2023, Number 1
Role of hydrogen peroxide (H2O2) as a redox signaling molecule and in the diabetes mellitus-related oxidative stress
Language: Spanish
References: 114
Page: 1-14
PDF size: 444.43 Kb.
ABSTRACT
Cellular metabolism is a constant source of reactive oxygen species (ROS). The production of hydrogen peroxide (H2O2) is particularly relevant, due to its role in cellular physiology. H2O2 can act as a classical intracellular signaling molecule in several processes like cell proliferation, hormone synthesis and secretion, immune cell regulation, angiogenesis, and apoptosis. However, H2O2 overproduction and accumulation, derived from increased mitochondrial electron transport chain activity, glucose autoxidation, and increased polyol flux, contribute to an imbalance in the redox state of the cells. High concentration of H2O2 induces cellular dysfunction through oxidation of macromolecules like proteins, lipids, carbohydrates and nucleic acids. H2O2-induced oxidative damage can contribute to the development and progression of degenerative diseases such as diabetes mellitus. Indeed, chronic hyperglycemia has been shown to cause an increased H2O2 concentration and oxidative damage that contribute to the pathogenesis and progression of diabetes complications.REFERENCES
Adeshara, K. A., Bangar, N., Diwan, A. G. & Tupe, R. S.(2022). Plasma glycation adducts and various RAGEisoforms are intricately associated with oxidative stressand inflammatory markers in type 2 diabetes patients withvascular complications. Diabetes & Metabolic Syndrome:Clinical Research & Reviews, 16(3), 102441. DOI:10.1016/j.dsx.2022.102441
Bae, Y. S., Kang, S. W., Seo, M. S., Baines, I. C., Tekle, E.,Chock, P. B. & Rhee, S. G. (1997). Epidermal growth factor(EGF)-induced generation of hydrogen peroxide. Role inEGF receptor-mediated tyrosine phosphorylation. TheJournal of Biological Chemistry, 272(1), 217–221. DOI:10.1074/jbc.272.1.217.
Basuroy, S., Tcheranova, D., Bhattacharya, S., Leffler, C. W.& Parfenova, H. (2011). Nox4 NADPH oxidase-derivedreactive oxygen species, via endogenous carbon monoxide,promote survival of brain endothelial cells during TNF-α-induced apoptosis. American Journal of Physiology.Cell Physiology, 300(2), C256-265. DOI: 10.1152/ajpcell.00272.2010.
Cai, W., Torreggiani, M., Zhu, L., Chen, X., He, J. C., Striker,G. E. & Vlassara, H. (2010). AGER1 regulates endothelialcell NADPH oxidase-dependent oxidant stress via PKCdelta:implications for vascular disease. American Journalof Physiology Cell Physiology, 298(3), C624-634. DOI:10.1152/ajpcell.00463.2009.
Caldini, R., Chevanne, M., Mocali, A., Tombaccini, D. & Paoletti,F. (1998). Premature induction of aging in sublethallyH2O2-treated young MRC5 fibroblasts correlates withincreased glutathione peroxidase levels and resistance toDNA breakage. Mechanisms of Ageing and Development,105(1–2), 137–150. DOI: 10.1016/s0047-6374(98)00085-2.
de Piña, M. Z., Vázquez-Meza, H., Pardo, J. P., Rendón, J. L.,Villalobos-Molina, R., Riveros-Rosas, H. & Piña, E. (2008).Signaling the signal, cyclic AMP-dependent protein kinaseinhibition by insulin-formed H2O2 and reactivation bythioredoxin. The Journal of Biological Chemistry, 283(18),12373–12386. DOI: 10.1074/jbc.M706832200.
Diamond-Stanic, M. K., Marchionne, E. M., Teachey, M.K., Durazo, D. E., Kim, J. S. & Henriksen, E. J. (2011).Critical role of the transient activation of p38 MAPK inthe etiology of skeletal muscle insulin resistance inducedby low-level in vitro oxidant stress. Biochemical andBiophysical Research Communications, 405(3), 439–444.DOI: 10.1016/j.bbrc.2011.01.049
Dokken, B. B., Saengsirisuwan, V., Kim, J. S., Teachey, M. K.& Henriksen, E. J. (2008). Oxidative stress-induced insulinresistance in rat skeletal muscle: role of glycogen synthasekinase-3. American Journal of Physiology-Endocrinologyand Metabolism, 294(3), E615–E621. DOI: 10.1152/ajpendo.00578.2007.
Gianturco, V., Bellomo, A., D’Ottavio, E., Formosa, V., Iori,A., Mancinella, M., Troisi, G. & Marigliano, V. (2009).Impact of therapy with α-lipoic acid (ALA) on theoxidative stress in the controlled niddm: a possiblepreventive way against the organ dysfunction? Archives ofGerontology and Geriatrics, 49, 129–133. DOI: 10.1016/j.archger.2009.09.022.
Giorgio, M., Migliaccio, E., Orsini, F., Paolucci, D., Moroni, M.,Contursi, C., Pelliccia, G., Luzi, L., Minucci, S., Marcaccio,M., Pinton, P., Rizzuto, R., Bernardi, P., Paolucci, F. &Pelicci, P. G. (2005). Electron transfer between cytochromec and p66Shc generates reactive oxygen species that triggermitochondrial apoptosis. Cell, 122(2), 221–233. DOI:10.1016/j.cell.2005.05.011.
Gross, E., Sevier, C. S., Heldman, N., Vitu, E., Bentzur, M.,Kaiser, C. A., Thorpe, C. & Fass, D. (2006). Generatingdisulfides enzymatically: reaction products and electronacceptors of the endoplasmic reticulum thiol oxidase Ero1p.Proceedings of the National Academy of Sciences of theUnited States of America, 103(2), 299–304. DOI: 10.1073/pnas.0506448103.
Inoguchi, T., Li, P., Umeda, F., Yu, H. Y., Kakimoto, M.,Imamura, M., Aoki, T., Etoh, T., Hashimoto, T., Naruse, M.,Sano, H., Utsumi, H. & Nawata, H. (2000). High glucoselevel and free fatty acid stimulate reactive oxygen speciesproduction through protein kinase C-dependent activationof NAD(P)H oxidase in cultured vascular cells. Diabetes,49(11), 1939–1945. DOI: 10.2337/diabetes.49.11.1939.
Juarez, J. C., Manuia, M., Burnett, M. E., Betancourt, O., Boivin,B., Shaw, D. E., Tonks, N. K. Mazar, A. P. & Doñate, F.(2008). Superoxide dismutase 1 (SOD1) is essential forH2O2-mediated oxidation and inactivation of phosphatasesin growth factor signaling. Proceedings of the NationalAcademy of Sciences of the United States of America,105(20), 7147–7152. DOI: 10.1073/pnas.0709451105.
Jung, S.-N., Yang, W. K., Kim, J., Kim, H. S., Kim, E. J., Yun,H., Park, H., Soo, K., Choe, W., Kang, I. & Ha, J. (2008).Reactive oxygen species stabilize hypoxia-induciblefactor-1 alpha protein and stimulate transcriptionalactivity via AMP-activated protein kinase in DU145 humanprostate cancer cells. Carcinogenesis, 29(4), 713–721. DOI:10.1093/carcin/bgn032.
Lacy, M. E., Moran, C., Gilsanz, P., Beeri, M. S., Karter, A. J. &Whitmer, R. A. (2022). Comparison of cognitive functionin older adults with type 1 diabetes, type 2 diabetes, and nodiabetes: results from the Study of Longevity in Diabetes(SOLID). BMJ Open Diabetes Research and Care, 10(2),e002557. DOI: 10.1136/bmjdrc-2021-002557.
Manczak, M., Mao, P., Calkins, M. J., Cornea, A., Reddy,A. P., Murphy, M. P., Szeto, H. H., Park, B. & Reddy, P.H. (2010). Mitochondria-targeted antioxidants protectagainst amyloid-beta toxicity in Alzheimer’s diseaseneurons. Journal of Alzheimer’s Disease: JAD, 20 Suppl2(Suppl 2), S609-3. DOI: 10.3233/JAD-2010-100564.
Meira, L. B., Bugni, J. M., Green, S. L., Lee, C.W., Pang, B.,Borenshtein, D., Rickman, B. H., Rogers, A. B., Moroski-Erkul, C. A., McFaline, J. L., Schauer, D. B., Dedon, P. C.,Fox, J. G. & Samson, L. D. (2008). DNA damage inducedby chronic inflammation contributes to colon carcinogenesisin mice. The Journal of Clinical Investigation, 118(7),2516–2525. DOI:10.1172/JCI35073.
Milman, U., Blum, S., Shapira, C., Aronson, D., Miller-Lotan, R.,Anbinder, Y., Alshiek, J., Bennett, L., Kostenko, M., Landau,M., Keidar, S., Levy. Y., Khemlin, A., Radan, A. & Levy, A. P.(2008). Vitamin E supplementation reduces cardiovascularevents in a subgroup of middle-aged individuals with bothtype 2 diabetes mellitus and the haptoglobin 2-2 genotype:a prospective double-blinded clinical trial. Arteriosclerosis,Thrombosis, and Vascular Biology, 28(2), 341–347. DOI:10.1161/ATVBAHA.107.153965.
Mishin, V., Heck, D. E., Laskin, D. L. & Laskin, J. D.(2014). Human recombinant cytochrome P450 enzymesdisplay distinct hydrogen peroxide generating activitiesduring substrate independent NADPH oxidase reactions.Toxicological Sciences: An Official Journal of the Society ofToxicology, 141(2), 344–352. DOI: 10.1093/toxsci/kfu133.
Neri, S., Signorelli, S. S., Torrisi, B., Pulvirenti, D., Mauceri,B., Abate, G., Ignaccolo, L., Bordonaro, F., Cilio, D.,Calvagno, S. & Leotta, C. (2005). Effects of antioxidantsupplementation on postprandial oxidative stressand endothelial dysfunction: a single-blind, 15-day clinicaltrial in patients with untreated type 2 diabetes, subjectswith impaired glucose tolerance, and healthy controls.Clinical Therapeutics, 27(11), 1764–1773. DOI: 10.1016/j.clinthera.2005.11.006.
Palma, F. R., He, C., Danes, J. M., Paviani, V., Coelho, D. R.,Gantner, B. N. & Bonini, M. G. (2020). MitochondrialSuperoxide Dismutase: What the Established, the Intriguing,and the Novel Reveal About a Key Cellular Redox Switch.Antioxidants & Redox Signaling, 32(10), 701–714. DOI:10.1089/ars.2019.7962.
Peskin, A. V, Dickerhof, N., Poynton, R. A., Paton, L. N.,Pace, P. E., Hampton, M. B. & Winterbourn, C. C. (2013).Hyperoxidation of peroxiredoxins 2 and 3: rate constantsfor the reactions of the sulfenic acid of the peroxidaticcysteine. The Journal of Biological Chemistry, 288(20),14170–14177. DOI: 10.1074/jbc.M113.460881
Pirinen, E., Cantó, C., Jo, Y. S., Morato, L., Zhang, H., Menzies,K. J., Williams, E. G., Mouchiroud, L., Moullan, N.,Hagberg, C., Li, W., Timmers, S., Imhor, R., Verbeek,J., Pujol, A., van Loon, B., Viscomi, C., Zeviani, M.,Schrauwen, P., Sauve, A., Schoonjans, K. & Auwerx, J.(2014). Pharmacological Inhibition of poly (ADP-ribose)polymerases improves fitness and mitochondrial functionin skeletal muscle. Cell Metabolism, 19(6), 1034–1041.DOI: 10.1016/j.cmet.2014.04.002.
Ramana, K. V, Friedrich, B., Tammali, R., West, M. B.,Bhatnagar, A. & Srivastava, S. K. (2005). Requirement ofaldose reductase for the hyperglycemic activation of proteinkinase C and formation of diacylglycerol in vascular smoothmuscle cells. Diabetes, 54(3), 818–829. DOI: 10.2337/diabetes.54.3.818.
Santos, F. R., Diamond-Stanic, M. K., Prasannarong, M.& Henriksen, E. J. (2012). Contribution of the serinekinase c-Jun N-terminal kinase (JNK) to oxidant-inducedinsulin resistance in isolated rat skeletal muscle. Archivesof Physiology and Biochemistry, 118(5), 231–236. DOI:10.3109/13813455.2012.713366.
Sarwar, N., Gao, P., Seshasai, S. R. K., Gobin, R., Kaptoge,S., Di Angelantonio, E., Ingelsson, E., Lawlor, D. A.,Selvin, E., Stampfer, M., Stehouwer, C. D., Lewington,S., Pennells, L., Thompson, A., Sattar, N., White, I. R.,Ray, K. K. & Danesh, J. (2010). Diabetes mellitus, fastingblood glucose concentration, and risk of vascular disease:a collaborative meta-analysis of 102 prospective studies.Lancet (London, England), 375(9733), 2215–2222. DOI:10.1016/S0140-6736(10)60484-9.
Schoonbroodt, S., Ferreira, V., Best-Belpomme, M., Boelaert,J. R., Legrand-Poels, S., Korner, M. & Piette, J. (2000).Crucial role of the amino-terminal tyrosine residue 42 andthe carboxyl-terminal PEST domain of I kappa B alpha inNF-kappa B activation by an oxidative stress. Journal ofImmunology (Baltimore, Md.: 1950), 164(8), 4292–4300.DOI: 10.4049/jimmunol.164.8.4292.
Sharifi-Rad, M., Anil Kumar, N. V, Zucca, P., Varoni, E. M., Dini,L., Panzarini, E., Rajkovic, J., Tsouh Fokou, P. V., Azzini,E., Peluso, I., Mishra, A. P., Nigam, M., El Rayess, Y., ElBeyrouthy, M., Polito, L., Iriti, M., Martins, N., Martonell,M., Docea, A. O., Setzer, W. N., Calina, D., Cho, W. C.& Sharifi-Rad, J. (2020). Lifestyle, Oxidative Stress, andAntioxidants: Back and Forth in the Pathophysiology ofChronic Diseases. Frontiers in Physiology, 11, 694. DOI:10.3389/fphys.2020.00694.
Silva-Rodrigues, T., de-Souza-Ferreira, E., Machado, C. M.,Cabral-Braga, B., Rodrigues-Ferreira, C. & Galina, A.(2020). Hyperglycemia in a type 1 Diabetes Mellitusmodel causes a shift in mitochondria coupled-glucosephosphorylation and redox metabolism in rat brain. FreeRadical Biology and Medicine, 160, 796–806. DOI:10.1016/j.freeradbiomed.2020.09.017.
Storozhevykh, T. P., Senilova, Y. E., Persiyantseva, N. A., Pinelis,V. G. & Pomytkin, I. A. (2007). Mitochondrial respiratorychain is involved in insulin-stimulated hydrogen peroxideproduction and plays an integral role in insulin receptorautophosphorylation in neurons. BMC Neuroscience, 8,84. DOI: 10.1186/1471-2202-8-84.
Teo, Z. L., Tham, Y.-C., Yu, M., Chee, M. L., Rim, T. H.,Cheung, N., Bikbov, M. M., Wang, Y. X., Tang, Y., Lu,Y., Wong, I. Y., Ting, DSW., Tan, G. S.W., Jonas. J, B.,Sabanayagam, C., Wong, T. Y. & Cheng, C.-Y. (2021).Global Prevalence of Diabetic Retinopathy and Projectionof Burden through 2045: Systematic Review and Metaanalysis.Ophthalmology, 128(11), 1580–1591. DOI:10.1016/j.ophtha.2021.04.027.
Trinei, M., Giorgio, M., Cicalese, A., Barozzi, S., Ventura,A., Migliaccio, E., Milia, E., Padura, I. M., Raker, V. A.,Maccarana, M., Petronilli, V., Minucci, S., Bernardi, P.,Lanfrancone, L. & Pelicci, P. G. (2002). A p53-p66Shcsignalling pathway controls intracellular redox status, levelsof oxidation-damaged DNA and oxidative stress-inducedapoptosis. Oncogene, 21(24), 3872–3878. DOI: 10.1038/sj.onc.1205513.
Tyurin-Kuzmin, P. A., Zhdanovskaya, N. D., Sukhova, A. A.,Sagaradze, G. D., Albert, E. A., Ageeva, L. V, Sharonov,G. V., Vorotnikov, A.V. & Tkachuk, V. A. (2016). Nox4and Duox1/2 Mediate Redox Activation of MesenchymalCell Migration by PDGF. PloS One, 11(4), e0154157. DOI:10.1371/journal.pone.0154157.
Yamakawa, H., Ito, Y., Naganawa, T., Banno, Y., Nakashima,S., Yoshimura, S., Sawada, M., Nishimura, Y., Nozawa,Y. & Sakai, N. (2000). Activation of caspase-9 and -3during H2O2-induced apoptosis of PC12 cells independentof ceramide formation. Neurological Research, 22(6),556–564. DOI: 10.1080/01616412.2000.11740718.
Yoshino, G., Tanaka, M., Nakano, S., Matsumoto, T., Kojima, M.,Murakami, E. & Morita, T. (2009). Effect of rosuvastatin onconcentrations of plasma lipids, urine and plasma oxidativestress markers, and plasma high-sensitivity C-reactiveprotein in hypercholesterolemic patients with and withouttype 2 diabetes mellitus: A 12-week, open-label, pilot study.Current Therapeutic Research, Clinical and Experimental,70(6), 439–448. DOI: 10.1016/j.curtheres.2009.12.003.
Zang, L. Y. & Misra, H. P. (1992). EPR kinetic studies ofsuperoxide radicals generated during the autoxidationof1-methyl-4-phenyl-2,3-dihydropyridinium, a bioactivatedintermediate of parkinsonian-inducing neurotoxin1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. The Journalof Biological Chemistry, 267(33), 23601–23608. DOI:10.1016/S0021-9258(18)35881-2.
Zhang, L., Nguyen, M. V. C., Lardy, B., Jesaitis, A. J., Grichine,A., Rousset, F., Talbot, M., Paclet, M-H., Qian, G. &Morel, F. (2011). New insight into the Nox4 subcellularlocalization in HEK293 cells: first monoclonal antibodiesagainst Nox4. Biochimie, 93(3), 457–468. DOI: 10.1016/j.biochi.2010.11.001.