Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy.
Open accessAbstract
Advanced glycation end products (AGEs) include a variety of protein adducts whose accumulation alters the structure and function of tissue proteins and stimulates cellular responses. They have been implicated in tissue damage associated with diabetic complications. To assess the possible link between AGE accumulation and the development of diabetic nephropathy (DN), we have examined the immunohistochemical localization of various AGE structures postulated to date, i.e., pentosidine, Nepsilon-(carboxymethyl)lysine (CML), and pyrraline, in diabetic and control kidneys. CML and pentosidine accumulate in the expanded mesangial matrix and thickened glomerular capillary walls of early DN and in nodular lesions and arterial walls of advanced DN, but were absent in control kidneys. By contrast, pyrraline was not found within diabetic glomeruli but was detected in the interstitial connective tissue of both normal and diabetic kidneys. Although the distribution of pyrraline was topographically identical to type III collagen, distribution of pentosidine and CML was not specific for collagen type, suggesting that difference in matrix protein composition per se could not explain heterogeneous AGE localization. Since oxidation is linked closely to the formation of pentosidine and CML, we also immunostained malondialdehyde (MDA), a lipid peroxidation product whose formation is accelerated by oxidative stress, assuming that local oxidative stress may serve as a mechanism of pentosidine and CML accumulation. Consistent with our assumption, diabetic nodular lesions were stained positive for MDA. These findings show that AGE localization in DN varies according to AGE structure, and suggest that the colocalization of markers of glycoxidation (pentosidine and CML) with a marker of lipid peroxidation reflects a local oxidative stress in association with the pathogenesis of diabetic glomerular lesions. Thus, glycoxidation markers may serve as useful biomarkers of oxidative damage in DN.
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Excessive AGE formation is particularly associated with cross-linking of matrix proteins such as collagen, vitronectin, and laminin.
“Excessive AGE formation is particularly associated with cross-linking of matrix proteins such as collagen, vitronectin, and laminin.[2,10,11]”
From The Role of Dietary Advanced Glycation End Products in Metabolic Dysfunction (2021) · cites this paper as [2]
The rate of AGE formation in the body is greatly enhanced in diabetes.
“The rate of AGE formation in the body is greatly enhanced in diabetes.[2,3]”
From The Role of Dietary Advanced Glycation End Products in Metabolic Dysfunction (2021) · cites this paper as [2]
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Self-citationReceptor for Advanced-Glycation End Products: Key Modulator of Myocardial Ischemic Injury
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“It has been shown that when 3-deoxyglucosone reacts with lysine, pyrraline is formed [18] whereas with arginine it yields a hydroimidazolone [19, 20].”
BackgroundDiabetic nephropathy and antioxidants
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The Role of Dietary Advanced Glycation End Products in Metabolic Dysfunction
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“Increased amounts of AGEs have been reported to be present in diabetic renal glomeruli [60].”
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“Control(1) RSA(2) AOPPs-RSA(3) Control(4) RSA (5) AOPPs-RSA(6) F1 F2 F3”
Understanding Diabetic Neuropathy: Focus on Oxidative Stress
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“The AGE and PKC pathway modify proteins, lipids, and DNAs via a direct [77–80] or an indirect effect of glucose [81, 82].”
BackgroundSindhu, R. K., Koo, J.-R., Roberts, C. K., & Vaziri, N. D. (2004) · Clinical and Experimental Hypertension · doi:10.1081/ceh-120027330 · Cited by 183 · see citing works
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“Recently, Horie et al. [ 22 ] reported colocalization of”
BackgroundSelf-citationAGE/RAGE produces endothelial dysfunction in coronary arterioles in Type 2 diabetic mice
Gao, X. J., Zhang, H., Schmidt, A. M., & Zhang, C. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00464.2008 · Cited by 174 · see citing works
“A previous report showed AGE production increased in diabetic retinal vessels (21) and renal glomeruli (11).”
The innate immune response to products of phospholipid peroxidation
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Self-citationPlasma levels of pentosidine in diabetic patients
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Self-citationDiet and Chronic Kidney Disease.
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“Receptors for AGEs are also found on mesangial cells, and when activated, they stimulate production of collagen and matrix, which accelerates glomerular sclerosis (40, 41).”
BackgroundSitte, N., Merker, K., von Zglinicki, T., Davies, K. J. A., & Grune, T. (2000) · The FASEB Journal · doi:10.1096/fj.00-0210com · Cited by 157 · see citing works
“Further modification and oxidation processes are also involved in the formation of these age-linked fluorophores, such as modification by lipid peroxidation products and by glycation (2, 8).”
BackgroundNew insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy
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“generation [33–35], that in turn activate a number of signaling pathways that lead to enhanced ECM production directly via PKC β stimulation [36, 37] of AP-1 transcriptional activation, ERK pathways and, critically, TGF-β1 synthesis [38, 39] which in an autocrine and paracrine fashion stimulates its signaling pathways…”
Molecular mechanism of diabetic nephropathy
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Evidence that pioglitazone, metformin and pentoxifylline are inhibitors of glycation
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Potential Role of Serum and Urinary Biomarkers in Diagnosis and Prognosis of Diabetic Nephropathy
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The role of innate immunity in atherogenesis
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“plaques (8), but MDA modified proteins in diabetic kidneys (9) and Heyman nephritis (10), as well as in Alzheimer plaques (11).”
BackgroundSelf-citationAdvanced glycation end-products: Implications for diabetic and non-diabetic nephropathies
Daroux, M., Prévost, G., Maillard, H., Gaxatte, C., D’Agati, V. D., Schmidt, A. M., & Boulanger, É. (2009) · Diabetes & Metabolism · doi:10.1016/j.diabet.2009.06.005 · Cited by 142 · see citing works
“nation; main localizations are shown in bold [27,33,63].”
BackgroundInfluentialIncreased oxidative stress in mouse kidneys with unilateral ureteral obstruction
Kawada, N., Moriyama, T., Ando, A., Fukunaga, M., Miyata, T., Kurokawa, K., Imai, E., & Hori, M. (1999) · Kidney International · doi:10.1046/j.1523-1755.1999.00612.x · Cited by 140 · see citing works
“This antiserum was demonstrated to react with proteins lbovine serum albumin (BSA), b2-microglobulin, and KLHr modified with CML, but not with their counterparts modified with pentosidine nor pyrralin”
BackgroundSelf-citationMiyata, T., Inagi, R., Asahi, K., Yamada, Y., Horie, K., Sakai, H., Uchida, K., & Kurokawa, K. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01079-5 · Cited by 140 · see citing works
Self-citationRAGE and the pathogenesis of chronic kidney disease
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“An accumulation of AGEs occurs throughout the diabetic kidney, ultimately affecting glomerular, tubular, and vascular compartments”
BackgroundJain, S. K., Kannan, K., & Lim, G. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00140-3 · Cited by 135 · see citing works
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Self-citationCobalt ameliorates renal injury in an obese, hypertensive type 2 diabetes rat model
Ohtomo, S., Nangaku, M., Izuhara, Y., Takizawa, S., de Strihou, C. V. Y., & Miyata, T. (2007) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfm715 · Cited by 132 · see citing works
Self-citationAdvanced Oxidation Protein Products Accelerate Renal Fibrosis in a Remnant Kidney Model
Li, H. Y., Hou, F. F., Zhang, X., Chen, P. Y., Liu, S. X., Feng, J., Liu, Z., Shan, Y., Wang, G. B., Zhou, Z. M., et al. (2007) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006070781 · Cited by 132 · see citing works
“In vivo, plasma concentration of AOPP closely correlated with levels of dityrosine, a hallmark of oxidized protein, and pentosidine, a marker of protein glycoxidation that is tightly related to oxidative stress (5).”
BackgroundEarly oxidative stress in the diabetic kidney: effect of DL-α-lipoic acid
Obrosova, I. G., Fathallah, L., Liu, E., & Nourooz‐Zadeh, J. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01195-4 · Cited by 129 · see citing works
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Self-citationChew, P., Yuen, D. Y. C., Stefanovic, N., Pete, J., Coughlan, M. T., Jandeleit-Dahm, K. A. M., Thomas, M. C., Rosenfeldt, F., Cooper, M. E., & de Haan, J. B. (2010) · Diabetes · doi:10.2337/db10-0195 · Cited by 125 · see citing works
“Types I and III collagens are expressed mainly in the interstitial regions, whereas type IV collagen plays a significant role in glomerular pathology (40,41).”
Liu, B.-F., Miyata, S., Hirota, Y., Higo, S., Miyazaki, H., Fukunaga, M., Hamada, Y., Ueyama, S., Muramoto, O., Uriuhara, A., et al. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00829.x · Cited by 125 · see citing works
Self-citationJain, S. K., McVie, R., & Smith, T. (2000) · Diabetes Care · doi:10.2337/diacare.23.9.1389 · Cited by 123 · see citing works
Szweda, P. A., Friguet, B., & Szweda, L. I. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00837-7 · Cited by 120 · see citing works
Role of ERAB/l-3-Hydroxyacyl-coenzyme A Dehydrogenase Type II Activity in Aβ-induced Cytotoxicity
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Apoptosis in ischemic renal injury: Roles of GTP depletion and p53
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Nerpin, E., Risérus, U., Ingelsson, E., Sundström, J., Jobs, M., Larsson, A. O., Basu, S., & Ärnlöv, J. (2008) · Diabetes Care · doi:10.2337/dc08-0369 · Cited by 118 · see citing works
“Moreover, insulin resistance and hyperinsulinemia is closely associated with oxidative stress (14), which could promote renal injury via decreased production and availability of nitric oxide (15), accelerated formation of glycoxidation and lipid peroxidation products (16-18).”
BackgroundBaba, S. P., Barski, O. A., Ahmed, Y., O’Toole, T. E., Conklin, D. J., Bhatnagar, A., & Srivastava, S. (2009) · Diabetes · doi:10.2337/db09-0375 · Cited by 117 · see citing works
“Excessive AGE formation has been linked to crosslinking of matrix molecules such as collagen, vitronectin, and laminin (3,5,6).”
BackgroundKaramouzis, I., Sarafidis, P., Karamouzis, M., Iliadis, S., Haidich, A., Sioulis, A., Triantos, A., Vavatsi-Christaki, N., & Grekas, D. (2007) · American Journal of Nephrology · doi:10.1159/000112413 · Cited by 125 · see citing works
“With regard to diabetic nephropathy, one of the mechanisms is the contribution of oxidant stress to the formation of glycoxidation products, which are a type of advanced glycation end products; these substances accumulate in the characteristic glomerular lesions of diabetic nephropathy and lead to elevated expression…”
BackgroundZhou, J., Cai, B., Jang, Y. P., Pachydaki, S., Schmidt, A. M., & Sparrow, J. R. (2005) · Experimental Eye Research · doi:10.1016/j.exer.2004.11.009 · Cited by 113 · see citing works
Sodium-Glucose Cotransporter Inhibition Prevents Oxidative Stress in the Kidney of Diabetic Rats
Osorio‐Alonso, H., Coronel, I., Arellano, A., Pacheco, U., Bautista, R., Franco, M., & Escalante, B. (2012) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2012/542042 · Cited by 113 · see citing works
“The functional and pathophysiological role of excessive oxidative stress in diabetic kidney disease was indicated by the presence of increased levels of lipid peroxides and 8-hydroxydeoxyguanosine in the kidney of STZ-induced diabetic rats [22, 23].”
BackgroundRAGE and Modulation of Ischemic Injury in the Diabetic Myocardium
Bucciarelli, L. G., Ananthakrishnan, R., Hwang, Y. C., Kaneko, M., Song, F., Sell, D. R., Strauch, C., Monnier, V. M., Yan, S. F., Schmidt, A. M., et al. (2008) · Diabetes · doi:10.2337/db07-0326 · Cited by 113 · see citing works
“First, we examined epitopes for CML AGEs (27,28).”
BackgroundSelf-citationPremature senescence of endothelial cells: Methusaleh's dilemma
Chen, J., & Goligorsky, M. S. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01103.2005 · Cited by 110 · see citing works
“During diabetes, AGEs are formed at an accelerating rate (157) resulting in very high tissue levels (23, 70).”
BackgroundCombet, S., Ferrier, M.-L., Landschoot, M. V., Stoenoiu, M. S., MOULIN, P., Miyata, T., Lameire, N. H., & Devuyst, O. (2001) · Journal of the American Society of Nephrology · doi:10.1681/asn.v12102146 · Cited by 111 · see citing works
Self-citation
- Authors
- Horie, K., Miyata, T., Maeda, K., Miyata, S., Sugiyama, S., Sakai, H., van Ypersole de Strihou, C., Monnier, V. M., Witztum, J. L., & Kurokawa, K.
- Affiliations
- Nagoya University (JP)
- Tokai University (JP)
- Kobe University (JP)
- Chukyo Hospital (JP)
- Case Western Reserve University (US)
- University of California San Diego (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1997-12-15
- Volume
- 100
- Issue
- 12
- Pages
- 2995-3004
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508511
- OpenAlex
- W2085341182
- Cited by
- 433
- References
- 56
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 5 · 2023: 7 · 2022: 9 · 2021: 14 · 2020: 10 · 2019: 10 · 2018: 7 · 2017: 12 · 2016: 10 · 2015: 8 · 2014: 14 · 2013: 9 · 2012: 15
- FWCI
- 14.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DIAL (Catholic University of Leuven) (submittedVersion, other-oa)
- Funders
- Japan Society for the Promotion of Science (96L00303)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
- Health Sciences › Medicine › Nephrology › Chronic Kidney Disease and Diabetes
- Health Sciences › Medicine › Nephrology › Renal Diseases and Glomerulopathies
- Keywords
- advanced glycation end products, glycoxidation, lipid peroxidation, diabetic nephropathy, pentosidine, carboxymethyllysine, pyrraline, malondialdehyde, oxidative stress, glomerular lesions, mesangial matrix, type III collagen, oxidative damage biomarkers
- MeSH terms
- Adolescent, Adult, Aged, Animals, Antibodies, Arginine, Collagen, Diabetes Mellitus, Type 2, Diabetic Nephropathies, Female, Humans, Immunoenzyme Techniques, Kidney Glomerulus, Lysine, Male, Malondialdehyde, Middle Aged, Nephrotic Syndrome, Norleucine, Pyrroles, Rabbits, Lipid Peroxidation, Glycation End Products, Advanced, Mice
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