Gnaiger E (2024) Complex II ambiguities ― FADH2 in the electron transfer system. J Biol Chem 300:105470. https://doi.org/10.1016/j.jbc.2023.105470 |
Gnaiger Erich (2024) J Biol Chem
Abstract:
The prevailing notion that reduced cofactors NADH and FADH2 transfer electrons from the tricarboxylic acid cycle to the mitochondrial electron transfer system creates ambiguities regarding respiratory Complex II (CII). CII is the only membrane-bound enzyme in the tricarboxylic acid cycle and is part of the electron transfer system of the mitochondrial inner membrane feeding electrons into the coenzyme Q-junction. The succinate dehydrogenase subunit SDHA of CII oxidizes succinate and reduces the covalently bound prosthetic group FAD to FADH2 in the canonical forward tricarboxylic acid cycle. However, several graphical representations of the electron transfer system depict FADH2 in the mitochondrial matrix as a substrate to be oxidized by CII. This leads to the false conclusion that FADH2 from the β-oxidation cycle in fatty acid oxidation feeds electrons into CII. In reality, dehydrogenases of fatty acid oxidation channel electrons to the Q-junction but not through CII. The ambiguities surrounding Complex II in the literature and educational resources call for quality control, to secure scientific standards in current communications of bioenergetics, and ultimately support adequate clinical applications. This review aims to raise awareness of the inherent ambiguity crisis, complementing efforts to address the well-acknowledged issues of credibility and reproducibility. • Keywords: coenzyme; cofactor; prosthetic group; coenzyme Q junction, Q-junction; Complex II, CII; H+-linked electron transfer; electron transfer system, ETS; matrix-ETS; membrane-ETS; fatty acid oxidation, FAO; flavin adenine dinucleotide, FAD/FADH2; nicotinamide adenine dinucleotide, NAD+/NADH; succinate dehydrogenase, SDH; tricarboxylic acid cycle, TCA; substrate; Gibbs force
• O2k-Network Lab: AT Innsbruck Oroboros
ORCID: Gnaiger Erich, Oroboros Instruments, Innsbruck, Austria
» Links: Ambiguity crisis, Complex II ambiguities, Complex I and hydrogen ion ambiguities in the electron transfer system
Correction
- The original Figure 1b contained a ‘typo’, misrepresenting Succinate2- and Fumarate2- (corrected in the figure on the right) as Succinate2+ and Fumarate2+ (correction 2024-09-09). This mistake did not occur in Tables 1 and 2.
MitoFit Preprint
- Gnaiger E (2023) Complex II ambiguities ― FADH2 in the electron transfer system. MitoFit Preprints 2023.3.v6. https://doi.org/10.26124/mitofit:2023-0003.v6
Post-publication additions to 312 references on CII-ambiguities in JBC 2024
- Living Communication with updated references on CII ambiguities.
Last update 2024-10-11
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SDH: FAD ⟶ FADH2; CII: FADH2 ⟶ FAD
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FADH2 ⟶ FAD
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FADH2 ⟶ FAD + H+
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FADH2 ⟶ FAD + 2H+
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FADH2 ⟶ FAD+ (+H+ or +2H+)
- FADH2 ⟶ FAD+
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- While CI functions as a proton pump, CII does not. Depicting CII as a proton pump would be analogous to falsely portraying FADH2 as the substrate of CII, as if it were a copy of CI, which functions as a proton pump with NADH as its substrate.
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- FADH2 ⟶ FAD+ + H+
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- FADH2 ⟶ FAD+ + 2H+
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- FADH2 ⟶ FAD2+
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FADH2 ⟶ FADH or FADH+
- FADH2 ⟶ FADH
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- FADH2 ⟶ FADH +H+
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- FADH2 ⟶ FADH+
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FADH or FADH+ ⟶
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- FADH ⟶ FAD
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- FADH ⟶ FAD+
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- FADH ⟶ FAD+ +H+
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- FADH ⟶ FAD +2H+
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- FADH+ ⟶ FAD
- 7f.1. Ref 343 Catania A, Iuso A, Bouchereau J, Kremer LS, Paviolo M, Terrile C, Bénit P, Rasmusson AG, Schwarzmayr T, Tiranti V, Rustin P, Rak M, Prokisch H, Schiff M (2019) Arabidopsis thaliana alternative dehydrogenases: a potential therapy for mitochondrial complex I deficiency? Perspectives and pitfalls. Orphanet J Rare Dis 14:236. - »Bioblast link«
FAD or FAD+ ⟶ or other
- FAD ⟶
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- FAD+ ⟶ FADH2
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- FADH2+ Succinate ⟶ Fumarate +2H+
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- FADH2 ⟶ CI ⟶ CII
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- ETF ⟶ CII
- 8e.1. Ref 350 Bindra S, McGill MA, Triplett MK, Tyagi A, Thaker PH, Dahmoush L, Goodheart MJ, Ogden RT, Owusu-Ansah E, R Karan K, Cole S, Sood AK, Lutgendorf SK, Picard M (2021) Mitochondria in epithelial ovarian carcinoma exhibit abnormal phenotypes and blunted associations with biobehavioral factors. Sci Rep 11:11595. - »Bioblast link«
- 8e.2. Ref 351 Bugarski M, Martins JR, Haenni D, Hall AM (2018) Multiphoton imaging reveals axial differences in metabolic autofluorescence signals along the kidney proximal tubule. Am J Physiol Renal Physiol 315:F1613-25. - »Bioblast link«
- 8e.3. Ref 352 Cortassa S, Aon MA, Sollott SJ (2019) Control and regulation of substrate selection in cytoplasmic and mitochondrial catabolic networks. A systems biology analysis. Front Physiol 10:201. - »Bioblast link«
- 8e.4. Ref 353 Karan KR, Trumpff C, McGill MA, Thomas JE, Sturm G, Lauriola V, Sloan RP, Rohleder N, Kaufman BA, Marsland AL, Picard M (2020) Mitochondrial respiratory capacity modulates LPS-induced inflammatory signatures in human blood. Brain Behav Immun Health 5:100080. - »Bioblast link«
- 8e.5. Ref 354 Picard M, McEwen BS (2018) Psychological stress and mitochondria: a systematic review. Psychosom Med 80:141-53. - »Bioblast link«
- 8e.6. Ref 355 Picard M, Prather AA, Puterman E, Cuillerier A, Coccia M, Aschbacher K, Burelle Y, Epel ES (2018) A mitochondrial health index sensitive to mood and caregiving stress. Biol Psychiatry 84:9-17. - »Bioblast link«
- 8e.7. Ref 356 Rausser S, Trumpff C, McGill MA, Junker A, Wang W, Ho SH, Mitchell A, Karan KR, Monk C, Segerstrom SC, Reed RG, Picard M (2021) Mitochondrial phenotypes in purified human immune cell subtypes and cell mixtures. Elife 10:e70899. - »Bioblast link«
FAO and CII ambiguitiy
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- Ref 351 Bugarski M, Martins JR, Haenni D, Hall AM (2018) Multiphoton imaging reveals axial differences in metabolic autofluorescence signals along the kidney proximal tubule. Am J Physiol Renal Physiol 315:F1613-25. - »Bioblast link«
- Ref 352 Cortassa S, Aon MA, Sollott SJ (2019) Control and regulation of substrate selection in cytoplasmic and mitochondrial catabolic networks. A systems biology analysis. Front Physiol 10:201. - »Bioblast link«
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- Ref 205 Frangos SM, DesOrmeaux GJ, Holloway GP (2023) Acidosis attenuates CPT-I supported bioenergetics as a potential mechanism limiting lipid oxidation. J Biol Chem 299:105079. - »Bioblast link«
- Ref 71 Hinder LM, Sas KM, O'Brien PD, Backus C, Kayampilly P, Hayes JM, Lin CM, Zhang H, Shanmugam S, Rumora AE, Abcouwer SF, Brosius FC 3rd, Pennathur S, Feldman EL (2019) Mitochondrial uncoupling has no effect on microvascular complications in type 2 diabetes. Sci Rep 9:881. - »Bioblast link«
- Ref 349 Huss JM, Kelly DP (2005) Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 115:547-55. - »Bioblast link«
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- Ref 291 Merritt JL 2nd, MacLeod E, Jurecka A, Hainline B (2020) Clinical manifestations and management of fatty acid oxidation disorders. Rev Endocr Metab Disord 21:479-93. - »Bioblast link«
- Ref 221 Murray AJ (2009) Metabolic adaptation of skeletal muscle to high altitude hypoxia: how new technologies could resolve the controversies. Genome Med 1:117. - »Bioblast link«
- Ref 226 Picard M, Jung B, Liang F, Azuelos I, Hussain S, Goldberg P, Godin R, Danialou G, Chaturvedi R, Rygiel K, Matecki S, Jaber S, Des Rosiers C, Karpati G, Ferri L, Burelle Y, Turnbull DM, Taivassalo T, Petrof BJ (2012) Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med 186:1140-9. - »Bioblast link«
- Ref 354 Picard M, McEwen BS (2018) Psychological stress and mitochondria: a systematic review. Psychosom Med 80:141-53. - »Bioblast link«
- Ref 355 Copied by: Picard M, Prather AA, Puterman E, Cuillerier A, Coccia M, Aschbacher K, Burelle Y, Epel ES (2018) A mitochondrial health index sensitive to mood and caregiving stress. Biol Psychiatry 84:9-17. - »Bioblast link«
- Ref 353 Copied by: Karan KR, Trumpff C, McGill MA, Thomas JE, Sturm G, Lauriola V, Sloan RP, Rohleder N, Kaufman BA, Marsland AL, Picard M (2020) Mitochondrial respiratory capacity modulates LPS-induced inflammatory signatures in human blood. Brain Behav Immun Health 5:100080. - »Bioblast link«
- Ref 350 Copied by: Bindra S, McGill MA, Triplett MK, Tyagi A, Thaker PH, Dahmoush L, Goodheart MJ, Ogden RT, Owusu-Ansah E, R Karan K, Cole S, Sood AK, Lutgendorf SK, Picard M (2021) Mitochondria in epithelial ovarian carcinoma exhibit abnormal phenotypes and blunted associations with biobehavioral factors. Sci Rep 11:11595. - »Bioblast link«
- Ref 356 Copied by: Rausser S, Trumpff C, McGill MA, Junker A, Wang W, Ho SH, Mitchell A, Karan KR, Monk C, Segerstrom SC, Reed RG, Picard M (2021) Mitochondrial phenotypes in purified human immune cell subtypes and cell mixtures. Elife 10:e70899. - »Bioblast link«
- Ref 228 Prasun P (2020) Role of mitochondria in pathogenesis of type 2 diabetes mellitus. J Diabetes Metab Disord 19:2017-22. - »Bioblast link«
- Ref 300 Rinaldo P, Matern D, Bennett MJ (2002) Fatty acid oxidation disorders. Annu Rev Physiol 64:477-502. - »Bioblast link«
- Ref 284 Bennett MJ, Sheng F, Saada A (2020) Biochemical assays of TCA cycle and β-oxidation metabolites. Methods Cell Biol 155:83-120. - »Bioblast link«
- Ref 97 Toleikis A, Trumbeckaite S, Liobikas J, Pauziene N, Kursvietiene L, Kopustinskiene DM (2020) Fatty acid oxidation and mitochondrial morphology changes as key modulators of the affinity for ADP in rat heart mitochondria. Cells 9:340. - »Bioblast link«
- Ref 237 Vockley J (2021) Inborn errors of fatty acid oxidation. In: Suchy FS, Sokol RJ, Balistreri WF (eds) Liver disease in children. Cambridge Univ Press:611-27. https://doi.org/10.1017/9781108918978.034 - »Bioblast link«
- Ref 240 Zhang X, Tomar N, Kandel SM, Audi SH, Cowley AW Jr, Dash RK (2021) Substrate- and calcium-dependent differential regulation of mitochondrial oxidative phosphorylation and energy production in the heart and kidney. Cells 11:131. - »Bioblast link«
From CGpDH and other pathways to FADH2 to CII
- Comment (Cardoso Luiza, Gnaiger Erich, 2023-08-06):
Fig. 9.19 from Blanco, Blanco (2017), Fig. 1 from Willson et al (2022), and Fig. 1 from Rai et al (2022) show FADH2 (1) to be formed in the mitochondrial matrix from GPDH, GPD2, or GPO1 (all indicating CGpDH) and from the TCA cycle (Fig. 1 Rai et al (2022)), then (2) feeding electrons further 'To respiratory chain', the 'ETC', or 'Electron Transport Chain' (ETS). Combined with FADH2 shown (1) to be formed in the mt-matrix from the TCA cycle and (2) feeding into CII (Fig. 1 from Koopman et al (2016); among >120 examples discussed as CII-ambiguities), one may arrive at the erroneous conclusion on a direct role of CII in the oxidation of glycerophosphate, analogous to false representations of CII involved in fatty acid oxidation.
- Ref 366 Blanco A, Blanco G (2017) Chapter 9 - Biological oxidations: bioenergetics. In Blanco A, Blanco G, eds, Medical biochemistry. Academic Press:177-204. - »Bioblast link«
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- Ref 368 Hashimoto T, Hussien R, Brooks GA (2006) Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am J Physiol Endocrinol Metab 290:E1237-44. - »Bioblast link«
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- Ref 371 Xiao W, Wang RS, Handy DE, Loscalzo J (2018) NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid Redox Signal 28:251–72. - »Bioblast link«
CII as a H+ pump
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- Ref 373 Dumollard R, Ward Z, Carroll J, Duchen MR (2007) Regulation of redox metabolism in the mouse oocyte and embryo. Development 134:455-65. - »Bioblast link«
- Ref 374 Jian C, Fu J, Cheng X, Shen LJ, Ji YX, Wang X, Pan S, Tian H, Tian S, Liao R, Song K, Wang HP, Zhang X, Wang Y, Huang Z, She ZG, Zhang XJ, Zhu L, Li H (2020) Low-dose sorafenib acts as a mitochondrial uncoupler and ameliorates nonalcoholic steatohepatitis. Cell Metab 31:892-908. - »Bioblast link«
- While CI functions as a proton pump, CII does not. Depicting CII as a proton pump would be analogous to falsely portraying FADH2 as the substrate of CII, as if it were a copy of CI, which functions as a proton pump with NADH as its substrate.
- Ref 304 Shirakawa R, Nakajima T, Yoshimura A, Kawahara Y, Orito C, Yamane M, Handa H, Takada S, Furihata T, Fukushima A, Ishimori N, Nakagawa M, Yokota I, Sabe H, Hashino S, Kinugawa S, Yokota T (2023) Enhanced mitochondrial oxidative metabolism in peripheral blood mononuclear cells is associated with fatty liver in obese young adults. Sci Rep 13:5203. - »Bioblast link«
- While CI functions as a proton pump, CII does not. Depicting CII as a proton pump would be analogous to falsely portraying FADH2 as the substrate of CII, as if it were a copy of CI, which functions as a proton pump with NADH as its substrate.
- Ref 342 Xing Yunxie (2022) Is genome instability a significant cause of aging? A review. Atlantis Press. - »Bioblast link«
- Bioblast links: Substrates and cofactors - >>>>>>> - Click on [Expand] or [Collapse] - >>>>>>>
- Cofactor
- » Cofactor
- » Coenzyme, cosubstrate
- » Nicotinamide adenine dinucleotide
- » Coenzyme Q2
- » Prosthetic group
- » Flavin adenine dinucleotide
- Cofactor
- Referennces
- » Gnaiger E (2023) Complex II ambiguities ― FADH2 in the electron transfer system. MitoFit Preprints 2023.3.v6. https://doi.org/10.26124/mitofit:2023-0003.v6
- Referennces
Cited by
- Gnaiger E (2024) Addressing the ambiguity crisis in bioenergetics and thermodynamics. MitoFit Preprints 2024.3. https://doi.org/10.26124/mitofit:2024-0003
Labels:
Enzyme: Complex II;succinate dehydrogenase
Ambiguity crisis, FAT4BRAIN, Publication:FAT4BRAIN, Gnaiger 2024 MitoFit