Selected Functions and Disorders of Mitochondrial Metabolism under Lead Exposure
Abstract
1. Introduction
2. Energy Supply—A Crucial Function of Mitochondria
Inhibition of ATP Generation in the Cell by Lead
3. Apoptosis and Necrosis
Lead as a Modifying Factor in the Cell Death
4. Mitophagy, Mitochondrial Dynamics, and Quality Control
Lead-Induced Disruptions in Mitochondrial Dynamics and Mitophagy
5. Mitochondria and Oxidative Stress
Involvement of Lead in Inducing Oxidative Stress
6. Mitochondria and Inflammation
Lead-Induced Mitochondrial Dysfunction as a Cause of an Inflammatory Response
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Ballard, J.W.O.; Whitlock, M.C. The Incomplete Natural History of Mitochondria. Mol. Ecol. 2004, 13, 729–744. [Google Scholar] [CrossRef] [PubMed]
- Duchen, M.R. Roles of Mitochondria in Health and Disease. Diabetes 2004, 53, S96–S102. [Google Scholar] [CrossRef]
- Chen, Y.; Zhou, Z.; Min, W. Mitochondria, Oxidative Stress and Innate Immunity. Front. Physiol. 2018, 9, 1487. [Google Scholar] [CrossRef]
- Lee, S.R.; Han, J. Mitochondrial Nucleoid: Shield and Switch of the Mitochondrial Genome. Oxidative Med. Cell. Longev. 2017, 2017, 8060949. [Google Scholar] [CrossRef]
- Frey, T.G.; Renken, C.W.; Perkins, G.A. Insight into Mitochondrial Structure and Function from Electron Tomography. Biochim. Biophys. Acta 2002, 1555, 196–203. [Google Scholar] [CrossRef]
- Bhatti, J.S.; Bhatti, G.K.; Reddy, P.H. Mitochondrial Dysfunction and Oxidative Stress in Metabolic Disorders—A Step towards Mitochondria Based Therapeutic Strategies. Biochim. Biophys. Acta Mol. Basis Dis. 2017, 1863, 1066–1077. [Google Scholar] [CrossRef]
- Flora, G.; Gupta, D.; Tiwari, A. Toxicity of Lead: A Review with Recent Updates. Interdiscip. Toxicol. 2012, 5, 47–58. [Google Scholar] [CrossRef] [PubMed]
- Virgolini, M.B.; Aschner, M. Molecular mechanisms of lead neurotoxicity. Adv. Neurotoxicol. 2021, 5, 159–213. [Google Scholar] [CrossRef]
- Dallner, G.; Sindelar, P.J. Regulation of Ubiquinone Metabolism. Free Radic. Biol. Med. 2000, 29, 285–294. [Google Scholar] [CrossRef]
- Andreyev, A.Y.; Kushnareva, Y.E.; Starkov, A.A. Mitochondrial Metabolism of Reactive Oxygen Species. Biochem. Mosc. 2005, 70, 200–214. [Google Scholar] [CrossRef]
- Sherratt, H.S. Mitochondria: Structure and Function. Rev. Neurol. 1991, 147, 417–430. [Google Scholar] [PubMed]
- Baranowska-Bosiacka, I.; Gutowska, I.; Marchetti, C.; Rutkowska, M.; Marchlewicz, M.; Kolasa, A.; Prokopowicz, A.; Wiernicki, I.; Piotrowska, K.; Baśkiewicz, M.; et al. Altered Energy Status of Primary Cerebellar Granule Neuronal Cultures from Rats Exposed to Lead in the Pre- and Neonatal Period. Toxicology 2011, 280, 24–32. [Google Scholar] [CrossRef] [PubMed]
- Yun, S.W.; Hoyer, S. Effects of Low-Level Lead on Glycolytic Enzymes and Pyruvate Dehydrogenase of Rat Brain in Vitro: Relevance to Sporadic Alzheimer’s Disease? J. Neural Transm. 2000, 107, 355–368. [Google Scholar] [CrossRef] [PubMed]
- Das, P.; Pal, S. Metabolic Energy Insufficiency in Mice Kidney Following Short-Term Exposure to Lead: An In-Vivo Study. Indian J. Physiol. Allied Sci. 2022, 74, 17–25. [Google Scholar] [CrossRef]
- Omar, U.M.; Elmorsy, E.M. Effect of Lead on the Bioenergetics of the Isolated Human Monocytes. Pak. J. Med. Health Sci. 2022, 16, 603. [Google Scholar] [CrossRef]
- Huettenbrenner, S.; Maier, S.; Leisser, C.; Polgar, D.; Strasser, S.; Grusch, M.; Krupitza, G. The Evolution of Cell Death Programs as Prerequisites of Multicellularity. Mutat. Res. 2003, 543, 235–249. [Google Scholar] [CrossRef] [PubMed]
- Kanduc, D.; Mittelman, A.; Serpico, R.; Sinigaglia, E.; Sinha, A.A.; Natale, C.; Santacroce, R.; Di Corcia, M.G.; Lucchese, A.; Dini, L.; et al. Cell Death: Apoptosis versus Necrosis (Review). Int. J. Oncol. 2002, 21, 165–170. [Google Scholar] [CrossRef]
- Renu, K.; Chakraborty, R.; Myakala, H.; Koti, R.; Famurewa, A.C.; Madhyastha, H.; Vellingiri, B.; George, A.; Valsala Gopalakrishnan, A. Molecular Mechanism of Heavy Metals (Lead, Chromium, Arsenic, Mercury, Nickel and Cadmium)—Induced Hepatotoxicity—A Review. Chemosphere 2021, 271, 129735. [Google Scholar] [CrossRef] [PubMed]
- Vanden Berghe, T.; Kalai, M.; Denecker, G.; Meeus, A.; Saelens, X.; Vandenabeele, P. Necrosis Is Associated with IL-6 Production but Apoptosis Is Not. Cell. Signal. 2006, 18, 328–335. [Google Scholar] [CrossRef]
- Kerr, J.F.; Wyllie, A.H.; Currie, A.R. Apoptosis: A Basic Biological Phenomenon with Wide-Ranging Implications in Tissue Kinetics. Br. J. Cancer 1972, 26, 239–257. [Google Scholar] [CrossRef]
- Häcker, G. The Morphology of Apoptosis. Cell Tissue Res. 2000, 301, 5–17. [Google Scholar] [CrossRef] [PubMed]
- Carson, D.A.; Ribeiro, J.M. Apoptosis and Disease. Lancet 1993, 341, 1251–1254. [Google Scholar] [CrossRef] [PubMed]
- Gupta, S.; Kass, G.E.N.; Szegezdi, E.; Joseph, B. The Mitochondrial Death Pathway: A Promising Therapeutic Target in Diseases. J. Cell. Mol. Med. 2009, 13, 1004–1033. [Google Scholar] [CrossRef] [PubMed]
- Vaseva, A.V.; Moll, U.M. The Mitochondrial P53 Pathway. Biochim. Biophys. Acta BBA-Bioenerg. 2009, 1787, 414–420. [Google Scholar] [CrossRef] [PubMed]
- Brunelle, J.K.; Letai, A. Control of Mitochondrial Apoptosis by the Bcl-2 Family. J. Cell Sci. 2009, 122, 437–441. [Google Scholar] [CrossRef]
- Dewson, G.; Kluck, R.M. Mechanisms by Which Bak and Bax Permeabilise Mitochondria during Apoptosis. J. Cell Sci. 2009, 122, 2801–2808. [Google Scholar] [CrossRef]
- Yang, E.; Zha, J.; Jockel, J.; Boise, L.H.; Thompson, C.B.; Korsmeyer, S.J. Bad, a Heterodimeric Partner for Bcl-xL and Bcl-2, Displaces Bax and Promotes Cell Death. Cell 1995, 80, 285–291. [Google Scholar] [CrossRef] [PubMed]
- Gardai, S.J.; Hildeman, D.A.; Frankel, S.K.; Whitlock, B.B.; Frasch, S.C.; Borregaard, N.; Marrack, P.; Bratton, D.L.; Henson, P.M. Phosphorylation of Bax Ser184 by Akt Regulates Its Activity and Apoptosis in Neutrophils. J. Biol. Chem. 2004, 279, 21085–21095. [Google Scholar] [CrossRef]
- Simonyan, L.; Renault, T.T.; da Costa Novais, M.J.; Sousa, M.J.; Côrte-Real, M.; Camougrand, N.; Gonzalez, C.; Manon, S. Regulation of Bax/Mitochondria Interaction by AKT. FEBS Lett. 2016, 590, 13–21. [Google Scholar] [CrossRef]
- Korsmeyer, S.J.; Wei, M.C.; Saito, M.; Weiler, S.; Oh, K.J.; Schlesinger, P.H. Pro-Apoptotic Cascade Activates BID, Which Oligomerizes BAK or BAX into Pores That Result in the Release of Cytochrome c. Cell Death Differ. 2000, 7, 1166–1173. [Google Scholar] [CrossRef]
- Vaux, D.L. Apoptogenic Factors Released from Mitochondria. Biochim. Biophys. Acta BBA-Mol. Cell Res. 2011, 1813, 546–550. [Google Scholar] [CrossRef] [PubMed]
- Verhagen, A.M.; Ekert, P.G.; Pakusch, M.; Silke, J.; Connolly, L.M.; Reid, G.E.; Moritz, R.L.; Simpson, R.J.; Vaux, D.L. Identification of DIABLO, a Mammalian Protein That Promotes Apoptosis by Binding to and Antagonizing IAP Proteins. Cell 2000, 102, 43–53. [Google Scholar] [CrossRef]
- Althaus, J.; Siegelin, M.D.; Dehghani, F.; Cilenti, L.; Zervos, A.S.; Rami, A. The Serine Protease Omi/HtrA2 Is Involved in XIAP Cleavage and in Neuronal Cell Death Following Focal Cerebral Ischemia/Reperfusion. Neurochem. Int. 2007, 50, 172–180. [Google Scholar] [CrossRef]
- Hu, Y.; Benedict, M.A.; Ding, L.; Núñez, G. Role of Cytochrome c and dATP/ATP Hydrolysis in Apaf-1-mediated Caspase-9 Activation and Apoptosis. EMBO J. 1999, 18, 3586–3595. [Google Scholar] [CrossRef] [PubMed]
- Decaudin, D. Peripheral Benzodiazepine Receptor and Its Clinical Targeting. Anticancer. Drugs 2004, 15, 737. [Google Scholar] [CrossRef] [PubMed]
- Baines, C.P.; Kaiser, R.A.; Sheiko, T.; Craigen, W.J.; Molkentin, J.D. Voltage-Dependent Anion Channels Are Dispensable for Mitochondrial-Dependent Cell Death. Nat. Cell Biol. 2007, 9, 550–555. [Google Scholar] [CrossRef] [PubMed]
- Kroemer, G. Mitochondrial Control of Apoptosis: An Introduction. Biochem. Biophys. Res. Commun. 2003, 304, 433–435. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.-S.; He, L.; Lemasters, J.J. Mitochondrial Permeability Transition: A Common Pathway to Necrosis and Apoptosis. Biochem. Biophys. Res. Commun. 2003, 304, 463–470. [Google Scholar] [CrossRef] [PubMed]
- Bernardi, P.; Rasola, A.; Forte, M.; Lippe, G. The Mitochondrial Permeability Transition Pore: Channel Formation by F-ATP Synthase, Integration in Signal Transduction, and Role in Pathophysiology. Physiol. Rev. 2015, 95, 1111–1155. [Google Scholar] [CrossRef]
- van Loo, G.; Schotte, P.; van Gurp, M.; Demol, H.; Hoorelbeke, B.; Gevaert, K.; Rodriguez, I.; Ruiz-Carrillo, A.; Vandekerckhove, J.; Declercq, W.; et al. Endonuclease G: A Mitochondrial Protein Released in Apoptosis and Involved in Caspase-Independent DNA Degradation. Cell Death Differ. 2001, 8, 1136–1142. [Google Scholar] [CrossRef]
- Yu, S.-W.; Wang, H.; Poitras, M.F.; Coombs, C.; Bowers, W.J.; Federoff, H.J.; Poirier, G.G.; Dawson, T.M.; Dawson, V.L. Mediation of Poly(ADP-Ribose) Polymerase-1-Dependent Cell Death by Apoptosis-Inducing Factor. Science 2002, 297, 259–263. [Google Scholar] [CrossRef] [PubMed]
- Nakagawa, T.; Shimizu, S.; Watanabe, T.; Yamaguchi, O.; Otsu, K.; Yamagata, H.; Inohara, H.; Kubo, T.; Tsujimoto, Y. Cyclophilin D-Dependent Mitochondrial Permeability Transition Regulates Some Necrotic but Not Apoptotic Cell Death. Nature 2005, 434, 652–658. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.-H.; Mu, F.-F.; Zhao, J.-H.; He, Q.; Cao, C.-L.; Yang, H.; Liu, Q.; Liu, X.-H.; Sun, S.-J. Lead Induces Apoptosis and Histone Hyperacetylation in Rat Cardiovascular Tissues. PLoS ONE 2015, 10, e0129091. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Wang, H.; Guan, J.; Guan, W.; Liu, Z. Lead Induces Mouse Skin Fibroblast Apoptosis by Disrupting Intracellular Homeostasis. Sci. Rep. 2023, 13, 9670. [Google Scholar] [CrossRef] [PubMed]
- Tousson, E.; Rafat, B.M.; Hessien, M.; El Barbary, A.A.; Sami, A. P53 and Bcl2 Apoptosis Proteins in Meso-2,3-Dimercaptosuccinic Acid Treated Lead-Intoxicated Rabbits. Toxicol. Ind. Health 2011, 27, 271–278. [Google Scholar] [CrossRef] [PubMed]
- Ma, L.; Liu, J.-Y.; Dong, J.-X.; Xiao, Q.; Zhao, J.; Jiang, F.-L. Toxicity of Pb2+ on Rat Liver Mitochondria Induced by Oxidative Stress and Mitochondrial Permeability Transition. Toxicol. Res. 2017, 6, 822–830. [Google Scholar] [CrossRef]
- Ye, F.; Li, X.; Li, F.; Li, J.; Chang, W.; Yuan, J.; Chen, J. Cyclosporin A Protects against Lead Neurotoxicity through Inhibiting Mitochondrial Permeability Transition Pore Opening in Nerve Cells. Neurotoxicology 2016, 57, 203–213. [Google Scholar] [CrossRef]
- Liu, G.; Wang, Z.-K.; Wang, Z.-Y.; Yang, D.-B.; Liu, Z.-P.; Wang, L. Mitochondrial Permeability Transition and Its Regulatory Components Are Implicated in Apoptosis of Primary Cultures of Rat Proximal Tubular Cells Exposed to Lead. Arch. Toxicol. 2016, 90, 1193–1209. [Google Scholar] [CrossRef]
- Mizushima, N. Autophagy: Process and Function. Genes Dev. 2007, 21, 2861–2873. [Google Scholar] [CrossRef]
- Xie, Z.; Klionsky, D.J. Autophagosome Formation: Core Machinery and Adaptations. Nat. Cell Biol. 2007, 9, 1102–1109. [Google Scholar] [CrossRef]
- Li, W.; Li, J.; Bao, J. Microautophagy: Lesser-Known Self-Eating. Cell. Mol. Life Sci. 2012, 69, 1125–1136. [Google Scholar] [CrossRef]
- Cuervo, A.M.; Wong, E. Chaperone-Mediated Autophagy: Roles in Disease and Aging. Cell Res. 2014, 24, 92–104. [Google Scholar] [CrossRef]
- Tanida, I. Autophagy Basics. Microbiol. Immunol. 2011, 55, 1–11. [Google Scholar] [CrossRef]
- Pernas, L.; Scorrano, L. Mito-Morphosis: Mitochondrial Fusion, Fission, and Cristae Remodeling as Key Mediators of Cellular Function. Annu. Rev. Physiol. 2016, 78, 505–531. [Google Scholar] [CrossRef]
- Chen, H.; Detmer, S.A.; Ewald, A.J.; Griffin, E.E.; Fraser, S.E.; Chan, D.C. Mitofusins Mfn1 and Mfn2 Coordinately Regulate Mitochondrial Fusion and Are Essential for Embryonic Development. J. Cell Biol. 2003, 160, 189–200. [Google Scholar] [CrossRef]
- Hoppins, S.; Nunnari, J. The Molecular Mechanism of Mitochondrial Fusion. Biochim. Biophys. Acta BBA-Mol. Cell Res. 2009, 1793, 20–26. [Google Scholar] [CrossRef]
- Otera, H.; Wang, C.; Cleland, M.M.; Setoguchi, K.; Yokota, S.; Youle, R.J.; Mihara, K. Mff Is an Essential Factor for Mitochondrial Recruitment of Drp1 during Mitochondrial Fission in Mammalian Cells. J. Cell Biol. 2010, 191, 1141–1158. [Google Scholar] [CrossRef]
- Elgass, K.; Pakay, J.; Ryan, M.T.; Palmer, C.S. Recent Advances into the Understanding of Mitochondrial Fission. Biochim. Biophys. Acta BBA-Mol. Cell Res. 2013, 1833, 150–161. [Google Scholar] [CrossRef]
- Liang, H.; Ward, W.F. PGC-1α: A Key Regulator of Energy Metabolism. Adv. Physiol. Educ. 2006, 30, 145–151. [Google Scholar] [CrossRef]
- Rodgers, J.T.; Lerin, C.; Gerhart-Hines, Z.; Puigserver, P. Metabolic Adaptations through the PGC-1 Alpha and SIRT1 Pathways. FEBS Lett. 2008, 582, 46–53. [Google Scholar] [CrossRef]
- Scarpulla, R.C. Transcriptional Paradigms in Mammalian Mitochondrial Biogenesis and Function. Physiol. Rev. 2008, 88, 611–638. [Google Scholar] [CrossRef] [PubMed]
- Sweeney, G.; Song, J. The Association between PGC-1α and Alzheimer’s Disease. Anat. Cell Biol. 2016, 49, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Ciechanover, A. The Ubiquitin-Proteasome Proteolytic Pathway. Cell 1994, 79, 13–21. [Google Scholar] [CrossRef] [PubMed]
- Ni, H.-M.; Williams, J.A.; Ding, W.-X. Mitochondrial Dynamics and Mitochondrial Quality Control. Redox Biol. 2015, 4, 6–13. [Google Scholar] [CrossRef] [PubMed]
- Poole, A.C.; Thomas, R.E.; Andrews, L.A.; McBride, H.M.; Whitworth, A.J.; Pallanck, L.J. The PINK1/Parkin Pathway Regulates Mitochondrial Morphology. Proc. Natl. Acad. Sci. USA 2008, 105, 1638–1643. [Google Scholar] [CrossRef] [PubMed]
- Yoo, S.-M.; Jung, Y.-K. A Molecular Approach to Mitophagy and Mitochondrial Dynamics. Mol. Cells 2018, 41, 18–26. [Google Scholar] [CrossRef] [PubMed]
- Deas, E.; Plun-Favreau, H.; Wood, N.W. PINK1 Function in Health and Disease. EMBO Mol. Med. 2009, 1, 152–165. [Google Scholar] [CrossRef]
- Jin, S.M.; Lazarou, M.; Wang, C.; Kane, L.A.; Narendra, D.P.; Youle, R.J. Mitochondrial Membrane Potential Regulates PINK1 Import and Proteolytic Destabilization by PARL. J. Cell Biol. 2010, 191, 933–942. [Google Scholar] [CrossRef]
- Kazlauskaite, A.; Martínez-Torres, R.J.; Wilkie, S.; Kumar, A.; Peltier, J.; Gonzalez, A.; Johnson, C.; Zhang, J.; Hope, A.G.; Peggie, M.; et al. Binding to Serine 65-phosphorylated Ubiquitin Primes Parkin for Optimal PINK1-dependent Phosphorylation and Activation. EMBO Rep. 2015, 16, 939–954. [Google Scholar] [CrossRef] [PubMed]
- Chan, N.C.; Salazar, A.M.; Pham, A.H.; Sweredoski, M.J.; Kolawa, N.J.; Graham, R.L.J.; Hess, S.; Chan, D.C. Broad Activation of the Ubiquitin–Proteasome System by Parkin Is Critical for Mitophagy. Hum. Mol. Genet. 2011, 20, 1726–1737. [Google Scholar] [CrossRef]
- Riley, B.E.; Olzmann, J.A. A Polyubiquitin Chain Reaction: Parkin Recruitment to Damaged Mitochondria. PLoS Genet. 2015, 11, e1004952. [Google Scholar] [CrossRef] [PubMed]
- Lazarou, M.; Sliter, D.A.; Kane, L.A.; Sarraf, S.A.; Wang, C.; Burman, J.L.; Sideris, D.P.; Fogel, A.I.; Youle, R.J. The Ubiquitin Kinase PINK1 Recruits Autophagy Receptors to Induce Mitophagy. Nature 2015, 524, 309–314. [Google Scholar] [CrossRef] [PubMed]
- Richter, B.; Sliter, D.A.; Herhaus, L.; Stolz, A.; Wang, C.; Beli, P.; Zaffagnini, G.; Wild, P.; Martens, S.; Wagner, S.A.; et al. Phosphorylation of OPTN by TBK1 Enhances Its Binding to Ub Chains and Promotes Selective Autophagy of Damaged Mitochondria. Proc. Natl. Acad. Sci. USA 2016, 113, 4039–4044. [Google Scholar] [CrossRef] [PubMed]
- Chinnadurai, G.; Vijayalingam, S.; Gibson, S.B. BNIP3 Subfamily BH3-Only Proteins: Mitochondrial Stress Sensors in Normal and Pathological Functions. Oncogene 2008, 27, S114–S127. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Chiang, W.-C.; Sumpter, R.; Mishra, P.; Levine, B. Prohibitin 2 Is an Inner Mitochondrial Membrane Mitophagy Receptor. Cell 2017, 168, 224–238.e10. [Google Scholar] [CrossRef] [PubMed]
- Han, Y.; Li, C.; Su, M.; Wang, Z.; Jiang, N.; Sun, D. Antagonistic Effects of Selenium on Lead-Induced Autophagy by Influencing Mitochondrial Dynamics in the Spleen of Chickens. Oncotarget 2017, 8, 33725–33735. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Li, X.; Jiang, A.; Li, X.; Chang, W.; Chen, J.; Ye, F. Metformin Alleviates Lead-Induced Mitochondrial Fragmentation via AMPK/Nrf2 Activation in SH-SY5Y Cells. Redox Biol. 2020, 36, 101626. [Google Scholar] [CrossRef] [PubMed]
- Dabrowska, A.; Venero, J.L.; Iwasawa, R.; Hankir, M.-K.; Rahman, S.; Boobis, A.; Hajji, N. PGC-1α Controls Mitochondrial Biogenesis and Dynamics in Lead-Induced Neurotoxicity. Aging 2015, 7, 629–647. [Google Scholar] [CrossRef]
- Guan, X.; Shen, J.; Xu, Y.; Feng, X.; Zhou, R. Heme Oxygenase-1 Enhances Autophagy by Modulating the AMPK/mTORC1 Signaling Pathway as a Renoprotective Mechanism to Mitigate Lead-Induced Nephrotoxicity. Am. J. Transl. Res. 2020, 12, 4807–4818. [Google Scholar] [PubMed]
- Liu, J.; Liao, G.; Tu, H.; Huang, Y.; Peng, T.; Xu, Y.; Chen, X.; Huang, Z.; Zhang, Y.; Meng, X.; et al. A Protective Role of Autophagy in Pb-Induced Developmental Neurotoxicity in Zebrafish. Chemosphere 2019, 235, 1050–1058. [Google Scholar] [CrossRef]
- Gu, X.; Qi, Y.; Feng, Z.; Ma, L.; Gao, K.; Zhang, Y. Lead (Pb) Induced ATM-Dependent Mitophagy via PINK1/Parkin Pathway. Toxicol. Lett. 2018, 291, 92–100. [Google Scholar] [CrossRef] [PubMed]
- Bandaru, L.J.M.; Ayyalasomayajula, N.; Murumulla, L.; Dixit, P.K.; Challa, S. Defective Mitophagy and Induction of Apoptosis by the Depleted Levels of PINK1 and Parkin in Pb and β-Amyloid Peptide Induced Toxicity. Toxicol. Mech. Methods 2022, 32, 559–568. [Google Scholar] [CrossRef] [PubMed]
- Gao, K.; Zhang, C.; Tian, Y.; Naeem, S.; Zhang, Y.; Qi, Y. The Role of Endoplasmic Reticulum Stress in Lead (Pb)-Induced Mitophagy of HEK293 Cells. Toxicol. Ind. Health 2020, 36, 1002–1009. [Google Scholar] [CrossRef] [PubMed]
- Murphy, M.P. How Mitochondria Produce Reactive Oxygen Species. Biochem. J. 2008, 417, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Starkov, A.A. The Role of Mitochondria in Reactive Oxygen Species Metabolism and Signaling. Ann. N. Y. Acad. Sci. 2008, 1147, 37–52. [Google Scholar] [CrossRef] [PubMed]
- Fukai, T.; Ushio-Fukai, M. Superoxide Dismutases: Role in Redox Signaling, Vascular Function, and Diseases. Antioxid. Redox Signal. 2011, 15, 1583–1606. [Google Scholar] [CrossRef] [PubMed]
- Rhee, S.G. H2O2, a Necessary Evil for Cell Signaling. Science 2006, 312, 1882–1883. [Google Scholar] [CrossRef]
- Lipinski, B. Hydroxyl Radical and Its Scavengers in Health and Disease. Oxidative Med. Cell. Longev. 2011, 2011, e809696. [Google Scholar] [CrossRef] [PubMed]
- Blokhina, O.; Virolainen, E.; Fagerstedt, K.V. Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: A Review. Ann. Bot. 2003, 91, 179–194. [Google Scholar] [CrossRef]
- Pizzino, G.; Irrera, N.; Cucinotta, M.; Pallio, G.; Mannino, F.; Arcoraci, V.; Squadrito, F.; Altavilla, D.; Bitto, A. Oxidative Stress: Harms and Benefits for Human Health. Oxidative Med. Cell. Longev. 2017, 2017, e8416763. [Google Scholar] [CrossRef]
- Catalá, A. Lipid Peroxidation of Membrane Phospholipids Generates Hydroxy-Alkenals and Oxidized Phospholipids Active in Physiological and/or Pathological Conditions. Chem. Phys. Lipids 2009, 157, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Valenzuela, A. The Biological Significance of Malondialdehyde Determination in the Assessment of Tissue Oxidative Stress. Life Sci. 1991, 48, 301–309. [Google Scholar] [CrossRef] [PubMed]
- Del Rio, D.; Stewart, A.J.; Pellegrini, N. A Review of Recent Studies on Malondialdehyde as Toxic Molecule and Biological Marker of Oxidative Stress. Nutr. Metab. Cardiovasc. Dis. 2005, 15, 316–328. [Google Scholar] [CrossRef] [PubMed]
- Marnett, L.J. Lipid Peroxidation—DNA Damage by Malondialdehyde. Mutat. Res. Mol. Mech. Mutagen. 1999, 424, 83–95. [Google Scholar] [CrossRef] [PubMed]
- Baranowska-Bosiacka, I.; Gutowska, I.; Marchlewicz, M.; Marchetti, C.; Kurzawski, M.; Dziedziejko, V.; Kolasa, A.; Olszewska, M.; Rybicka, M.; Safranow, K.; et al. Disrupted Pro- and Antioxidative Balance as a Mechanism of Neurotoxicity Induced by Perinatal Exposure to Lead. Brain Res. 2012, 1435, 56–71. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Liu, Y.; Liu, R.; Liu, C.; Chen, Y. Molecular Mechanism of Lead-Induced Superoxide Dismutase Inactivation in Zebrafish Livers. J. Phys. Chem. B 2014, 118, 14820–14826. [Google Scholar] [CrossRef] [PubMed]
- Jefferies, H.; Coster, J.; Khalil, A.; Bot, J.; McCauley, R.D.; Hall, J.C. Glutathione. ANZ J. Surg. 2003, 73, 517–522. [Google Scholar] [CrossRef] [PubMed]
- Kaur, G.; Singh, H.P.; Batish, D.R.; Kohli, R.K. Adaptations to Oxidative Stress in Zea Mays Roots under Short-Term Pb2+ Exposure. Biologia 2015, 70, 190–197. [Google Scholar] [CrossRef]
- Małecka, A.; Derba-Maceluch, M.; Kaczorowska, K.; Piechalak, A.; Tomaszewska, B. Reactive Oxygen Species Production and Antioxidative Defense System in Pea Root Tissues Treated with Lead Ions: Mitochondrial and Peroxisomal Level. Acta Physiol. Plant. 2009, 31, 1065–1075. [Google Scholar] [CrossRef]
- Nehru, B.; Kanwar, S.S. N-Acetylcysteine Exposure on Lead-Induced Lipid Peroxidative Damage and Oxidative Defense System in Brain Regions of Rats. Biol. Trace Elem. Res. 2004, 101, 257–264. [Google Scholar] [CrossRef]
- Elsheikh, N.A.H.; Omer, N.A.E.; Li-lian; Wang, G.-L. Lead Induced Oxidative Stress and Affected the Expression of Steroidogenesis -Related Genes in Testis of Male Mice. Indian J. Forensic Med. Toxicol. 2022, 16, 248–254. [Google Scholar] [CrossRef]
- Ai, H.; Xiong, W.; Zhu, P.; Chen, Y.; Ji, Y.; Jiang, X.; Xin, T.; Xia, B.; Zou, Z. Regulation of Three Subtypes of SOD Gene in Aleuroglyphus Ovatus (Acari:Acaridae) under Lead Stress. Arch. Insect Biochem. Physiol. 2023, 114, e22043. [Google Scholar] [CrossRef]
- Olorunsogo, O.O. Oxidative Stress in Workers Occupationally Exposed to Lead. Arch. Basic Appl. Med. 2014, 2, 93–97. [Google Scholar]
- Ho, K.-J.; Chen, T.-H.; Yang, C.-C.; Chuang, Y.-C.; Chuang, H.-Y. Interaction of Smoking and Lead Exposure among Carriers of Genetic Variants Associated with a Higher Level of Oxidative Stress Indicators. Int. J. Environ. Res. Public. Health 2021, 18, 8325. [Google Scholar] [CrossRef]
- Gurer-Orhan, H.; Sabir, H.U.; Ozgüneş, H. Correlation between Clinical Indicators of Lead Poisoning and Oxidative Stress Parameters in Controls and Lead-Exposed Workers. Toxicology 2004, 195, 147–154. [Google Scholar] [CrossRef]
- Casado, M.F.; Cecchini, A.L.; Simão, A.N.C.; Oliveira, R.D.; Cecchini, R. Free Radical-Mediated Pre-Hemolytic Injury in Human Red Blood Cells Subjected to Lead Acetate as Evaluated by Chemiluminescence. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2007, 45, 945–952. [Google Scholar] [CrossRef]
- Ahamed, M.; Akhtar, M.J.; Verma, S.; Kumar, A.; Siddiqui, M.K.J. Environmental Lead Exposure as a Risk for Childhood Aplastic Anemia. Biosci. Trends 2011, 5, 38–43. [Google Scholar] [CrossRef] [PubMed]
- Conterato, G.M.M.; Bulcão, R.P.; Sobieski, R.; Moro, A.M.; Charão, M.F.; de Freitas, F.A.; de Almeida, F.L.; Moreira, A.P.L.; Roehrs, M.; Tonello, R.; et al. Blood Thioredoxin Reductase Activity, Oxidative Stress and Hematological Parameters in Painters and Battery Workers: Relationship with Lead and Cadmium Levels in Blood. J. Appl. Toxicol. 2013, 33, 142–150. [Google Scholar] [CrossRef] [PubMed]
- Subramaniam, S.R.; Chesselet, M.-F. Mitochondrial Dysfunction and Oxidative Stress in Parkinson’s Disease. Prog. Neurobiol. 2013, 106–107, 17–32. [Google Scholar] [CrossRef]
- Tönnies, E.; Trushina, E. Oxidative Stress, Synaptic Dysfunction, and Alzheimer’s Disease. J. Alzheimers Dis. 2017, 57, 1105–1121. [Google Scholar] [CrossRef]
- Kryston, T.B.; Georgiev, A.B.; Pissis, P.; Georgakilas, A.G. Role of Oxidative Stress and DNA Damage in Human Carcinogenesis. Mutat. Res. Mol. Mech. Mutagen. 2011, 711, 193–201. [Google Scholar] [CrossRef] [PubMed]
- Nathan, C.; Ding, A. Nonresolving Inflammation. Cell 2010, 140, 871–882. [Google Scholar] [CrossRef]
- Meyer, A.; Laverny, G.; Bernardi, L.; Charles, A.L.; Alsaleh, G.; Pottecher, J.; Sibilia, J.; Geny, B. Mitochondria: An Organelle of Bacterial Origin Controlling Inflammation. Front. Immunol. 2018, 9, 536. [Google Scholar] [CrossRef]
- Marchi, S.; Guilbaud, E.; Tait, S.W.G.; Yamazaki, T.; Galluzzi, L. Mitochondrial Control of Inflammation. Nat. Rev. Immunol. 2023, 23, 159–173. [Google Scholar] [CrossRef] [PubMed]
- Weinberg, S.E.; Sena, L.A.; Chandel, N.S. Mitochondria in the Regulation of Innate and Adaptive Immunity. Immunity 2015, 42, 406–417. [Google Scholar] [CrossRef]
- Rongvaux, A. Innate Immunity and Tolerance toward Mitochondria. Mitochondrion 2018, 41, 14–20. [Google Scholar] [CrossRef]
- Akira, S.; Hemmi, H. Recognition of Pathogen-Associated Molecular Patterns by TLR Family. Immunol. Lett. 2003, 85, 85–95. [Google Scholar] [CrossRef]
- Land, W.G. The Role of Damage-Associated Molecular Patterns in Human Diseases. Sultan Qaboos Univ. Med. J. 2015, 15, e9–e21. [Google Scholar]
- Zhang, Q.; Raoof, M.; Chen, Y.; Sumi, Y.; Sursal, T.; Junger, W.; Brohi, K.; Itagaki, K.; Hauser, C.J. Circulating Mitochondrial DAMPs Cause Inflammatory Responses to Injury. Nature 2010, 464, 104–107. [Google Scholar] [CrossRef] [PubMed]
- Ablasser, A.; Schmid-Burgk, J.L.; Hemmerling, I.; Horvath, G.L.; Schmidt, T.; Latz, E.; Hornung, V. Cell Intrinsic Immunity Spreads to Bystander Cells via the Intercellular Transfer of cGAMP. Nature 2013, 503, 530–534. [Google Scholar] [CrossRef]
- Decout, A.; Katz, J.D.; Venkatraman, S.; Ablasser, A. The cGAS–STING Pathway as a Therapeutic Target in Inflammatory Diseases. Nat. Rev. Immunol. 2021, 21, 548–569. [Google Scholar] [CrossRef] [PubMed]
- Muruve, D.A.; Pétrilli, V.; Zaiss, A.K.; White, L.R.; Clark, S.A.; Ross, P.J.; Parks, R.J.; Tschopp, J. The Inflammasome Recognizes Cytosolic Microbial and Host DNA and Triggers an Innate Immune Response. Nature 2008, 452, 103–107. [Google Scholar] [CrossRef]
- Kawai, T.; Akira, S. The Role of Pattern-Recognition Receptors in Innate Immunity: Update on Toll-like Receptors. Nat. Immunol. 2010, 11, 373–384. [Google Scholar] [CrossRef] [PubMed]
- Zhou, R.; Yazdi, A.S.; Menu, P.; Tschopp, J. A Role for Mitochondria in NLRP3 Inflammasome Activation. Nature 2011, 469, 221–225. [Google Scholar] [CrossRef]
- Gurung, P.; Lukens, J.R.; Kanneganti, T.-D. Mitochondria: Diversity in the Regulation of the NLRP3 Inflammasome. Trends Mol. Med. 2015, 21, 193–201. [Google Scholar] [CrossRef] [PubMed]
- Tian, J.; Avalos, A.M.; Mao, S.-Y.; Chen, B.; Senthil, K.; Wu, H.; Parroche, P.; Drabic, S.; Golenbock, D.; Sirois, C.; et al. Toll-like Receptor 9-Dependent Activation by DNA-Containing Immune Complexes Is Mediated by HMGB1 and RAGE. Nat. Immunol. 2007, 8, 487–496. [Google Scholar] [CrossRef]
- Raoof, M.; Zhang, Q.; Itagaki, K.; Hauser, C.J. Mitochondrial Peptides Are Potent Immune Activators That Activate Human Neutrophils Via FPR-1. J. Trauma Acute Care Surg. 2010, 68, 1328. [Google Scholar] [CrossRef]
- Dieudé, M.; Striegl, H.; Tyznik, A.J.; Wang, J.; Behar, S.M.; Piccirillo, C.A.; Levine, J.S.; Zajonc, D.M.; Rauch, J. Cardiolipin Binds to CD1d and Stimulates CD1d-Restricted Γδ T Cells in the Normal Murine Repertoire. J. Immunol. 2011, 186, 4771–4781. [Google Scholar] [CrossRef]
- Cicko, S.; Köhler, T.C.; Ayata, C.K.; Müller, T.; Ehrat, N.; Meyer, A.; Hossfeld, M.; Zech, A.; Di Virgilio, F.; Idzko, M. Extracellular ATP Is a Danger Signal Activating P2X7 Receptor in a LPS Mediated Inflammation (ARDS/ALI). Oncotarget 2018, 9, 30635–30648. [Google Scholar] [CrossRef]
- Bhagirath, V.C.; Dwivedi, D.J.; Liaw, P.C. Comparison of the Proinflammatory and Procoagulant Properties of Nuclear, Mitochondrial, and Bacterial DNA. Shock 2015, 44, 265. [Google Scholar] [CrossRef]
- Metryka, E.; Chibowska, K.; Gutowska, I.; Falkowska, A.; Kupnicka, P.; Barczak, K.; Chlubek, D.; Baranowska-Bosiacka, I. Lead (Pb) Exposure Enhances Expression of Factors Associated with Inflammation. Int. J. Mol. Sci. 2018, 19, 1813. [Google Scholar] [CrossRef] [PubMed]
- Banoth, B.; Cassel, S.L. Mitochondria in Innate Immune Signaling. Transl. Res. J. Lab. Clin. Med. 2018, 202, 52–68. [Google Scholar] [CrossRef] [PubMed]
- Walsh, M.C.; Lee, J.; Choi, Y. Tumor Necrosis Factor Receptor- Associated Factor 6 (TRAF6) Regulation of Development, Function, and Homeostasis of the Immune System. Immunol. Rev. 2015, 266, 72–92. [Google Scholar] [CrossRef] [PubMed]
- West, A.P.; Brodsky, I.E.; Rahner, C.; Woo, D.K.; Erdjument-Bromage, H.; Tempst, P.; Walsh, M.C.; Choi, Y.; Shadel, G.S.; Ghosh, S. TLR Signalling Augments Macrophage Bactericidal Activity through Mitochondrial ROS. Nature 2011, 472, 476–480. [Google Scholar] [CrossRef]
- Liu, J.-T.; Chen, B.-Y.; Zhang, J.-Q.; Kuang, F.; Chen, L.-W. Lead Exposure Induced Microgliosis and Astrogliosis in Hippocampus of Young Mice Potentially by Triggering TLR4-MyD88-NFκB Signaling Cascades. Toxicol. Lett. 2015, 239, 97–107. [Google Scholar] [CrossRef] [PubMed]
- Chibowska, K.; Korbecki, J.; Gutowska, I.; Metryka, E.; Tarnowski, M.; Goschorska, M.; Barczak, K.; Chlubek, D.; Baranowska-Bosiacka, I. Pre- and Neonatal Exposure to Lead (Pb) Induces Neuroinflammation in the Forebrain Cortex, Hippocampus and Cerebellum of Rat Pups. Int. J. Mol. Sci. 2020, 21, 1083. [Google Scholar] [CrossRef]
- Metryka, E.; Kupnicka, P.; Kapczuk, P.; Simińska, D.; Tarnowski, M.; Goschorska, M.; Gutowska, I.; Chlubek, D.; Baranowska-Bosiacka, I. Lead (Pb) as a Factor Initiating and Potentiating Inflammation in Human THP-1 Macrophages. Int. J. Mol. Sci. 2020, 21, 2254. [Google Scholar] [CrossRef]
- Attafi, I.M.; Bakheet, S.A.; Korashy, H.M. The Role of NF-κB and AhR Transcription Factors in Lead-Induced Lung Toxicity in Human Lung Cancer A549 Cells. Toxicol. Mech. Methods 2020, 30, 197–207. [Google Scholar] [CrossRef]
- Attafi, I.M.; Bakheet, S.A.; Ahmad, S.F.; Belali, O.M.; Alanazi, F.E.; Aljarboa, S.A.; Al-Alallah, I.A.; Korashy, H.M. Lead Nitrate Induces Inflammation and Apoptosis in Rat Lungs Through the Activation of NF-κB and AhR Signaling Pathways. Environ. Sci. Pollut. Res. Int. 2022, 29, 64959–64970. [Google Scholar] [CrossRef]
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Chlubek, M.; Baranowska-Bosiacka, I. Selected Functions and Disorders of Mitochondrial Metabolism under Lead Exposure. Cells 2024, 13, 1182. https://doi.org/10.3390/cells13141182
Chlubek M, Baranowska-Bosiacka I. Selected Functions and Disorders of Mitochondrial Metabolism under Lead Exposure. Cells. 2024; 13(14):1182. https://doi.org/10.3390/cells13141182
Chicago/Turabian StyleChlubek, Mikołaj, and Irena Baranowska-Bosiacka. 2024. "Selected Functions and Disorders of Mitochondrial Metabolism under Lead Exposure" Cells 13, no. 14: 1182. https://doi.org/10.3390/cells13141182
APA StyleChlubek, M., & Baranowska-Bosiacka, I. (2024). Selected Functions and Disorders of Mitochondrial Metabolism under Lead Exposure. Cells, 13(14), 1182. https://doi.org/10.3390/cells13141182