene polymorphisms and breast cancer risk in Punjabi population from North West India. Tumor Biol. 35, 11171–11181 (2014). https://doi.org/10.1007/s13277-014-2404-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13277-014-2404-0

Keywords

Navigation