Reductive stress in mitochondria isolated from the carotid body of type 1 diabetic male Wistar rats.
carotid body
glutathione
mitochondria
reductive stress
streptozotocin‐induced diabetes
Journal
Physiological reports
ISSN: 2051-817X
Titre abrégé: Physiol Rep
Pays: United States
ID NLM: 101607800
Informations de publication
Date de publication:
Sep 2024
Sep 2024
Historique:
revised:
12
08
2024
received:
07
03
2024
accepted:
12
08
2024
medline:
19
9
2024
pubmed:
19
9
2024
entrez:
18
9
2024
Statut:
ppublish
Résumé
The carotid body (CB) senses changes in arterial O
Substances chimiques
Glutathione
GAN16C9B8O
Reactive Oxygen Species
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e70016Subventions
Organisme : Program for Teaching Professional Development
ID : DSA/103.5 /15/10869
Informations de copyright
© 2024 The Author(s). Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.
Références
Akerboom, T. P., & Sies, H. (1981). Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods in Enzymology, 77, 373–382. https://doi.org/10.1016/s0076‐6879(81)77050‐2
Alvarez‐Buylla, R., & de Alvarez‐Buylla, E. R. (1988). Carotid sinus receptors participate in glucose homeostasis. Respiration Physiology, 72, 347–359. https://doi.org/10.1016/0034‐5687(88)90093‐x
Alvarez‐Buylla, R., & Roces de Alvarez‐Buylla, E. (1994). Changes in blood glucose concentration in the carotid body‐sinus modify brain glucose retention. Brain Research, 654, 167–170. https://doi.org/10.1016/0006‐8993(94)91585‐7
Aquilano, K., Baldelli, S., & Ciriolo, M. R. (2014). Glutathione: New roles in redox signaling for an old antioxidant. Frontiers in Pharmacology, 5, 1–12. https://doi.org/10.3389/fphar.2014.00196
Chiao, Y. A., Chakraborty, A. D., Light, C. M., Tian, R., Sadoshima, J., Shi, X., Gu, H., & Lee, C. F. (2021). NAD+ redox imbalance in the heart exacerbates diabetic cardiomyopathy. Circulation. Heart Failure, 14, e008170. https://doi.org/10.1161/CIRCHEARTFAILURE.120.008170
De Castro, F. (1926). Sur la structure et l'innervation de la glande intercarotidienne (glomuscaroticum) de l'homme et des mammifères, et sur un nouveausystèmed'innervationautonome du nerfglosopharyngien. Travail Laboratoire Recherche Biologique, 24, 365–432.
Diaz Vivancos, P., Wolff, T., Markovic, J., Pallardo, F. V., & Foyer, C. H. (2010). A nuclear glutathione cycle within the cell cycle. The Biochemical Journal, 431, 169–178. https://doi.org/10.1042/BJ20100409
Eyzaguirre, C., & Zapata, P. (1984). Perspectives in carotid body research. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology, 57, 931–957. https://doi.org/10.1152/jappl.1984.57.4.931
Forman, H. J., Zhang, H., & Rinna, A. (2009). Glutathione: Overview of its protective roles, measurement, and biosynthesis. Molecular Aspects of Medicine, 30, 1–12. https://doi.org/10.1016/j.mam.2008.08.006
Gao, L., Ortega‐Saenz, P., Garcia‐Fernandez, M., Gonzalez‐Rodriguez, P., Caballero‐Eraso, C., & Lopez‐Barneo, J. (2014). Glucose sensing by carotid body glomus cells: Potential implications in disease. Frontiers in Physiology, 398, 1–9. https://doi.org/10.3389/fphys.2014.00398
Garcia‐Ruiz, C., Colell, A., Morales, A., Kaplowitz, N., & Fernandez‐Checa, J. C. (1995). Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor kappa‐b: Studies with isolated mitochondria and rat hepatocytes. Molecular Pharmacology, 48, 825–834.
Ghafourifar, P., & Saavedra‐Molina, A. (2005). Functions of mitochondrial nitric oxide synthase. In S. Lamas & E. Cadenas (Eds.), Nitric oxide, cell signaling, and gene expression. 1st (pp. 77–98). Taylor & Francis.
Giustarini, D., Tsikas, D., Colombo, G., Milzani, A., Dalle‐Donne, I., Fanti, P., & Rossi, R. (2016). Pitfalls in the analysis of the physiological antioxidant glutathione (GSH) and its disulfide (GSSG) in biological samples: An elephant in the room. Journal of Chromatography. B: Analytical Technologies in the Biomedical and Life Sciences, 1019, 21–28. https://doi.org/10.1016/j.jchromb.2016.02.015
Gores, G. J., Flarsheim, C. E., Dawson, T. L., Nieminen, A. L., Herman, B., & Lemasters, J. J. (1989). Swelling, reductive stress, and cell death during chemical hypoxia in hepatocytes. The American Journal of Physiology, 257, C347–C354. https://doi.org/10.1152/ajpcell.1989.257.2.C347
Guarner, V., & Alvarez‐Buylla, R. (1991). Changes in brain glucose retention produced by the stimulation of an insulin‐sensitive reflexogenic zone in rats. Journal of the Autonomic Nervous System, 34, 89–94. https://doi.org/10.1016/0165‐1838(91)90011‐q
Hernandez‐Leal, A., Tejeda‐Chavez, H. R., Montero, S., Lemus, M., Castro, E., Ramirez‐Flores, M., & Roces de Alvarez‐Buylla, E. (2018). Expression of neuronal NO synthase and the hyperglycemic reflex to anoxic stimulation of the carotid body in normoglycemic and hyperglycemic rats. Neurophysiology, 50, 93–98. https://doi.org/10.1007/s11062‐018‐9722‐6
Joyner, M. J., Limberg, J. K., Wehrwein, E. A., & Johnson, B. D. (2018). Role of the carotid body chemoreceptors in glucose homeostasis and thermoregulation in humans. The Journal of Physiology, 596, 3079–3085. https://doi.org/10.1113/jp274354
Koyama, Y., Coker, R. H., Stone, E. E., Lacy, D. B., Jabbour, K., Williams, P. E., & Wasserman, D. H. (2000). Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes, 49, 1434–1442. https://doi.org/10.2337/diabetes.49.9.1434
Kumar, P., & Prabhakar, N. R. (2012). Peripheral chemoreceptors: Function and plasticity of the carotid body. Comprehensive Physiology, 2, 141–219. https://doi.org/10.1002/cphy.c100069
Likidlilid, A., Patchanans, N., Poldee, S., & Peerapatdit, T. (2007). Glutathione and glutathione peroxidase in type 1 diabetic patients. Journal of the Medical Association of Thailand, 90, 1759–1767.
Lopez‐Barneo, J., Ortega‐Saenz, P., Pardal, R., Pascual, A., Piruat, J. I., Duran, R., & Gomez‐Diaz, R. (2009). Oxygen sensing in the carotid body. Annals of the New York Academy of Sciences, 1177, 119–131. https://doi.org/10.1111/j.1749‐6632.2009.05033.x
Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry, 193, 265–275.
Luc, K., Schramm‐Luc, A., Guzik, T. J., & Mikolajczyk, T. P. (2019). Oxidative stress and inflammatory markers in prediabetes and diabetes. Journal of Physiology and Pharmacology, 70, 809–824.
Lushchak, V. I. (2012). Glutathione homeostasis and functions: Potential targets for medical interventions. Journal of Amino Acids, 2012, 736–837. https://doi.org/10.1155/2012/736837
Ma, W. X., Li, C. Y., Tao, R., Wang, X. P., & Yan, L. J. (2020). Reductive stress‐induced mitochondrial dysfunction and cardiomyopathy. Oxidative Medicine and Cellular Longevity, 2020, 5136957. https://doi.org/10.1155/2020/5136957
Mari, M., Morales, A., Colell, A., Garcia‐Ruiz, C., & Fernandez‐Checa, J. (2009). Mitochondrial glutathione, a key survival antioxidant. Antioxidants & Redox Signaling, 11, 2685–2700. https://doi.org/10.1089/ARS.2009.2695
McDonald, D. M., & Blewett, R. W. (1981). Location and size of carotid body‐like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye. Journal of Neurocytology, 10, 607–643.
Moree, S. S., Kavishankar, G. B., & Rajesha, J. (2013). Antidiabetic effect of secoisolariciresinol diglucoside in streptozotocin‐induced diabetic rats. Phytomedicine, 20, 237–245. https://doi.org/10.1016/j.phymed.2012.11.011
Ortiz‐Avila, O., Esquivel‐Martinez, M., Olmos‐Orizaba, B. E., Saavedra‐Molina, A., Rodriguez‐Orozco, A. R., & Cortes‐Rojo, C. (2015). Avocado oil improves mitochondrial function and decreases oxidative stress in brain of diabetic rats. Journal Diabetes Research, 2015, 1–9. https://doi.org/10.1155/2015/485759
Pardal, R., & Lopez‐Barneo, J. (2002). Low glucose–sensing cells in the carotid body. Nature Neuroscience, 5, 197–198. https://doi.org/10.1038/nn812
Perez‐Gallardo, R. V., Noriega‐Cisneros, R., Esquivel‐Gutierrez, E., Calderon‐Cortes, E., Cortes‐Rojo, C., Manzo‐Avalos, S., Campos‐Garcia, J., Salgado‐Garciglia, R., Montoya‐Perez, R., Boldogh, I., & Saavedra‐Molina, A. (2014). Effects of diabetes on oxidative and nitrosative stress in kidney mitochondria from aged rats. Journal of Bioenergetics and Biomembranes, 46, 511–518. https://doi.org/10.1007/s10863‐014‐9594‐4
Peris, E., Micallef, P., Paul, A., Palsdottir, V., Enejder, A., Bauza‐Thorbrugge, M., Olofson, C. S., & Asterholm, I. W. (2019). Antioxidant treatment induces reductive stress associated with mitochondrial dysfunction in adipocytes. The Journal of Biological Chemistry, 294, 2340–2352. https://doi.org/10.1074/jbc.RA118.004253
Poret, J. M., Gaudet, D. A., Braymer, H. D., & Primeaux, S. D. (2021). Sex differences in markers of metabolic syndrome and adipose tissue inflammation in obesity‐prone, Osborne‐Mendel and obesity‐resistant, S5B/Pl rats. Life Sciences, 273, 119–290. https://doi.org/10.1016/j.lfs.2021.119290
Powers, A. C., Niswender, K. D., & Evans‐Molina, C. (2022). Diabetes mellitus: Diagnosis, classification, and pathophysiology. In J. Loscalzo, A. Fauci, D. Kasper, et al. (Eds.), Harrison's principles of internal medicine. 21st (pp. 3094–3102). McGraw‐Hill.
Saavedra‐Molina, A., & Devlin, T. M. (1997). Effect of extra‐ and intra‐mitochondrial calcium on citrulline synthesis. Amino Acids, 12, 293–298.
Sanchez‐Duarte, S., Marquez‐Gamino, S., Montoya‐Perez, R., Villicana‐Gomez, E. A., Vera‐Delgado, K. S., Caudillo‐Cisneros, C., Sotelo‐Barroso, F., Melchor‐Moreno, M. T., & Sanchez‐Duarte, E. (2021). Nicorandil decreases oxidative stress in slow‐ and fast‐twitch muscle fibers of diabetic rats by improving the glutathione system functioning. Journal of Diabetes Investigation, 12, 1152–1161. https://doi.org/10.1111/jdi.13513
Sanz‐Alfayate, G., Obeso, A., Agapito, M. T., & Gonzalez, C. (2001). Reduced to oxidized glutathione ratios and oxygen sensing in calf and rabbit carotid body chemoreceptor cells. The Journal of Physiology, 537, 209–220. https://doi.org/10.1111/j.1469‐7793.2001.0209k.x
Sims, N. R. (1990). Rapid isolation of metabolically active mitochondria from rat brain and sub‐regions using percoll density gradient centrifugation. Journal of Neurochemistry, 55, 698–707. https://doi.org/10.1111/j.1471‐4159.1990.tb04189.x
Singh, F., Charles, A. L., Schlagowski, A. I., Bouitbir, J., Bonifacio, A., Piquard, F., Krahenbuhl, S., Geny, B., & Zoll, J. (2015). Reductive stress impairs myoblasts mitochondrial function and triggers mitochondrial hormesis. Biochimica et Biophysica Acta, 1853, 1574–1585. https://doi.org/10.1016/j.bbamcr.2015.03.006
Skyler, J. S., Bakris, G. L., Bonifacio, E., Darsow, T., Eckel, R. H., Groop, L., Groop, P. H., Handelsman, Y., Insel, R. A., Mathieu, C., McElvaine, A. T., Palmer, J. P., Pugliese, A., Schatz, D. A., Sosenko, J. M., Wilding, J. P. H., & Ratner, R. E. (2017). Differentiation of diabetes by pathophysiology, natural history, and prognosis. Diabetes, 66, 241–255. https://doi.org/10.2337/db16‐0806
Szkudelski, T. (2001). The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiological Research, 50, 537–546.
Tejeda‐Chavez, H. R., Montero, S. A., Lemus, M., Leal, C. A., Portilla‐de Buen, E., Hernandez, A. G., & Roces de Alvarez‐Buylla, E. (2010). Concomitant effects of nitric oxide and carotid chemoreceptor stimulation on brain glucose in normoglycemic and hyperglycemic rats. Archives of Medical Research, 41, 487–496. https://doi.org/10.1016/j.arcmed.2010.09.008
Wall, S. B., Smith, M. R., Ricart, K., Zhou, F., Vayalil, P. K., Oh, J. Y., & Landar, A. (2014). Detection of electrophile‐sensitive proteins. Biochimica et Biophysica Acta, 1840, 913–922. https://doi.org/10.1016/j.bbagen.2013.09.003
Waynfort, H. B., & Flecknell, P. A. (Eds.). (1995). Experimental and surgical technique in the rat. Academic Press.
Wendel, A. (1987). Measurement of in vivo lipid peroxidation and toxicological significance. Free Radical Biology & Medicine, 3, 355–358. https://doi.org/10.1016/s0891‐5849(87)80047‐3
Wu, J., Jin, Z., & Yan, L. J. (2017). Redox imbalance and mitochondrial abnormalities in the diabetic lung. Redox Biology, 11, 51–59. https://doi.org/10.1016/j.redox.2016.11.003
Xiao, W., & Loscalzo, J. (2020). Metabolic responses to reductive stress. Antioxidants & Redox Signaling, 32, 1330–1347. https://doi.org/10.1089/ars.2019.7803
Yu, Q., Lee, C. F., Lee, C. F., Wang, W., Karamanlidis, G., Kuroda, J., Matsushima, S., Sadoshima, J., & Tian, R. (2014). Elimination of NADPH oxidase activity promotes reductive stress and sensitizes the heart to ischemic injury. Journal of the American Heart Association, 3, 1–16. https://doi.org/10.1161/JAHA.113.000555
Zhang, H., Limphong, P., Pieper, J., Liu, Q., Rodesch, C. K., Christians, E., & Benjamin, I. J. (2012). Glutathione‐dependent reductive stress triggers mitochondrial oxidation and cytotoxicity. The FASEB Journal, 26, 1442–1451. https://doi.org/10.1096/fj.11‐199869
Zhang, P., Li, S., Guo, Z., & Lu, S. (2019). Nitric oxide regulates glutathione synthesis and cold tolerance in forage legumes. Environmental and Experimental Botany, 167, 1–8. https://doi.org/10.1016/j.envexpbot.2019.103851