Dietary advanced glycation end products (AGE) and female infertility

Öz

Advanced glycation end products (AGEs) are molecules formed by non-enzymatic reactions between reducing sugars and proteins, nucleic acids, or lipids. Advanced glycation end products may be formed endogenously under normal metabolic conditions or metabolic conditions such as diabetes and hyperglycemia, or exogenously during processing of foods at high temperatures and low humidity, including roasting, grilling, and frying. The accumulation of AGEs has a significant role in the development of disorders associated with infertility. Infertility is an increasingly common health problem in recent years. Dietary habits and nutrient intake are among the many factors affecting infertility in women. Receptor AGEs (RAGE) and AGEs have been observed in theca and granulosa cells of the ovaries. High levels of AGEs affect fertility through ovarian dysfunction, follicular growth, oocyte number, fertilization rate, embryo development, adverse effects on pregnancy rate, insulin resistance, apoptosis, endothelial dysfunction, increased inflammation, and reactive oxygen species (ROS). This review aims to investigate the pathophysiology of AGEs and their receptors, as well as their possible implications for female reproductive health.

Anahtar Kelimeler

• female infertility
• polycystic ovary syndrome
• advanced glycation end products

Diyet ileri glikasyon son ürünleri (AGE) ve kadın infertilitesi

Öz

İleri glikasyon son ürünleri (AGE), indirgen şekerler ile proteinler, nükleik asitler veya lipitler arasındaki enzimatik olmayan reaksiyonlar sonucu oluşan moleküllerdir. İleri glikasyon son ürünleri; normal metabolik koşullar veya diyabet, hiperglisemi gibi metabolik koşullarda endojen olarak oluşabildiği gibi, ızgara, kavurma ve kızartma dahil olmak üzere besinlerin yüksek sıcaklıklarda ve düşük nemde işlenmesi sırasında ekzojen olarak da oluşabilmektedir. İleri glikasyon son ürünlerinin birikimi infertilite ile ilişkili hastalıkların patogenezinde önemli bir rol oynamaktadır. İnfertilite, son yıllarda giderek yaygınlaşan bir sağlık sorundur. Kadınlarda infertiliteyi etkileyen birçok etmen arasında beslenme alışkanlıkları ve besin ögesi alımları da yer almaktadır. Reseptör AGE (RAGE) ve AGE’ler yumurtalıkların teka ve granülosa hücrelerinde gözlenmiştir. Yüksek AGE düzeyi; ovaryum disfonksiyonu, foliküler büyüme, oosit sayısı, fertilizasyon oranı, embriyo gelişimi, gebelik oranının olumsuz etkilenmesi, insülin direnci, apoptoz, endotel disfonksiyon, inflamasyon ve reaktif oksijen türlerinde (ROS) artış yollarıyla fertilite üzerinde etki göstermektedir. Bu derlemede, AGE’lerin ve reseptörlerinin patogenezi ve bunların kadın üreme sağlığı üzerindeki potansiyel etkileri incelenmiştir.

Anahtar Kelimeler

• ileri glikasyon son ürünleri
• kadın infertilitesi
• polikistik over sendromu

Kaynakça

1. Papagrigoraki A, Maurelli M, Del Giglio M, Gisondi P, Girolomoni G. Advanced Glycation End Products in the Pathogenesis of Psoriasis. Int J Mol Sci. 2017;18(11):2471.
2. Kang Q, Dai H, Jiang S, Yu L. Advanced glycation end products in diabetic retinopathy and phytochemical therapy. Front Nutr. 2022;9:1037186.
3. Santos HO, Penha-Silva N. Translating the advanced glycation end products (AGEs) knowledge into real-world nutrition strategies. European journal of clinical nutrition. 2022;76(7):922-8.
4. Zhu JL, Cai YQ, Long SL, Chen Z, Mo ZC. The role of advanced glycation end products in human infertility. Life Sci. 2020;255:117830.
5. Khalid M, Petroianu G, Adem A. Advanced glycation end products and diabetes mellitus: Mechanisms and perspectives. Biomolecules. 2022;12(4):542.
6. 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;11(8):1312.
7. Snelson M, Coughlan MT. Dietary Advanced Glycation End Products: Digestion, Metabolism and Modulation of Gut Microbial Ecology. Nutrients. 2019;11(2):215.
8. Perrone A, Giovino A, Benny J, Martinelli F. Advanced Glycation End Products (AGEs): Biochemistry, Signaling, Analytical Methods, and Epigenetic Effects. Oxidative medicine and cellular longevity. 2020;2020:3818196-.

9. Ottum MS, Mistry AM. Advanced glycation end-products: modifiable environmental factors profoundly mediate insulin resistance. J Clin Biochem Nutr. 2015;57(1):1-12.
10. Uribarri J, del Castillo MD, de la Maza MP, Filip R, Gugliucci A, Luevano-Contreras C, et al. Dietary advanced glycation end products and their role in health and disease. Advances in nutrition. 2015;6(4):461-73.
11. Uribarri J, Woodruff S, Goodman S, Cai W, Chen X, Pyzik R, et al. Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc. 2010;110(6):911-16.e12.
12. Nie C, Li Y, Qian H, Ying H, Wang L. Advanced glycation end products in food and their effects on intestinal tract. Crit Rev Food Sci Nutr. 2022;62(11):3103-15.
13. Uribarri J, Cai W, Sandu O, Peppa M, Goldberg T, Vlassara H. Diet‐derived advanced glycation end products are major contributors to the body's AGE pool and induce inflammation in healthy subjects. Annals of the New York Academy of Sciences. 2005;1043(1):461-6.
14. Jara N, Leal M, Bunout D, Hirsch S, Barrera G, Leiva L, et al. Dietary intake increases serum levels of carboxymethil-lysine (CML) in diabetic patients. Nutrición Hospitalaria. 2012;27(4):1272-8.
15. Uribarri J, Cai W, Pyzik R, Goodman S, Chen X, Zhu L, et al. Suppression of native defense mechanisms, SIRT1 and PPARγ, by dietary glycoxidants precedes disease in adult humans; relevance to lifestyle-engendered chronic diseases. Amino Acids. 2014;46:301-9.
16. Cordova R, Knaze V, Viallon V, Rust P, Schalkwijk C, Weiderpass E, et al. Dietary intake of advanced glycation end products (AGEs) and changes in body weight in European adults. European journal of nutrition. 2020;59:2893-904.
17. Mayén AL, Aglago EK, Knaze V, Cordova R, Schalkwijk CG, Wagner KH, et al. Dietary intake of advanced glycation endproducts and risk of hepatobiliary cancers: A multinational cohort study. International journal of cancer. 2021;149(4):854-64.
18. Waqas K, Chen J, Lu T, van der Eerden B, Rivadeneira F, Uitterlinden AG, et al. Dietary advanced glycation end-products (dAGEs) intake and its relation to sarcopenia and frailty–The Rotterdam Study. Bone. 2022;165:116564.
19. Nowotny K, Schröter D, Schreiner M, Grune T. Dietary advanced glycation end products and their relevance for human health. Ageing research reviews. 2018;47:55-66.
20. Zawada A, Machowiak A, Rychter AM, Ratajczak AE, Szymczak-Tomczak A, Dobrowolska A, et al. Accumulation of Advanced Glycation End-Products in the Body and Dietary Habits. Nutrients. 2022;14(19):3982.
21. D'Cunha NM, Sergi D, Lane MM, Naumovski N, Gamage E, Rajendran A, et al. The Effects of Dietary Advanced Glycation End-Products on Neurocognitive and Mental Disorders. Nutrients. 2022;14(12):2421.
22. Ribeiro PVM, Tavares JF, Costa MAC, Mattar JB, Alfenas RCG. Effect of reducing dietary advanced glycation end products on obesity-associated complications: a systematic review. Nutr Rev. 2019;77(10):725-34.
23. Kellow NJ, Coughlan MT. Effect of diet-derived advanced glycation end products on inflammation. Nutr Rev. 2015;73(11):737-59.
24. Bansal S, Burman A, Tripathi AK. Advanced glycation end products: Key mediator and therapeutic target of cardiovascular complications in diabetes. World Journal of Diabetes. 2023;14(8):1146.
25. Poulsen MW, Hedegaard RV, Andersen JM, de Courten B, Bügel S, Nielsen J, et al. Advanced glycation endproducts in food and their effects on health. Food and Chemical Toxicology. 2013;60:10-37.
26. Chen J-H, Lin X, Bu C, Zhang X. Role of advanced glycation end products in mobility and considerations in possible dietary and nutritional intervention strategies. Nutrition & metabolism. 2018;15(1):72.
27. Gill V, Kumar V, Singh K, Kumar A, Kim J-J. Advanced glycation end products (AGEs) may be a striking link between modern diet and health. Biomolecules. 2019;9(12):888.
28. Koschinsky T, He CJ, Mitsuhashi T, Bucala R, Liu C, Buenting C, et al. Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci U S A. 1997;94(12):6474-9.
29. Zhao D, Sheng B, Wu Y, Li H, Xu D, Nian Y, et al. Comparison of free and bound advanced glycation end products in food: A review on the possible influence on human health. Journal of agricultural and food chemistry. 2019;67(51):14007-18.
30. Sergi D, Boulestin H, Campbell FM, Williams LM. The role of dietary advanced glycation end products in metabolic dysfunction. Molecular Nutrition & Food Research. 2021;65(1):1900934.
31. Erusalimsky JD. The use of the soluble receptor for advanced glycation-end products (sRAGE) as a potential biomarker of disease risk and adverse outcomes. Redox Biol. 2021;42:101958.
32. 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.
33. Salazar J, Navarro C, Ortega Á, Nava M, Morillo D, Torres W, et al. Advanced glycation end products: new clinical and molecular perspectives. Int J Environ Res Public Health. 2021;18(14):7236.
34. Steenbeke M, De Bruyne S, De Buyzere M, Lapauw B, Speeckaert R, Petrovic M, et al. The role of soluble receptor for advanced glycation end-products (sRAGE) in the general population and patients with diabetes mellitus with a focus on renal function and overall outcome. Crit Rev Clin Lab Sci. 2021;58(2):113-30.
35. Prasad K. Is there any evidence that AGE/sRAGE is a universal biomarker/risk marker for diseases? Mol Cell Biochem. 2019;451(1-2):139-44.
36. Peppa M, Mavroeidi I. Experimental Animal Studies Support the Role of Dietary Advanced Glycation End Products in Health and Disease. Nutrients. 2021;13(10).
37. World Health Organization (WHO). Infertility 2020 [Available from: https://www.who.int/news-room/fact-sheets/detail/infertility. Accessed July 28, 2023
38. Centers for Disease Control and Prevention (CDC). Reproductive Health. İnfertility FAQs. 2022 [Available from: https://www.cdc.gov/reproductivehealth/infertility/index.htm. Accessed July 28, 2023
39. World Health Organization (WHO). Infertility. [Available from: https://www.who.int/health-topics/infertility#tab=tab_1. Accessed July 28, 2023
40. Carson SA, Kallen AN. Diagnosis and Management of Infertility: A Review. Jama. 2021;326(1):65-76.
41. Tamrakar SR, Bastakoti R. Determinants of Infertility in Couples. J Nepal Health Res Counc. 2019;17(1):85-9.
42. Bala R, Singh V, Rajender S, Singh K. Environment, Lifestyle, and Female Infertility. Reprod Sci. 2021;28(3):617-38.
43. Zauner G, Girardi G. Potential causes of male and female infertility in Qatar. J Reprod Immunol. 2020;141:103173.
44. Chen J, Fang Y, Xu Y, Sun H. Role of m6A modification in female infertility and reproductive system diseases. Int J Biol Sci. 2022;18(9):3592-604.
45. Zheng W, Hu H, Zhang S, Xu X, Gao Y, Gong F, et al. The comprehensive variant and phenotypic spectrum of TUBB8 in female infertility. J Assist Reprod Genet. 2021;38(9):2261-72.
46. Benjamin JJ, Koshy T, Kumar KM, Maruthy KN, Padmavathi R. Meta-analysis of association between il-6-174 g/c polymorphism and female infertility related disorders. J Reprod Immunol. 2020;140:103134.
47. Wasilewski T, Łukaszewicz-Zając M, Wasilewska J, Mroczko B. Biochemistry of infertility. Clin Chim Acta. 2020;508:185-90.
48. Merhi Z. Advanced glycation end products and their relevance in female reproduction. Hum Reprod. 2014;29(1):135-45.
49. Collée J, Mawet M, Tebache L, Nisolle M, Brichant G. Polycystic ovarian syndrome and infertility: overview and insights of the putative treatments. Gynecol Endocrinol. 2021;37(10):869-74.
50. Sadeghi HM, Adeli I, Calina D, Docea AO, Mousavi T, Daniali M, et al. Polycystic Ovary Syndrome: A Comprehensive Review of Pathogenesis, Management, and Drug Repurposing. Int J Mol Sci. 2022;23(2):583.
51. Christakou C, Economou F, Livadas S, Piperi C, Adamopoulos C, Marinakis E, et al. Strong and positive association of endothelin-1 with AGEs in PCOS: a causal relationship or a bystander? Hormones (Athens). 2011;10(4):292-7.
52. Diamanti-Kandarakis E, Piperi C, Kalofoutis A, Creatsas G. Increased levels of serum advanced glycation end-products in women with polycystic ovary syndrome. Clin Endocrinol (Oxf). 2005;62(1):37-43.
53. Wang B, Li J, Yang Q, Zhang F, Hao M, Guo Y. Decreased levels of sRAGE in follicular fluid from patients with PCOS. Reproduction. 2017;153(3):285-92.
54. Garg D, Grazi R, Lambert-Messerlian GM, Merhi Z. Correlation between follicular fluid levels of sRAGE and vitamin D in women with PCOS. J Assist Reprod Genet. 2017;34(11):1507-13.
55. Chatzigeorgiou A, Kandaraki E, Piperi C, Livadas S, Papavassiliou AG, Koutsilieris M, et al. Dietary glycotoxins affect scavenger receptor expression and the hormonal profile of female rats. J Endocrinol. 2013;218(3):331-7.
56. Diamanti-Kandarakis E, Piperi C, Patsouris E, Korkolopoulou P, Panidis D, Pawelczyk L, et al. Immunohistochemical localization of advanced glycation end-products (AGEs) and their receptor (RAGE) in polycystic and normal ovaries. Histochem Cell Biol. 2007;127(6):581-9.
57. Azhary JMK, Harada M, Kunitomi C, Kusamoto A, Takahashi N, Nose E, et al. Androgens Increase Accumulation of Advanced Glycation End Products in Granulosa Cells by Activating ER Stress in PCOS. Endocrinology. 2020;161(2):bqaa015..
58. Toulis KA, Goulis DG, Mintziori G, Kintiraki E, Eukarpidis E, Mouratoglou SA, et al. Meta-analysis of cardiovascular disease risk markers in women with polycystic ovary syndrome. Hum Reprod Update. 2011;17(6):741-60.
59. Irani M, Minkoff H, Seifer DB, Merhi Z. Vitamin D increases serum levels of the soluble receptor for advanced glycation end products in women with PCOS. J Clin Endocrinol Metab. 2014;99(5):E886-90.
60. Liao Y, Huang R, Sun Y, Yue J, Zheng J, Wang L, et al. An inverse association between serum soluble receptor of advanced glycation end products and hyperandrogenism and potential implication in polycystic ovary syndrome patients. Reprod Biol Endocrinol. 2017;15(1):9.
61. Emami N, Alizadeh A, Maleki-Hajiagha A, Dizavi A, Vesali S, Moini A. Serum and follicular fluid levels of soluble receptor for advanced glycation end-products in women with and without polycystic ovary syndrome. J Ovarian Res. 2023;16(1):127.
62. Zeng X, Xie YJ, Liu YT, Long SL, Mo ZC. Polycystic ovarian syndrome: Correlation between hyperandrogenism, insulin resistance and obesity. Clin Chim Acta. 2020;502:214-21.
63. Diamanti-Kandarakis E, Piperi C, Korkolopoulou P, Kandaraki E, Levidou G, Papalois A, et al. Accumulation of dietary glycotoxins in the reproductive system of normal female rats. Journal of molecular medicine (Berlin, Germany). 2007;85:1413-20.
64. Tong YW, Ko JKY, Lam KSL, Tam S, Lee VCY, Ho PC, et al. Advanced glycation end-products and its soluble receptor are not independent predictors of incident dysglycaemia or metabolic syndrome in women with polycystic ovary syndrome: a prospective observational study. Reprod Biol Endocrinol. 2023;21(1):41.
65. Tantalaki E, Piperi C, Livadas S, Kollias A, Adamopoulos C, Koulouri A, et al. Impact of dietary modification of advanced glycation end products (AGEs) on the hormonal and metabolic profile of women with polycystic ovary syndrome (PCOS). Hormones (Athens). 2014;13(1):65-73.
66. Goudarzi R, Sedaghat M, Hedayati M, Hekmatdoost A, Sohrab G. Low advanced Glycation end product diet improves the central obesity, insulin resistance and inflammatory profiles in Iranian patients with metabolic syndrome: a randomized clinical trial. J Diabetes Metab Disord. 2020;19(2):1129-38.
67. de Courten B, de Courten MP, Soldatos G, Dougherty SL, Straznicky N, Schlaich M, et al. Diet low in advanced glycation end products increases insulin sensitivity in healthy overweight individuals: a double-blind, randomized, crossover trial. Am J Clin Nutr. 2016;103(6):1426-33.
68. Mark AB, Poulsen MW, Andersen S, Andersen JM, Bak MJ, Ritz C, et al. Consumption of a diet low in advanced glycation end products for 4 weeks improves insulin sensitivity in overweight women. Diabetes Care. 2014;37(1):88-95.
69. Sohouli MH, Fatahi S, Sharifi-Zahabi E, Santos HO, Tripathi N, Lari A, et al. The Impact of Low Advanced Glycation End Products Diet on Metabolic Risk Factors: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Adv Nutr. 2021;12(3):766-76.
70. Sohouli MH, Sharifi-Zahabi E, Lari A, Fatahi S, Shidfar F. The impact of low advanced glycation end products diet on obesity and related hormones: a systematic review and meta-analysis. Sci Rep. 2020;10(1):22194.
71. Oliveira JS, de Almeida C, de Souza  MN, da Cruz LD, Alfenas RCG. Effect of dietary advanced glycation end-products restriction on type 2 diabetes mellitus control: a systematic review. Nutr Rev. 2022;80(2):294-305.
72. Demirer B, Yardımcı H, Erem Basmaz S. Inflammation level in type 2 diabetes is associated with dietary advanced glycation end products, Mediterranean diet adherence and oxidative balance score: A pathway analysis. J Diabetes Complications. 2023;37(1):108354.
73. Rodríguez JM, Leiva Balich L, Concha MJ, Mizón C, Bunout Barnett D, Barrera Acevedo G, et al. Reduction of serum advanced glycation end-products with a low calorie Mediterranean diet. Nutr Hosp. 2015;31(6):2511-7.
74. Lopez-Moreno J, Quintana-Navarro GM, Delgado-Lista J, Garcia-Rios A, Alcala-Diaz JF, Gomez-Delgado F, et al. Mediterranean Diet Supplemented With Coenzyme Q10 Modulates the Postprandial Metabolism of Advanced Glycation End Products in Elderly Men and Women. J Gerontol A Biol Sci Med Sci. 2018;73(3):340-6.
75. Diamanti-Kandarakis E, Chatzigeorgiou A, Papageorgiou E, Koundouras D, Koutsilieris M. Advanced glycation end-products and insulin signaling in granulosa cells. Exp Biol Med (Maywood). 2016;241(13):1438-45.
76. Silber M, Miller I, Bar-Joseph H, Ben-Ami I, Shalgi R. Elucidating the role of pigment epithelium-derived factor (PEDF) in metabolic PCOS models. J Endocrinol. 2020;244(2):297-308.
77. Imbar T, Klipper E, Greenfield C, Hurwitz A, Haimov-Kochman R, Meidan R. Altered endothelin expression in granulosa-lutein cells of women with polycystic ovary syndrome. Life Sci. 2012;91(13-14):703-9.
78. Rashad NM, Ateya MA, Saraya YS, Elnagar WM, Helal KF, Lashin ME, et al. Association of miRNA - 320 expression level and its target gene endothelin-1 with the susceptibility and clinical features of polycystic ovary syndrome. J Ovarian Res. 2019;12(1):39.
79. Zhang C, Ma J, Wang W, Sun Y, Sun K. Lysyl oxidase blockade ameliorates anovulation in polycystic ovary syndrome. Hum Reprod. 2018;33(11):2096-106.
80. Berbrier DE, Leone CA, Adler TE, Bender JR, Taylor HS, Stachenfeld NS, et al. Effects of androgen excess and body mass index on endothelial function in women with polycystic ovary syndrome. J Appl Physiol (1985). 2023;134(4):868-78.
81. de la Cruz-Ares S, Cardelo MP, Gutiérrez-Mariscal FM, Torres-Peña JD, García-Rios A, Katsiki N, et al. Endothelial Dysfunction and Advanced Glycation End Products in Patients with Newly Diagnosed Versus Established Diabetes: From the CORDIOPREV Study. Nutrients. 2020;12(1):238.
82. Dube R. Does endothelial dysfunction correlate with endocrinal abnormalities in patients with polycystic ovary syndrome? Avicenna J Med. 2016;6(4):91-102.
83. Pertynska-Marczewska M, Diamanti-Kandarakis E, Zhang J, Merhi Z. Advanced glycation end products: A link between metabolic and endothelial dysfunction in polycystic ovary syndrome? Metabolism. 2015;64(11):1564-73.
84. Stirban A, Negrean M, Stratmann B, Gawlowski T, Horstmann T, Götting C, et al. Benfotiamine prevents macro- and microvascular endothelial dysfunction and oxidative stress following a meal rich in advanced glycation end products in individuals with type 2 diabetes. Diabetes Care. 2006;29(9):2064-71.
85. Kellow NJ, Savige GS. Dietary advanced glycation end-product restriction for the attenuation of insulin resistance, oxidative stress and endothelial dysfunction: a systematic review. Eur J Clin Nutr. 2013;67(3):239-48.
86. Adamopoulos C, Piperi C, Gargalionis AN, Dalagiorgou G, Spilioti E, Korkolopoulou P, et al. Advanced glycation end products upregulate lysyl oxidase and endothelin-1 in human aortic endothelial cells via parallel activation of ERK1/2-NF-κB and JNK-AP-1 signaling pathways. Cell Mol Life Sci. 2016;73(8):1685-98.
87. Papachroni KK, Piperi C, Levidou G, Korkolopoulou P, Pawelczyk L, Diamanti-Kandarakis E, et al. Lysyl oxidase interacts with AGE signalling to modulate collagen synthesis in polycystic ovarian tissue. J Cell Mol Med. 2010;14(10):2460-9.
88. Mancini A, Bruno C, Vergani E, d'Abate C, Giacchi E, Silvestrini A. Oxidative Stress and Low-Grade Inflammation in Polycystic Ovary Syndrome: Controversies and New Insights. Int J Mol Sci. 2021;22(4):1667.
89. Li W, Liu C, Yang Q, Zhou Y, Liu M, Shan H. Oxidative stress and antioxidant imbalance in ovulation disorder in patients with polycystic ovary syndrome. Front Nutr. 2022;9:1018674.
90. El-Bassossy HM, Neamatallah T, Balamash KS, Abushareb AT, Watson ML. Arginase overexpression and NADPH oxidase stimulation underlie impaired vasodilation induced by advanced glycation end products. Biochem Biophys Res Commun. 2018;499(4):992-7.
91. Guimarães EL, Empsen C, Geerts A, van Grunsven LA. Advanced glycation end products induce production of reactive oxygen species via the activation of NADPH oxidase in murine hepatic stellate cells. J Hepatol. 2010;52(3):389-97.
92. Dabravolski SA, Nikiforov NG, Eid AH, Nedosugova LV, Starodubova AV, Popkova TV, et al. Mitochondrial Dysfunction and Chronic Inflammation in Polycystic Ovary Syndrome. Int J Mol Sci. 2021;22(8):3923.
93. Takahashi N, Harada M, Azhary JMK, Kunitomi C, Nose E, Terao H, et al. Accumulation of advanced glycation end products in follicles is associated with poor oocyte developmental competence. Mol Hum Reprod. 2019;25(11):684-94.
94. Wang BJ, Qian L, Li J, Wang F, Yang QL, Li G, et al. sRAGE plays a role as a protective factor in the development of PCOS by inhibiting inflammation. Gynecol Endocrinol. 2020;36(2):148-51.
95. Gutierrez-Mariscal FM, Cardelo MP, de la Cruz S, Alcala-Diaz JF, Roncero-Ramos I, Guler I, et al. Reduction in Circulating Advanced Glycation End Products by Mediterranean Diet Is Associated with Increased Likelihood of Type 2 Diabetes Remission in Patients with Coronary Heart Disease: From the Cordioprev Study. Mol Nutr Food Res. 2021;65(1):e1901290.
96. 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. Biochem Biophys Res Commun. 2018;495(3):2195-201.
97. Nonaka K, Kajiura Y, Bando M, Sakamoto E, Inagaki Y, Lew JH, et al. Advanced glycation end-products increase IL-6 and ICAM-1 expression via RAGE, MAPK and NF-κB pathways in human gingival fibroblasts. J Periodontal Res. 2018;53(3):334-44.
98. Chen H, Liu W, Wu X, Gou M, Shen J, Wang H. Advanced glycation end products induced IL-6 and VEGF-A production and apoptosis in osteocyte-like MLO-Y4 cells by activating RAGE and ERK1/2, P38 and STAT3 signalling pathways. Int Immunopharmacol. 2017;52:143-9.
99. Chen YJ, Chan DC, Chiang CK, Wang CC, Yang TH, Lan KC, et al. Advanced glycation end-products induced VEGF production and inflammatory responses in human synoviocytes via RAGE-NF-κB pathway activation. J Orthop Res. 2016;34(5):791-800.
100. Ohashi K, Takahashi HK, Mori S, Liu K, Wake H, Sadamori H, et al. Advanced glycation end products enhance monocyte activation during human mixed lymphocyte reaction. Clin Immunol. 2010;134(3):345-53.
101. Jin X, Yao T, Zhou Z, Zhu J, Zhang S, Hu W, et al. Advanced Glycation End Products Enhance Macrophages Polarization into M1 Phenotype through Activating RAGE/NF-κB Pathway. Biomed Res Int. 2015;2015:732450.
102. Seno K, Sase S, Ozeki A, Takahashi H, Ohkuchi A, Suzuki H, et al. Advanced glycation end products regulate interleukin-1β production in human placenta. J Reprod Dev. 2017;63(4):401-8.
103. Jhun J, Lee S, Kim H, Her YM, Byun JK, Kim EK, et al. HMGB1/RAGE induces IL-17 expression to exaggerate inflammation in peripheral blood cells of hepatitis B patients. J Transl Med. 2015;13:310.
104. Kandaraki E, Chatzigeorgiou A, Piperi C, Palioura E, Palimeri S, Korkolopoulou P, et al. Reduced ovarian glyoxalase-I activity by dietary glycotoxins and androgen excess: a causative link to polycystic ovarian syndrome. Mol Med. 2012;18(1):1183-9.
105. Merhi Z, Buyuk E, Cipolla M. Advanced glycation end products alter steroidogenic gene expression by granulosa cells: an effect partially reversible by vitamin D. MHR: Basic science of reproductive medicine. 2018;24(6):318-26.
106. Merhi Z, Du XQ, Charron MJ. Perinatal exposure to high dietary advanced glycation end products affects the reproductive system in female offspring in mice. Mol Hum Reprod. 2020;26(8):615-23.
107. Kandaraki EA, Chatzigeorgiou A, Papageorgiou E, Piperi C, Adamopoulos C, Papavassiliou AG, et al. Advanced glycation end products interfere in luteinizing hormone and follicle stimulating hormone signaling in human granulosa KGN cells. Exp Biol Med (Maywood). 2018;243(1):29-33.
108. Merhi Z. Vitamin D attenuates the effect of advanced glycation end products on anti-Mullerian hormone signaling. Mol Cell Endocrinol. 2019;479:87-92.
109. Merhi Z, Irani M, Doswell AD, Ambroggio J. Follicular fluid soluble receptor for advanced glycation end-products (sRAGE): a potential indicator of ovarian reserve. The Journal of Clinical Endocrinology & Metabolism. 2014;99(2):E226-E33.
110. Li YJ, Chen JH, Sun P, Li JJ, Liang XY. Intrafollicular soluble RAGE benefits embryo development and predicts clinical pregnancy in infertile patients of advanced maternal age undergoing in vitro fertilization. J Huazhong Univ Sci Technolog Med Sci. 2017;37(2):243-7.
111. Yao Q, Liang Y, Shao Y, Bian W, Fu H, Xu J, et al. Advanced glycation end product concentrations in follicular fluid of women undergoing IVF/ICSI with a GnRH agonist protocol. Reproductive BioMedicine Online. 2018;36(1):20-5.
112. Iyer RP, Thalakkattoor FL, Pillai A, Tharadevi P, Krishnan S, Nagaraj A. Association of Follicular Fluid Advanced Glycation End-Products with Oocyte Response and Clinical Pregnancy in Assisted Reproduction Cycles. J Hum Reprod Sci. 2021;14(1):42-8.
113. Seven B, Tascı Y, Gülerman C, Candar T, Kokanalı K, Yüksel Y, et al. Do follicular fluid advanced glycation end products levels affect the ovarian response in unexplained infertility? Gynecol Endocrinol. 2021;37(9):802-6.
114. Ravichandran G, Lakshmanan DK, Raju K, Elangovan A, Nambirajan G, Devanesan AA, et al. Food advanced glycation end products as potential endocrine disruptors: An emerging threat to contemporary and future generation. Environ Int. 2019;123:486-500.
115. Zhu J-l, Cai Y-q, Long S-l, Chen Z, Mo Z-C. The role of advanced glycation end products in human infertility. Life Sciences. 2020;255:117830.