Associations between variants on ADIPOQ and ADIPOR1 with colorectal cancer risk: a chinese case-control study and updated meta-analysis

BMC Medical Genetics

Hui Wang⁶  Jia Cao²  Junsheng Guo³  Kazuo Tajima⁴  Jinyi Liu²  Chenglin Li¹  Ziyuan Zhou⁵  Peizhan Chen¹  Yiyi Ou⁷ 

[1] Key Laboratory of Food Safety Research, Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai, P. R China;Toxicology Institute, Key Lab of Medical Protection for Electromagnetic Radiation, Ministry of Education of China, College of Preventive Medicine; Third Military Medical University, Chongqing, P. R. China;Department of Military Hygiene, Faculty of Naval Medicine, Second Military Medical University, Shanghai, P. R. China;Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan;Department of Environment Health, College of Preventive Medicine; Third Military Medical University, Chongqing, P. R. China;School of Life Science and Technology, ShanghaiTech University, Shanghai, P. R. China;Medical Department, The General Hospital of Navy, Beijing, P. R China

关键词: Meta-analysis;    Colorectal cancer;    ADIPOR1;    ADIPOQ;   

Others  :  1090043
DOI  :  10.1186/s12881-014-0137-y

 received in 2014-07-25, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

Epidemiological studies have suggested that variants on adiponectin (ADIPOQ) and its receptor ADIPOR1 (adiponectin receptor 1) are associated with colorectal cancer (CRC) risk; however, the results were inconclusive. The aim of the study was to evaluate the associations between the variants on ADIPOQ and ADIPOR1 and the CRC risk with a hospital-based case-control study in the Chinese population along with meta-analysis of available epidemiological studies.

Methods

With a hospital-based case-control study of 341 cases and 727 controls, the associations between the common variants on ADIPOQ (rs266729, rs822395, rs2241766 and rs1501299) and ADIPOR1 (rs1342387 and rs12733285) and CRC susceptibility were evaluated. Meta-analysis of the published epidemiological studies was performed to investigate the associations between the variants and CRC risk.

Results

For the population study, we found that variant rs1342387 of ADIPOR1 was associated with a reduced risk for CRC [adjusted odds ratio (OR) = 0.74, 95% confidential intervals (95% CI) = 0.57-0.97; CT/TT vs. CC]. The meta-analysis also suggested a significant association for rs1342387 and CRC risk; the pooled OR was 0.79 (95% CI = 0.66-0.95) for the CT/TT carriers compared to CC homozygotes under the random-effects model (Q = 8.06, df = 4, P = 0.089; I² = 50.4%). The case-control study found no significant association for variants rs266729, rs822395, rs2241766, and rs1501299 on ADIPOQ or variant rs12733285 on ADIPOR1 and CRC susceptibility, which were consistent with results from the meta-analysis studies.

Conclusions

These data suggested that variant rs1342387 on ADIPOR1 may be a novel CRC susceptibility factor.

【 授权许可】

   
2014 Ou et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Siddiqui AA: Metabolic syndrome and its association with colorectal cancer: a review. Am J Med Sci 2011, 341:227-231.
• [2]Tsai CJ, Giovannucci EL: Hyperinsulinemia, Insulin Resistance, Vitamin D, and Colorectal Cancer Among Whites and African Americans. Dig Dis Sci 2012, 57:2497-503.
• [3]Esteve E, Ricart W, Fernandez-Real JM: Adipocytokines and insulin resistance: the possible role of lipocalin-2, retinol binding protein-4, and adiponectin. Diabetes Care 2009, 32(Suppl 2):S362-367.
• [4]Wei EK, Giovannucci E, Fuchs CS, Willett WC, Mantzoros CS: Low plasma adiponectin levels and risk of colorectal cancer in men: a prospective study. J Natl Cancer Inst 2005, 97:1688-1694.
• [5]Yoon MJ, Lee GY, Chung JJ, Ahn YH, Hong SH, Kim JB: Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 2006, 55:2562-2570.
• [6]Rasmussen MS, Lihn AS, Pedersen SB, Bruun JM, Rasmussen M, Richelsen B: Adiponectin receptors in human adipose tissue: effects of obesity, weight loss, and fat depots. Obesity (Silver Spring) 2006, 14:28-35.
• [7]Fujisawa T, Endo H, Tomimoto A, Sugiyama M, Takahashi H, Saito S, Inamori M, Nakajima N, Watanabe M, Kubota N, Yamauchi T, Kadowaki T, Wada K, Nakagama H, Nakajima A: Adiponectin suppresses colorectal carcinogenesis under the high-fat diet condition. Gut 2008, 57:1531-1538.
• [8]Nishihara T, Baba M, Matsuda M, Inoue M, Nishizawa Y, Fukuhara A, Araki H, Kihara S, Funahashi T, Tamura S, Hayashi N, Iishi H, Shimomura I: Adiponectin deficiency enhances colorectal carcinogenesis and liver tumor formation induced by azoxymethane in mice. World J Gastroenterol 2008, 14:6473-6480.
• [9]Kaklamani VG, Wisinski KB, Sadim M, Gulden C, Do A, Offit K, Baron JA, Ahsan H, Mantzoros C, Pasche B: Variants of the adiponectin (ADIPOQ) and adiponectin receptor 1 (ADIPOR1) genes and colorectal cancer risk. JAMA 2008, 300:1523-1531.
• [10]Pechlivanis S, Bermejo JL, Pardini B, Naccarati A, Vodickova L, Novotny J, Hemminki K, Vodicka P, Forsti A: Genetic variation in adipokine genes and risk of colorectal cancer. Eur J Endocrinol 2009, 160:933-940.
• [11]Gornick MC, Rennert G, Moreno V, Gruber SB: Adiponectin gene and risk of colorectal cancer. Br J Cancer 2011, 105:562-564.
• [12]He B, Pan Y, Zhang Y, Bao Q, Chen L, Nie Z, Gu L, Xu Y, Wang S: Effects of genetic variations in the adiponectin pathway genes on the risk of colorectal cancer in the Chinese population. BMC Med Genet 2011, 12:94. BioMed Central Full Text
• [13]Liu L, Zhong R, Wei S, Yin JY, Xiang H, Zou L, Chen W, Chen JG, Zheng XW, Huang LJ, Zhu BB, Chen Q, Duan SY, Rui R, Yang BF, Sun JW, Xie DS, Xu YH, Miao XP, Nie SF: Interactions between Genetic Variants in the Adiponectin, Adiponectin Receptor 1 and Environmental Factors on the Risk of Colorectal Cancer. PLoS One 2011, 6:e27301.
• [14]Li M, Zhou Y, Chen P, Yang H, Yuan X, Tajima K, Cao J, Wang H: Genetic variants on chromosome 8q24 and colorectal neoplasia risk: a case-control study in China and a meta-analysis of the published literature. PLoS One 2011, 6:e18251.
• [15]Wu X, Chen P, Ou Y, Liu J, Li C, Wang H, Qiang F: Association of variants on ADIPOQ and AdipoR1 and the prognosis of gastric cancer patients after gastrectomy treatment.Mol Biol Rep 2014, [Epub ahead of print].
• [16]Loibl S, von Minckwitz G, Schwedler K, Schmidt KA, Hoper D, Kaufmann M, Costa SD: Mitomycin C, 5-fluorouracil and folinic acid (Mi-Fu-Fo) as salvage chemotherapy in breast cancer patients with liver metastases and impaired hepatic function: a phase II study. Anticancer Drugs 2004, 15:719-724.
• [17]Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315:629-634.
• [18]Yang H, Zhou Y, Zhou Z, Liu J, Yuan X, Matsuo K, Takezaki T, Tajima K, Cao J: A novel polymorphism rs1329149 of CYP2E1 and a known polymorphism rs671 of ALDH2 of alcohol metabolizing enzymes are associated with colorectal cancer in a southwestern Chinese population. Cancer Epidemiol Biomarkers Prev 2009, 18:2522-2527.
• [19]Carvajal-Carmona LG, Spain S, Kerr D, Houlston R, Cazier JB, Tomlinson I: Common variation at the adiponectin locus is not associated with colorectal cancer risk in the UK. Hum Mol Genet 2009, 18:1889-1892.
• [20]Al Khaldi RM, Al Mulla F, Al Awadhi S, Kapila K, Mojiminiyi OA: Associations of single nucleotide polymorphisms in the adiponectin gene with adiponectin levels and cardio-metabolic risk factors in patients with cancer. Dis Markers 2011, 30:197-212.
• [21]Yi N, Kaklamani VG, Pasche B: Bayesian analysis of genetic interactions in case-control studies, with application to adiponectin genes and colorectal cancer risk. Ann Hum Genet 2011, 75:90-104.
• [22]Tsilidis KK, Helzlsouer KJ, Smith MW, Grinberg V, Hoffman-Bolton J, Clipp SL, Visvanathan K, Platz EA: Association of common polymorphisms in IL10, and in other genes related to inflammatory response and obesity with colorectal cancer. Cancer Causes Control 2009, 20:1739-1751.
• [23]Partida-Perez M, de la Luz A-MM, Peregrina-Sandoval J, Macias-Gomez N, Moreno-Ortiz J, Leal-Ugarte E, Cardenas-Meza M, Centeno-Flores M, Maciel-Gutierrez V, Cabrales E, Cervantes-Ortiz S, Gutiérrez-Angulo M: Association of LEP and ADIPOQ common variants with colorectal cancer in Mexican patients. Cancer Biomark 2010, 7:117-121.
• [24]Al-Harithy RN, Al-Zahrani MH: The adiponectin gene, ADIPOQ, and genetic susceptibility to colon cancer. Oncol Lett 2012, 3:176-180.
• [25]Keku TO, Vidal A, Oliver S, Hoyo C, Hall IJ, Omofoye O, McDoom M, Worley K, Galanko J, Sandler RS, Millikan R: Genetic variants in IGF-I, IGF-II, IGFBP-3, and adiponectin genes and colon cancer risk in African Americans and Whites. Cancer Causes Control 2012, 23:1127-38.
• [26]Hu X, Yuan P, Yan J, Feng F, Li X, Liu W, Yang Y: Gene Polymorphisms of +45 T > G, -866G > A, and Ala54Thr on the Risk of Colorectal Cancer: A Matched Case-Control Study. PLoS One 2013, 8:e67275.
• [27]Qi L, Doria A, Giorgi E, Hu FB: Variations in adiponectin receptor genes and susceptibility to type 2 diabetes in women: a tagging-single nucleotide polymorphism haplotype analysis. Diabetes 2007, 56:1586-91.
• [28]Siitonen N, Pulkkinen L, Mager U, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, Keinanen-Kiukaanniemi S, Tuomilehto J, Laakso M, Uusitupa M: Association of sequence variations in the gene encoding adiponectin receptor 1 (ADIPOR1) with body size and insulin levels. The Finnish Diabetes Prevention Study. Diabetologia 2006, 49:1795-1805.
• [29]Damcott CM, Ott SH, Pollin TI, Reinhart LJ, Wang J, O'Connell JR, Mitchell BD, Shuldiner AR: Genetic variation in adiponectin receptor 1 and adiponectin receptor 2 is associated with type 2 diabetes in the Old Order Amish. Diabetes 2005, 54:2245-2250.
• [30]Crimmins NA, Martin LJ: Polymorphisms in adiponectin receptor genes ADIPOR1 and ADIPOR2 and insulin resistance. Obes Rev 2007, 8:419-423.
• [31]Ong KL, Li M, Tso AW, Xu A, Cherny SS, Sham PC, Tse HF, Lam TH, Cheung BM, Lam KS: Association of genetic variants in the adiponectin gene with adiponectin level and hypertension in Hong Kong Chinese. Eur J Endocrinol 2010, 163:251-257.
• [32]Persson J, Lindberg K, Gustafsson TP, Eriksson P, Paulsson-Berne G, Lundman P: Low plasma adiponectin concentration is associated with myocardial infarction in young individuals. J Intern Med 2010, 268:194-205.
• [33]Prior SL, Gable DR, Cooper JA, Bain SC, Hurel SJ, Humphries SE, Stephens JW: Association between the adiponectin promoter rs266729 gene variant and oxidative stress in patients with diabetes mellitus. Eur Heart J 2009, 30:1263-1269.
• [34]Han LY, Wu QH, Jiao ML, Hao YH, Liang LB, Gao LJ, Legge DG, Quan H, Zhao MM, Ning N, Kang Z, Sun H: Associations between single-nucleotide polymorphisms (+45 T > G, +276G > T, -11377C > G, -11391G > A) of adiponectin gene and type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetologia 2011, 54(9):2303-2314.
• [35]Zhao T, Zhao J: Genetic effects of adiponectin on blood lipids and blood pressure. Clin Endocrinol (Oxf) 2011, 74:214-222.
• [36]Pischon T, Pai JK, Manson JE, Hu FB, Rexrode KM, Hunter D, Rimm EB: Single nucleotide polymorphisms at the adiponectin locus and risk of coronary heart disease in men and women. Obesity (Silver Spring) 2007, 15:2051-2060.
• [37]Kyriakou T, Collins LJ, Spencer-Jones NJ, Malcolm C, Wang X, Snieder H, Swaminathan R, Burling KA, Hart DJ, Spector TD, O'Dell SD: Adiponectin gene ADIPOQ SNP associations with serum adiponectin in two female populations and effects of SNPs on promoter activity. J Hum Genet 2008, 53:718-727.
• [38]Laumen H, Saningong AD, Heid IM, Hess J, Herder C, Claussnitzer M, Baumert J, Lamina C, Rathmann W, Sedlmeier EM, Klopp N, Thorand B, Wichmann HE, Illig T, Hauner H: Functional characterization of promoter variants of the adiponectin gene complemented by epidemiological data. Diabetes 2009, 58:984-991.
• [39]Xu Y, He B, Pan Y, Gu L, Nie Z, Chen L, Li R, Gao T, Wang S: The roles of ADIPOQ genetic variations in cancer risk: evidence from published studies. Mol Biol Rep 2013, 40:1135-1144.