Cited by 126Mitochondrial Function and PathologyBioactive Compounds and Antitumor AgentsRedox biology and oxidative stress

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Inhibitors of Succinate: Quinone Reductase/Complex II Regulate Production of Mitochondrial Reactive Oxygen Species and Protect Normal Cells from Ischemic Damage but Induce Specific Cancer Cell Death

Ralph, Stephen J., Moreno-Sánchez, Rafael, Neuzil, Jiri, Rodríguez-Enríquez, Sara·2011·Pharmaceutical Research

DOI 10.1007/s11095-011-0566-7

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Abstract

Succinate:quinone reductase (SQR) of Complex II occupies a unique central point in the mitochondrial respiratory system as a major source of electrons driving reactive oxygen species (ROS) production. It is an ideal pharmaceutical target for modulating ROS levels in normal cells to prevent oxidative stress-induced damage or alternatively,increase ROS in cancer cells, inducing cell death.The value of drugs like diazoxide to prevent ROS production,protecting normal cells, whereas vitamin E analogues promote ROS in cancer cells to kill them is highlighted. As pharmaceuticals these agents may prevent degenerative disease and their modes of action are presently being fully explored. The evidence that SDH/Complex II is tightly coupled to the NADH/NAD+ ratio in all cells,impacted by the available supplies of Krebs cycle intermediates as essential NAD-linked substrates, and the NAD+-dependent regulation of SDH/Complex II are reviewed, as are links to the NAD+-dependent dehydrogenases, Complex I and the E3 dihiydrolipoamide dehydrogenase to produce ROS. This review collates and discusses diverse sources of information relating to ROS production in different biological systems, focussing on evidence for SQR as the main source of ROS production in mitochondria, particularly its relevance to protection from oxidative stress and to the mitochondrial-targeted anti cancer drugs (mitocans) as novel cancer therapies [corrected].

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WITHDRAWN: Oxidative stress in aging: Theoretical outcomes and clinical evidences in humans
del Valle, L. G. (2010) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2010.09.010 · Cited by 36
Retracted
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Parsons, D. W., Jones, S., Zhang, X., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I.-M., Gallia, G. L., et al. (2008) · Science · doi:10.1126/science.1164382 · Cited by 5,857
Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses
Jones, S., Zhang, X., Parsons, D. W., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. (2008) · Science · doi:10.1126/science.1164368 · Cited by 3,969
Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction
Berridge, M. V., Herst, P. M., & Tan, A. S. (2005) · Biotechnology Annual Review · doi:10.1016/s1387-2656(05)11004-7 · Cited by 2,222
Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase
Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., & Gottlieb, E. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.11.022 · Cited by 2,108
Mammalian Sirtuins: Biological Insights and Disease Relevance
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Cellular energy utilization and molecular origin of standard metabolic rate in mammals
Rolfe, D. F., & Brown, G. C. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.3.731 · Cited by 2,021
High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria
Korshunov, S. S., Skulachev, V. P., & Starkov, A. A. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01159-9 · Cited by 1,727
A Mitochondria-K+ Channel Axis Is Suppressed in Cancer and Its Normalization Promotes Apoptosis and Inhibits Cancer Growth
Bonnet, S., Archer, S. L., Allalunis‐Turner, J., Haromy, A., Beaulieu, C., Thompson, R. B., Lee, C. T., Lopaschuk, G. D., Puttagunta, L., Bonnet, S. B., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2006.10.020 · Cited by 1,552
The unique physiology of solid tumors: opportunities (and problems) for cancer therapy.
Brown, J. M., & Giaccia, A. J. (1998) · PubMed · Cited by 1,499

Show all 292 references

Research works printed but not linked: 5

E.Gnaiger. Mitochondrial Pathways through Complexes I and II: Convergent Electron Transfer at the Q-Junction and Additive Effects of Substrate Combinations. In E.Gnaiger (ed.), Mitochondrial Pathways and Respiratory Control, OROBOROS MiPNet publications, Innsbruck, 2007, pp. 1–13.
M.Gutman. Kinetic analysis of electron flux through the quinones in the mitochondrial system. In G.Ed.Lenaz (ed.), Coenzyme Q, John Wiley, Chichester, UK, 1985, pp. 215–234.
Gutman M. In: Lenaz G, editor. Kinetic analysis of electron flux through the quinones in the mitochondrial system. Chichester: Coenzyme Q, John Wiley; 1985. p. 215–34.
Pisarenko OI, Khlopkov VN, Ruuge EK. A 1H NMR study of succinate synthesis from exogenous precursors in oxygen-deprived rat heart mitochondria. Biochem Int. 1986;12:145–53.
Neuzil J, Wang XF, Dong LF, Low P, Ralph SJ. Molecular mechanism of ‘mitocan’-induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins. FEBS Lett. 2006;580:5125–9. · DOI

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Authors: Ralph, S. J., Moreno-Sánchez, R., Neuzil, J., & Rodríguez-Enríquez, S.
Affiliations: Griffith University (AU)
Corresponding author: Ralph, Stephen J.
ORCID: Ralph, Stephen J.
Venue: Pharmaceutical Research
Publisher: Springer Science and Business Media LLC
Published: 2011-08-24
Volume: 28
Issue: 11
Pages: 2695-2730
ISSN: 0724-8741 (ISSN-L)
1573-904X
DOI: 10.1007/s11095-011-0566-7
OpenAlex: W1983521123
Cited by: 126
References: 292
Citations by year: 2026: 2 · 2025: 4 · 2024: 12 · 2023: 12 · 2022: 6 · 2021: 12 · 2020: 11 · 2019: 8 · 2018: 9 · 2017: 9 · 2016: 5 · 2015: 9 · 2014: 12 · 2013: 6 · 2012: 9
FWCI: 0.78
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Pharmaceutical Research (publishedVersion)
PubMed (publishedVersion)
ASEP (submittedVersion, public-domain)
Griffith Research Online (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Bioactive Compounds and Antitumor Agents
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: succinate dehydrogenase, mitochondrial reactive oxygen species, oxidative stress, ischemic injury, cancer cell death, diazoxide, vitamin E analogues, NAD+/NADH ratio, Krebs cycle intermediates, NAD-dependent dehydrogenase, mitocans
MeSH terms: Coenzyme A, Fatty Acids, Nonesterified, Humans, Dihydrolipoamide Dehydrogenase, Mitochondria, Neoplasms, Organophosphorus Compounds, Ubiquinone, NAD(P)H Dehydrogenase (Quinone), Cell Death, Reactive Oxygen Species, Succinic Acid, Protective Agents, alpha-Tocopherol

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Inhibitors of Succinate: Quinone Reductase/Complex II Regulate Production of Mitochondrial Reactive Oxygen Species and Protect Normal Cells from Ischemic Damage but Induce Specific Cancer Cell Death

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