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SDH5 , a Gene Required for Flavination of Succinate Dehydrogenase, Is Mutated in Paraganglioma
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Tapping the Mitochondrial Proteome: Mitochondria produce the energy that cells need to survive, function, and divide. A growing list of human disorders has been traced to defects in mitochondrial function. About 300 mammalian mitochondrial proteins are functionally uncharacterized, and Hao et al. (p. 1139 , published online 23 July) reasoned that the most highly conserved proteins within this group might provide insights into human disease. A combination of bioinformatics, yeast genetics, biochemistry, and human genetics was used to show that a previously uncharacterized mitochondrial protein (Sdh5) is required for the activity of respiratory complex II. Inactivating mutations in the human gene encoding SDH5 were found in individuals with hereditary paraganglioma, a rare neuroendocrine tumor. Thus, analysis of a mitochondrial protein in yeast has revealed a human tumor susceptibility gene.
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“Despite ubiquitous expression of the metabolic enzyme succinate dehydrogenase (SDH), germline mutations in subunits of this complex cause cancer only in a few sites, including neuroendocrine tissues (paraganglioma), the adrenal gland (pheochromocytoma), and the stomach and small intestine (gastrointestinal stromal tumors) (8–10).”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [10]
In the citing paper
“Germline SDH mutations have been identified in the SDH subunits SDHA–SDHD and also in SDH assembly factor 2 in tumor predisposition syndromes (Hao et al., 2009; Korpershoek et al., 2011; Neumann et al., 2004; Niemann and Müller, 2000; Oudijk et al., 2013; Pollard et al., 2005; Ricketts et al., 2008; Ricketts et al., 2010).”
From SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways (2013) · cites this paper as Hao et al., 2009
In the citing paper
“Consistently, heterozygous germline mutations in genes encoding the TCA cycle enzymes involved in the breakdown of these metabolites—SDH and FH—have been shown to facilitate the pathogenesis of certain rare cancers (e.g., paragangliomas) and inherited cancer-predisposition syndromes (181, 182, 183).”
From Regulation and function of the mammalian tricarboxylic acid cycle (2023) · cites this paper as [182]
In the citing paper
“Loss-of-function mutations have been identified in all four subunits of the SDH complex (Baysal, 2008; Burnichon et al., 2010), and in SDH5, which encodes a protein involved in incorporation of SDH’s flavin adenine dinucleotide cofactor (Hao et al., 2009).”
From Cellular Metabolism and Disease: What Do Metabolic Outliers Teach Us? (2012) · cites this paper as Hao et al., 2009
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“As this complex exists independent of all other SDH subunits and accumulates in strains that prevent SDH assembly, it is clear that the actions of Sdh5 and the process of flavinylation are early steps in the SDH assembly pathway (Hao et al., 2009; Kim et al., 2012).”
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“Around 30–40% of these tumors are genetically determined (1), and up to 10 susceptibility genes have now been described: the RET protooncogene (2) and the NF1 (3), VHL (4), SDHA (5), SDHB (6), SDHC (7), SDHD (8), SDHAF2 (9), TMEM127 (10), and MAX (11) tumor suppressor genes.”
BackgroundMitochondrial respiratory chain complexes: apoptosis sensors mutated in cancer?
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“(2010) identified in PGL a relatively rare mutation of SDHAF2 (SDH5), a SDH assembly factor involved in the addition of the flavin-adenine nucleotide (FAD) prosthetic group of SDHA (Hao et al., 2009; Bayley et al., 2010).”
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“Like bacterial SDH, human SDH is composed four subunits encoded by four distinct genes, SDHA, SDHB, SDHC and SDHD, and is activated by a newly discovered assembly factor, SDHAF2 (also known as SDH5) [42].”
BackgroundBayley, J., & Devilee, P. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.02.008 · Cited by 119
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“Mutations in genes coding subunits of succinate dehydrogenase (SDH) in the TCA cycle are associated with the development of paraganglioma and pheochromocytoma (Favier et al, 2005; Gottlieb and Tomlinson, 2005; Hao et al, 2009).”
BackgroundNa, U., Yu, W., Cox, J. E., Bricker, D. K., Brockmann, K., Rutter, J. P., Thummel, C. S., & Winge, D. R. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.05.014 · Cited by 114
“Cells lacking Sdh5 are compromised in Sdh1 flavinylation, leading to a reduced stability of Sdh1 (Hao et al., 2009; Kim et al., 2012).”
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“Moreover, LCA extends yeast chronological life span by altering the age-related dynamics of mitochondria-confined respiration and ROS production [86], both of which are integrated into convergent mechanisms underlying aging and cancer [24-32].”
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“Human l Metabolism 20, 241–252, August 5, 2014 ª2014 Elsevier Inc. 241 patients with loss-of-function mutations in SDHAF1 or SDHAF2 display reduced SDH complex levels and activity and present with infantile leukoencephalopathy and neuroendocrine tumors, respectively (Ghezzi et al., 2009; Hao et al., 2009).”
BackgroundInfluentialSelf-citationPheochromocytomas: The (pseudo)-hypoxia hypothesis
Favier, J., & Gimenez‐Roqueplo, A. (2010) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2010.10.004 · Cited by 117
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“Some cancer cells also exhibited Impaired mitochondria metabolism, including mutations of succinate dehydrogenase [14], fumerate hydratase [15], isocitrate dehydrogenase 2 [16-18] in Krebs cycle, and mutations in mictochondria DNA that affects respiratory chain, among others.”
BackgroundMitochondrial complex II, a novel target for anti-cancer agents
Kluckova, K., Bezawork-Geleta, A., Rohlena, J., Dong, L., & Neuzil, J. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.10.015 · Cited by 104
“SDH assembly factor-1 (SDHAF1) is required for the insertion of iron-sulfur clusters in SDHB [39] and SDHAF2, also known as SDH5, for the flavination of SDHA [36].”
InfluentialEvenepoel, L., Papathomas, T. G., Krol, N. M. G., Korpershoek, E., de Krijger, R. R., Persu, A., & Dinjens, W. N. M. (2014) · Genetics in Medicine · doi:10.1038/gim.2014.162 · Cited by 107
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“H2O2 is able to leave the mitochondrion (Bienert et al., 2007; Henzler and Steudle, 2000); therefore, the resulting reactive oxygen species that are measured using DCFDA can be assumed to be H2O2.”
BackgroundCurrent perspectives between metabolic syndrome and cancer
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“Furthermore certain types of cancer have been associated with some Tricarboxylic Acid Cycle (TCA) enzymes mutations, including isocitrate dehydrogenase (IDH1 and IDH2) [50], succinate dehydrogenase (SDH) and fumarate hydratase (FH) [51, 52].”
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“On the other hand, while a Utah group was working on characterization of mammalian mitochondrial proteome, they found in yeast model that SDH5 protein is heavily involved in flavination of SDHA subunit and its' mutation dramatically affects SDHA function (15).”
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“Furthermore, silencing of SDHD, SDHB, and SDHAF2 did not lead to increased trimethylation of H3K4 or H3K27 in HEK293 cells.”
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“The stronger, higher MW band represents FAD-Sdh1p and the lower migrating bands represent other mitochondrial flavoproteins.(47) Affinity assay data are represented as the band intensity of the predominant middle wash fraction (in most cases Wash 2B) compared with the band intensity of this wash fraction combined with…”
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BackgroundOncometabolites: A New Paradigm for Oncology, Metabolism, and the Clinical Laboratory
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“SDHAF1 is required for stable assembly of CII [Ghezzi et al., 2009] while SDH5 is required for covalent insertion of FAD into the catalytic SDHA subunit [Hao et al., 2009; Rutter et al., 2010].”
BackgroundGenetics of hereditary head and neck paragangliomas
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“These include mutations in isocitrate dehydrogenase (IDH1 and IDH2) [17], and in pathways affecting succinate dehydrogenase (SDH) and fumarate hydratase (FH) [18,19].”
BackgroundRespiratory chain complex II as general sensor for apoptosis
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“apparently a simple loss of function mutation in yeast [10], the recurrence of this mutation and absence of other mutations [8, 30] may suggest that the SDHAF2 protein with the specific p.”
BackgroundInfluentialSelf-citationGenetics and molecular pathogenesis of pheochromocytoma and paraganglioma
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“SDHAF2 Mutations in SDHAF2 cause Familial Paraganglioma type 2 (OMIM #601650) which is characterised by head and neck paragangliomas (Hao et al. 2009).”
BackgroundThe quinone-binding and catalytic site of complex II
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“Recently a new gene termed SDH5 which is an assembly factor required for the covalent-flavination of SdhA has also been shown to be associated with tumor formation [17] although the protein product of this gene is not assembled into the mature complex II.”
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Self-citationThe genomic landscape of phaeochromocytoma
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“PGL2 (MIM: 613019) is associated with mutations in the SDHAF2 gene, required for the flavination of SDH, and has similar clinical phenotype to PGL1 with the exception of adrenal PCC, which have not been reported (Hao et al., 2009).”
BackgroundMitochondrial Redox Signaling and Tumor Progression
Chen, Y., Zhang, H., Zhou, H. J., Ji, W., & Wang, M. (2016) · Cancers · doi:10.3390/cancers8040040 · Cited by 80
“Moreover, cancer-associated mutations have been identified in gene encoding for several metabolic enzymes such as succinate dehydrogenase (SDH), fumarate hydratase (FH), and isocitrate dehydrogenase (IDH), all enzymes of the tricarboxylic acid cycle (TCA cycle) in mitochondria [6,7].”
BackgroundCatalytic mechanisms of complex II enzymes: A structural perspective
Iverson, T. M. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.09.008 · Cited by 83
“The mechanism of covalent attachment of the FAD to the protein hasn’t been delineated, but FAD insertion may be facilitated by a complex II-specific assembly factor termed Sdh5 in yeast [32], and SdhE in bacteria [33].”
BackgroundThe management of head-and-neck paragangliomas
Capatina, C. A.-M., Ntali, G., Karavitaki, N., & Grossman, A. B. (2013) · Endocrine Related Cancer · doi:10.1530/erc-13-0223 · Cited by 79
“The causal mutation of the PGL-2 syndrome has only recently been described (SDHAF2 gene; Hao et al. 2009), is very rare (Bayley et al. 2010) and its transmission is also consistent with genomic imprinting (Kunst et al. 2011).”
BackgroundParagangliomas/Pheochromocytomas: Clinically Oriented Genetic Testing
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Clinical implications of the oncometabolite succinate in SDHx ‐mutation carriers
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“SDH5 is a gene required for flavination of SDH [4].”
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“However, flavinylation of succinate dehydrogenase (at His) was recently reported to require a specific protein (SdhE) as an FAD chaperone (20, 21).”
BackgroundHead and neck paragangliomas: genetic spectrum and clinical variability in 79 consecutive patients
Piccini, V., Rapizzi, E., Bacca, A., Trapani, G. D., Pulli, R., Giaché, V., Zampetti, B., Cordisco, E. L., Canu, L., Corsini, E., et al. (2012) · Endocrine Related Cancer · doi:10.1530/erc-11-0369 · Cited by 78
“2001); SDHC , located on 1q21 (Niemann & Mueller 2000); and SDHAF2 , located on 11q12, which is responsible for SDHA flavination (Hao et al .”
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Currás-Freixes, M., Piñeiro-Yáñez, E., Montero‐Conde, C., Apellániz-Ruiz, M., Calsina, B., Mančíková, V., Remacha, L., Richter, S., Ercolino, T., Rogowski-Lehmann, N., et al. (2017) · Journal of Molecular Diagnostics · doi:10.1016/j.jmoldx.2017.04.009 · Cited by 78
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The future of model organisms in human disease research
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“Jared Rutter's laboratory discovered that the yeast SDH5 gene (also known as EMI5 ), which is the homologue of the PGL2 gene mutated in the hereditary cancer paraganglioma, is required to modify key respiratory protein”
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“dehydrogenase assembly factor (SDHAF2) is required for SDH1 flavination in human and yeast (Hao et al., 2009).”
BackgroundMethodInfluentialPheochromocytoma and Paraganglioma
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“We note, however, that the Rutter group showed that apo-Sdh1 was relatively stable in flx1Δ cells, but lacking almost completely its flavinylation [12].”
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Renal cancer in von Hippel–Lindau disease and related syndromes
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Self-citationThe Tricarboxylic Acid Cycle at the Crossroad Between Cancer and Immunity
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“Later, mutations in SDHA and in SDHAF2 were associated with PGG/PHEO syndrome as well (10, 39, 60).”
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“Succinate dehydrogenase complex assembly factor 2 (SDHAF2)-mutated PPGLs have also been identified as part of cluster 1 (63).”
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Bezawork‐Geleta, A., Wen, H., Dong, L., Yan, B., Vider, J., Boukalová, Š., Krobova, L., Vanova, K. H., Zobalová, R., Sobol, M. A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04603-z · Cited by 73
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Phaeochromocytoma: a catecholamine and oxidative stress disorder
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Genetics of pheochromocytomas and paragangliomas
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Acetoacetate Accelerates Muscle Regeneration and Ameliorates Muscular Dystrophy in Mice
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“demonstrated that increases in the levels of these oncometabolites play causal roles in tumorigenesis (26-34).”
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“We were unable to detect a homolog of the assembly factor SDH5/ SDHAF that acts in flavin attachment to SDHA (Hao et al. 2009), suggesting that the CII of Mastigamoeba is unusual.”
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“[24].”
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Pheochromocytoma and Paraganglioma
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Carney triad can be (rarely) associated with germline succinate dehydrogenase defects
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Adrenal Medullary Hyperplasia Is a Precursor Lesion for Pheochromocytoma in MEN2 Syndrome
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“These include multiple endocrine neoplasia type 2 (MEN2) caused by germ-line activating rearranged during transfection (RET) proto-oncogene mutations, von Hippel-Lindau disease due to inactivating von HippelLindau gene mutations, neurofibromatosis type 1 as a result of neurofibromatosis type 1 gene inactivation, and t…”
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“Recently, mutations in Sdh5, a protein that associates with the SDH complex and may mediate incorporation of FAD, have been identified in familial paraganglioma (Hao et al .”
SDH5 mutations and familial paraganglioma: somewhere Warburg is smiling
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“1, which is the location for hSDH5.”
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“…years, mutations in the other three SDH genes (A, B and C) and its assembly factor (SDHAF2) were also observed, adding considerable evidential weight to SDHx genes being critical tumour suppressors linked to PPGL (Astuti et al. 2001; Burnichon et al. 2010; Hao et al. 2009; Niemann and Muller 2000).”
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“SDHB is the catalytic core component of heterotetrameric complex SDH, of which loss-of-function mutations lead to enzymatic dysfunction and are associated with cancer formation mostly reported in hereditary paragangliomas to date [7].”
BackgroundMyc-mediated SDHA acetylation triggers epigenetic regulation of gene expression and tumorigenesis
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Metadata
- Authors
- Hao, H.-X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J.-P., Kunst, H., Devilee, P., Cremers, C. W. R. J., Schiffman, J. D., Bentz, B. G., Gygi, S. P., Winge, D. R., Kremer, H., & Rutter, J.
- Affiliations
- University of Utah (US)
- Radboud University Medical Center (NL)
- Harvard University (US)
- Leiden University Medical Center (NL)
- Corresponding author
- Rutter, Jared
- ORCID
- Venue
- Science
- Published
- 2009-08-28
- Volume
- 325
- Issue
- 5944
- Pages
- 1139-1142
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3881419
- OpenAlex
- W2028117213
- Cited by
- 702
- References
- 26
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 12 · 2023: 26 · 2022: 31 · 2021: 29 · 2020: 37 · 2019: 39 · 2018: 38 · 2017: 47 · 2016: 42 · 2015: 48 · 2014: 64 · 2013: 68 · 2012: 76
- FWCI
- 65.83
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Lincoln (University of Nebraska) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM087346, GM087346)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK071962)
- National Institute of Environmental Health Sciences (R01ES003817)
- Topics
- Health Sciences › Medicine › Surgery › Adrenal and Paraganglionic Tumors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
- Keywords
- succinate dehydrogenase, flavin adenine dinucleotide, paraganglioma, hereditary paraganglioma, germline mutations, mitochondrial proteins, cancer susceptibility genes, mitochondrial electron transport chain, TCA cycle, yeast model
- MeSH terms
- Amino Acid Sequence, Cell Line, Flavin-Adenine Dinucleotide, Female, Flavoproteins, Haplotypes, Humans, Male, Mitochondria, Molecular Sequence Data, Oxygen Consumption, Paraganglioma, Pedigree, Saccharomyces cerevisiae, Succinate Dehydrogenase, Germ-Line Mutation, Protein Subunits, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins, Inheritance Patterns, Proteomics, Cell Line, Tumor
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