A defect in molybdenum cofactor binding causes an attenuated form of sulfite oxidase deficiency.
S-sulfocysteine
impaired maturation
isolated sulfite oxidase deficiency
molybdenum cofactor
sulfite oxidase
Journal
Journal of inherited metabolic disease
ISSN: 1573-2665
Titre abrégé: J Inherit Metab Dis
Pays: United States
ID NLM: 7910918
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
03
11
2021
received:
19
02
2021
accepted:
04
11
2021
pubmed:
7
11
2021
medline:
10
5
2022
entrez:
6
11
2021
Statut:
ppublish
Résumé
Isolated sulfite oxidase deficiency (ISOD) is a rare recessive and infantile lethal metabolic disorder, which is caused by functional loss of sulfite oxidase (SO) due to mutations of the SUOX gene. SO is a mitochondrially localized molybdenum cofactor (Moco)- and heme-dependent enzyme, which catalyzes the vital oxidation of toxic sulfite to sulfate. Accumulation of sulfite and sulfite-related metabolites such as S-sulfocysteine (SSC) are drivers of severe neurodegeneration leading to early childhood death in the majority of ISOD patients. Full functionality of SO is dependent on correct insertion of the heme cofactor and Moco, which is controlled by a highly orchestrated maturation process. This maturation involves the translation in the cytosol, import into the intermembrane space (IMS) of mitochondria, cleavage of the mitochondrial targeting sequence, and insertion of both cofactors. Moco insertion has proven as the crucial step in this maturation process, which enables the correct folding of the homodimer and traps SO in the IMS. Here, we report on a novel ISOD patient presented at 17 months of age carrying the homozygous mutation NM_001032386.2 (SUOX):c.1097G > A, which results in the expression of SO variant R366H. Our studies show that histidine substitution of Arg366, which is involved in coordination of the Moco-phosphate, causes a severe reduction in Moco insertion efficacy in vitro and in vivo. Expression of R366H in HEK SUOX
Substances chimiques
Coenzymes
0
Metalloproteins
0
Molybdenum Cofactors
0
Pteridines
0
Sulfites
0
Heme
42VZT0U6YR
Sulfite Oxidase
EC 1.8.3.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
169-182Informations de copyright
© 2021 The Authors. Journal of Inherited Metabolic Disease published by John Wiley & Sons Ltd on behalf of SSIEM.
Références
Schwarz G. Molybdenum Cofactor and Human Disease. Curr Opin Chem Biol. 2016;31:179-187.
Kappler U, Enemark JH. Sulfite-oxidizing enzymes. JBIC J Biol Inorg Chem. 2015;20(2):253-264.
Kohl JB, Mellis A-T, Schwarz G. Homeostatic impact of sulfite and hydrogen sulfide on cysteine catabolism. Br J Pharmacol. 2019;176(4):554-570.
Claerhout H, Witters P, Régal L, et al. Isolated sulfite oxidase deficiency. J Inherit Metab Dis. 2018;41(1):101-108.
Del Rizzo M, Burlina AP, Sass JO, et al. Metabolic stroke in a late-onset form of isolated sulfite oxidase deficiency. Mol Genet Metab. 2013;108(4):263-266.
Tian M, Qu Y, Huang L, et al. Stable clinical course in three siblings with late-onset isolated sulfite oxidase deficiency: a case series and literature review. BMC Pediatr. 2019;19(1):510.
Misko AL, Liang Y, Kohl JB, Eichler F. Delineating the phenotypic spectrum of sulfite oxidase and molybdenum cofactor deficiency. Neurol Genet. 2020;6(4):e486.
Bender D, Kaczmarek AT, Kuester S, Burlina AB, Schwarz G. Oxygen and nitrite reduction by heme-deficient sulphite oxidase in a patient with mild sulphite oxidase deficiency. J Inherit Metab Dis. 2020;43(4):748-757.
Kumar A, Dejanovic B, Hetsch F, et al. S-sulfocysteine/NMDA receptor-dependent signaling underlies neurodegeneration in molybdenum cofactor deficiency. J Clin Invest. 2017;127(12):4365-4378.
Abbas A-K, Xia W, Tranberg M, Wigström H, Weber SG, Sandberg M. S-sulfo-cysteine is an endogenous amino acid in neonatal rat brain but an unlikely mediator of cysteine neurotoxicity. Neurochem Res. 2008;33(2):301-307.
Wyse ATS, Grings M, Wajner M, Leipnitz G. The role of oxidative stress and bioenergetic dysfunction in sulfite oxidase deficiency: insights from animal models. Neurotox Res. 2019;35(2):484-494.
Touati G, Rusthoven E, Depondt E, et al. Dietary therapy in two patients with a mild form of sulphite oxidase deficiency. Evidence for clinical and biological improvement. J Inherit Metab Dis. 2000;23(1):45-53.
Del Rizzo M, Burlina AP, Sass JO, Beermann F, Zanco C, Cazzorla C, Bordugo A, Giordano L, Manara R, Burlina AB. Metabolic stroke in a late-onset form of isolated sulfite oxidase deficiency. Mol Genet Metab. 2013;108(4):263-266.
Tan W-H. Isolated sulfite oxidase deficiency: a case report with a novel mutation and review of the literature. Pediatrics. 2005;116(3):757-766.
Kisker C, Schindelin H, Pacheco A, et al. Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell. 1997;91(7):973-983.
Klein JM, Schwarz G. Cofactor-dependent maturation of mammalian sulfite oxidase links two mitochondrial import pathways. J Cell Sci. 2012;125(20):4876-4885.
Ono H, Ito A, Omura T. Biosynthesis of sulfite oxidase in rat liver-determination of the site of synthesis. J Biochem. 1982;91(1):107-116.
Bender D, Kaczmarek AT, Santamaria-Araujo JA, et al. Impaired mitochondrial maturation of sulfite oxidase in a patient with severe sulfite oxidase deficiency. Hum Mol Genet. 2019;28(17):2885-2899.
Hille R. The reaction mechanism of oxomolybdenum enzymes. Biochim Biophys Acta. 1994;1184(2-3):143-169.
Johnson JL, Coyne KE, Garrett RM, et al. Isolated sulfite oxidase deficiency: identification of 12 novel SUOX mutations in 10 patients. Hum Mutat. 2002;20(1):74-74.
Davis AC, Johnson-Winters K, Arnold AR, Tollin G, Enemark JH. Kinetic results for mutations of conserved residues H304 and R309 of human sulfite oxidase point to mechanistic complexities. Metallomics. 2014;6(9):1664-1670.
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680-685.
Kaczmarek AT, Strampraad MJF, Hagedoorn P-L, Schwarz G. Reciprocal regulation of sulfite oxidation and nitrite reduction by mitochondrial sulfite oxidase. Nitric Oxide. 2019;89:22-31.
Palmer T, Santini C-L, Iobbi-Nivol C, Eaves DJ, Boxer DH, Giordano G. Involvement of the narJ and mob gene products in distinct steps in the biosynthesis of the molybdo enzyme nitrate reductase in Escherichia coli. Mol Microbiol. 1996;20(4):875-884.
Hänzelmann P, Schwarz G, Mendel RR. Functionality of alternative splice forms of the first enzymes involved in human molybdenum cofactor biosynthesis. J Biol Chem. 2002;277(21):18303-18312.
Johnson JL, Hainline BE, Rajagopalan KV, Arison BH. The pterin component of the molybdenum factor. Structural characterization of two fluorescent derivatives. J Biol Chem. 1984;259(9):5414-5422.
Veldman A, Santamaria-Araujo JA, Sollazzo S, et al. Successful treatment of molybdenum cofactor deficiency type A with cPMP. Pediatrics. 2010;125(5):e1249-e1254.
Bamborschke D, Özdemir Ö, Kreutzer M, et al. Ultra-rapid emergency genomic diagnosis of Donahue syndrome in a preterm infant within 17 hours. Am J Med Genet A. 2021;185(1):90-96.
Houge G, Laner A, Cirak S, de Leeuw N, Scheffer H, den Dunnen JT. Stepwise ABC system for classification of any type of genetic variant. Eur J Hum Genet. 2021. https://doi.org/10.1038/s41431-021-00903-z
Leimkühler S, Rajagopalan KV. In vitro incorporation of nascent molybdenum cofactor into human sulfite oxidase. J Biol Chem. 2001;276(3):1837-1844.
Belaidi AA, Schwarz G. Metal insertion into the molybdenum cofactor: Product-substrate channelling demonstrates the functional origin of domain fusion in gephyrin. Biochem J. 2013;450(1):149-157.
Schlake T, Bode J. Use of mutated flp recognition target (FRT) sites for the exchange of expression cassettes at defined chromosomal loci. Biochemistry. 1994;33(43):12746-12751.
Kaczmarek AT, Bahlmann N, Thaqi B, May P, Schwarz G. Machine learning-based identification and characterization of 15 novel pathogenic SUOX missense mutations. Mol Genet Metab. 2021;134(1-2):188-194.
Rajapakshe A, Tollin G, Enemark JH. Kinetic and thermodynamic effects of mutations of human sulfite oxidase. Chem Biodivers. 2012;9(9):1621-1634.
Hahn A, Engelhard C, Reschke S, et al. Structural insights into the incorporation of the mo cofactor into sulfite oxidase from site-directed spin labeling. Angew Chemie Int Ed. 2015;54(40):11865-11869.
Ono H, Ito A. Evidence for participation of the inner membrane in the import of sulfite oxidase into the intermembrane space of liver mitochondria. Biochem Biophys Res Commun. 1982;107(1):258-264.
Ono H, Ito A. Transport of the precursor for sulfite oxidase into intermembrane space of liver mitochondria: characterization of import and processing activities. J Biochem. 1984;95(2):345-352.