The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin.
Open accessAbstract
This study determined whether retinal degeneration during diabetes includes retinal neural cell apoptosis. Image analysis of retinal sections from streptozotocin (STZ) diabetic rats after 7.5 months of STZ diabetes identified 22% and 14% reductions in the thickness of the inner plexiform and inner nuclear layers, respectively (P < 0. 001). The number of surviving ganglion cells was also reduced by 10% compared to controls (P < 0.001). In situ end labeling of DNA terminal dUTP nick end labeling (TUNEL) identified a 10-fold increase in the frequency of retinal apoptosis in whole-mounted rat retinas after 1, 3, 6, and 12 months of diabetes (P < 0.001, P < 0. 001, P < 0.01, and P < 0.01, respectively). Most TUNEL-positive cells were not associated with blood vessels and did not colocalize with the endothelial cell-specific antigen, von Willebrand factor. Insulin implants significantly reduced the number of TUNEL-positive cells (P < 0.05). The number of TUNEL-positive cells was also increased in retinas from humans with diabetes. These data indicate that retinal neural cell death occurs early in diabetes. This is the first quantitative report of an increase in neural cell apoptosis in the retina during diabetes, and indicates that neurodegeneration is an important component of diabetic retinopathy.
Overview
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
Verification
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics
Kerr, J. F. R., Wyllie, A. H., & Currie, A. R. (1972) · British Journal of Cancer · doi:10.1038/bjc.1972.33 · Cited by 15,725
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444
Cell Death: The Significance of Apoptosis
Wyllie, A. H., Kerr, J. F. R., & Currie, A. R. (1980) · International Review of Cytology · doi:10.1016/s0074-7696(08)62312-8 · Cited by 7,162
(2007) · Developments in Ophthalmology · doi:10.1159/isbn.978-3-318-01439-6 · Cited by 5,583
Apoptosis, oncosis, and necrosis. An overview of cell death.
Majno, G., & Joris, I. (1995) · PubMed · Cited by 3,306
Astrocytes induce blood–brain barrier properties in endothelial cells
Janzer, R. C., & Raff, M. C. (1987) · Nature · doi:10.1038/325253a0 · Cited by 1,626
Programmed Cell Death and the Control of Cell Survival: Lessons from the Nervous System
Raff, M. C., Barres, B. A., Burne, J. F., Coles, H. S., Ishizaki, Y., & Jacobson, M. D. (1993) · Science · doi:10.1126/science.8235590 · Cited by 1,460
Theory and Practice of Histotechnology
Sheehan, D. C., & Hrapchak, B. B. (1973) · Medical Entomology and Zoology · Cited by 1,128
Theory and Practice of Histotechnology
Drury, R. (1981) · Journal of Clinical Pathology · doi:10.1136/jcp.34.12.1406-c · Cited by 1,112
Meyer-Franke, A., Kaplan, M. R., Pfieger, F. W., & Barres, B. A. (1995) · Neuron · doi:10.1016/0896-6273(95)90172-8 · Cited by 848
A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA.
Wijsman, J. H., Jonker, R. R., Keijzer, R., van de Velde, C. J., Cornelisse, C. J., & van Dierendonck, J. H. (1993) · Journal of Histochemistry & Cytochemistry · doi:10.1177/41.1.7678025 · Cited by 802
Multiple extracellular signals are required for long-term oligodendrocyte survival
Barres, B. A., Schmid, R., Sendnter, M., & Raff, M. C. (1993) · Development · doi:10.1242/dev.118.1.283 · Cited by 712
Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy.
Mizutani, M., Kern, T. S., & Lorenzi, M. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118746 · Cited by 706
Immunohistochemical evidence for apoptosis in Alzheimerʼs disease
Su, J. H., Anderson, A. J., Cummings, B. J., & Cotman, C. W. (1994) · NeuroReport · doi:10.1097/00001756-199412000-00031 · Cited by 571
Müller cell changes in human diabetic retinopathy.
Mizutani, M., Gerhardinger, C., & Lorenzi, M. (1998) · Diabetes · doi:10.2337/diabetes.47.3.445 · Cited by 481
Lieth, E., Barber, A. J., Xu, B., Dice, C., Ratz, M. J., Tanase, D., & Strother, J. M. (1998) · Diabetes · doi:10.2337/diabetes.47.5.815 · Cited by 467
Self-citationTUNEL-Positive Ganglion Cells in Human Primary Open-angle Glaucoma
Kerrigan, L. A. (1997) · Archives of Ophthalmology · doi:10.1001/archopht.1997.01100160201010 · Cited by 465
Histochemical detection of apoptosis in Parkinson's disease
Mochizuki, H., Goto, K., Mori, H., & Mizuno, Y. (1996) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(95)00336-z · Cited by 452
Studies of Retinal Vascular Patterns
Kuwabara, T. (1960) · Archives of Ophthalmology · doi:10.1001/archopht.1960.01840010906012 · Cited by 438
Anderson, A., Su, J., & Cotman, C. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01710.1996 · Cited by 389
Evidence of apoptotic cell death in HIV encephalitis.
Petito, C. K., & Roberts, B. (1995) · Europe PMC (PubMed Central) · Cited by 299
Hammes, H.-P., Federoff, H. J., & Brownlee, M. (1995) · Molecular Medicine · doi:10.1007/bf03401589 · Cited by 246
Quantitation of ischemic damage in the rat retina
Hughes, W. F. (1991) · Experimental Eye Research · doi:10.1016/0014-4835(91)90215-z · Cited by 240
Quantitative analysis of proliferation and cell cycle length during development of the rat retina
Alexiades, M. R., & Cepko, C. (1996) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199603)205:3<293::aid-aja9>3.0.co;2-d · Cited by 206
Retinal Nerve Fiber Layer Defect as an Early Manifestation of Diabetic Retinopathy
Chihara, E., Matsuoka, T., Ogura, Y., & Matsumura, M. (1993) · Ophthalmology · doi:10.1016/s0161-6420(93)31513-7 · Cited by 190
Apoptosis of Retinal Ganglion Cells in Anterior Ischemic Optic Neuropathy
Levin, L. A. (1996) · Archives of Ophthalmology · doi:10.1001/archopht.1996.01100130484027 · Cited by 176
Insulin Attenuates Ischemic Brain Damage Independent of its Hypoglycemic Effect
Voll, C. L., & Auer, R. N. (1991) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1991.168 · Cited by 166
Büchi, E. R. (1992) · Experimental Eye Research · doi:10.1016/s0014-4835(05)80173-3 · Cited by 153
Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cells.
Gardner, T. W., Lieth, E., Khin, S. A., Barber, A. J., Bonsall, D. J., Lesher, T., Rice, K., & Brennan, W. A. (1997) · PubMed · Cited by 145
Self-citationRetinopathy in animal models of diabetes
Engerman, R. L., & Kern, T. S. (1995) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610110203 · Cited by 145
Versaux‐Botteri, C., Martin‐Martinelli, E., Nguyen-Legros, J., Geffard, M., Vigny, A., & Denoroy, L. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902430311 · Cited by 127
Regulation by insulin of a unique neuronal Ca2+ pool and of neuropeptide secretion
Jonas, E. A., Knox, R. J., Smith, T. C. M., Wayne, N. L., Connor, J. A., & Kaczmarek, L. K. (1997) · Nature · doi:10.1038/385343a0 · Cited by 120
DNA strand breaks in rat tissues as detected by in situ nick translation
Iseki, S. (1986) · Experimental Cell Research · doi:10.1016/0014-4827(86)90172-2 · Cited by 89
Bloodworth, J. M. B. (1962) · PubMed · Cited by 82
Expression of cell cycle-related genes in dying cells in retinal ischemic injury.
Kuroiwa, S., Katai, N., Shibuki, H., Kurokawa, T., Umihira, J., Nikaido, T., Kametani, K., & Yoshimura, N. (1998) · PubMed · doi:10.11501/3149134 · Cited by 79
Apoptosis, retinitis pigmentosa, and degeneration
WONG, P. W. K. (1994) · Biochemistry and Cell Biology · doi:10.1139/o94-066 · Cited by 72
Effect of Postmortem Interval on In Situ End-Labeling of DNA Oligonucleosomes
Petito, C. K., & Roberts, B. (1995) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199511000-00002 · Cited by 56
Chapter 1 Mechanisms of Nerve Cell Death: Apoptosis or Necrosis After Cerebral Ischaemia
Chalmers-Redman, R. M. E., Fraser, A., Ju, W. Y. H., Wadia, J. S., Tatton, N. A., & Tatton, W. G. (1996) · International review of neurobiology · doi:10.1016/s0074-7742(08)60713-8 · Cited by 48
Yamaguchi, T., Keino‐Masu, K., & Fukuda, J. (1995) · Neurochemistry International · doi:10.1016/0197-0186(94)00127-g · Cited by 24
Cited by
Mechanisms of Diabetic Complications
Forbes, J. M., & Cooper, M. E. (2013) · Physiological Reviews · doi:10.1152/physrev.00045.2011 · Cited by 2,890
Antonetti, D. A., Klein, R., & Gardner, T. W. (2012) · New England Journal of Medicine · doi:10.1056/nejmra1005073 · Cited by 1,659
Self-citationEffects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology
Matés, >. M. (2000) · Toxicology · doi:10.1016/s0300-483x(00)00306-1 · Cited by 1,518
Diabetic Retinopathy: Pathophysiology and Treatments
Wang, W., & Lo, A. C. Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061816 · Cited by 1,358
Inflammation in diabetic retinopathy
Tang, J., & Kern, T. S. (2011) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2011.05.002 · Cited by 1,116
Metadata
- Authors
- Barber, A. J., Lieth, E., Khin, S. A., Antonetti, D. A., Buchanan, A. G., & Gardner, T. W.
- Venue
- Journal of Clinical Investigation
- Published
- 1998-08-15
- Volume
- 102
- Issue
- 4
- Pages
- 783-791
- ISSN
- 0021-9738 (ISSN-L)
- OpenAlex
- W1993968665
- Cited by
- 1,295
- References
- 39
- FWCI
- 11.99
- Type
- journal article
- Language
- en
- Open access
- bronze
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
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.