Soluble Receptor for Advanced Glycation End-products (sRAGE) and Colorectal Cancer Risk: A Case-Control Study Nested within a European Prospective Cohort.
Journal
Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology
ISSN: 1538-7755
Titre abrégé: Cancer Epidemiol Biomarkers Prev
Pays: United States
ID NLM: 9200608
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
08
06
2020
revised:
31
07
2020
accepted:
09
10
2020
pubmed:
22
10
2020
medline:
27
11
2021
entrez:
21
10
2020
Statut:
ppublish
Résumé
Overexpression of the receptor for advanced glycation end-product (RAGE) has been associated with chronic inflammation, which in turn has been associated with increased colorectal cancer risk. Soluble RAGE (sRAGE) competes with RAGE to bind its ligands, thus potentially preventing RAGE-induced inflammation. To investigate whether sRAGE and related genetic variants are associated with colorectal cancer risk, we conducted a nested case-control study in the European Prospective Investigation into Cancer and Nutrition (EPIC). Plasma sRAGE concentrations were measured by ELISA in 1,361 colorectal cancer matched case-control sets. Twenty-four SNPs encoded in the genes associated with sRAGE concentrations were available for 1,985 colorectal cancer cases and 2,220 controls. Multivariable adjusted ORs and 95% confidence intervals (CIs) were computed using conditional and unconditional logistic regression for colorectal cancer risk and circulating sRAGE and SNPs, respectively. Higher sRAGE concentrations were inversely associated with colorectal cancer (OR Prediagnostic sRAGE concentrations were inversely associated with colorectal cancer risk in men, but not in women. An SNP located within Further studies are needed to confirm our observed sex difference in the association and better explore the potential involvement of genetic variants of sRAGE in colorectal cancer development.
Sections du résumé
BACKGROUND
Overexpression of the receptor for advanced glycation end-product (RAGE) has been associated with chronic inflammation, which in turn has been associated with increased colorectal cancer risk. Soluble RAGE (sRAGE) competes with RAGE to bind its ligands, thus potentially preventing RAGE-induced inflammation.
METHODS
To investigate whether sRAGE and related genetic variants are associated with colorectal cancer risk, we conducted a nested case-control study in the European Prospective Investigation into Cancer and Nutrition (EPIC). Plasma sRAGE concentrations were measured by ELISA in 1,361 colorectal cancer matched case-control sets. Twenty-four SNPs encoded in the genes associated with sRAGE concentrations were available for 1,985 colorectal cancer cases and 2,220 controls. Multivariable adjusted ORs and 95% confidence intervals (CIs) were computed using conditional and unconditional logistic regression for colorectal cancer risk and circulating sRAGE and SNPs, respectively.
RESULTS
Higher sRAGE concentrations were inversely associated with colorectal cancer (OR
CONCLUSIONS
Prediagnostic sRAGE concentrations were inversely associated with colorectal cancer risk in men, but not in women. An SNP located within
IMPACT
Further studies are needed to confirm our observed sex difference in the association and better explore the potential involvement of genetic variants of sRAGE in colorectal cancer development.
Identifiants
pubmed: 33082206
pii: 1055-9965.EPI-20-0855
doi: 10.1158/1055-9965.EPI-20-0855
doi:
Substances chimiques
Membrane Proteins
0
Receptor for Advanced Glycation End Products
0
Amyloid Precursor Protein Secretases
EC 3.4.-
ADAM10 Protein
EC 3.4.24.81
ADAM10 protein, human
EC 3.4.24.81
Types de publication
Journal Article
Multicenter Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
182-192Subventions
Organisme : Cancer Research UK
ID : C8221/A29017
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : British Heart Foundation
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC-UU_12015/1
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N003284/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C864/A14136
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1000143
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0500300
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M012190/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M012190/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C8221/A19170
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0401527
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C570/A16491
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 25004
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 14136
Pays : United Kingdom
Informations de copyright
©2020 American Association for Cancer Research.
Références
Gugliucci A. Formation of fructose-mediated advanced glycation end products and their roles in metabolic and inflammatory diseases. Adv Nutr. 2017;8:54–62.
Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, et al. Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A. 1997;94:13915–20.
Scheijen J, Clevers E, Engelen L, Dagnelie PC, Brouns F, Stehouwer CDA, et al. Analysis of advanced glycation endproducts in selected food items by ultra-performance liquid chromatography tandem mass spectrometry: presentation of a dietary AGE database. Food Chem. 2016;190:1145–50.
Takeuchi M, Takino J-I, Furuno S, Shirai H, Kawakami M, Muramatsu M, et al. Assessment of the concentrations of various advanced glycation end-products in beverages and foods that are commonly consumed in Japan. PLoS One. 2015;10:e0118652.
Rabbani N, Thornalley PJ. Advanced glycation end products in the pathogenesis of chronic kidney disease. Kidney Int. 2018;93:803–13.
Semba RD, Nicklett EJ, Ferrucci L. Does accumulation of advanced glycation end products contribute to the aging phenotype?. J Gerontol A Biol Sci Med Sci. 2010;65:963–75.
Ott C, Jacobs K, Haucke E, Navarrete Santos A, Grune T, Simm A. Role of advanced glycation end products in cellular signaling. Redox Biol. 2014;2:411–29.
Riehl A, Nemeth J, Angel P, Hess J. The receptor RAGE: bridging inflammation and cancer. Cell Commun Signal. 2009;7:12.
Hsieh HL, Schafer BW, Sasaki N, Heizmann CW. Expression analysis of S100 proteins and RAGE in human tumors using tissue microarrays. Biochem Biophys Res Commun. 2003;307:375–81.
Turner DP. Advanced glycation end-products: a biological consequence of lifestyle contributing to cancer disparity. Cancer Res. 2015;75:1925–9.
Yamagishi S, Matsui T. Soluble form of a receptor for advanced glycation end products (sRAGE) as a biomarker. Front Biosci. 2010;2:1184–95.
Ramasamy R, Yan SF, Schmidt AM. RAGE: therapeutic target and biomarker of the inflammatory response–the evidence mounts. J Leukoc Biol. 2009;86:505–12.
Duan Z, Chen G, Chen L, Stolzenberg-Solomon R, Weinstein SJ, Mannisto S, et al. Determinants of concentrations of N(epsilon)-carboxymethyl-lysine and soluble receptor for advanced glycation end products and their associations with risk of pancreatic cancer. Int J Mol Epidemiol Genet. 2014;5:152–63.
Prakash J, Pichchadze G, Trofimov S, Livshits G. Age and genetic determinants of variation of circulating levels of the receptor for advanced glycation end products (RAGE) in the general human population. Mech Ageing Dev. 2015;145:18–25.
Norata GD, Garlaschelli K, Grigore L, Tibolla G, Raselli S, Redaelli L, et al. Circulating soluble receptor for advanced glycation end products is inversely associated with body mass index and waist/hip ratio in the general population. Nutr Metab Cardiovasc Dis. 2009;19:129–34.
Moriya S, Yamazaki M, Murakami H, Maruyama K, Uchiyama S. Two soluble isoforms of receptors for advanced glycation end products (RAGE) in carotid atherosclerosis: the difference of soluble and endogenous secretory RAGE. J Stroke Cerebrovasc Dis. 2014;23:2540–6.
Maruthur NM, Li M, Halushka MK, Astor BC, Pankow JS, Boerwinkle E, et al. Genetics of plasma soluble receptor for advanced glycation end-products and cardiovascular outcomes in a community-based population: results from the Atherosclerosis Risk in Communities study. PLoS One. 2015;10:e0128452.
Salonen KM, Ryhanen SJ, Forbes JM, Harkonen T, Ilonen J, Laine AP, et al. Circulating concentrations of soluble receptor for AGE are associated with age and AGER gene polymorphisms in children with newly diagnosed type 1 diabetes. Diabetes Care. 2014;37:1975–81.
Gaens KH, Ferreira I, van der Kallen CJ, van Greevenbroek MM, Blaak EE, Feskens EJ, et al. Association of polymorphism in the receptor for advanced glycation end products (RAGE) gene with circulating RAGE levels. J Clin Endocrinol Metab. 2009;94:5174–80.
Lim SC, Dorajoo R, Zhang X, Wang L, Ang SF, Tan CSH, et al. Genetic variants in the receptor for advanced glycation end products (RAGE) gene were associated with circulating soluble RAGE level but not with renal function among Asians with type 2 diabetes: a genome-wide association study. Nephrol Dial Transplant. 2017;32:1697–704.
Huang WH, Chen W, Jiang LY, Yang YX, Yao LF, Li KS. Influence of ADAM10 polymorphisms on plasma level of soluble receptor for advanced glycation end products and the association with Alzheimer's disease risk. Front Genet. 2018;9:540.
Jiao L, Taylor PR, Weinstein SJ, Graubard BI, Virtamo J, Albanes D, et al. Advanced glycation end products, soluble receptor for advanced glycation end products, and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2011;20:1430–8.
Chen L, Duan Z, Tinker L, Sangi-Haghpeykar H, Strickler H, Ho GY, et al. A prospective study of soluble receptor for advanced glycation end-products and colorectal cancer risk in postmenopausal women. Cancer Epidemiol. 2016;42:115–23.
Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5:1113–24.
Wareham NJ, Jakes RW, Rennie KL, Mitchell J, Hennings S, Day NE. Validity and repeatability of the EPIC-Norfolk Physical Activity Questionnaire. Int J Epidemiol. 2002;31:168–74.
Wu F, Afanasyeva Y, Zeleniuch-Jacquotte A, Zhang J, Schmidt AM, Chen Y. Temporal reliability of serum soluble and endogenous secretory receptors for advanced glycation end-products (sRAGE and esRAGE) in healthy women. Cancer Causes Control. 2018;29:901–5.
Huyghe JR, Bien SA, Harrison TA, Kang HM, Chen S, Schmit SL, et al. Discovery of common and rare genetic risk variants for colorectal cancer. Nat Genet. 2019;51:76–87.
Sessa L, Gatti E, Zeni F, Antonelli A, Catucci A, Koch M, et al. The receptor for advanced glycation end-products (RAGE) is only present in mammals, and belongs to a family of cell adhesion molecules (CAMs). PLoS One. 2014;9:e86903.
Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, et al. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J. 2008;22:3716–27.
Schalkwijk CG, Stehouwer CDA. Methylglyoxal, a highly reactive dicarbonyl compound, in diabetes, its vascular complications, and other age-related diseases. Physiol Rev. 2020;100:407–61.
Chocholaty M, Jachymova M, Schmidt M, Havlova K, Krepelova A, Zima T, et al. Polymorphisms of the receptor for advanced glycation end-products and glyoxalase I in patients with renal cancer. Tumour Biol. 2015;36:2121–6.
Krechler T, Jachymova M, Mestek O, Zak A, Zima T, Kalousova M. Soluble receptor for advanced glycation end-products (sRAGE) and polymorphisms of RAGE and glyoxalase I genes in patients with pancreas cancer. Clin Biochem. 2010;43:882–6.
Li T, Qin W, Liu Y, Li S, Qin X, Liu Z. Effect of RAGE gene polymorphisms and circulating sRAGE levels on susceptibility to gastric cancer: a case-control study. Cancer Cell Int. 2017;17:19.
Adams JN, Raffield LM, Martelle SE, Freedman BI, Langefeld CD, Carr JJ, et al. Genetic analysis of advanced glycation end products in the DHS MIND study. Gene. 2016;584:173–9.
Daborg J, von Otter M, Sjolander A, Nilsson S, Minthon L, Gustafson DR, et al. Association of the RAGE G82S polymorphism with Alzheimer's disease. J Neural Transm. 2010;117:861–7.
Yamaguchi K, Iwamoto H, Horimasu Y, Ohshimo S, Fujitaka K, Hamada H, et al. AGER gene polymorphisms and soluble receptor for advanced glycation end product in patients with idiopathic pulmonary fibrosis. Respirology. 2017;22:965–71.
Miyashita M, Watanabe T, Ichikawa T, Toriumi K, Horiuchi Y, Kobori A, et al. The regulation of soluble receptor for AGEs contributes to carbonyl stress in schizophrenia. Biochem Biophys Res Commun. 2016;479:447–52.
Peculis R, Konrade I, Skapare E, Fridmanis D, Nikitina-Zake L, Lejnieks A, et al. Identification of glyoxalase 1 polymorphisms associated with enzyme activity. Gene. 2013;515:140–3.
Serveaux-Dancer M, Jabaudon M, Creveaux I, Belville C, Blondonnet R, Gross C, et al. Pathological implications of receptor for advanced glycation end-product (AGER) gene polymorphism. Dis Markers. 2019;2019:2067353.
Jabaudon M, Berthelin P, Pranal T, Roszyk L, Godet T, Faure JS, et al. Receptor for advanced glycation end-products and ARDS prediction: a multicentre observational study. Sci Rep. 2018;8:2603.
Kalousova M, Jachymova M, Germanova A, Kubena AA, Tesar V, Zima T. Genetic predisposition to advanced glycation end products toxicity is related to prognosis of chronic hemodialysis patients. Kidney Blood Press Res. 2010;33:30–6.
Ivancovsky-Wajcman D, Zelber-Sagi S, Fliss Isakov N, Webb M, Zemel M, Shibolet O, et al. Serum soluble receptor for AGE (sRAGE) levels are associated with unhealthy lifestyle and nonalcoholic fatty liver disease. Clin Transl Gastroenterol. 2019;10:1–10.
Waist circumference and waist–hip ratio: report of a WHO expert consultation. 2008;39.
Leclerc E, Fritz G, Vetter SW, Heizmann CW. Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta. 2009;1793:993–1007.
Ciccocioppo R, Vanoli A, Klersy C, Imbesi V, Boccaccio V, Manca R, et al. Role of the advanced glycation end products receptor in Crohn's disease inflammation. World J Gastroenterol. 2013;19:8269–81.
Kuniyasu H, Chihara Y, Kondo H. Differential effects between amphoterin and advanced glycation end products on colon cancer cells. Int J Cancer. 2003;104:722–7.
Sakellariou S, Fragkou P, Levidou G, Gargalionis AN, Piperi C, Dalagiorgou G, et al. Clinical significance of AGE-RAGE axis in colorectal cancer: associations with glyoxalase-I, adiponectin receptor expression and prognosis. BMC Cancer. 2016;16:174.
Yilmaz Y, Yonal O, Eren F, Atug O, Hamzaoglu HO. Serum levels of soluble receptor for advanced glycation endproducts (sRAGE) are higher in ulcerative colitis and correlate with disease activity. J Crohns Colitis. 2011;5:402–6.
Chen Y, Yan SS, Colgan J, Zhang HP, Luban J, Schmidt AM, et al. Blockade of late stages of autoimmune diabetes by inhibition of the receptor for advanced glycation end products. J Immunol. 2004;173:1399–405.
Moy KA, Jiao L, Freedman ND, Weinstein SJ, Sinha R, Virtamo J, et al. Soluble receptor for advanced glycation end products and risk of liver cancer. Hepatology. 2013;57:2338–45.
White DL, Hoogeveen RC, Chen L, Richardson P, Ravishankar M, Shah P, et al. A prospective study of soluble receptor for advanced glycation end products and adipokines in association with pancreatic cancer in postmenopausal women. Cancer Med. 2018;7:2180–91.
Mukherjee TK, Reynolds PR, Hoidal JR. Differential effect of estrogen receptor alpha and beta agonists on the receptor for advanced glycation end product expression in human microvascular endothelial cells. Biochim Biophys Acta. 2005;1745:300–9.
Lin J, Zuo G-Y, Xu Y, Xiong J, Zheng Z, Wang S, et al. Estrogen reduces advanced glycation end products induced HUVEC inflammation via NF-kappa B pathway. Lat Am J Pharm. 2014;33:93–100.
Pouwels SD, Klont F, Kwiatkowski M, Wiersma VR, Faiz A, van den Berge M, et al. Reply to Biswas: acute and chronic effects of cigarette smoking on sRAGE. Am J Respir Crit Care Med. 2019;199:806–7.
Pouwels SD, Klont F, Kwiatkowski M, Wiersma VR, Faiz A, van den Berge M, et al. Cigarette smoking acutely decreases serum levels of the chronic obstructive pulmonary disease biomarker sRAGE. Am J Respir Crit Care Med. 2018;198:1456–8.
Biswas SK. Acute and chronic effects of cigarette smoking on sRAGE. Am J Respir Crit Care Med. 2019;199:805.
Xu Y, Lu Z, Shen N, Wang X. Association of RAGE rs1800625 polymorphism and cancer risk: a meta-analysis of 18 case-control studies. Med Sci Monit. 2019;25:7026–34.
Przemyslaw L, Boguslaw HA, Elzbieta S, Malgorzata SM. ADAM and ADAMTS family proteins and their role in the colorectal cancer etiopathogenesis. BMB Rep. 2013;46:139–50.
Huang Q, Mi J, Wang X, Liu F, Wang D, Yan D, et al. Genetically lowered concentrations of circulating sRAGE might cause an increased risk of cancer: meta-analysis using Mendelian randomization. J Int Med Res. 2016;44:179–91.
Rebholz CM, Astor BC, Grams ME, Halushka MK, Lazo M, Hoogeveen RC, et al. Association of plasma levels of soluble receptor for advanced glycation end products and risk of kidney disease: the Atherosclerosis Risk in Communities study. Nephrol Dial Transplant. 2015;30:77–83.