Advanced glycation end products and breast cancer: a review of the literature
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Abstract
Advanced glycation end products (AGEs) are mediators of chronic inflammation, which is recognized as an underlying process in carcinogenesis. The role of AGEs in cancers is the focus of recent studies. Breast cancer (BC) is the most common cancer in the world and the etiology is unknown, but some risk factors have been defined; including obesity and diabetes. Both of these disorders are linked to AGEs; thus, BC and AGEs might be associated. AGEs in the human body either derive from the glycation of proteins and lipids in the blood, or from the dietary AGEs (dAGE). AGEs are mainly associated with disease states or aging, including diabetes mellitus, cardiovascular and cerebrovascular disorders, Alzheimer, renal failure, arthritis, skin problems, viral infections, and osteoporosis. Some bioeffects of AGEs are consistent with the chain of events that occur during carcinogenesis. However, the studies about the role of AGEs in specific cancers are not conclusive, and some recent literature, especially clinical studies does not support the theory of the association between AGEs and cancers,. There does not exist a great deal of studies about the role of AGEs in BC, but the subject has been addressed recently. The present evidence is rather in favor of the association of AGEs and breast cancer; however, the direction and type of this association are unclear. In-vitro studies show that AGEs promote features of invasiveness in BC, but clinical studies show diverse findings. In this study, we present an overview of the core existing knowledge about AGEs and their relation with diseases; then provide a brief review of the results of studies that have investigated the association of AGEs and cancer, and then proceed to a concise discussion about studies on AGEs and BC.
1. Twarda-Clapa A, Olczak A, Białkowska AM, Koziołkiewicz M. Advanced Glycation End-Products (AGEs): Formation, Chemistry, Classification, Receptors, and Diseases Related to AGEs. Cells. 2022 Apr 12;11(8):1312.
2. Giaquinto AN, Sung H, Miller KD, et al. Breast cancer statistics, 2022. CA: A Cancer Journal for Clinicians. 2022 Nov;72(6):524-41.
3. Ahmadi H, Eslami B, Alipour S, Yazdankhahkenary A, Omranipour R. Impact of body mass index on breast cancer subtypes in Iranian women. Clinical Cancer Investigation Journal. 2019 Mar 1;8(2):52-.
4. Larsson SC, Mantzoros CS, Wolk A. Diabetes mellitus and risk of breast cancer: a meta‐analysis. International journal of cancer. 2007 Aug 15;121(4):856-62.
5. Nowotny K, Schröter D, Schreiner M, Grune T. Dietary advanced glycation end products and their relevance for human health. Ageing research reviews. 2018 Nov 1;47:55-66.
6. Yamagishi SI, Matsui T. Therapeutic potential of DNA-aptamers raised against AGE-RAGE axis in diabetes-related complications. Current Pharmaceutical Design. 2018 Jul 1;24(24):2802-9.
7. Dariya B, Nagaraju GP. Advanced glycation end products in diabetes, cancer and phytochemical therapy. Drug Discovery Today. 2020 Sep 1;25(9):1614-23.
8. Lin JA, Wu CH, Lu CC, Hsia SM, Yen GC. Glycative stress from advanced glycation end products (AGEs) and dicarbonyls: An emerging biological factor in cancer onset and progression. Molecular nutrition & food research. 2016 Aug;60(8):1850-64.
9. Malik P, Chaudhry N, Mittal R, Mukherjee TK. Role of receptor for advanced glycation end products in the complication and progression of various types of cancers. Biochimica et Biophysica Acta (BBA)-General Subjects. 2015 Sep 1;1850(9):1898-904.
10. Abe R, Shimizu T, Sugawara H, et al. Regulation of human melanoma growth and metastasis by AGE–AGE receptor interactions. Journal of Investigative Dermatology. 2004 Feb 1;122(2):461-7.
11. Schraml P, Bendik I, Ludwig CU. Differential messenger RNA and protein expression of the receptor for advanced glycosylated end products in normal lung and non-small cell lung carcinoma. Cancer research. 1997 Sep 1;57(17):3669-71.
12. Takada M, Koizumi T, Toyama H, Suzuki Y, Kuroda Y. Differential expression of RAGE in human pancreatic carcinoma cells. Hepato-gastroenterology. 2001 Nov 1;48(42):1577-8.
13. Kuniyasu H, Chihara Y, Kondo H. Differential effects between amphoterin and advanced glycation end products on colon cancer cells. International journal of cancer. 2003 May 10;104(6):722-7.
14. Hirata K, Takada M, Suzuki Y, Kuroda Y. Expression of receptor for advanced glycation end products (RAGE) in human biliary cancer cells. Hepato-gastroenterology. 2003 Sep 1;50(53):1205-7.
15. Bhawal UK, Ozaki Y, Nishimura M, et al. Association of expression of receptor for advanced glycation end products and invasive activity of oral squamous cell carcinoma. Oncology. 2005;69(3):246-55.
16. Ishiguro H, Nakaigawa N, Miyoshi Y, Fujinami K, Kubota Y, Uemura H. Receptor for advanced glycation end products (RAGE) and its ligand, amphoterin are overexpressed and associated with prostate cancer development. The Prostate. 2005 Jun 15;64(1):92-100.
17. Chen H, Wu L, Li Y, et al. Advanced glycation end products increase carbohydrate responsive element binding protein expression and promote cancer cell proliferation. Molecular and cellular endocrinology. 2014 Sep 1;395(1-2):69-78.
18. Menini S, Iacobini C, De Latouliere L,et al. . Diabetes promotes invasive pancreatic cancer by increasing systemic and tumour carbonyl stress in KrasG12D/+ mice. Journal of Experimental & Clinical Cancer Research. 2020 Dec;39(1):1-6.
19. Jiao L, Weinstein SJ, Albanes D, et al. Evidence That Serum Levels of the Soluble Receptor for Advanced Glycation End Products Are Inversely Associated with Pancreatic Cancer Risk: A Prospective StudyAdvanced Glycation End Products and Pancreatic Cancer. Cancer research. 2011 May 15;71(10):3582-9.
20. Jiao L, Stolzenberg-Solomon R, Zimmerman TP, et al. . Dietary consumption of advanced glycation end products and pancreatic cancer in the prospective NIH-AARP Diet and Health Study. The American journal of clinical nutrition. 2015 Jan 1;101(1):126-34.
21. Jiao L, Taylor PR, Weinstein SJ, et al. Advanced Glycation End Products, Soluble Receptor for Advanced Glycation End Products, and Risk of Colorectal CancersRAGE and Colorectal Cancer Risk. Cancer epidemiology, biomarkers & prevention. 2011 Jul 1;20(7):1430-8.
22. Grote VA, Nieters A, Kaaks R, et al. The Associations of Advanced Glycation End Products and Its Soluble Receptor with Pancreatic Cancer Risk: A Case–Control Study within the Prospective EPIC CohortAdvanced Glycation and Pancreatic Cancer Risk. Cancer epidemiology, biomarkers & prevention. 2012 Apr 1;21(4):619-28.
23. Moy KA, Jiao L, Freedman ND, et al. Soluble receptor for advanced glycation end products and risk of liver cancer. Hepatology. 2013 Jun;57(6):2338-45.
24. Mayén AL, Aglago EK, Knaze V, et al. Dietary intake of advanced glycation endproducts and risk of hepatobiliary cancers: A multinational cohort study. International journal of cancer. 2021 Aug 15;149(4):854-64.
25. Wada K, Nakashima Y, Yamakawa M, et al. Dietary advanced glycation end products and cancer risk in Japan: from the Takayama study. Cancer Science.
26. Córdova R, Mayén AL, Knaze V, et al. Dietary intake of advanced glycation endproducts (AGEs) and cancer risk across more than 20 anatomical sites: A multinational cohort study. Cancer Communications. 2022 Oct;42(10):1041-5.
27. van Heijst JW, Niessen HW, Hoekman K, Schalkwijk CG. Advanced Glycation End Products in Human Cancer Tissues: Detection of Nε‐(Carboxymethyl) lysine and Argpyrimidine. Annals of the New York Academy of Sciences. 2005 Jun;1043(1):725-33.
28. Foster D, Spruill L, Walter KR, et al. AGE Metabolites: A Biomarker Linked to Cancer Disparity? AGEs in Cancer Disparity. Cancer Epidemiology, Biomarkers & Prevention. 2014 Oct 1;23(10):2186-91.
29. Yang S, Pinney SM, Mallick P, Ho SM, Bracken B, Wu T. Impact of oxidative stress biomarkers and carboxymethyllysine (an advanced glycation end product) on prostate cancer: a prospective study. Clinical genitourinary cancer. 2015 Oct 1;13(5):e347-51.
30. Sasahira T, Kirita T, Bhawal UK, et al. Receptor for advanced glycation end products (RAGE) is important in the prediction of recurrence in human oral squamous cell carcinoma. Histopathology. 2007 Aug;51(2):166-72.
31. Rahimi F, Karimi J, Goodarzi MT, et al. Overexpression of receptor for advanced glycation end products (RAGE) in ovarian cancer. Cancer Biomarkers. 2017 Jan 1;18(1):61-8.
32. Jing R, Cui M, Wang J, Wang H. Receptor for advanced glycation end products (RAGE) soluble form (sRAGE): a new biomarker for lung cancer. Neoplasma. 2010 Jan 1;57(1):55-61.
33. Wang H, Li Y, Yu W, Ma L, Ji X, Xiao W. Expression of the receptor for advanced glycation end products and frequency of polymorphism in lung cancer. Oncology letters. 2015 Jul 1;10(1):51-60.
34. Kong SY, Takeuchi M, Hyogo H, et al. The Association between Glyceraldehyde-Derived Advanced Glycation End-Products and Colorectal Cancer RiskAdvanced Glycation End-Products and Colorectal Cancer Risk. Cancer Epidemiology, Biomarkers & Prevention. 2015 Dec 1;24(12):1855-63.
35. Aglago EK, Schalkwijk CG, Freisling H, et al. Plasma concentrations of advanced glycation end-products and colorectal cancer risk in the EPIC study. Carcinogenesis. 2021 May;42(5):705-13.
36. Wang D, Li T, Ye G, et al. Overexpression of the receptor for advanced glycation endproducts (RAGE) is associated with poor prognosis in gastric cancer. PloS one. 2015 Apr 10;10(4):e0122697.
37. Ishibashi Y, Matsui T, Takeuchi M, Yamagishi S. Metformin inhibits advanced glycation end products (AGEs)-induced growth and VEGF expression in MCF-7 breast cancer cells by suppressing AGEs receptor expression via AMP-activated protein kinase. Hormone and metabolic research. 2013 May;45(05):387-90.
38. Sharaf H, Matou-Nasri S, Wang Q, et al. Advanced glycation endproducts increase proliferation, migration and invasion of the breast cancer cell line MDA-MB-231. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2015 Mar 1;1852(3):429-41.
39. Lee KJ, Yoo JW, Kim YK, Choi JH, Ha TY, Gil M. Advanced glycation end products promote triple negative breast cancer cells via ERK and NF-κB pathway. Biochemical and biophysical research communications. 2018 Jan 15;495(3):2195-201.
40. Pan S, Guan Y, Ma Y, et al. Advanced glycation end products correlate with breast cancer metastasis by activating RAGE/TLR4 signaling. BMJ Open Diabetes Research and Care. 2022 Mar 1;10(2):e002697.
41. Nass N, Ignatov A, Andreas L, Weißenborn C, Kalinski T, Sel S. Accumulation of the advanced glycation end product carboxymethyl lysine in breast cancer is positively associated with estrogen receptor expression and unfavorable prognosis in estrogen receptor-negative cases. Histochemistry and cell biology. 2017 May;147(5):625-34.
42. Pan S, Guan Y, Ma Y, et al. Advanced glycation end products correlate with breast cancer metastasis by activating RAGE/TLR4 signaling. BMJ Open Diabetes Research and Care. 2022 Mar 1;10(2):e002697.
43. Walter KR, Ford ME, Gregoski MJ, et al. Advanced glycation end products are elevated in estrogen receptor-positive breast cancer patients, alter response to therapy, and can be targeted by lifestyle intervention. Breast cancer research and treatment. 2019 Feb;173(3):559-71.
44. Omofuma Od Glycation End-products (AGE) and Risk of Breast Cancer in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial (PLCO) Dietary Advanced Glycation End-products and Breast Cancer. Cancer Prevention Research. 2020 Jul 1;13O, Turner DP, Peterson LL, Merchant AT, Zhang J, Steck SE. Dietary Advance(7):601-10.
45. glycation end products and the risk of postmenopausal breast cancer in the National Institutes of Health‐AARP Diet and Health Study. Cancer. 2020 Jun 1;126(11):2648-57.Peterson LL, Park S, Park Y, Colditz GA, Anbardar N, Turner DP. Dietary advanced
2. Giaquinto AN, Sung H, Miller KD, et al. Breast cancer statistics, 2022. CA: A Cancer Journal for Clinicians. 2022 Nov;72(6):524-41.
3. Ahmadi H, Eslami B, Alipour S, Yazdankhahkenary A, Omranipour R. Impact of body mass index on breast cancer subtypes in Iranian women. Clinical Cancer Investigation Journal. 2019 Mar 1;8(2):52-.
4. Larsson SC, Mantzoros CS, Wolk A. Diabetes mellitus and risk of breast cancer: a meta‐analysis. International journal of cancer. 2007 Aug 15;121(4):856-62.
5. Nowotny K, Schröter D, Schreiner M, Grune T. Dietary advanced glycation end products and their relevance for human health. Ageing research reviews. 2018 Nov 1;47:55-66.
6. Yamagishi SI, Matsui T. Therapeutic potential of DNA-aptamers raised against AGE-RAGE axis in diabetes-related complications. Current Pharmaceutical Design. 2018 Jul 1;24(24):2802-9.
7. Dariya B, Nagaraju GP. Advanced glycation end products in diabetes, cancer and phytochemical therapy. Drug Discovery Today. 2020 Sep 1;25(9):1614-23.
8. Lin JA, Wu CH, Lu CC, Hsia SM, Yen GC. Glycative stress from advanced glycation end products (AGEs) and dicarbonyls: An emerging biological factor in cancer onset and progression. Molecular nutrition & food research. 2016 Aug;60(8):1850-64.
9. Malik P, Chaudhry N, Mittal R, Mukherjee TK. Role of receptor for advanced glycation end products in the complication and progression of various types of cancers. Biochimica et Biophysica Acta (BBA)-General Subjects. 2015 Sep 1;1850(9):1898-904.
10. Abe R, Shimizu T, Sugawara H, et al. Regulation of human melanoma growth and metastasis by AGE–AGE receptor interactions. Journal of Investigative Dermatology. 2004 Feb 1;122(2):461-7.
11. Schraml P, Bendik I, Ludwig CU. Differential messenger RNA and protein expression of the receptor for advanced glycosylated end products in normal lung and non-small cell lung carcinoma. Cancer research. 1997 Sep 1;57(17):3669-71.
12. Takada M, Koizumi T, Toyama H, Suzuki Y, Kuroda Y. Differential expression of RAGE in human pancreatic carcinoma cells. Hepato-gastroenterology. 2001 Nov 1;48(42):1577-8.
13. Kuniyasu H, Chihara Y, Kondo H. Differential effects between amphoterin and advanced glycation end products on colon cancer cells. International journal of cancer. 2003 May 10;104(6):722-7.
14. Hirata K, Takada M, Suzuki Y, Kuroda Y. Expression of receptor for advanced glycation end products (RAGE) in human biliary cancer cells. Hepato-gastroenterology. 2003 Sep 1;50(53):1205-7.
15. Bhawal UK, Ozaki Y, Nishimura M, et al. Association of expression of receptor for advanced glycation end products and invasive activity of oral squamous cell carcinoma. Oncology. 2005;69(3):246-55.
16. Ishiguro H, Nakaigawa N, Miyoshi Y, Fujinami K, Kubota Y, Uemura H. Receptor for advanced glycation end products (RAGE) and its ligand, amphoterin are overexpressed and associated with prostate cancer development. The Prostate. 2005 Jun 15;64(1):92-100.
17. Chen H, Wu L, Li Y, et al. Advanced glycation end products increase carbohydrate responsive element binding protein expression and promote cancer cell proliferation. Molecular and cellular endocrinology. 2014 Sep 1;395(1-2):69-78.
18. Menini S, Iacobini C, De Latouliere L,et al. . Diabetes promotes invasive pancreatic cancer by increasing systemic and tumour carbonyl stress in KrasG12D/+ mice. Journal of Experimental & Clinical Cancer Research. 2020 Dec;39(1):1-6.
19. Jiao L, Weinstein SJ, Albanes D, et al. Evidence That Serum Levels of the Soluble Receptor for Advanced Glycation End Products Are Inversely Associated with Pancreatic Cancer Risk: A Prospective StudyAdvanced Glycation End Products and Pancreatic Cancer. Cancer research. 2011 May 15;71(10):3582-9.
20. Jiao L, Stolzenberg-Solomon R, Zimmerman TP, et al. . Dietary consumption of advanced glycation end products and pancreatic cancer in the prospective NIH-AARP Diet and Health Study. The American journal of clinical nutrition. 2015 Jan 1;101(1):126-34.
21. Jiao L, Taylor PR, Weinstein SJ, et al. Advanced Glycation End Products, Soluble Receptor for Advanced Glycation End Products, and Risk of Colorectal CancersRAGE and Colorectal Cancer Risk. Cancer epidemiology, biomarkers & prevention. 2011 Jul 1;20(7):1430-8.
22. Grote VA, Nieters A, Kaaks R, et al. The Associations of Advanced Glycation End Products and Its Soluble Receptor with Pancreatic Cancer Risk: A Case–Control Study within the Prospective EPIC CohortAdvanced Glycation and Pancreatic Cancer Risk. Cancer epidemiology, biomarkers & prevention. 2012 Apr 1;21(4):619-28.
23. Moy KA, Jiao L, Freedman ND, et al. Soluble receptor for advanced glycation end products and risk of liver cancer. Hepatology. 2013 Jun;57(6):2338-45.
24. Mayén AL, Aglago EK, Knaze V, et al. Dietary intake of advanced glycation endproducts and risk of hepatobiliary cancers: A multinational cohort study. International journal of cancer. 2021 Aug 15;149(4):854-64.
25. Wada K, Nakashima Y, Yamakawa M, et al. Dietary advanced glycation end products and cancer risk in Japan: from the Takayama study. Cancer Science.
26. Córdova R, Mayén AL, Knaze V, et al. Dietary intake of advanced glycation endproducts (AGEs) and cancer risk across more than 20 anatomical sites: A multinational cohort study. Cancer Communications. 2022 Oct;42(10):1041-5.
27. van Heijst JW, Niessen HW, Hoekman K, Schalkwijk CG. Advanced Glycation End Products in Human Cancer Tissues: Detection of Nε‐(Carboxymethyl) lysine and Argpyrimidine. Annals of the New York Academy of Sciences. 2005 Jun;1043(1):725-33.
28. Foster D, Spruill L, Walter KR, et al. AGE Metabolites: A Biomarker Linked to Cancer Disparity? AGEs in Cancer Disparity. Cancer Epidemiology, Biomarkers & Prevention. 2014 Oct 1;23(10):2186-91.
29. Yang S, Pinney SM, Mallick P, Ho SM, Bracken B, Wu T. Impact of oxidative stress biomarkers and carboxymethyllysine (an advanced glycation end product) on prostate cancer: a prospective study. Clinical genitourinary cancer. 2015 Oct 1;13(5):e347-51.
30. Sasahira T, Kirita T, Bhawal UK, et al. Receptor for advanced glycation end products (RAGE) is important in the prediction of recurrence in human oral squamous cell carcinoma. Histopathology. 2007 Aug;51(2):166-72.
31. Rahimi F, Karimi J, Goodarzi MT, et al. Overexpression of receptor for advanced glycation end products (RAGE) in ovarian cancer. Cancer Biomarkers. 2017 Jan 1;18(1):61-8.
32. Jing R, Cui M, Wang J, Wang H. Receptor for advanced glycation end products (RAGE) soluble form (sRAGE): a new biomarker for lung cancer. Neoplasma. 2010 Jan 1;57(1):55-61.
33. Wang H, Li Y, Yu W, Ma L, Ji X, Xiao W. Expression of the receptor for advanced glycation end products and frequency of polymorphism in lung cancer. Oncology letters. 2015 Jul 1;10(1):51-60.
34. Kong SY, Takeuchi M, Hyogo H, et al. The Association between Glyceraldehyde-Derived Advanced Glycation End-Products and Colorectal Cancer RiskAdvanced Glycation End-Products and Colorectal Cancer Risk. Cancer Epidemiology, Biomarkers & Prevention. 2015 Dec 1;24(12):1855-63.
35. Aglago EK, Schalkwijk CG, Freisling H, et al. Plasma concentrations of advanced glycation end-products and colorectal cancer risk in the EPIC study. Carcinogenesis. 2021 May;42(5):705-13.
36. Wang D, Li T, Ye G, et al. Overexpression of the receptor for advanced glycation endproducts (RAGE) is associated with poor prognosis in gastric cancer. PloS one. 2015 Apr 10;10(4):e0122697.
37. Ishibashi Y, Matsui T, Takeuchi M, Yamagishi S. Metformin inhibits advanced glycation end products (AGEs)-induced growth and VEGF expression in MCF-7 breast cancer cells by suppressing AGEs receptor expression via AMP-activated protein kinase. Hormone and metabolic research. 2013 May;45(05):387-90.
38. Sharaf H, Matou-Nasri S, Wang Q, et al. Advanced glycation endproducts increase proliferation, migration and invasion of the breast cancer cell line MDA-MB-231. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2015 Mar 1;1852(3):429-41.
39. Lee KJ, Yoo JW, Kim YK, Choi JH, Ha TY, Gil M. Advanced glycation end products promote triple negative breast cancer cells via ERK and NF-κB pathway. Biochemical and biophysical research communications. 2018 Jan 15;495(3):2195-201.
40. Pan S, Guan Y, Ma Y, et al. Advanced glycation end products correlate with breast cancer metastasis by activating RAGE/TLR4 signaling. BMJ Open Diabetes Research and Care. 2022 Mar 1;10(2):e002697.
41. Nass N, Ignatov A, Andreas L, Weißenborn C, Kalinski T, Sel S. Accumulation of the advanced glycation end product carboxymethyl lysine in breast cancer is positively associated with estrogen receptor expression and unfavorable prognosis in estrogen receptor-negative cases. Histochemistry and cell biology. 2017 May;147(5):625-34.
42. Pan S, Guan Y, Ma Y, et al. Advanced glycation end products correlate with breast cancer metastasis by activating RAGE/TLR4 signaling. BMJ Open Diabetes Research and Care. 2022 Mar 1;10(2):e002697.
43. Walter KR, Ford ME, Gregoski MJ, et al. Advanced glycation end products are elevated in estrogen receptor-positive breast cancer patients, alter response to therapy, and can be targeted by lifestyle intervention. Breast cancer research and treatment. 2019 Feb;173(3):559-71.
44. Omofuma Od Glycation End-products (AGE) and Risk of Breast Cancer in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial (PLCO) Dietary Advanced Glycation End-products and Breast Cancer. Cancer Prevention Research. 2020 Jul 1;13O, Turner DP, Peterson LL, Merchant AT, Zhang J, Steck SE. Dietary Advance(7):601-10.
45. glycation end products and the risk of postmenopausal breast cancer in the National Institutes of Health‐AARP Diet and Health Study. Cancer. 2020 Jun 1;126(11):2648-57.Peterson LL, Park S, Park Y, Colditz GA, Anbardar N, Turner DP. Dietary advanced
| Files | ||
| Issue | Vol 14 No 2 (2022) | |
| Section | Reviews | |
| DOI | https://doi.org/10.18502/bccr.v14i2.14374 | |
| Keywords | ||
| Advanced glycation end products, Breast cancer, Carcinogenesis, Diet, Glycosilation | ||
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How to Cite
1.
Eskandari A, Alipour sadaf. Advanced glycation end products and breast cancer: a review of the literature. Basic Clin Cancer Res. 2023;14(2):70-77.
