Overexpression of Fibronectin Induced by Diabetes or High Glucose: Phenomenon With a Memory
Open accessAbstract
To identify events and mechanisms that might contribute to the poor reversibility of diabetic complications, we examined whether diabetes or high glucose induces changes in gene expression and whether such changes outlast the presence of the metabolic abnormalities. The study focused on fibronectin because the increased amounts of this glycoprotein found in diabetic tissues and thickened basement membranes are as yet unexplained. In streptozotocin-induced diabetic rats, fibronectin mRNA levels were increased to 304 +/- 295% of control (mean +/- SD) in the kidney cortex (P less than 0.02), and to 271 +/- 273% of control in the heart (P less than 0.02), while actin mRNA levels remained unchanged. Elevation of fibronectin mRNA persisted for weeks after restoration of near-normoglycemia. In cultured human endothelial cells, high glucose-induced overexpression of fibronectin and collagen IV remained detectable after replating and multiple cell divisions in the absence of high glucose. Cells shifted to normal-glucose medium after prolonged exposure to high glucose also exhibited a proliferative advantage over cells chronically maintained in normal glucose. Thus, diabetes increases fibronectin expression in tissues that are known targets of the complications, and the effect is not readily reversible. The in vitro studies suggest that hyperglycemia may be responsible for these events through induction of self-perpetuating changes in gene expression.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Data from streptozotocin-induced diabetic rats and endothelial cells in culture indicate that glucose-elevated fibronectin expression is not reversed when normal glycaemia is restored.
“Data from studies of tissues from streptozotocin-induced diabetic rats and also of endothelial cells in culture indicate that glucose-elevated fibronectin expression is not reversed when normal glycaemia is restored (192).”
From A Critical Review of the Evidence That Metformin Is a Putative Anti-Aging Drug That Enhances Healthspan and Extends Lifespan (2021) · cites this paper as [192]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Lee, T. S., Saltsman, K., Ohashi, H., & King, G. L. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.13.5141 · Cited by 373 · see citing works
RetractedIsolation of biologically active ribonucleic acid from sources enriched in ribonuclease
Chirgwin, J. M., Przybyla, A., MacDonald, R. J., & Rutter, W. J. (1979) · Biochemistry · doi:10.1021/bi00591a005 · Cited by 21,725 · see citing works
Jaffe, E. A., Nachman, R., Becker, C. G., & Minick, C. (1973) · Journal of Clinical Investigation · doi:10.1172/jci107470 · Cited by 7,146 · see citing works
Angel, P. E., Imagawa, M., Chiu, R., Stein, B., Imbra, R. J., Rahmsdorf, H. J., Jonat, C., Herrlich, P. A., & Karin, M. (1987) · Cell · doi:10.1016/0092-8674(87)90611-8 · Cited by 2,930 · see citing works
Advanced Glycosylation End Products in Tissue and the Biochemical Basis of Diabetic Complications
Flier, J. S., Underhill, L. H., Brownlee, M., Cerami, A., & Vlassara, H. (1988) · New England Journal of Medicine · doi:10.1056/nejm198805193182007 · Cited by 2,512 · see citing works
(1984) · PubMed · Cited by 1,200 · see citing works
CELL SURFACE INTERACTIONS WITH EXTRACELLULAR MATERIALS
Yamada, K. M. (1983) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.52.070183.003553 · Cited by 1,140 · see citing works
Glomerular hemodynamics in experimental diabetes mellitus
Hostetter, T. H., Troy, J. L., & Brenner, B. M. (1981) · Kidney International · doi:10.1038/ki.1981.33 · Cited by 794 · see citing works
Molecular Biology of Fibronectin
Hynes, R. O. (1985) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.01.110185.000435 · Cited by 608 · see citing works
Progression of Incipient Diabetic Retinopathy During Good Glycemic Control
Engerman, R. L., & Kern, T. S. (1987) · Diabetes · doi:10.2337/diab.36.7.808 · Cited by 490 · see citing works
Zaret, K. S., & Yamamoto, K. R. (1984) · Cell · doi:10.1016/0092-8674(84)90523-3 · Cited by 432 · see citing works
EFFECT OF 1 YEAR OF NEAR-NORMAL BLOOD GLUCOSE LEVELS ON RETINOPATHY IN INSULIN-DEPENDENT DIABETICS
Lauritzen, T., Larsen, H., Frost-Larsen, K., Deckert, T., & The Steno Study Group (1983) · The Lancet · doi:10.1016/s0140-6736(83)92585-0 · Cited by 372 · see citing works
Ramsay, R. C., Goetz, F. C., Sutherland, D. E. R., Mauer, S. M., Robison, L. L., Cantrill, H. L., Knobloch, W. H., & Najarian, J. S. (1988) · New England Journal of Medicine · doi:10.1056/nejm198801283180403 · Cited by 362 · see citing works
Craven, P. A., & DeRubertis, F. R. (1989) · Journal of Clinical Investigation · doi:10.1172/jci114066 · Cited by 321 · see citing works
Lorenzi, M., Cagliero, E., & TOLEDO, S. P. (1985) · Diabetes · doi:10.2337/diab.34.7.621 · Cited by 302 · see citing works
Self-citationBilous, R. W., Mauer, S. M., Sutherland, D. E. R., Najarian, J. S., Goetz, F. C., & Steffes, M. W. (1989) · New England Journal of Medicine · doi:10.1056/nejm198907133210204 · Cited by 297 · see citing works
Diabetes Mellitus Induces Changes in Cardiac Myosin of the Rat
DILLMANN, W. H. (1980) · Diabetes · doi:10.2337/diab.29.7.579 · Cited by 290 · see citing works
Capillary Microaneurysms in the Human Diabetic Heart
Factor, S. M., Okun, E. M., & Minase, T. (1980) · New England Journal of Medicine · doi:10.1056/nejm198002143020706 · Cited by 285 · see citing works
Lauritzen, T., Frost-Larsen, K., Larsen, H., Deckert, T., & The Steno Study Group (1985) · Diabetes · doi:10.2337/diab.34.3.s74 · Cited by 252 · see citing works
Fein, F. S., & Sonnenblick, E. H. (1985) · Progress in Cardiovascular Diseases · doi:10.1016/0033-0620(85)90009-x · Cited by 250 · see citing works
Polyantigenic Expansion of Basement Membrane Constituents in Diabetic Nephropathy
Falk, R. J., Scheinman, J. I., Mauer, S. M., & Michael, A. F. (1983) · Diabetes · doi:10.2337/diab.32.2.s34 · Cited by 206 · see citing works
Cagliero, E., Maiello, M., Boeri, D., Roy, S., & Lorenzi, M. (1988) · Journal of Clinical Investigation · doi:10.1172/jci113655 · Cited by 196 · see citing works
Self-citationPrevention of Kidney Graft Diabetic Nephropathy by Pancreas Transplantation in Man
Bohman, S. O., Tydén, G., Wilczek, H., Lundgren, G., Jaremko, G., GUNNARSSON, R., Östman, J., & Groth, C. G. (1985) · Diabetes · doi:10.2337/diab.34.3.306 · Cited by 193 · see citing works
Use of protein-based standards in automated colorimetric determinations of fructosamine in serum.
Baker, J. R., Metcalf, P. A., Johnson, R. N., Newman, D. J., & Rietz, P. (1985) · Clinical Chemistry · doi:10.1093/clinchem/31.9.1550 · Cited by 167 · see citing works
Myocardial composition and function in diabetes. The effects of chronic insulin use.
Regan, T. J., Wu, C. F., Yeh, C. K., Oldewurtel, H. A., & Haider, B. (1981) · Circulation Research · doi:10.1161/01.res.49.6.1268 · Cited by 160 · see citing works
Raskin, P., Pietri, A., Unger, R. H., & Shannon, W. A. (1983) · New England Journal of Medicine · doi:10.1056/nejm198312223092504 · Cited by 141 · see citing works
Capillary Basal Laminar Thickness in Diabetic Human Myocardium
Fischer, V. W., Barner, H. B., & Leskiw, M. L. (1979) · Diabetes · doi:10.2337/diab.28.8.713 · Cited by 123 · see citing works
High Glucose Prolongs Cell-Cycle Traversal of Cultured Human Endothelial Cells
Lorenzi, M., Nordberg, J. A., & TOLEDO, S. P. (1987) · Diabetes · doi:10.2337/diab.36.11.1261 · Cited by 108 · see citing works
Self-citationSteffes, M. W., Sutherland, D. E. R., Goetz, F. C., Rich, S. S., & Mauer, S. M. (1985) · New England Journal of Medicine · doi:10.1056/nejm198505163122003 · Cited by 106 · see citing works
The pro α2(V) collagen gene is evolutionarily related to the major fibrillar-forming collagens
Weil, D., Bernard, M. P., Gargano, S., & Ramirez, F. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.1.181 · Cited by 97 · see citing works
Distribution of fibronectin in normal and diseased human kidneys.
Dixon, A. J., Burns, J. M., Dunnill, M. S., & McGee, J. O. (1980) · Journal of Clinical Pathology · doi:10.1136/jcp.33.11.1021 · Cited by 88 · see citing works
Immunofluorescent localization of fibronectin in the human kidney.
Weiss, M. A., Ooi, B. S., Ooi, Y. M., Engvall, E., & Ruoslahti, E. I. (1979) · PubMed · Cited by 75 · see citing works
Glomerular basement membrane thickness following islet transplantation in the diabetic rat.
Steffes, M. W., Dm, B., Basgen, J. M., Matas, A. J., & Mauer, S. M. (1979) · PubMed · Cited by 73 · see citing works
Estrogen Memory Effect in Human Hepatocytes During Repeated Cell Division Without Hormone
Tam, S. P., Haché, R. J. G., & Deeley, R. G. (1986) · Science · doi:10.1126/science.3022381 · Cited by 63 · see citing works
Alterations in the distribution of fibronectin and laminin in the diabetic human eye.
Kohno, T., Sorgente, N., Goodnight, R., & Ryan, S. J. (1987) · PubMed · Cited by 51 · see citing works
Cohen, M. P., & Khalifa, A. S. (1977) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(77)90030-7 · Cited by 49 · see citing works
Gøtzsche, O., Gundersen, H. J. G., & Østerby, R. (1981) · Diabetes · doi:10.2337/diab.30.6.481 · Cited by 46 · see citing works
Oldberg, Å., Linney, E. A., & Ruoslahti, E. I. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)44437-1 · Cited by 46 · see citing works
Increased biosynthesis and processing of fibronectin in fibroblasts from diabetic mice.
Phan‐Thanh, L., Robert, L., Derouette, J. C., & Labat‐Robert, J. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.7.1911 · Cited by 44 · see citing works
Muscle capillary basement membrane width in patients with vacor-induced diabetes mellitus.
Feingold, K. R., Lee, T. H., Chung, M., & Siperstein, M. D. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112537 · Cited by 33 · see citing works
Plasma and tissue fibronectin in diabetes.
Labat‐Robert, J., Leuténegger, M., Llopis, G., Ricard, Y., & Derouette, J. C. (1984) · PubMed · Cited by 33 · see citing works
Caution in the Use of Drugs in the Elderly
Lorenzi, M., Goldbaum, M. H., Spencer, E., & Cheney, C. (1983) · New England Journal of Medicine · doi:10.1056/nejm198306303082614 · Cited by 7 · see citing works
Self-citationCagliero, E., Barrieux, A., Lehman, C., & DILLMANN, W. H. (1988) · Journal of Molecular and Cellular Cardiology · doi:10.1016/s0022-2828(88)80134-2 · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- [35]Lee, T. S., Saltsman, K. A., Ohashi, H. & King, G. L. (1989) Proc. Natl. Acad. Sci. USA 86, 5141–5145.
- J. (1987) Proc. Natl. Acad. Sci. USA 84, 1911–1915.
Cited by
Sorted by citations
Thomas, M. C., Brownlee, M., Suszták, K., Sharma, K., Jandeleit-Dahm, K. A. M., Zoungas, S., Rossing, P. R., Groop, P., & Cooper, M. E. (2015) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2015.18 · Cited by 1,282 · see citing works
Reversal of Lesions of Diabetic Nephropathy after Pancreas Transplantation
Fioretto, P., Steffes, M. W., Sutherland, D. E. R., Goetz, F. C., & Mauer, M. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199807093390202 · Cited by 1,125 · see citing works
Diabetes mellitus and hypertension.
Epstein, M., & Sowers, J. R. (1992) · Hypertension · doi:10.1161/01.hyp.19.5.403 · Cited by 629 · see citing works
Ziyadeh, F. N., Sharma, K., Ericksen, M. B., & Wolf, G. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117004 · Cited by 598 · see citing works
Eelen, G., de Zeeuw, P., Treps, L., Harjes, U., Wong, B. W., & Carmeliet, P. (2017) · Physiological Reviews · doi:10.1152/physrev.00001.2017 · Cited by 591 · see citing works
Brasacchio, D., Okabe, J., Tikellis, C., Balcerczyk, A., George, P., Baker, E. K., Calkin, A. C., Brownlee, M., Cooper, M. E., & El‐Osta, A. (2009) · Diabetes · doi:10.2337/db08-1666 · Cited by 533 · see citing works
Diabetes Mellitus and Associated Hypertension, Vascular Disease, and Nephropathy
Sowers, J. R., & Epstein, M. (1995) · Hypertension · doi:10.1161/01.hyp.26.6.869 · Cited by 436 · see citing works
Ceriello, A., Ihnat, M. A., & Thorpe, J. E. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1824 · Cited by 411 · see citing works
Hormones and the physiological architecture of life history evolution
Finch, C. E., & Rose, M. R. (1995) · The Quarterly Review of Biology · doi:10.1086/418864 · Cited by 376 · see citing works
High glucose-induced proliferation in mesangial cells is reversed by autocrine TGF-β
Wolf, G., Sharma, K., Chen, Y., Ericksen, M. B., & Ziyadeh, F. N. (1992) · Kidney International · doi:10.1038/ki.1992.330 · Cited by 356 · see citing works
Endothelial dysfunction and diabetes: roles of hyperglycemia, impaired insulin signaling and obesity
Bakker, W., Eringa, E. C., Sipkema, P., & van Hinsbergh, V. W. M. (2008) · Cell and Tissue Research · doi:10.1007/s00441-008-0685-6 · Cited by 343 · see citing works
Potential mechanisms promoting restenosis in diabetic patients
Aronson, D., Bloomgarden, Z. T., & Rayfield, E. J. (1996) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(95)00496-3 · Cited by 328 · see citing works
Protein kinase C and the development of diabetic vascular complications
Way, K. J., Katai, N., & King, G. L. (2001) · Diabetic Medicine · doi:10.1046/j.0742-3071.2001.00638.x · Cited by 313 · see citing works
The role of epigenetics in the pathology of diabetic complications
Villeneuve, L. M., & Natarajan, R. D. (2010) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00200.2010 · Cited by 295 · see citing works
Fibrosis in diabetes complications: Pathogenic mechanisms and circulating and urinary markers
Twigg, S. (2008) · Vascular Health and Risk Management · doi:10.2147/vhrm.s1991 · Cited by 288 · see citing works
Zheng, Z., Chen, H., Li, J., Li, T., Zheng, B., Zheng, Y., Jin, H., He, Y., Gu, Q., & Xu, X. (2012) · Diabetes · doi:10.2337/db11-0416 · Cited by 282 · see citing works
Mohammed, I., Hollenberg, M. D., Ding, H., & Triggle, C. R. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.718942 · Cited by 278 · see citing works
The Extracellular Matrix in Diabetic Nephropathy
Ziyadeh, F. N. (1993) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(12)80440-9 · Cited by 258 · see citing works
Skolnik, E. Y., Yang, Z., Makita, Z., Radoff, S., Kirstein, M., & Vlassara, H. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.4.931 · Cited by 242 · see citing works
Epigenetic phenomena linked to diabetic complications
Pirola, L., Balcerczyk, A., Okabe, J., & El-Osta, A. (2010) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2010.188 · Cited by 239 · see citing works
Diabetes mellitus: A disease of abnormal cellular calcium metabolism?
Levy, J., Gavin, J. R., & Sowers, J. R. (1994) · The American Journal of Medicine · doi:10.1016/0002-9343(94)90152-x · Cited by 236 · see citing works
Cellular and molecular mechanisms of endothelial dysfunction in diabetes
Roberts, A., & Porter, K. E. (2013) · Diabetes and Vascular Disease Research · doi:10.1177/1479164113500680 · Cited by 226 · see citing works
Testa, R., Bonfigli, A. R., Prattichizzo, F., Sala, L. L., Nigris, V. D., & Ceriello, A. (2017) · Nutrients · doi:10.3390/nu9050437 · Cited by 230 · see citing works
Reactive oxygen species mediate a cellular ‘memory’ of high glucose stress signalling
Ihnat, M. A., Thorpe, J. E., Kamat, C. D., Szabó, C., Green, D. E., Warnke, L. A., Lacza, Z., Cselenyák, A., Ross, K., Shakir, S. F., et al. (2007) · Diabetologia · doi:10.1007/s00125-007-0684-2 · Cited by 225 · see citing works
Pirola, L., Balcerczyk, A., Tothill, R. W., Haviv, I., Kaspi, A., Lunke, S., Ziemann, M., Karagiannis, T. C., Tonna, S. J., Kowalczyk, A., et al. (2011) · Genome Research · doi:10.1101/gr.116095.110 · Cited by 220 · see citing works
Miyata, S., & Monnier, V. M. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115690 · Cited by 218 · see citing works
Cooper, M. E., & El‐Osta, A. (2010) · Circulation Research · doi:10.1161/circresaha.110.223552 · Cited by 211 · see citing works
Zhong, Q. P. W., & Kowluru, R. A. (2011) · Diabetes · doi:10.2337/db10-0133 · Cited by 210 · see citing works
Defective intracellular antioxidant enzyme production in type 1 diabetic patients with nephropathy.
Ceriello, A., Morocutti, A., Mercuri, F., Quagliaro, L., Moro, M., Damante, G., & Viberti, G. C. (2000) · Diabetes · doi:10.2337/diabetes.49.12.2170 · Cited by 209 · see citing works
Epigenetic mechanisms in diabetic vascular complications
Reddy, M. A., & Natarajan, R. D. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr024 · Cited by 198 · see citing works
Antioxidant Anti-Inflammatory Treatment in Type 2 Diabetes
Ceriello, A., & Testa, R. (2009) · Diabetes Care · doi:10.2337/dc09-s316 · Cited by 199 · see citing works
Haitoglou, C., Tsilibary, E. C., Brownlee, M., & CHARONIS, A. S. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42287-9 · Cited by 194 · see citing works
Schisano, B., Tripathi, G., McGee, K. C., McTernan, P. G., & Ceriello, A. (2011) · Diabetologia · doi:10.1007/s00125-011-2049-0 · Cited by 180 · see citing works
Way, K. J., Isshiki, K., Suzuma, K., Yokota, T., Zvagelsky, D., Schöen, F. J., Sandusky, G. E., Pechous, P. A., Vlahos, C. J., Wakasaki, H., et al. (2002) · Diabetes · doi:10.2337/diabetes.51.9.2709 · Cited by 180 · see citing works
The emerging challenge in diabetes: The “metabolic memory”
Ceriello, A. (2012) · Vascular Pharmacology · doi:10.1016/j.vph.2012.05.005 · Cited by 174 · see citing works
Madsen‐Bouterse, S. A., Mohammad, G., Kanwar, M., & Kowluru, R. A. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2932 · Cited by 171 · see citing works
Hypothesis: the ‘metabolic memory’, the new challenge of diabetes
Ihnat, M. A., Thorpe, J. E., & Ceriello, A. (2007) · Diabetic Medicine · doi:10.1111/j.1464-5491.2007.02138.x · Cited by 167 · see citing works
Mahimainathan, L., Das, F., Venkatesan, B. A., & Choudhury, G. G. (2006) · Diabetes · doi:10.2337/db05-1326 · Cited by 166 · see citing works
Fioretto, P. (1993) · The Lancet · doi:10.1016/0140-6736(93)92183-t · Cited by 166 · see citing works
Role of nitrosative stress in the pathogenesis of diabetic vascular dysfunction
Szabo, C. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2008.00086.x · Cited by 165 · see citing works
Metabolic memory: mechanisms and diseases
Dong, H., Sun, Y., Nie, L., Cui, A., Zhao, P., Leung, W. K., & Wang, Q. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01755-x · Cited by 181 · see citing works
Metabolic memory and diabetic nephropathy: potential role for epigenetic mechanisms
Tonna, S. J., El‐Osta, A., Cooper, M. E., & Tikellis, C. (2010) · Nature Reviews Nephrology · doi:10.1038/nrneph.2010.55 · Cited by 152 · see citing works
Bangstad, H. ‐., Dahl‐Jørgensen, K., Hanssen, K. F., Østerby, R., Berg, K. J., & Hartmann, A. (1994) · Diabetologia · doi:10.1007/s001250050136 · Cited by 147 · see citing works
Glucose‐induced metabolic imbalances in the pathogenesis of diabetic vascular disease
Pugliese, G., Tilton, R. G., & Williamson, J. R. (1991) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610070106 · Cited by 146 · see citing works
Nahman, N. S., Leonhart, K. L., Cosio, F. G., & Hebert, C. L. (1992) · Kidney International · doi:10.1038/ki.1992.55 · Cited by 136 · see citing works
Olsen, A. S., Sarras, M. P., Leontovich, A. A., & Intine, R. V. A. (2012) · Diabetes · doi:10.2337/db11-0588 · Cited by 134 · see citing works
Treatment with a glycosaminoglycan formulation ameliorates experimental diabetic nephropathy
Gambaro, G., Venturini, A. P., Noonan, D. M., Fries, W., Re, G., Garbisa, S., Milanesi, C., Pesarini, A., Borsatti, A., Marchi, E., et al. (1994) · Kidney International · doi:10.1038/ki.1994.335 · Cited by 133 · see citing works
Periodontal Disease as a Complication of Diabetes Mellitus
Nishimura, F., Takahashi, K., Kurihara, M., Takashiba, S., & Murayama, Y. (1998) · Annals of Periodontology · doi:10.1902/annals.1998.3.1.20 · Cited by 131 · see citing works
Epigenetic programming, early life nutrition and the risk of metabolic disease
Block, T., & El-Osta, A. (2017) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2017.09.003 · Cited by 130 · see citing works
Yang, T., Feng, Q., Guo, F., Shao, M., Song, Y., Ren, G., Zhao, L., Qin, G., & Zhao, Y. (2024) · Molecular Medicine · doi:10.1186/s10020-024-00824-9 · Cited by 144 · see citing works
Beltramo, E., Berrone, E., Tarallo, S., & Porta, M. (2008) · Acta Diabetologica · doi:10.1007/s00592-008-0042-y · Cited by 130 · see citing works
Epigenetics: deciphering its role in diabetes and its chronic complications
Villeneuve, L. M., Reddy, M. A., & Natarajan, R. D. (2011) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2011.05497.x · Cited by 125 · see citing works
Retinal capillary basement membrane thickening: Role in the pathogenesis of diabetic retinopathy
Roy, S., & Kim, D. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100903 · Cited by 127 · see citing works
Self-citationHuang, Q., & Sheibani, N. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00322.2008 · Cited by 127 · see citing works
Tewari, S., Zhong, Q. P. W., dos Santos, J. M., & Kowluru, R. A. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9732 · Cited by 126 · see citing works
Fioretto, P., Bruseghin, M., Berto, I., Gallina, P., Manzato, E., & Mussap, M. (2006) · Journal of the American Society of Nephrology · doi:10.1681/asn.2005121343 · Cited by 121 · see citing works
Hypothesis: the “metabolic memory”, the new challenge of diabetes
Ceriello, A. (2009) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(09)70002-6 · Cited by 121 · see citing works
Mishra, M., Zhong, Q. P. W., & Kowluru, R. A. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-15193 · Cited by 119 · see citing works
SIRT1, p66Shc, and Set7/9 in Vascular Hyperglycemic Memory
Paneni, F., Volpe, M., Lüscher, T. F., & Cosentino, F. (2013) · Diabetes · doi:10.2337/db12-1648 · Cited by 118 · see citing works
Ding, H., & Triggle, C. R. (2005) · Vascular Health and Risk Management · doi:10.2147/vhrm.1.1.55.58939 · Cited by 118 · see citing works
Fibronectin overexpression in retinal microvessels of patients with diabetes.
Roy, S., Cagliero, E., & Lorenzi, M. (1996) · PubMed · Cited by 113 · see citing works
Self-citationThe role of CTGF in diabetic retinopathy
Klaassen, I., van Geest, R. J., Kuiper, E. J., Noorden, C. J. F. V., & Schlingemann, R. O. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2014.10.016 · Cited by 112 · see citing works
Innate immune memory: Implications for host responses to damage‐associated molecular patterns
Crișan, T. O., Netea, M. G., & Joosten, L. A. B. (2016) · European Journal of Immunology · doi:10.1002/eji.201545497 · Cited by 112 · see citing works
Recent developments in epigenetics of acute and chronic kidney diseases
Reddy, M. A., & Natarajan, R. D. (2015) · Kidney International · doi:10.1038/ki.2015.148 · Cited by 111 · see citing works
Park, S.-H., Marso, S. P., Zhou, Z., Foroudi, F., Topol, E. J., & Lincoff, A. M. (2001) · Circulation · doi:10.1161/hc3301.092789 · Cited by 110 · see citing works
Mishra, M., Zhong, Q. P. W., & Kowluru, R. A. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.07.001 · Cited by 108 · see citing works
Glycemic memory associated epigenetic changes
Siebel, A. L., Fernández, A. Z., & El‐Osta, A. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.06.005 · Cited by 103 · see citing works
Epigenetic Modifications in the Pathogenesis of Diabetic Nephropathy
Reddy, M. A., Park, J. T., & Natarajan, R. D. (2013) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2013.05.006 · Cited by 102 · see citing works
Pathophysiological Fundamentals of Diabetic Cardiomyopathy
Hu, X., Bai, T., Xu, Z., Liu, Q., Zheng, Y., & Cai, L. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160021 · Cited by 103 · see citing works
Gao, P., You, M., Li, L., Zhang, Q., Fang, X., Wei, X., Zhou, Q., Zhang, H., Wang, M., Lu, Z., et al. (2022) · Circulation · doi:10.1161/circulationaha.121.055600 · Cited by 98 · see citing works
dos Santos, J. M., & Kowluru, R. A. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-8203 · Cited by 97 · see citing works
Sato, T., & Roy, S. (2002) · PubMed · Cited by 97 · see citing works
Self-citationRenal tubular basement membrane and collagen type IV in diabetes mellitus
Ziyadeh, F. N. (1993) · Kidney International · doi:10.1038/ki.1993.19 · Cited by 97 · see citing works
Abnormal Cell Calcium Homeostasis in Type 2 Diabetes Mellitus: A New Look on Old Disease
Levy, J. (1999) · Endocrine · doi:10.1385/endo:10:1:1 · Cited by 97 · see citing works
Endothelial cell metabolic memory causes cardiovascular dysfunction in diabetes
Yao, Y., Song, Q., Hu, C., Da, X., Yu, Y., He, Z., Xu, C., Chen, Q., & Wang, Q. K. (2021) · Cardiovascular Research · doi:10.1093/cvr/cvab013 · Cited by 96 · see citing works
Siddiqi, F. S., Majumder, S., Thai, K., Abdalla, M., Hu, P., Advani, S. L., White, K., Bowskill, B. B., Guarna, G., dos Santos, C. C., et al. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014090898 · Cited by 96 · see citing works
Pichika, R., Natarajan, R. D., Nadler, J. L., Kumar, D., & Kalra, V. K. (1991) · Journal of Cellular Physiology · doi:10.1002/jcp.1041490113 · Cited by 96 · see citing works
Aiello, L. P., Robinson, G. S., Lin, Y. W., Nishio, Y., & King, G. L. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.13.6231 · Cited by 96 · see citing works
Effect of hypertension on fibronectin expression in the rat aorta.
Takasaki, I., Chobanian, A. V., Sarzani, R., & Brecher, P. I. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45828-0 · Cited by 93 · see citing works
Glucose toxicity in the vascular complications of diabetes: The cellular perspective
Lorenzi, M. (1992) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610080202 · Cited by 92 · see citing works
Self-citationMaloney-Hinds, C., PETROFSKY, J. S., Zimmerman, G. J., & Hessinger, D. A. (2009) · Diabetes Technology & Therapeutics · doi:10.1089/dia.2008.0011 · Cited by 89 · see citing works
Roy, S., Sato, T., Paryani, G., & Kao, R. S. (2003) · Diabetes · doi:10.2337/diabetes.52.5.1229 · Cited by 89 · see citing works
Self-citationAronson, D., & Edelman, E. R. (2010) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-010-9135-3 · Cited by 88 · see citing works
Metabolic Memory and Chronic Diabetes Complications: Potential Role for Epigenetic Mechanisms
Intine, R. V. A., & Sarras, M. P. (2012) · Current Diabetes Reports · doi:10.1007/s11892-012-0302-7 · Cited by 88 · see citing works
Diabetic retinopathy, metabolic memory and epigenetic modifications
Kowluru, R. A. (2017) · Vision Research · doi:10.1016/j.visres.2017.02.011 · Cited by 87 · see citing works
Epigenetic changes in diabetes
Keating, S. T., & El‐Osta, A. (2013) · Clinical Genetics · doi:10.1111/cge.12121 · Cited by 86 · see citing works
Understanding Metabolic Memory: A Tale of Two Studies
Miller, R. G., & Orchard, T. J. (2020) · Diabetes · doi:10.2337/db19-0514 · Cited by 85 · see citing works
Oshitari, T., Polewski, P. J., Chadda, M., Li, A.-F., Sato, T., & Roy, S. (2006) · Diabetes · doi:10.2337/diabetes.55.01.06.db05-0186 · Cited by 85 · see citing works
Self-citationGlucose induced genes in bovine aortic smooth muscle cells identified by mRNA differential display
Nishio, Y., Aiello, L. P., & King, G. L. (1994) · The FASEB Journal · doi:10.1096/fasebj.8.1.8299882 · Cited by 85 · see citing works
C-peptide replacement therapy as an emerging strategy for preventing diabetic vasculopathy
Bhatt, M. P., Lim, Y.-C., & Ha, K. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu211 · Cited by 86 · see citing works
The Distribution and Regulation of Integrin-Linked Kinase in Normal and Diabetic Kidneys
Guo, L., Sanders, P. W., Woods, A., & Wu, C. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63020-9 · Cited by 84 · see citing works
Periodontal disease as a complication of diabetes mellitus
Taylor, G. W., Graves, D. T., & Lamster, I. B. (2014) · doi:10.1002/9781118887837.ch6 · Cited by 83 · see citing works
Epigenetics in diabetic nephropathy, immunity and metabolism
Keating, S. T., van Diepen, J. A., Riksen, N. P., & El-Osta, A. (2018) · Diabetologia · doi:10.1007/s00125-017-4490-1 · Cited by 82 · see citing works
Xie, L., Zhu, X., Hu, Y., Li, T., Gao, Y., Shi, Y., & Tang, S. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-1364 · Cited by 82 · see citing works
Metabolic memory and diabetic retinopathy: Role of inflammatory mediators in retinal pericytes
Kowluru, R. A., Zhong, Q. P. W., & Kanwar, M. (2010) · Experimental Eye Research · doi:10.1016/j.exer.2010.02.006 · Cited by 82 · see citing works
Kowluru, R. (2013) · Current Medicinal Chemistry · doi:10.2174/09298673113209990029 · Cited by 81 · see citing works
Phillips, A. O., Steadman, R., Morrisey, K., Martin, J. T., Eynstone, L. V., & Williams, J. D. (1997) · Kidney International · doi:10.1038/ki.1997.419 · Cited by 81 · see citing works
Grant, M. B., & Guay, C. (1991) · PubMed · Cited by 79 · see citing works
Legacy Effects from DCCT and UKPDS: What They Mean and Implications for Future Diabetes Trials
Murray, P. T., Chune, G., & Raghavan, V. A. (2010) · Current Atherosclerosis Reports · doi:10.1007/s11883-010-0128-1 · Cited by 78 · see citing works
Hammes, H., Str�dter, D., Weiss, A., Bretzel, R. G., Federlin, K., & Brownlee, M. (1995) · Diabetologia · doi:10.1007/bf00401835 · Cited by 78 · see citing works
- Authors
- Roy, S., Sala, R., Cagliero, E., & Lorenzi, M.
- Affiliations
- Eye Research Institute of Retina Foundation, Boston, MA 02114.
- Harvard University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1990-01
- Volume
- 87
- Issue
- 1
- Pages
- 404-408
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC53272
- OpenAlex
- W2043406584
- Cited by
- 409
- References
- 43
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 11 · 2023: 8 · 2022: 11 · 2021: 11 · 2020: 12 · 2019: 13 · 2018: 6 · 2017: 21 · 2016: 12 · 2015: 22 · 2014: 24 · 2013: 18 · 2012: 25
- FWCI
- 7.11
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01hl036861-03)
- National Heart, Lung, and Blood Institute (HL-36861)
- 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 › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Keywords
- fibronectin, diabetes mellitus, high glucose, hyperglycemia, diabetes complications, endothelial cells, type IV collagen, renal cortex, heart, basement membrane thickening, streptozotocin-induced diabetes, cell proliferation
- MeSH terms
- Animals, Cells, Cultured, Diabetes Mellitus, Experimental, Endothelium, Vascular, Female, Fibronectins, Gene Expression Regulation, Glucose, Humans, Kidney Cortex, Male, Myocardium, Pregnancy, Rats, Inbred Strains, Reference Values, RNA, Messenger, Transcription, Genetic, Umbilical Veins, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review