Protein Glycation: An Old Villain is Shedding Secrets

Author(s): Gerald H. Lushington*, Anthony C. Barnes.

Journal Name: Combinatorial Chemistry & High Throughput Screening
Accelerated Technologies for Biotechnology, Bioassays, Medicinal Chemistry and Natural Products Research

Volume 22 , Issue 6 , 2019

Become EABM
Become Reviewer

Abstract:

The glycation of proteins is non-physiological post-translational incorporation of carbohydrates onto the free amines or guanidines of proteins and some lipids. Although the existence of glycated proteins has been known for forty years, a full understanding of their pathogenic nature has been slow in accruing. In recent years, however, glycation has gained widespread acceptance as a contributing factor in numerous metabolic, autoimmune, and neurological disorders, tying together several confounding aspects of disease etiology. From diabetes, arthritis, and lupus, to multiple sclerosis, amyotrophic lateral sclerosis, Alzheimer’s, and Parkinson’s diseases, an emerging glycation/inflammation paradigm now offers significant new insight into a physiologically important toxicological phenomenon. It exposes novel drug targets and treatment options, and may even lay foundations for long-awaited breakthroughs.

This ‘current frontier’ article briefly profiles current knowledge regarding the underlying causes of glycation, the structural biology implications of such modifications, and their pathological consequences. Although several emerging therapeutic strategies for addressing glycation pathologies are introduced, the primary purpose of this mini-review is to raise awareness of the challenges and opportunities inherent in this emerging new medicinal target area.

Keywords: Glycation, glycotoxicity, Advanced Glycation End-products (AGE), inflammation, autoimmune, diabetes, lupus, NPSLE, neurodegeneration.

[1]
Koschinsky, T.; He, C-J.; Mitsuhashi, T.; Bucala, R.; Liu, C.; Buenting, C.; Heitmann, K.; Vlassara, H. Orally absorbed reactive glycation products (glycotoxins): An environmental risk factor in diabetic nephropathy. Proc. Natl. Acad. Sci. USA, 1997, 94(12), 6474-6479.
[http://dx.doi.org/10.1073/pnas.94.12.6474] [PMID: 9177242]
[2]
Monnier, V.M.; Stevens, V.J.; Cerami, A. Nonenzymatic glycosylation, sulfhydryl oxidation, and aggregation of lens proteins in experimental sugar cataracts. J. Exp. Med., 1979, 150(5), 1098-1107.
[http://dx.doi.org/10.1084/jem.150.5.1098] [PMID: 501285]
[3]
Zimmerman, G.A.; Meistrell, M., III; Bloom, O.; Cockroft, K.M.; Bianchi, M.; Risucci, D.; Broome, J.; Farmer, P.; Cerami, A.; Vlassara, H. Neurotoxicity of advanced glycation endproducts during focal stroke and neuroprotective effects of aminoguanidine. Proc. Natl. Acad. Sci. USA, 1995, 92(9), 3744-3748.
[http://dx.doi.org/10.1073/pnas.92.9.3744] [PMID: 7731977]
[4]
Yan, S.D.; Chen, X.; Fu, J.; Chen, M.; Zhu, H.; Roher, A.; Slattery, T.; Zhao, L.; Nagashima, M.; Morser, J.; Migheli, A.; Nawroth, P.; Stern, D.; Schmidt, A.M. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer’s disease. Nature, 1996, 382(6593), 685-691.
[http://dx.doi.org/10.1038/382685a0] [PMID: 8751438]
[5]
DeChristopher, L.R. Perspective: The paradox in dietary advanced glycation end products research-the source of the serum and urinary advanced glycation end products is the intestines, not the food. Adv. Nutr., 2017, 8(5), 679-683.
[http://dx.doi.org/10.3945/an.117.016154] [PMID: 28916568]
[6]
Fishman, S.L.; Sonmez, H.; Basman, C.; Singh, V.; Poretsky, L. The role of advanced glycation end-products in the development of coronary artery disease in patients with and without diabetes mellitus: A review. Mol. Med., 2018, 24(1), 59.
[http://dx.doi.org/10.1186/s10020-018-0060-3] [PMID: 30470170]
[7]
Brownlee, M.; Cerami, A.; Vlassara, H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med., 1988, 318(20), 1315-1321.
[http://dx.doi.org/10.1056/NEJM198805193182007] [PMID: 3283558]
[8]
Taniguchi, N.; Takahashi, M.; Kizuka, Y.; Kitazume, S.; Shuvaev, V.V.; Ookawara, T.; Furuta, A. Glycation vs. glycosylation: a tale of two different chemistries and biology in Alzheimer’s disease. Glycoconj. J., 2016, 33(4), 487-497.
[http://dx.doi.org/10.1007/s10719-016-9690-2] [PMID: 27325408]
[9]
Chilukuri, H.; Kulkarni, M.J.; Fernandes, M. Revisiting amino acids and peptides as anti-glycation agents. MedChemComm, 2018, 9(4), 614-624.
[http://dx.doi.org/10.1039/C7MD00514H] [PMID: 30108952]
[10]
Bathaie, Z.; Bahmani, F.; Farajzadeh, A. Role of Amino Acids on Prevention of Nonenzymatic Glycation of Lens Proteins in Senile and Diabetic Cataracts. In: Handbook of Nutrition, Diet and the Eye; Preedy, V., Ed.; Academic Press: Oxford, UK, 2014; pp. 141-155.
[http://dx.doi.org/10.1016/B978-0-12-401717-7.00015-0]
[11]
Hsia, T.C.; Yin, M.C.; Mong, M.C. Advanced glycation end-products enhance lung cancer cell invasion and migration. Int. J. Mol. Sci., 2016, 17(8)E1289
[http://dx.doi.org/10.3390/ijms17081289] [PMID: 27517907]
[12]
Pankov, R.; Yamada, K.M. Fibronectin at a glance. J. Cell Sci., 2002, 115(Pt 20), 3861-3863.
[http://dx.doi.org/10.1242/jcs.00059] [PMID: 12244123]
[13]
Fournet, M.; Bonté, F.; Desmoulière, A. Glycation damage: A possible hub for major pathophysiological disorders and aging. Aging Dis., 2018, 9(5), 880-900.
[http://dx.doi.org/10.14336/AD.2017.1121] [PMID: 30271665]
[14]
Labat-Robert, J.; Leutenegger, M.; Llopis, G.; Ricard, Y.; Derouette, J.C. Plasma and tissue fibronectin in diabetes. Clin. Physiol. Biochem., 1984, 2(1), 39-48.
[PMID: 6386277]
[15]
Terrell, J.R.; Gumpper, R.H.; Luo, M. Hemoglobin crystals immersed in liquid oxygen reveal diffusion channels. Biochem. Biophys. Res. Commun., 2018, 495(2), 1858-1863.
[http://dx.doi.org/10.1016/j.bbrc.2017.12.038] [PMID: 29246762]
[16]
Saraswathi, N.T.; Syakhovich, V.E.; Bokut, S.B.; Moras, D.; Ruff, M. Crystal Structure of Glycated Human Haemoglobin., 2007.Available at. https://www.rcsb.org/structure/3b75
[17]
Lee, E.J.; Kim, J.Y.; Oh, S.H. Advanced glycation end products (AGEs) promote melanogenesis through receptor for AGEs. Sci. Rep., 2016, 6, 27848.
[http://dx.doi.org/10.1038/srep27848] [PMID: 27293210]
[18]
Nowotny, K.; Jung, T.; Höhn, A.; Weber, D.; Grune, T. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules, 2015, 5(1), 194-222.
[http://dx.doi.org/10.3390/biom5010194] [PMID: 25786107]
[19]
Fournet, M.; Bonté, F.; Desmoulière, A. Glycation damage: A possible hub for major pathophysiological disorders and aging. Aging Dis., 2018, 9(5), 880-900.
[http://dx.doi.org/10.14336/AD.2017.1121] [PMID: 30271665]
[20]
Singh, V.P.; Bali, A.; Singh, N.; Jaggi, A.S. Advanced glycation end products and diabetic complications. Korean J. Physiol. Pharmacol., 2014, 18(1), 1-14.
[http://dx.doi.org/10.4196/kjpp.2014.18.1.1] [PMID: 24634591]
[21]
Lapolla, A.; Molin, L.; Traldi, P. Protein glycation in diabetes as determined by mass spectrometry. Int. J. Endocrinol., 2013, 2013412103
[http://dx.doi.org/10.1155/2013/412103] [PMID: 23573087]
[22]
Brahimaj, A.; Ligthart, S.; Ikram, M.A.; Hofman, A.; Franco, O.H.; Sijbrands, E.J.G.; Kavousi, M.; Dehghan, A. serum levels of apolipoproteins and incident type 2 diabetes: A prospective cohort study. Diabetes Care, 2017, 40(3), 346-351.
[http://dx.doi.org/10.2337/dc16-1295] [PMID: 28031419]
[23]
Ashraf, J.M.; Ahmad, S.; Choi, I.; Ahmad, N.; Farhan, M.; Tatyana, G.; Shahab, U. Recent advances in detection of AGEs: Immunochemical, bioanalytical and biochemical approaches. IUBMB Life, 2015, 67(12), 897-913.
[http://dx.doi.org/10.1002/iub.1450] [PMID: 26597014]
[24]
Reddy, H.M.; Sharma, A.; Dehzangi, A.; Shigemizu, D.; Chandra, A.A.; Tsunoda, T. GlyStruct: Glycation prediction using structural properties of amino acid residues. BMC Bioinformatics, 2019, 19(Suppl. 13), 547.
[http://dx.doi.org/10.1186/s12859-018-2547-x] [PMID: 30717650]
[25]
Carroll, L.; Hannawi, S.; Marwick, T.; Thomas, R. Rheumatoid arthritis: links with cardiovascular disease and the receptor for advanced glycation end products. Wien. Med. Wochenschr., 2006, 156, 42-52.
[http://dx.doi.org/10.1007/s10354-005-0242-9]
[26]
Huang, C.; Liu, Y.; Wu, H.; Sun, D.; Li, Y. Characterization of IgG glycosylation in rheumatoid arthritis patients by MALDI-TOF-MSn and capillary electrophoresis. Anal. Bioanal. Chem., 2017, 409(15), 3731-3739.
[http://dx.doi.org/10.1007/s00216-017-0302-1] [PMID: 28397166]
[27]
Miyoshi, E.; Shinzaki, S.; Fujii, H.; Iijima, H.; Kamada, Y.; Takehara, T. Role of aberrant IgG glycosylation in the pathogenesis of inflammatory bowel disease. Proteomics Clin. Appl., 2016, 10(4), 384-390.
[http://dx.doi.org/10.1002/prca.201500089] [PMID: 26427763]
[28]
Sjöwall, C.; Zapf, J.; von Löhneysen, S.; Magorivska, I.; Biermann, M.; Janko, C.; Winkler, S.; Bilyy, R.; Schett, G.; Herrmann, M.; Muñoz, L.E. Altered glycosylation of complexed native IgG molecules is associated with disease activity of systemic lupus erythematosus. Lupus, 2015, 24(6), 569-581.
[http://dx.doi.org/10.1177/0961203314558861] [PMID: 25389233]
[29]
Argyropoulos, C.P.; Chen, S.S.; Ng, Y-H.; Roumelioti, M.E.; Shaffi, K.; Singh, P.P.; Tzamaloukas, A.H. Rediscovering beta-2 microglobulin as a biomarker across the spectrum of kidney diseases. Front. Med. (Lausanne), 2017, 4, 73.
[http://dx.doi.org/10.3389/fmed.2017.00073] [PMID: 28664159]
[30]
Nehring, J.; Schirmbeck, L.A.; Friebus-Kardash, J.; Dubler, D.; Huynh-Do, U.; Chizzolini, C.; Ribi, C.; Trendelenburg, M. Autoantibodies Against Albumin in Patients With Systemic Lupus Erythematosus. Front. Immunol., 2018, 9, 2090.
[http://dx.doi.org/10.3389/fimmu.2018.02090] [PMID: 30333817]
[31]
Merle, N.S.; Noe, R.; Halbwachs-Mecarelli, L.; Fremeaux-Bacchi, V.; Roumenina, L.T. Complement system part II: Role in immunity. Front. Immunol., 2015, 6, 257.
[http://dx.doi.org/10.3389/fimmu.2015.00257] [PMID: 26074922]
[32]
Afshar-Kharghan, V. The role of the complement system in cancer. J. Clin. Invest., 2017, 127(3), 780-789.
[http://dx.doi.org/10.1172/JCI90962] [PMID: 28248200]
[33]
Chikazawa, M.; Shibata, T.; Hatasa, Y.; Hirose, S.; Otaki, N.; Nakashima, F.; Ito, M.; Machida, S.; Maruyama, S.; Uchida, K. Identification of C1q as a binding protein for advanced glycation end products. Biochemistry, 2016, 55(3), 435-446.
[http://dx.doi.org/10.1021/acs.biochem.5b00777] [PMID: 26731343]
[34]
Xie, J.; Selvarajah, S.; Kawasaki, R.; Nicolaou, T.E.; Sanmugasundram, S.; Wang, J.J.; Wong, T.Y.; Lamoureux, E. How much does glycated hemoglobin A1c explain the risk of diabetic retinopathy in persons with type 2 diabetes? The Diabetes Management Project (DMP). Invest. Ophthalmol. Vis. Sci., 2012, 53, 5742.
[35]
Subashree, R. Medical management of trigeminal neuralgia. IOSR J. Dental Medical Sci., 2013, 12, 36-39.
[http://dx.doi.org/ 10.9790/0853-1223639]
[36]
Liang, M.H. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum., 1999, 42(4), 599-608.
[http://dx.doi.org/10.1002/1529-0131(199904)42:4<599:AID-ANR2>3.0.CO;2-F] [PMID: 10211873]
[37]
Yamagishi, Si.; Yonekura, H.; Yamamoto, Y.; Katsuno, K.; Sato, F.; Mita, I.; Ooka, H.; Satozawa, N.; Kawakami, T.; Nomura, M.; Yamamoto, H. Advanced glycation end products-driven angiogenesis in vitro. Induction of the growth and tube formation of human microvascular endothelial cells through autocrine vascular endothelial growth factor. J. Biol. Chem., 1997, 272(13), 8723-8730.
[http://dx.doi.org/10.1074/jbc.272.13.8723] [PMID: 9079706]
[38]
Shimizu, F.; Sano, Y.; Tominaga, O.; Maeda, T.; Abe, M.A.; Kanda, T. Advanced glycation end-products disrupt the blood-brain barrier by stimulating the release of transforming growth factor-β by pericytes and vascular endothelial growth factor and matrix metalloproteinase-2 by endothelial cells in vitro. Neurobiol. Aging, 2013, 34(7), 1902-1912.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.01.012] [PMID: 23428182]
[39]
Wen, J.; Stock, A.D.; Chalmers, S.A.; Putterman, C. The role of B cells and autoantibodies in neuropsychiatric lupus. Autoimmun. Rev., 2016, 15(9), 890-895.
[http://dx.doi.org/10.1016/j.autrev.2016.07.009] [PMID: 27389531]
[40]
Mak, A.; Kow, N.Y. The pathology of T cells in systemic lupus erythematosus. J. Immunol. Res., 2014, 2014419029
[41]
Smith, L.K.; He, Y.; Park, J.S.; Bieri, G.; Snethlage, C.E.; Lin, K.; Gontier, G.; Wabl, R.; Plambeck, K.E.; Udeochu, J.; Wheatley, E.G.; Bouchard, J.; Eggel, A.; Narasimha, R.; Grant, J.L.; Luo, J.; Wyss-Coray, T.; Villeda, S.A. β2-microglobulin is a systemic pro-aging factor that impairs cognitive function and neurogenesis. Nat. Med., 2015, 21(8), 932-937.
[http://dx.doi.org/10.1038/nm.3898] [PMID: 26147761]
[42]
Zhang, P.; Zeng, D.; Yi, Y-L.; Tang, Y-Y.; Zou, W.; Yang, X-F.; Wang, C.Y.; Tang, X.Q. β2-microglobulin induces depressive- and anxiety-like behaviors in rat. PLoS One, 2018, 13(5)e0198027
[http://dx.doi.org/10.1371/journal.pone.0198027] [PMID: 29795686]
[43]
Pullmann, R., Jr; Skerenová, M.; Hybenová, J.; Lukác, J.; Rovenský, J.; Pullmann, R. Apolipoprotein E polymorphism in patients with neuropsychiatric SLE. Clin. Rheumatol., 2004, 23(2), 97-101.
[http://dx.doi.org/10.1007/s10067-003-0796-0] [PMID: 15045621]
[44]
Byder, L.; Halter, C.; Rudolph, A.; Shults, C.W.; Conneally, P.M.; Foroud, T.; Nichols, W.C. Presence of an APOE4 allele results in significantly earlier onset of Parkinson’s disease and a higher risk with dementia. Mov. Disord., 2006, 21, 45-49.
[http://dx.doi.org/10.1002/mds.20663]
[45]
Zhang, H.L.; Wu, J.; Zhu, J. The immune-modulatory role of apolipoprotein E with emphasis on multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Dev. Immunol., 2010, 2010186813
[http://dx.doi.org/10.1155/2010/186813] [PMID: 20613949]
[46]
Li, X.H.; Du, L.L.; Cheng, X.S.; Jiang, X.; Zhang, Y.; Lv, B.L.; Liu, R.; Wang, J.Z.; Zhou, X.W. Glycation exacerbates the neuronal toxicity of β-amyloid. Cell Death Dis., 2013, 4e673
[http://dx.doi.org/10.1038/cddis.2013.180] [PMID: 23764854]
[47]
Liu, K.; Liu, Y.; Li, L.; Qin, P.; Iqbal, J.; Deng, Y.; Qing, H. Glycation alter the process of Tau phosphorylation to change Tau isoforms aggregation property. Biochim. Biophys. Acta, 2016, 1862(2), 192-201.
[http://dx.doi.org/10.1016/j.bbadis.2015.12.002] [PMID: 26655600]
[48]
König, A.; Vicente Miranda, H.; Outeiro, T.F. Alpha-synuclein glycation and the action of anti-diabetic agents in parkinson’s disease. J. Parkinsons Dis., 2018, 8(1), 33-43.
[http://dx.doi.org/10.3233/JPD-171285] [PMID: 29480231]
[49]
Vicente Miranda, H.; Gomes, M.A.; Branco-Santos, J.; Breda, C.; Lázaro, D.F.; Lopes, L.V.; Herrera, F.; Giorgini, F.; Outeiro, T.F. Glycation potentiates neurodegeneration in models of Huntington’s disease. Sci. Rep., 2016, 6, 36798.
[http://dx.doi.org/10.1038/srep36798] [PMID: 27857176]
[50]
Aaron, C.; Beaudry, G.; Parker, J.A.; Therrien, M. Maple SYRUP DECREASES TDP-43 proteotoxicity in a caenorhabditis elegans model of Amyotrophic Lateral Sclerosis (ALS). J. Agric. Food Chem., 2016, 64(17), 3338-3344.
[http://dx.doi.org/10.1021/acs.jafc.5b05432] [PMID: 27071850]
[51]
Anwar, A.; Abruzzo, P.M.; Pasha, S.; Rajpoot, K.; Bolotta, A.; Ghezzo, A.; Marini, M.; Posar, A.; Visconti, P.; Thornalley, P.J.; Rabbani, N. Advanced glycation endproducts, dityrosine and arginine transporter dysfunction in autism - a source of biomarkers for clinical diagnosis. Mol. Autism, 2018, 9, 3.
[52]
Tani, E.; Ohnuma, T.; Hirose, H.; Nakayama, K.; Mao, W.; Nakadaira, M.; Orimo, N.; Yamashita, H.; Takebayashi, Y.; Miki, Y.; Katsuta, N.; Nishimon, S.; Hasegawa, T.; Komiyama, E.; Suga, Y.; Ikeda, S.; Arai, H. Skin advanced glycation end products as biomarkers of photosensitivity in schizophrenia. Int. J. Methods Psychiatr. Res., 2019, 28(1)e1769
[http://dx.doi.org/10.1002/mpr.1769] [PMID: 30701623]
[53]
Bellier, J.; Nokin, M.J.; Lardé, E.; Karoyan, P.; Peulen, O.; Castronovo, V.; Bellahcène, A. Methylglyoxal, a potent inducer of AGEs, connects between diabetes and cancer. Diabetes Res. Clin. Pract., 2019, 148, 200-211.
[http://dx.doi.org/10.1016/j.diabres.2019.01.002] [PMID: 30664892]
[54]
Rasheed, S.; Sánchez, S.S.; Yousuf, S.; Honoré, S.M.; Choudhary, M.I. Drug repurposing: In-vitro anti-glycation properties of 18 common drugs. PLoS One, 2018, 13(1)e0190509
[http://dx.doi.org/10.1371/journal.pone.0190509] [PMID: 29300762]
[55]
Prasad, C.; Imrhan, V.; Marotta, F.; Juma, S.; Vijayagopal, P. Lifestyle and Advanced Glycation End Products (AGEs) burden: Its relevance to healthy aging. Aging Dis., 2014, 5(3), 212-217.
[http://dx.doi.org/10.14336/AD.2014.0500212] [PMID: 24900944]
[56]
Abbas, G.; Al-Harrasi, A.S.; Hussain, H.; Hussain, J.; Rashid, R.; Choudhary, M.I. Antiglycation therapy: Discovery of promising antiglycation agents for the management of diabetic complications. Pharm. Biol., 2016, 54(2), 198-206.
[http://dx.doi.org/10.3109/13880209.2015.1028080] [PMID: 25853955]
[57]
Eyileten, C.; Kaplon-Cieslicka, A.; Mirowska-Guzel, D.; Malek, L.; Postula, M. Antidiabetic Effect of Brain-Derived Neurotrophic Factor and Its Association with Inflammation in Type 2 Diabetes Mellitus. J. Diabetes Res., 2017, 20172823671
[http://dx.doi.org/10.1155/2017/2823671] [PMID: 29062839]
[58]
Elosta, A.; Ghous, T.; Ahmed, N. Natural products as anti-glycation agents: possible therapeutic potential for diabetic complications. Curr. Diabetes Rev., 2012, 8(2), 92-108.
[http://dx.doi.org/10.2174/157339912799424528] [PMID: 22268395]
[59]
Ramkissoon, J.S.; Mahomoodally, F.M.; Ahmed, N.; Hussein, A.; Subratty, N.A. Natural inhibitors of advanced glycation end-products. Nutr. Food Sci., 2012, 42, 397-404.
[http://dx.doi.org/10.1108/00346651211277645]
[60]
Liu, Y.H.; Lu, Y.L.; Liu, D.Z.; Hou, W.C. Antiglycation, radical scavenging, and semicarbazide-sensitive amine oxidase inhibitory activities of acetohydroxamic acid in vitro. Drug Des. Devel. Ther., 2017, 11, 2139-2147.
[http://dx.doi.org/10.2147/DDDT.S141740] [PMID: 28761331]
[61]
Sabbagh, M.N.; Agro, A.; Bell, J.; Aisen, P.S.; Schweizer, E.; Galasko, D. PF-04494700, an oral inhibitor of receptor for advanced glycation end products (RAGE), in Alzheimer disease. Alzheimer Dis. Assoc. Disord., 2011, 25(3), 206-212.
[http://dx.doi.org/10.1097/WAD.0b013e318204b550] [PMID: 21192237]
[62]
Bell, J.; Mancuso, J.Y.; Kupiec, J.W.; Sabbagh, M.N.; van Dyck, C.; Thomas, R.G.; Aisen, P.S. Clinical trial of an inhibitor of RAGE-Aβ interactions in Alzheimer disease. Neurology, 2014, 82, 1536-1542.
[http://dx.doi.org/10.1212/WNL.0000000000000364]
[63]
Bongarzone, S.; Savickas, V.; Luzi, F.; Gee, A.D. Targeting the Receptor for Advanced Glycation Endproducts (RAGE): A medicinal chemistry perspective. J. Med. Chem., 2017, 60(17), 7213-7232.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00058] [PMID: 28482155]
[64]
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. Nutr. Metab. (Lond.), 2018, 15, 72.
[http://dx.doi.org/10.1186/s12986-018-0306-7] [PMID: 30337945]
[65]
Iannuzzi, C.; Irace, G.; Sirangelo, I. Differential effects of glycation on protein aggregation and amyloid formation. Front. Mol. Biosci., 2014, 1, 9.
[http://dx.doi.org/10.3389/fmolb.2014.00009] [PMID: 25988150]
[66]
Loeffler, K.W.; Koehler, C.A.; Paul, N.M.; De Haan, D.O. Oligomer formation in evaporating aqueous glyoxal and methyl glyoxal solutions. Environ. Sci. Technol., 2006, 40(20), 6318-6323.
[http://dx.doi.org/10.1021/es060810w] [PMID: 17120559]
[67]
Aragno, M.; Mastrocola, R. Dietary sugars and endogenous formation of advanced glycation endproducts: Emerging Mechanisms Of Disease. Nutrients, 2017, 9(4)E385
[http://dx.doi.org/10.3390/nu9040385] [PMID: 28420091]
[68]
Crisan, M.; Taulescu, M.; Crisan, D.; Cosgarea, R.; Parvu, A.; Cãtoi, C.; Drugan, T. Expression of advanced glycation end-products on sun-exposed and non-exposed cutaneous sites during the ageing process in humans. PLoS One, 2013, 8(10)e75003
[http://dx.doi.org/10.1371/journal.pone.0075003] [PMID: 24116020]
[69]
Linetsky, M.; Raghavan, C.T.; Johar, K.; Fan, X.; Monnier, V.M.; Vasavada, A.R.; Nagaraj, R.H. UVA light-excited kynurenines oxidize ascorbate and modify lens proteins through the formation of advanced glycation end products: implications for human lens aging and cataract formation. J. Biol. Chem., 2014, 289(24), 17111-17123.
[http://dx.doi.org/10.1074/jbc.M114.554410] [PMID: 24798334]
[70]
Sanguineti, R.; Puddu, A.; Mach, F.; Montecucco, F.; Viviani, G.L. Advanced glycation end products play adverse proinflammatory activities in osteoporosis. Mediators Inflamm., 2014, 2014975872
[71]
Fuller, K.N.Z.; Miranda, E.R.; Thyfault, J.P.; Morris, J.K.; Haus, J.M. Metabolic derangements contribute to reduced srage isoforms in subjects with Alzheimer’s disease. Mediators Inflamm., 2018, 20182061376
[http://dx.doi.org/10.1155/2018/2061376] [PMID: 29681765]
[72]
Richarme, G.; Mihoub, M.; Dairou, J.; Bui, L.C.; Leger, T.; Lamouri, A. Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal- and glyoxal-glycated cysteine, arginine, and lysine residues. J. Biol. Chem., 2015, 290(3), 1885-1897.
[http://dx.doi.org/10.1074/jbc.M114.597815] [PMID: 25416785]
[73]
Grimm, S.; Ernst, L.; Grötzinger, N.; Höhn, A.; Breusing, N.; Reinheckel, T.; Grune, T. Cathepsin D is one of the major enzymes involved in intracellular degradation of AGE-modified proteins. Free Radic. Res., 2010, 44(9), 1013-1026.
[http://dx.doi.org/10.3109/10715762.2010.495127] [PMID: 20560835]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 22
ISSUE: 6
Year: 2019
Page: [362 - 369]
Pages: 8
DOI: 10.2174/1386207322666190704094356

Article Metrics

PDF: 16
HTML: 4
EPUB: 1
PRC: 1