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Research Articles

Retrograde response to mitochondrial dysfunctions associated to LOF variations in FLAD1 exon 2: unraveling the importance of RFVT2

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Pages 511-525 | Received 08 Aug 2022, Accepted 04 Nov 2022, Published online: 08 Dec 2022

References

  • Gregersen N, Wintzensen H, Christensen SK, et al. C6-C10-dicarboxylic aciduria: investigations of a patient with riboflavin responsive multiple acyl-CoA dehydrogenation defects. Pediatr Res. 1982;16(10):861–868.
  • Olsen RK, Olpin SE, Andresen BS, et al. ETFDH mutations as a major cause of riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Brain. 2007;130(Pt 8):2045–2054.
  • Grunert SC. Clinical and genetical heterogeneity of late-onset multiple acyl-coenzyme A dehydrogenase deficiency. Orphanet J Rare Dis. 2014;9:117.
  • Wen B, Tang S, Lv X, et al. Clinical, pathological and genetic features and follow-up of 110 patients with late-onset MADD: a single-center retrospective study. Hum Mol Genet. 2022;31(7):1115–1129.
  • Horvath R. Update on clinical aspects and treatment of selected vitamin-responsive disorders II (riboflavin and CoQ 10). J Inherit Metab Dis. 2012;35(4):679–687.
  • Frerman FE, Goodman SI. Defects of electron transfer flavoprotein and electron transfer flavoprotein-ubiquinone oxidoreductase: glutaric acidemia type II. In: Valle D, Beaudet AL, Vogelstein B, Kinzler KW, Antonarakis SE, Ballabio A, Gibson KMG, editors. The metabolic and molecular basis of inherited diseases. 939 ed. New York (NY): McGraw-Hill; 2001. p. 2357–2365.
  • Cornelius N, Frerman FE, Corydon TJ, et al. Molecular mechanisms of riboflavin responsiveness in patients with ETF-QO variations and multiple acyl-CoA dehydrogenation deficiency. Hum Mol Genet. 2012;21(15):3435–3448.
  • Henriques BJ, Rodrigues JV, Olsen RK, et al. Role of flavinylation in a mild variant of multiple acyl-CoA dehydrogenation deficiency: a molecular rationale for the effects of riboflavin supplementation. J Biol Chem. 2009;284(7):4222–4229.
  • Barile M, Giancaspero TA, Leone P, et al. Riboflavin transport and metabolism in humans. J Inherit Metab Dis. 2016;39(4):545–557.
  • Ho G, Yonezawa A, Masuda S, et al. Maternal riboflavin deficiency, resulting in transient neonatal-onset glutaric aciduria Type 2, is caused by a microdeletion in the riboflavin transporter gene GPR172B. Hum Mutat. 2011;32(1):E1976–E1984.
  • Mosegaard S, Bruun GH, Flyvbjerg KF, et al. An intronic variation in SLC52A1 causes exon skipping and transient riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Mol Genet Metab. 2017;122(4):182–188.
  • Bosch AM, Abeling NG, Ijlst L, et al. Brown-Vialetto-Van Laere and Fazio Londe syndrome is associated with a riboflavin transporter defect mimicking mild MADD: a new inborn error of metabolism with potential treatment. J Inherit Metab Dis. 2011;34(1):159–164.
  • Green P, Wiseman M, Crow YJ, et al. Brown-Vialetto-Van Laere syndrome, a ponto-bulbar palsy with deafness, is caused by mutations in c20orf54. Am J Hum Genet. 2010;86(3):485–489.
  • Schiff M, Veauville-Merllie A, Su CH, et al. SLC25A32 mutations and riboflavin-responsive exercise intolerance. N Engl J Med. 2016;374(8):795–797.
  • Hellebrekers D, Sallevelt S, Theunissen TEJ, et al. Novel SLC25A32 mutation in a patient with a severe neuromuscular phenotype. Eur J Hum Genet. 2017;25(7):886–888.
  • Olsen RKJ, Koňaříková E, Giancaspero TA, et al. Riboflavin-responsive and -non-responsive mutations in FAD synthase cause multiple acyl-CoA dehydrogenase and combined respiratory-chain deficiency. Am J Hum Genet. 2016;98(6):1130–1145.
  • Tolomeo M, Nisco A, Leone P, et al. Development of novel experimental models to study flavoproteome alterations in human neuromuscular diseases: the effect of Rf therapy. IJMS. 2020;21(15):5310.
  • Brizio C, Galluccio M, Wait R, et al. Over-expression in Escherichia coli and characterization of two recombinant isoforms of human FAD synthetase. Biochem Biophys Res Commun. 2006;344(3):1008–1016.
  • Torchetti EM, Bonomi F, Galluccio M, et al. Human FAD synthase (isoform 2): a component of the machinery that delivers FAD to apo-flavoproteins. FEBS J. 2011;278(22):4434–4449.
  • Leone P, Galluccio M, Barbiroli A, et al. Bacterial production, characterization and protein modeling of a novel monofuctional isoform of FAD synthase in humans: an emergency protein? Molecules. 2018;23(1):116.
  • Torchetti EM, Brizio C, Colella M, et al. Mitochondrial localization of human FAD synthetase isoform 1. Mitochondrion. 2010;10(3):263–273.
  • Giancaspero TA, Busco G, Panebianco C, et al. FAD synthesis and degradation in the nucleus create a local flavin cofactor pool. J Biol Chem. 2013;288(40):29069–29080.
  • Tolomeo M, Nisco A, Barile M. Alteration of flavin cofactor homeostasis in human neuromuscular pathologies. Methods Mol Biol. 2021;2280:275–295.
  • Leone P, Galluccio M, Brizio C, et al. The hidden side of the human FAD synthase 2. Int J Biol Macromol. 2019;138:986–995.
  • Leone P, Galluccio M, Quarta S, et al. Mutation of aspartate 238 in FAD synthase isoform 6 increases the specific activity by weakening the FAD binding. IJMS. 2019;20(24):6203.
  • Ryder B, Tolomeo M, Nochi Z, et al. A novel truncating FLAD1 variant, causing multiple acyl-CoA dehydrogenase deficiency (MADD) in an 8-year-old boy. JIMD Rep. 2019;45:37–44.
  • Lee YJ, Kim SY, Kim MJ, et al. Infant with early onset bilateral facial and bulbar weakness: successful treatment of riboflavin in multiple acyl-CoA dehydrogenase deficiency caused by biallelic nonsense FLAD1 variants. Neuromuscul Disord. 2021;31(11):1194–1198.
  • Vengalil S, Polavarapu K, Preethish-Kumar V, et al. Mutation spectrum of primary lipid storage myopathies. Ann Indian Acad Neurol. 2022;25(1):106–113.
  • Leone P, Tolomeo M, Piancone E, et al. Mimicking human riboflavin responsive neuromuscular disorders by silencing flad-1 gene in C. elegans: alteration of vitamin transport and cholinergic transmission. IUBMB Life. 2022;74(7):672–683.
  • Bruni F, Manzari C, Filice M, et al. D-MTERF5 is a novel factor modulating transcription in Drosophila mitochondria. Mitochondrion. 2012;12(5):492–499.
  • Latronico T, Depalo N, Valente G, et al. Cytotoxicity study on luminescent nanocrystals containing phospholipid micelles in primary cultures of rat astrocytes. PLoS One. 2016;11(4):e0153451.
  • Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682.
  • Gerbino A, Maiellaro I, Carmone C, et al. Glucose increases extracellular [Ca2+] in rat insulinoma (INS-1E) pseudoislets as measured with Ca2+-sensitive microelectrodes. Cell Calcium. 2012;51(5):393–401.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
  • Latronico T, Larocca M, Milella S, et al. Neuroprotective potential of isothiocyanates in an in vitro model of neuroinflammation. Inflammopharmacology. 2021;29(2):561–571.
  • Di Bari G, Gentile E, Latronico T, et al. Inhibitory effect of aqueous extracts from marine sponges on the activity and expression of gelatinases A (MMP-2) and B (MMP-9) in rat astrocyte cultures. PLoS One. 2015;10(6):e0129322.
  • Picca A, Pesce V, Fracasso F, et al. Aging and calorie restriction oppositely affect mitochondrial biogenesis through TFAM binding at both origins of mitochondrial DNA replication in rat liver. PLoS One. 2013;8(9):e74644.
  • Pastukh VM, Gorodnya OM, Gillespie MN, et al. Regulation of mitochondrial genome replication by hypoxia: the role of DNA oxidation in D-loop region. Free Radic Biol Med. 2016;96:78–88.
  • Chimienti G, Picca A, Fracasso F, et al. The age-sensitive efficacy of calorie restriction on mitochondrial biogenesis and mtDNA damage in rat liver. IJMS. 2021;22(4):1665.
  • Capriglia F, Rizzo F, Petrosillo G, et al. Exploring the ability of LARS2 carboxy-terminal domain in rescuing the MELAS phenotype. Life. 2021;11(7):674.
  • Garcia-Villoria J, De Azua B, Tort F, et al. FLAD1, encoding FAD synthase, is mutated in a patient with myopathy, scoliosis and cataracts. Clin Genet. 2018;94(6):592–593.
  • Liuzzi VC, Giancaspero TA, Gianazza E, et al. Silencing of FAD synthase gene in Caenorhabditis elegans upsets protein homeostasis and impacts on complex behavioral patterns. Biochim Biophys Acta. 2012;1820(4):521–531.
  • Giancaspero TA, Wait R, Boles E, et al. Succinate dehydrogenase flavoprotein subunit expression in Saccharomyces cerevisiae–involvement of the mitochondrial FAD transporter, Flx1p. FEBS J. 2008;275(6):1103–1117.
  • Tzagoloff A, Jang J, Glerum DM, et al. FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J Biol Chem. 1996;271(13):7392–7397.
  • Giacomello M, Pyakurel A, Glytsou C, et al. The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol. 2020;21(4):204–224.
  • Kogot-Levin A, Saada A, Leibowitz G, et al. Upregulation of mitochondrial content in cytochrome c oxidase deficient fibroblasts. PLoS One. 2016;11(10):e0165417.
  • Yamada K, Ito M, Kobayashi H, et al. Flavin adenine dinucleotide synthase deficiency due to FLAD1 mutation presenting as multiple acyl-CoA dehydrogenation deficiency-like disease: a case report. Brain Dev. 2019;41(7):638–642.
  • Miccolis A, Galluccio M, Giancaspero TA, et al. Bacterial over-expression and purification of the 3'phosphoadenosine 5'phosphosulfate (PAPS) reductase domain of human FAD synthase: functional characterization and homology modeling. Int J Mol Sci. 2012;13(12):16880–16898.
  • Giancaspero TA, Dipalo E, Miccolis A, et al. Alteration of ROS homeostasis and decreased lifespan in S. cerevisiae elicited by deletion of the mitochondrial translocator FLX1. Biomed Res Int. 2014;2014:101286.
  • Zhang Y, Zhang M, Zhu W, et al. Succinate accumulation induces mitochondrial reactive oxygen species generation and promotes status epilepticus in the kainic acid rat model. Redox Biol. 2020;28:101365.
  • Ryoo IG, Kwak MK. Regulatory crosstalk between the oxidative stress-related transcription factor Nfe2l2/Nrf2 and mitochondria. Toxicol Appl Pharmacol. 2018;359:24–33.
  • Chimienti G, Picca A, Sirago G, et al. Increased TFAM binding to mtDNA damage hot spots is associated with mtDNA loss in aged rat heart. Free Radic Biol Med. 2018;124:447–453.
  • Picca A, Riezzo G, Lezza AMS, et al. Mitochondria and redox balance in coeliac disease: a case-control study. Eur J Clin Invest. 2018;48(2):e12877.
  • Chimienti G, Picca A, Fracasso F, et al. Differences in liver TFAM binding to mtDNA and mtDNA damage between aged and extremely aged rats. IJMS. 2019;20(10):2601.
  • Chimienti G, Pesce V, Fracasso F, et al. Deletion of OGG1 results in a differential signature of oxidized purine base damage in mtDNA regions. IJMS. 2019;20(13):3302.
  • Chimienti G, Orlando A, Russo F, et al. The mitochondrial trigger in an animal model of nonalcoholic fatty liver disease. Genes. 2021;12(9):1439.
  • Coppi L, Ligorio S, Mitro N, et al. PGC1s and beyond: disentangling the complex regulation of mitochondrial and cellular metabolism. IJMS. 2021;22(13):6913.
  • Ristow M, Schmeisser K. Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS). Dose Response. 2014;12(2):288–341.
  • Olsen RK, Cornelius N, Gregersen N. Redox signalling and mitochondrial stress responses; lessons from inborn errors of metabolism. J Inherit Metab Dis. 2015;38(4):703–719.

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