Diabetes-induced up-regulation of uncoupling protein-2 results in increased mitochondrial uncoupling in kidney proximal tubular cells
Open accessAbstract
We have previously reported increased O(2) consumption unrelated to active transport by tubular cells and up-regulated mitochondrial uncoupling protein (UCP)-2 expressions in diabetic kidneys. It is presently unknown if the increased UCP-2 levels in the diabetic kidney results in mitochondrial uncoupling and increased O(2) consumption, which we therefore investigated in this study. The presence of UCP-2 in proximal tubular cells was confirmed by immunohistochemistry and found to be increased (western blot) in homogenized tissue and isolated mitochondria from kidney cortex of diabetic rats. Isolated proximal tubular cells had increased total and ouabain-insensitive O(2) consumption compared to controls. Isolated mitochondria from diabetic animals displayed increased glutamate-stimulated O(2) consumption (in the absence of ADP and during inhibition of the ATP-synthase by oligomycin) compared to controls. Guanosine diphosphate, an UCP inhibitor, and bovine serum albumin which removes fatty acids that are essential for UCP-2 uncoupling activity, independently prevented the increased glutamate-stimulated O(2) consumption in mitochondria from diabetic animals. In conclusion, diabetic rats have increased mitochondrial UCP-2 expression in renal proximal tubular cells, which results in mitochondrial uncoupling and increased O(2) consumption. This mechanism may be protective against diabetes-induced oxidative stress, but will increase O(2) usage. The subsequently reduced O(2) availability may contribute to diabetes-induced progressive kidney damage.
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In STZ diabetic rats, proximal tubular UCP2 expression is increased.
“Recent immunohistochemical studies revealed an increase in proximal tubular UCP2 expression in STZ diabetic rats (108).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [108]
Diabetic rats express increased mitochondrial UCP-2 in proximal tubular cells associated with increased oxygen use.
“Friederich et al. (108) showed that diabetic rats express increased mitochondrial UCP-2 in proximal tubular cells associated with increased oxygen use and suggested that the increase in UCP2 was protective against oxidative stress.”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [108]
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Sadri, S., Tomar, N., Yang, C., Audi, S. H., Cowley, A. W., & Dash, R. K. (2023) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2023.109690 · Cited by 17 · see citing works
Partners in diabetes epidemic: A global perspective
Wang, H., Akbari‐Alavijeh, S., Parhar, R. S., Gaugler, R. R., & Hashmi, S. (2023) · World Journal of Diabetes · doi:10.4239/wjd.v14.i10.1463 · Cited by 17 · see citing works
Sivertsson, E., Friederich‐Persson, M., Persson, P., Nangaku, M., Hansell, P., & Palm, F. (2022) · PLoS ONE · doi:10.1371/journal.pone.0264524 · Cited by 17 · see citing works
Self-citationBioenergetics: the evolutionary basis of progressive kidney disease
Chevalier, R. L. (2023) · Physiological Reviews · doi:10.1152/physrev.00029.2022 · Cited by 17 · see citing works
Rubattu, S. D., Cotugno, M., Bianchi, F., Sironi, L., Gelosa, P., Stanzione, R., Forte, M., Sanctis, C. D., Madonna, M., Marchitti, S., et al. (2017) · Journal of Hypertension · doi:10.1097/hjh.0000000000001374 · Cited by 16 · see citing works
Hyperbaric oxygen therapy reduces renal lactate production
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Self-citationLight-emitting diode modulates carbohydrate metabolism by pancreatic duct regeneration
Tatmatsu-Rocha, J. C., de Castro, C. A., Sene‐Fiorese, M., & Parizotto, N. A. (2017) · Lasers in Medical Science · doi:10.1007/s10103-017-2245-3 · Cited by 15 · see citing works
Cellular and subcellular localization of uncoupling protein 2 in the human kidney
Nigro, M., Sanctis, C. D., Formisano, P., Stanzione, R., Forte, M., Capasso, G., Gigliotti, G., Rubattu, S. D., & Viggiano, D. (2018) · Journal of Molecular Histology · doi:10.1007/s10735-018-9782-3 · Cited by 15 · see citing works
Relating glaucomatous visual field loss to retinal oxygen delivery and metabolism
Aref, A. A., Maleki, S., Tan, O., Huang, D., Varma, R., & Shahidi, M. (2019) · Acta Ophthalmologica · doi:10.1111/aos.14120 · Cited by 14 · see citing works
Jiang, L., Zhang, X., & Wu, X. (2025) · Integrative Medicine in Nephrology and Andrology · doi:10.1097/imna-d-25-00019 · Cited by 13 · see citing works
Sadri, S., Zhang, X., Audi, S. H., Cowley, A. W., & Dash, R. K. (2023) · Function · doi:10.1093/function/zqad038 · Cited by 10 · see citing works
Persson, P., Fasching, A., & Palm, F. (2019) · Acta Physiologica · doi:10.1111/apha.13254 · Cited by 10 · see citing works
Self-citationSivertsson, E., Friederich‐Persson, M., Öberg, C. M., Fasching, A., Hansell, P., Rippe, B., & Palm, F. (2017) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00033.2017 · Cited by 9 · see citing works
Self-citationBariatric surgery and kidney disease outcomes in severely obese youth
Bjornstad, P., Nehus, E. J., & van Raalte, D. H. (2020) · Seminars in Pediatric Surgery · doi:10.1016/j.sempedsurg.2020.150883 · Cited by 9 · see citing works
Oxidative Stress and Hypoxia in the Pathogenesis of Diabetic Nephropathy
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Self-citationCardoso, S., Santos, R. X., Carvalho, C., Correia, S. C., Santos, M. S., & Moreira, P. I. (2011) · Free Radicals and Antioxidants · doi:10.5530/ax.2011.2.3 · Cited by 8 · see citing works
Function and expression of renal organic anion transporters in experimental diabetes in mice
Lungkaphin, A., Srimaroeng, C., & Chatsudthipong, V. (2012) · Cited by 8 · see citing works
Pathophysiological Roles of Reactive Oxygen and Nitrogen Species
Kilgour, J. D., & Roberts, R. A. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_10 · Cited by 7 · see citing works
Persson, M. F., Welch, W. J., Wilcox, C. S., & Palm, F. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-4989-8_30 · Cited by 6 · see citing works
Self-citationDose-dependent regulation of kidney mitochondrial function by angiotensin II
Sivertsson, E., Ramilo, A. B., Schiffer, T. A., Hansell, P., Friederich‐Persson, M., Persson, P., & Palm, F. (2023) · Upsala Journal of Medical Sciences · doi:10.48101/ujms.v128.10312 · Cited by 5 · see citing works
Self-citationFranzén, S., & Palm, F. (2015) · Diabetologia · doi:10.1007/s00125-015-3690-9 · Cited by 5 · see citing works
Self-citationFriederich‐Persson, M., Welch, W. J., Luo, Z., Palm, F., & Nordquist, L. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0620-8_21 · Cited by 4 · see citing works
Self-citationReactive Oxygen Species (ROS) and Diabetic Nephropathy
Badal, S. S., Badal, S. S., & Danesh, F. R. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_186 · Cited by 3 · see citing works
Queiroz, A. L. F., Garcia, C. B., da Silva, J. P. M. D. O., Cavalini, D. F., Alexandrino, A. V., da Cunha, A. F., Vercesi, A. E., Castilho, R. F., & Shiguemoto, G. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms26010266 · Cited by 2 · see citing works
Mitochondrial Dysfunction in Renal Aging: A Vicious Cycle Driving Kidney Disease Progression
Yu, W., Ouyang, Q., Liu, W., Jia, L., & Wang, B. (2026) · Antioxidants and Redox Signaling · doi:10.1177/15230864251410936 · Cited by 3 · see citing works
Studies on the Function and Regulation of Mitochondrial Uncoupling Proteins
Porter, R. K. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3573-0_7 · Cited by 2 · see citing works
Podocytes and the struggle against glucose toxicity: New targets for treatment?
Gnudi, L. (2012) · Metabolism · doi:10.1016/j.metabol.2012.01.015 · Cited by 2 · see citing works
Diabetic Nephropathy in Children and Adolescents
Bjornstad, P. (2018) · Springer eBooks · doi:10.1007/978-3-319-93521-8_4 · Cited by 2 · see citing works
Garreta, E., Prado, P., Stanifer, M. L., Monteil, V., del Pozo, C. H., Ullate‐Agote, A., Vilas‐Zornoza, A., Romero, J. P., Jonsson, G., Oria, R., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.13.456228 · Cited by 2 · see citing works
Franzén, S. (2016) · Linköping University medical dissertations · doi:10.3384/diss.diva-125522 · Cited by 1 · see citing works
Inhibition of Mammalian Target of Rapamycin Induces Renal Mitochondrial Uncoupling in Rats
Sivertsson, E., & Friederich‐Persson, M. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-7411-1_41 · Cited by 1 · see citing works
Reactive Oxygen Species and Chronic Kidney Disease
You, Y.-H., & Sharma, K. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_111 · Cited by 1 · see citing works
Bertelsen, L. B., Nielsen, P. M., Qi, H., Mariager, C. Ø., Lindhardt, J. L., & Laustsen, C. (2018) · Tomography · doi:10.18383/j.tom.2018.00022 · Cited by 1 · see citing works
Mohamad, M. I., Aboelhussein, M. M., Elayat, W. M., & Elshormilisy, A. A. (2018) · Gene Reports · doi:10.1016/j.genrep.2018.03.007
- Authors
- Friederich, M., Fasching, A., Hansell, P., Nordquist, L., & Palm, F.
- Affiliations
- Uppsala University (SE)
- Corresponding author
- Palm, Fredrik
- Venue
- Biochimica et Biophysica Acta (BBA) - Bioenergetics
- Publisher
- Elsevier BV
- Published
- 2008-07
- Volume
- 1777
- Issue
- 7-8
- Pages
- 935-940
- ISSN
- 0005-2728 (ISSN-L)
- OpenAlex
- W2084502320
- Cited by
- 111
- References
- 29
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 6 · 2020: 9 · 2019: 7 · 2018: 9 · 2017: 7 · 2016: 6 · 2015: 4 · 2014: 11 · 2013: 5 · 2012: 12
- FWCI
- 2.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fondation pour la Recherche Médicale
- Svenska Sällskapet för Medicinsk Forskning
- Stiftelsen Familjen Ernfors Fond
- Marcus och Amalia Wallenbergs minnesfond
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (K99DK077858)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- UCP2, mitochondrial uncoupling, diabetes mellitus, diabetic kidney, proximal tubular epithelial cells, oxygen consumption, oxidative stress, kidney injury, guanosine diphosphate, fatty acids
- MeSH terms
- Uncoupling Protein 2, Animals, Diabetes Mellitus, Experimental, Hyperglycemia, Insulin, Ion Channels, Kidney Tubules, Proximal, Male, Mitochondria, Oxygen Consumption, Rats, Inbred WF, Up-Regulation, Mitochondrial Proteins, Rats
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