Loss of Prohibitin Induces Mitochondrial Damages Altering β-Cell Function and Survival and Is Responsible for Gradual Diabetes Development
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Prohibitins are highly conserved proteins mainly implicated in the maintenance of mitochondrial function and architecture. Their dysfunctions are associated with aging, cancer, obesity, and inflammation. However, their possible role in pancreatic β-cells remains unknown. The current study documents the expression of prohibitins in human and rodent islets and their key role for β-cell function and survival. Ablation of Phb2 in mouse β-cells sequentially resulted in impairment of mitochondrial function and insulin secretion, loss of β-cells, progressive alteration of glucose homeostasis, and, ultimately, severe diabetes. Remarkably, these events progressed over a 3-week period of time after weaning. Defective insulin supply in β-Phb2(-/-) mice was contributed by both β-cell dysfunction and apoptosis, temporarily compensated by increased β-cell proliferation. At the molecular level, we observed that deletion of Phb2 caused mitochondrial abnormalities, including reduction of mitochondrial DNA copy number and respiratory chain complex IV levels, altered mitochondrial activity, cleavage of L-optic atrophy 1, and mitochondrial fragmentation. Overall, our data demonstrate that Phb2 is essential for metabolic activation of mitochondria and, as a consequence, for function and survival of β-cells.
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Inactivation of PHB-2 alters beta-cell function in pancreas producing diabetes.
“or alters beta-cell function in pancreas producing diabetes (Supale et al., 2013).”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Supale et al., 2013
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Standards of medical care in diabetes—2013
American Diabetes Association (2013) · Diabetes Care · doi:10.2337/dc13-s011 · Cited by 4,369 · see citing works
Fission and selective fusion govern mitochondrial segregation and elimination by autophagy
Twig, G., Elorza, A., Molina, A. J. A., Mohamed, H., Wikstrom, J. D., Walzer, G., Stiles, L., Haigh, S. E., Katz, S., Las, G., et al. (2008) · The EMBO Journal · doi:10.1038/sj.emboj.7601963 · Cited by 3,082 · see citing works
Postic, C., Shiota, M., Niswender, K. D., Jetton, T. L., Chen, Y., Moates, J. M., Shelton, K. D., Lindner, J., Cherrington, A. D., & Magnuson, M. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.1.305 · Cited by 1,302 · see citing works
<i>miR-375</i> maintains normal pancreatic α- and β-cell mass
Poy, M. N., Hausser, J., Trajkovski, M., Braun, M., Collins, S., Rorsman, P., Zavolan, M., & Stoffel, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810550106 · Cited by 740 · see citing works
Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages
Herrera, P. L. (2000) · Development · doi:10.1242/dev.127.11.2317 · Cited by 674 · see citing works
Self-citationGlucagonocentric restructuring of diabetes: A pathophysiologic and therapeutic makeover
Unger, R. H., & Cherrington, A. D. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60016 · Cited by 670 · see citing works
Reversal of obesity by targeted ablation of adipose tissue
Kolonin, M. G., Saha, P., Chan, L., Pasqualini, R., & Arap, W. (2004) · Nature Medicine · doi:10.1038/nm1048 · Cited by 596 · see citing works
Prohibitins act as a membrane‐bound chaperone for the stabilization of mitochondrial proteins
Nijtmans, L. G. J., de Jong, L., Artal‐Sanz, M., Coates, P. J., BERDEN, J. A., Back, J. W., Muijsers, A. O., van der Spek, H., & Grivell, L. A. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2444 · Cited by 553 · see citing works
Merkwirth, C., Dargazanli, S., Tatsuta, T., Geimer, S., Löwer, B., Wunderlich, F. T., von Kleist-Retzow, J., Waisman, A., Westermann, B., & Langer, T. (2008) · Genes & Development · doi:10.1101/gad.460708 · Cited by 519 · see citing works
Self-citationSilva, J. P., Köhler, M., Graff, C., Oldfors, A., Magnuson, M. A., Berggren, P.-O., & Larsson, N.-G. (2000) · Nature Genetics · doi:10.1038/81649 · Cited by 433 · see citing works
Merkwirth, C., & Langer, T. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.05.013 · Cited by 405 · see citing works
Self-citationAnello, M., Lupi, R., Spampinato, D., Piro, S., Masini, M., Boggi, U., Del Prato, S., Rabuazzo, A. M., Purrello, F., & Marchetti, P. (2005) · Diabetologia · doi:10.1007/s00125-004-1627-9 · Cited by 385 · see citing works
Mitochondrial Networking Protects β-Cells From Nutrient-Induced Apoptosis
Molina, A. J. A., Wikstrom, J. D., Stiles, L., Las, G., Mohamed, H., Elorza, A., Walzer, G., Twig, G., Katz, S., Corkey, B. E., et al. (2009) · Diabetes · doi:10.2337/db07-1781 · Cited by 381 · see citing works
Fusaro, G., Dasgupta, P., Rastogi, S., Joshi, B., & Chellappan, S. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305171200 · Cited by 343 · see citing works
Leptin therapy in insulin-deficient type I diabetes
Wang, M.-Y., Chen, L., Clark, G. O., Lee, Y., Stevens, R. D., Ilkayeva, O. R., Wenner, B. R., Bain, J. R., Charron, M. J., Newgard, C. B., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909422107 · Cited by 327 · see citing works
The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins
Mühlenhoff, U. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.17.2025 · Cited by 326 · see citing works
Conditional Gene Targeting in Mouse Pancreatic β-Cells
Wicksteed, B. L., Briššová, M., Yan, W., Opland, D. M., Plank, J. L., Reinert, R. B., Dickson, L. M., Tamarina, N. A., Philipson, L. H., Shostak, A., et al. (2010) · Diabetes · doi:10.2337/db10-0624 · Cited by 321 · see citing works
Visualizing Superoxide Production in Normal and Diabetic Rat Islets of Langerhans
Bindokas, V. P., Kuznetsov, A., Sreenan, S., Polonsky, K. S., Roe, M. W., & Philipson, L. H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m206913200 · Cited by 239 · see citing works
Terashima, M., Kim, K. M., Adachi, T., Nielsen, P. J., Reth, M. G., Köhler, G., & Lamers, M. C. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06689.x · Cited by 236 · see citing works
Higa, M., Zhou, Y.-T., Ravazzola, M., Baetens, D., Orci, L., & Unger, R. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11513 · Cited by 235 · see citing works
Mitochondrial dysfunction in pancreatic β cells
Supale, S., Li, N., Brun, T., & Maechler, P. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.06.002 · Cited by 231 · see citing works
Self-citationInsulin independence after living-donor distal pancreatectomy and islet allotransplantation
Matsumoto, S., Okitsu, T., Iwanaga, Y., Noguchi, H., Nagata, H., Yonekawa, Y., Yamada, Y., Fukuda, K., Tsukiyama, K., Suzuki, H., et al. (2005) · The Lancet · doi:10.1016/s0140-6736(05)66383-0 · Cited by 214 · see citing works
Coates, P. J., Nenutil, R., McGregor, A., Picksley, S. M., Crouch, D. H., Hall, P. A., & Wright, E. G. (2001) · Experimental Cell Research · doi:10.1006/excr.2001.5166 · Cited by 207 · see citing works
Schleicher, M., Shepherd, B. R., Suárez, Y., Fernandez-Hernando, C. F., Yu, J. Q., Pan, Y., Acevedo, L. M., Shadel, G. S., & Sessa, W. C. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200706072 · Cited by 204 · see citing works
Zhang, Z., Wakabayashi, N., Wakabayashi, J., Tamura, Y., Song, W., Sereda, S., Clerc, P., Polster, B. M., Aja, S. M., Pletnikov, M. V., et al. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-12-0933 · Cited by 170 · see citing works
Merkwirth, C., Martinelli, P., Korwitz, A., Morbin, M., Brönneke, H. S., Jordan, S. D., Rugarli, E. I., & Langer, T. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003021 · Cited by 162 · see citing works
Self-citationEffects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells.
Kennedy, E. D., Maechler, P., & Wollheim, C. B. (1998) · Diabetes · doi:10.2337/diabetes.47.3.374 · Cited by 151 · see citing works
Self-citationPancreatic diabetes manifests when beta cell area declines by approximately 65% in humans
Meier, J. J., Breuer, T. G. K., Bonadonna, R. C., Tannapfel, A., Uhl, W. H., Schmidt, W. E., Schrader, H., & Menge, B. (2012) · Diabetologia · doi:10.1007/s00125-012-2466-8 · Cited by 144 · see citing works
Frataxin deficiency in pancreatic islets causes diabetes due to loss of β cell mass
Ristow, M., Mulder, H., Pomplun, D., Schulz, T. J., Schmehl, K., Krause, A., Fex, M., Puccio, H. M., Müller, J., Isken, F., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci18107 · Cited by 131 · see citing works
Li, N., Ли, Б., Brun, T., Deffert-Delbouille, C., Mahiout, Z., Daali, Y., Ma, X., Krause, K., & Maechler, P. (2012) · Diabetes · doi:10.2337/db12-0009 · Cited by 126 · see citing works
Self-citationExercise preconditioning and brain ischemic tolerance
Zhang, F., Wu, Y., & Jia, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.018 · Cited by 123 · see citing works
Park, K., Wiederkehr, A., Kirkpatrick, C. L., Mattenberger, Y., Martinou, J., Marchetti, P., Demaurex, N., & Wollheim, C. B. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806251200 · Cited by 114 · see citing works
Prohibitin Is a Novel Regulator of Antioxidant Response That Attenuates Colonic Inflammation in Mice
Theiss, A. L., Vijay–Kumar, M., Obertone, T. S., Jones, D. P., Hansen, J. M., Gewirtz, A. T., Merlin, D., & Sitaraman, S. V. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.03.033 · Cited by 113 · see citing works
de Andrade, P. B. M., Rubi, B., Frigerio, F., van den Ouweland, J. M. W., Maassen, J. A., & Maechler, P. (2006) · Diabetologia · doi:10.1007/s00125-006-0301-9 · Cited by 98 · see citing works
Self-citationCarobbio, S., Frigerio, F., Rubı́, B., Vetterli, L., Bloksgaard, M., Gjinovci, A., Pournourmohammadi, S., Herrera, P. L., Reith, W., Mandrup, S., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806295200 · Cited by 96 · see citing works
Self-citationCarobbio, S., Ishihara, H., Fernández‐Pascual, S., Bartley, C., Martín-del-Río, R., & Maechler, P. (2004) · Diabetologia · doi:10.1007/s00125-003-1306-2 · Cited by 91 · see citing works
Self-citationRole of Mitochondria in β-cell Function and Dysfunction
Maechler, P., Li, N., Casimir, M., Vetterli, L., Frigerio, F., & Brun, T. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-90-481-3271-3_9 · Cited by 69 · see citing works
Self-citationCasimir, M., Lasorsa, F. M., Rubı́, B., Caille, D., Palmieri, F., Meda, P., & Maechler, P. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.015495 · Cited by 65 · see citing works
Self-citationCasimir, M., de Andrade, P. B., Gjinovci, A., Montani, J., Maechler, P., & Dulloo, A. G. (2011) · Nutrition & Metabolism · doi:10.1186/1743-7075-8-2 · Cited by 19 · see citing works
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Zhang, G., Frederick, D. T., Wu, L. W., Wei, Z., Krepler, C., Srinivasan, S., Chae, Y. C., Xu, X., Choi, H., Dimwamwa, E., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci82661 · Cited by 282 · see citing works
Is Alzheimer’s disease a systemic disease?
Morris, J. K., Honea, R. A., Vidoni, E. D., Swerdlow, R. H., & Burns, J. M. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.04.012 · Cited by 219 · see citing works
Prohibitins: A Critical Role in Mitochondrial Functions and Implication in Diseases
Signorile, A., Sgaramella, G., Bellomo, F., & Rasmo, D. D. (2019) · Cells · doi:10.3390/cells8010071 · Cited by 209 · see citing works
Richter‐Dennerlein, R., Korwitz, A., Haag, M., Tatsuta, T., Dargazanli, S., Baker, M., Decker, T., Lamkemeyer, T., Rugarli, E. I., & Langer, T. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.04.016 · Cited by 200 · see citing works
Self-citationMultifaceted role of prohibitin in cell survival and apoptosis
Peng, Y., Chen, P., Ouyang, R., & Song, L. (2015) · APOPTOSIS · doi:10.1007/s10495-015-1143-z · Cited by 195 · see citing works
Prohibitin 2: At a communications crossroads
Bavelloni, A., Piazzi, M., Raffini, M., Faenza, I., & Blalock, W. L. (2015) · IUBMB Life · doi:10.1002/iub.1366 · Cited by 167 · see citing works
Age-Related Impairment of Pancreatic Beta-Cell Function: Pathophysiological and Cellular Mechanisms
Tata, V. D. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00138 · Cited by 144 · see citing works
Reddy, P. H. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-132060 · Cited by 136 · see citing works
ER-to-mitochondria miscommunication and metabolic diseases
López‐Crisosto, C., Bravo, R., Rodriguez–Peña, M., Mera, C., Castro, P., Quest, A. F. G., Rothermel, B. A., Cifuentes, M., & Lavandero, S. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.07.011 · Cited by 115 · see citing works
Malik, A. N., Czajka, A., & Cunningham, P. (2016) · Mitochondrion · doi:10.1016/j.mito.2016.05.003 · Cited by 113 · see citing works
Ježek, P., Jabůrek, M., Holendová, B., Engstová, H., & Dlasková, A. (2023) · Antioxidants and Redox Signaling · doi:10.1089/ars.2022.0173 · Cited by 111 · see citing works
Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity
López-Lluch, G. (2017) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.12.005 · Cited by 103 · see citing works
“Moreover, inactivation of PHB-2 in mice brain affects mitochondrial structure and activity resulting in neurodegeneration by hyperphosphorylation of Tau (Merkwirth et al., 2012) or alters beta-cell function in pancreas producing diabetes (Supale et al., 2013).”
BackgroundMitochondrial regulation of β-cell function: Maintaining the momentum for insulin release
Kaufman, B. A., Li, C., & Soleimanpour, S. A. (2015) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2015.01.004 · Cited by 103 · see citing works
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Chowdhury, I., Thompson, W. E., & Thomas, K. (2013) · Journal of Cellular Physiology · doi:10.1002/jcp.24531 · Cited by 97 · see citing works
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Fex, M., Nicholas, L. M., Vishnu, N., Medina, A., Sharoyko, V. V., Nicholls, D. G., Spégel, P., & Mulder, H. (2018) · Journal of Endocrinology · doi:10.1530/joe-17-0367 · Cited by 91 · see citing works
Zou, R., Tao, J., He, J., Wang, C., Tan, S., Xia, Y., Chang, X., Li, R., Wang, G., Zhou, H., et al. (2022) · Research · doi:10.34133/research.0001 · Cited by 72 · see citing works
Resveratrol Rescues Kidney Mitochondrial Function Following Hemorrhagic Shock
Wang, H., Guan, Y., Karamercan, M. A., Ye, L., Bhatti, T. R., Becker, L. B., Baur, J. A., & Sims, C. A. (2015) · Shock · doi:10.1097/shk.0000000000000390 · Cited by 71 · see citing works
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Wu, D., Jian, C., Peng, Q., Hou, T., Wu, K., Shang, B., Zhao, M., Wang, Y., Zheng, W. L., Ma, Q., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2374-7 · Cited by 68 · see citing works
The mitochondrial unfolded protein response in mammalian physiology
Mottis, A., Jovaisaite, V., & Auwerx, J. H. (2014) · Mammalian Genome · doi:10.1007/s00335-014-9525-z · Cited by 68 · see citing works
Fruit and vegetable consumption, cigarette smoke, and leukocyte mitochondrial DNA copy number
Wu, S., Li, X., Meng, S., Fung, T. T., Chan, A. T., Liang, G., Giovannucci, E. L., Vivo, I. D., Lee, J. H., & Nan, H. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy286 · Cited by 59 · see citing works
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Wang, X., Hart, J. E., Liu, Q., Wu, S., Nan, H., & Laden, F. (2020) · Environment International · doi:10.1016/j.envint.2020.105761 · Cited by 53 · see citing works
Li, L., Martin-Levilain, J., Jiménez‐Sánchez, C., Karaca, M., Foti, M., Martinou, J., & Maechler, P. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007601 · Cited by 48 · see citing works
Self-citationIn Vivo Deletion of β-Cell Drp1 Impairs Insulin Secretion Without Affecting Islet Oxygen Consumption
Hennings, T. G., Gambhir, D., DeLeon, E. R., VanDeusen, H. R., Sesaki, H., Merrins, M. J., & Ku, G. (2018) · Endocrinology · doi:10.1210/en.2018-00445 · Cited by 42 · see citing works
Sun, Y., Yan, C., He, L., Xiang, S., Wang, P., Li, Z., Chen, Y., Zhao, J., Yuan, Y., Wang, W., et al. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101899 · Cited by 40 · see citing works
Moncunill‐Massaguer, C., Saura‐Esteller, J., Pérez‐Perarnau, A., Palmeri, C. M., Núñez‐Vázquez, S., Cosialls, A. M., González‐Gironès, D. M., Pomares, H., Korwitz, A., Preciado, S., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.6154 · Cited by 38 · see citing works
Self-citationLi, L., Krznar, P., Erban, A., Agazzi, A., Martin-Levilain, J., Supale, S., Kopka, J., Zamboni, N., & Maechler, P. (2019) · Diabetes · doi:10.2337/db19-0131 · Cited by 35 · see citing works
Self-citationHahn, C., Tyka, K., Saba, J. D., Lenzen, S., & Gurgul-Convey, E. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.814491 · Cited by 35 · see citing works
Prohibitin overexpression improves myocardial function in diabetic cardiomyopathy
Dong, W., Chao, M., Lu, Q., Chai, W., Zhang, W., Chen, X., Liang, E., Wang, L., Tian, H., Chen, Y., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.6384 · Cited by 33 · see citing works
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Human Rights Here and Now: Celebrating the Universal Declaration of Human Rights.
Flowers, N. B. (1998) · Cited by 31 · see citing works
Georgiadou, E., Muralidharan, C., Irizarry, M. M. M., CHABOSSEAU, P. L., Akalestou, E., Tomás, A., Wern, F. Y. S., Stylianides, T., Wretlind, A., Legido‐Quigley, C., et al. (2022) · Diabetes · doi:10.2337/db21-0800 · Cited by 29 · see citing works
14-3-3ζ Constrains insulin secretion by regulating mitochondrial function in pancreatic β cells
Mugabo, Y., Zhao, C., Tan, J. J., Ghosh, A., Campbell, S. A., Fadzeyeva, E., Paré, F., Pan, S. S., Galipeau, M., Ast, J., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.156378 · Cited by 28 · see citing works
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Mishra, S., & Nyomba, B. L. G. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370217703976 · Cited by 28 · see citing works
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García-Aguilar, A., & Guillén, C. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1052317 · Cited by 26 · see citing works
Iommarini, L., Peralta, S., Torraco, A., & Díaz, F. (2015) · Mitochondrion · doi:10.1016/j.mito.2015.01.008 · Cited by 25 · see citing works
Prevalence of neoplasms in definite and probable mitochondrial disorders
Finsterer, J., & Frank, M. (2016) · Mitochondrion · doi:10.1016/j.mito.2016.05.002 · Cited by 25 · see citing works
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Darwish, R., Alcibahy, Y., Abu-Sharia, G., & Butler, A. E. (2025) · Cells · doi:10.3390/cells14231861 · Cited by 24 · see citing works
Li, T., Jiao, W., Li, W., & Li, H. (2016) · Endocrine Research · doi:10.3109/07435800.2015.1124437 · Cited by 24 · see citing works
Hong, S., Lee, J., Kwon, H., Park, S. E., Rhee, E., Park, C., Oh, K.-W., Park, S.-W., & Lee, W. (2018) · Endocrinology and Metabolism · doi:10.3803/enm.2018.33.3.403 · Cited by 23 · see citing works
Lourenço, A. B., Muñoz-Jiménez, C. M., Venegas‐Calerón, M., & Artal‐Sanz, M. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.06.003 · Cited by 22 · see citing works
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Gao, J., Sherpa, D., Kupko, N., Chino, H., Zeng, J., & Shao, S. (2025) · Nature Communications · doi:10.1038/s41467-025-65078-3 · Cited by 20 · see citing works
Zhang, Y., Wu, J., Jin, W., Shen, M., Yin, S., Lai, X., Ma, H., Jiang, M., Sun, D., & Yan, J. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/9233749 · Cited by 19 · see citing works
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Vetterli, L., Carobbio, S., Frigerio, F., Karaca, M., & Maechler, P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.707448 · Cited by 19 · see citing works
Self-citationSphingolipids in Type 1 Diabetes: Focus on Beta-Cells
Gurgul-Convey, E. (2020) · Cells · doi:10.3390/cells9081835 · Cited by 19 · see citing works
Li, B., Kalinowski, P., Kim, B., Pauls, A. D., & Poburko, D. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107995 · Cited by 19 · see citing works
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Zhang, Y., Ni, Q., Chen, Y., Pei, Z., & Xu, X. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.118499 · Cited by 18 · see citing works
Jiménez‐Sánchez, C., Mezza, T., Sinturel, F., Li, L., Giuseppe, G. D., Quero, G., Jornayvaz, F. R., Guessous, I., Dibner, C., Schrauwen, P., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac444 · Cited by 18 · see citing works
Self-citationMitoribosome insufficiency in β cells is associated with type 2 diabetes-like islet failure
Hong, H. J., Joung, K. H., Kim, Y. K., Choi, M. J., Kang, S., Kim, J. T., Kang, Y. E., Chang, J. Y., Moon, J. H., Jun, S., et al. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00797-x · Cited by 17 · see citing works
Xu, S., Gao, Z., Jiang, L., Li, J., Qin, Y., Zhang, D., Tian, P., Wang, W., Zhang, R., Zhang, R., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-70584-3 · Cited by 16 · see citing works
van Gastel, J., Leysen, H., Santos‐Otte, P., Hendrickx, J. O., Azmi, A., Martin, B., & Maudsley, S. R. (2019) · Aging · doi:10.18632/aging.102528 · Cited by 16 · see citing works
Prohibitin‐1 Is a Dynamically Regulated Blood Protein With Cardioprotective Effects in Sepsis
Mattox, T. A., Psaltis, C. E., Weihbrecht, K., Robidoux, J., Kilburg-Basnyat, B. J., Murphy, M. P., Gowdy, K. M., & Anderson, E. J. (2021) · Journal of the American Heart Association · doi:10.1161/jaha.120.019877 · Cited by 16 · see citing works
The Mitochondrial Prohibitin (PHB) Complex in C. elegans Metabolism and Ageing Regulation
Lourenço, A. B., & Artal‐Sanz, M. (2021) · Metabolites · doi:10.3390/metabo11090636 · Cited by 15 · see citing works
Light-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
Zhao, H., Shi, L., Li, Z., Kong, R., Ren, X., Ma, R., Jia, L., Ma, M., Xu, R., Xu, R., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2111711119 · Cited by 14 · see citing works
Xu, Y. X. Z., Bassi, G., & Mishra, S. (2019) · Biology of Sex Differences · doi:10.1186/s13293-019-0239-5 · Cited by 13 · see citing works
Mitochondrial Proteome Changes in Rett Syndrome
Golubiani, G., van Agen, L., Tsverava, L., Solomonia, R. O., & Müller, M. (2023) · Biology · doi:10.3390/biology12070956 · Cited by 12 · see citing works
Prohibitin Signaling at the Kidney Filtration Barrier
Ising, C., & Brinkkoetter, P. T. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-55330-6_29 · Cited by 11 · see citing works
Shen, Y., Si, Y., Lu, J., Ma, X., Zhang, L., Mo, Y., Lu, W., Zhu, W., Bao, Y., Hu, G., et al. (2020) · Journal of Diabetes Research · doi:10.1155/2020/4243053 · Cited by 10 · see citing works
Skeletal muscle transcriptomics dissects the pathogenesis of Friedreich’s ataxia
Indelicato, E., Kirchmair, A., Amprosi, M., Steixner, S. J. M., Nachbauer, W., Eigentler, A., Wahl, N., Apostolova, G., Krogsdam, A., Schneider, R., et al. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad051 · Cited by 10 · see citing works
Verdejo, H., Parra, V., del Campo, A., Vásquez-Trincado, C., Gatica, D., López‐Crisosto, C., Kuzmicic, J., Venegas-Zamora, L., Zúñiga-Cuevas, Ú., Troncoso, M. F., et al. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02240-w · Cited by 8 · see citing works
The Role of Prohibitin-2 in Diseases
Liu, F., Zhang, Y., Guo, Z., & Ren, A. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2809211 · Cited by 8 · see citing works
Lysophosphatidylinositols Are Upregulated After Human β-Cell Loss and Potentiate Insulin Release
Jiménez‐Sánchez, C., Sinturel, F., Mezza, T., Loizides‐Mangold, U., Montoya, J. P., Li, L., Giuseppe, G. D., Quero, G., Guessous, I., Jornayvaz, F. R., et al. (2023) · Diabetes · doi:10.2337/db23-0205 · Cited by 8 · see citing works
Self-citationWang, D., Zhao, Y.-Q., Han, Y., Hou, C.-C., & Zhu, J. (2017) · Fish Physiology and Biochemistry · doi:10.1007/s10695-017-0373-0 · Cited by 8 · see citing works
Wild, M. R., Hahn, F., Grau, B. W., Herrmann, L., Niesar, A., Schütz, M., Lorion, M. M., Ackermann, L., Tsogoeva, S. B., & Marschall, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155578 · Cited by 8 · see citing works
Sphingosine-1 Phosphate Lyase Regulates Sensitivity of Pancreatic Beta-Cells to Lipotoxicity
Tang, Y., Plötz, T., Gräler, M. H., & Gurgul-Convey, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910893 · Cited by 8 · see citing works
Phb1:Phb2 heterodimers in the mitochondria—beyond functional interdependence
Mishra, S. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.l119.010788 · Cited by 8 · see citing works
Role of Prohibitins as Guardians of mitochondrial homeostasis
Champsi, S., & Hood, D. A. (2025) · Mitochondrion · doi:10.1016/j.mito.2025.102075 · Cited by 7 · see citing works
Carotenoid metabolism in mitochondrial function
Lu, P., Wong, S. Y., Wu, L., & Lin, D. (2020) · Food Quality and Safety · doi:10.1093/fqsafe/fyaa023 · Cited by 7 · see citing works
Huo, Y., Song, Z., Wang, H., Zhang, Z., Xiao, N., Fang, R., Zhang, Y., & Zhang, L. (2022) · Insect Molecular Biology · doi:10.1111/imb.12766 · Cited by 6 · see citing works
Yang, K., Forman, M. R., Monahan, P. O., Graham, B. H., Chan, A. T., Zhang, X., Vivo, I. D., Giovannucci, E. L., Tabung, F. K., & Nan, H. (2020) · Journal of Nutrition · doi:10.1093/jn/nxaa146 · Cited by 6 · see citing works
Ye, X., Zhao, Y., Zhao, L., Sun, Y., Yang, J., & Yang, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109152 · Cited by 5 · see citing works
Yoshida, M., Yokoi, N., Takahashi, H., Hatano, N., Hayami, T., Ogawa, W., & Seino, S. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.03.036 · Cited by 5 · see citing works
Bettahi, I., Krishnankutty, R., Jaganjac, M., Suleiman, N., Ramanjaneya, M., Jerobin, J., Hassoun, S., Alkasem, M., Abdelhakam, I., Iskandarani, A., et al. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1024832 · Cited by 5 · see citing works
Li, S., Sun, J., Li, Y., Lv, X., Wang, L., & Song, L. (2024) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2024.105168 · Cited by 4 · see citing works
Kasperová, B. J., Cinkajzlová, A., Horváth, L., Svoboda, P., Haluzı́k, M., & Hubáčková, S. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1622107 · Cited by 4 · see citing works
He, L., Zhou, H., Liu, H., & Qu, H. (2017) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmx058 · Cited by 4 · see citing works
Fan, Y., Pang, P., Yang, K., Niu, X., Cheng, F., & Li, W. (2025) · Redox Biology · doi:10.1016/j.redox.2025.103991 · Cited by 3 · see citing works
Doucet, R., El-Seoudi, A., Rostami-Afshari, B., Elbakry, M., Taheri, M., Pellicelli, M., Picard, C., Lavoie, J.-F., Wang, D. S., Lavigne, P., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136281 · Cited by 2 · see citing works
A Putative Prohibitin-Calcium Nexus in β-Cell Mitochondria and Diabetes
Verma, G., Dixit, A., & Nunemaker, C. S. (2020) · Journal of Diabetes Research · doi:10.1155/2020/7814628 · Cited by 2 · see citing works
Herzig, S., Li, L., Jiménez‐Sánchez, C., Martinou, J., & Maechler, P. (2023) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2023.130492 · Cited by 2 · see citing works
Self-citationNa, B.-R., Lee, Y. E., Kang, M.-G., Won, Y., Kim, H. R., & Shin, M. (2020) · Laboratory Medicine Online · doi:10.3343/lmo.2020.10.3.214
The prohibitin complex in aging and neurodegeneration
González-Morales, A., Lachén‐Montes, M., Ausín, K., Cartas‐Cejudo, P., Mendizuri, N., Fernández‐Irigoyen, J., & Santamaría, E. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817990-1.00011-1
Prohibitin modulates periodontium differentiation in mice development
Aryal, Y. P., Han, S.-Y., Rana, B., Neupane, S., Kim, T., Pokharel, E., Ha, J., Jung, J., An, C.-H., Kim, J., et al. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1369634
Vogt, J. F., Merkwirth, C., Adams‐Quack, P., Zurkowski, E., Stylianakis, E., Uhlfelder, D. C., Michna, T., Nurbekova, A., Distler, U., Rojas-Charry, L., et al. (2026) · Communications Biology · doi:10.1038/s42003-026-10522-3
Self-citationZuo, Z., Liang, R., Fan, S., Shan, H., Zhang, H., Wang, X., & Teng, F. (2025) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2025.152093
Zhou, Y., Baez, N., Fu, T., Brun, T., & Maechler, P. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110661
Self-citationChalder, L., Elremaly, W., Li, D., Fang, Y., Caraus, I., Leveau, C., Elbakry, M., Franco, A., Godbout, C., Tomasso, G. D., et al. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-026-08162-6
Rivera, G. O., & Theiss, A. L. (2026) · Microbial Cell · doi:10.15698/mic2026.06.878
Bhatia, Y., & Mishra, S. (2026) · Mitochondrion · doi:10.1016/j.mito.2026.102231
- Authors
- Supale, S., Thorel, F., Merkwirth, C., Gjinovci, A., Herrera, P. L., Scorrano, L., Meda, P., Langer, T., & Maechler, P.
- Affiliations
- University of Geneva (CH)
- University of Cologne (DE)
- Corresponding author
- Maechler, Pierre
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2013-09-17
- Volume
- 62
- Issue
- 10
- Pages
- 3488-3499
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC3781460
- OpenAlex
- W2146424231
- Cited by
- 94
- References
- 39
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 3 · 2023: 9 · 2022: 11 · 2021: 8 · 2020: 9 · 2019: 7 · 2018: 4 · 2017: 6 · 2016: 7 · 2015: 9 · 2014: 6 · 2013: 1
- FWCI
- 7.50
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Diabetes (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030, 135704)
- National Institute of Diabetes and Digestive and Kidney Diseases (U01DK089572, P30DK020593)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
- Keywords
- prohibitin, PHB2, pancreatic beta cells, mitochondrial dysfunction, beta-cell apoptosis, beta-cell proliferation, insulin secretion, type 2 diabetes, mitochondrial DNA copy number, respiratory chain complex IV, mitochondrial fragmentation, glucose homeostasis, islets
- MeSH terms
- Insulin Secretion, Prohibitins, Animals, Blood Glucose, Cell Survival, Diabetes Mellitus, Type 2, DNA, Mitochondrial, Female, Humans, Insulin, Male, Mitochondria, Repressor Proteins, Apoptosis, Gene Deletion, Mice, Knockout, Disease Progression, GTP Phosphohydrolases, Cell Proliferation, Insulin-Secreting Cells, Mice
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