New insights into the nutritional genomics of adult-onset riboflavin-responsive diseases

LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24:160–8.

Article  CAS  PubMed  Google Scholar 

Powers HJ. Riboflavin (vitamin B-2) and health. Am J Clin Nutr. 2003;77:1352–60.

Article  CAS  PubMed  Google Scholar 

NRV NRVfAaNZ-: Riboflavin. 2005.

Subramanian VS, Sabui S, Teafatiller T, Bohl JA, Said HM. Structure/functional aspects of the human riboflavin transporter-3 (SLC52A3): role of the predicted glycosylation and substrate-interacting sites. Am J Physiol Cell Physiol. 2017;313:C228–38.

Article  PubMed  PubMed Central  Google Scholar 

Lienhart WD, Gudipati V, Macheroux P. The human flavoproteome. Arch Biochem Biophys. 2013;535:150–62.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Barile M, Giancaspero TA, Leone P, Galluccio M, Indiveri C. Riboflavin transport and metabolism in humans. J Inherit Metab Dis. 2016;39:545–57.

Article  CAS  PubMed  Google Scholar 

Chiong MA, Sim KG, Carpenter K, Rhead W, Ho G, Olsen RK, Christodoulou J. Transient multiple acyl-CoA dehydrogenation deficiency in a newborn female caused by maternal riboflavin deficiency. Mol Genet Metab. 2007;92:109–14.

Article  CAS  PubMed  Google Scholar 

Liu Z, Peng Q, Li J, Rao C, Lu X. BVVLS2 overlooked for 3 years in a pediatric patient caused by novel compound heterozygous mutations in SLC52A2 gene. Clin Chim Acta. 2021;523:402–6.

Article  CAS  PubMed  Google Scholar 

Australian Health Survey: Usual Nutrient Intakes [ http://www.nrv.gov.au/nutrients/riboflavin]

Zempleni J, Galloway JR, McCormick DB. Pharmacokinetics of orally and intravenously administered riboflavin in healthy humans. Am J Clin Nutr. 1996;63:54–66.

Article  CAS  PubMed  Google Scholar 

Anderson JJ, Suchindran CM, Roggenkamp KJ. Micronutrient intakes in two US populations of older adults: lipid research clinics program prevalence study findings. J Nutr Health Aging. 2009;13:595–600.

Article  CAS  PubMed  Google Scholar 

Powers HJ, Hill MH, Mushtaq S, Dainty JR, Majsak-Newman G, Williams EA. Correcting a marginal riboflavin deficiency improves hematologic status in young women in the United Kingdom (RIBOFEM). Am J Clin Nutr. 2011;93:1274–84.

Article  CAS  PubMed  Google Scholar 

Australian Bureau of Statistics -, 2014, Australian Health Survey: Nutrition First Results - Foods and Nutrients, 2011–12 [https://www.abs.gov.au/statistics/health/health-conditions-and-risks/australian-health-survey-usual-nutrient-intakes/latest-release#vitamins]

Mosegaard S, Dipace G, Bross P, Carlsen J, Gregersen N, Olsen RKJ. Riboflavin deficiency—implications for general human health and inborn errors of metabolism. Int J Mol Sci. 2020;21(11):3847.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Murgia C, Adamski MM. Translation of nutritional genomics into nutrition practice: the next step. Nutrients. 2017;9(4):366.

Article  PubMed  PubMed Central  Google Scholar 

O’Callaghan B, Bosch AM, Houlden H. An update on the genetics, clinical presentation, and pathomechanisms of human riboflavin transporter deficiency. J Inherit Metab Dis. 2019;42:598–607.

Article  PubMed  Google Scholar 

Mosegaard S, Bruun GH, Flyvbjerg KF, Bliksrud YT, Gregersen N, Dembic M, Annexstad E, Tangeraas T, Olsen RKJ, Andresen BS. An intronic variation in SLC52A1 causes exon skipping and transient riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Mol Genet Metab. 2017;122:182–8.

Article  CAS  PubMed  Google Scholar 

Ho G, Yonezawa A, Masuda S, Inui K, Sim KG, Carpenter K, Olsen RK, Mitchell JJ, Rhead WJ, Peters G, Christodoulou J. 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:E1976-1984.

Article  CAS  PubMed  Google Scholar 

Vir SC, Love AH, Thompson W. Riboflavin status during pregnancy. Am J Clin Nutr. 1981;34:2699–705.

Article  CAS  PubMed  Google Scholar 

Bosch AM, Abeling NG, Ijlst L, Knoester H, van der Pol WL, Stroomer AE, Wanders RJ, Visser G, Wijburg FA, Duran M, Waterham HR. 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;34:159–64.

Article  CAS  PubMed  Google Scholar 

Bosch AM, Stroek K, Abeling NG, Waterham HR, Ijlst L, Wanders RJ. The Brown-Vialetto-Van Laere and Fazio Londe syndrome revisited: natural history, genetics, treatment and future perspectives. Orphanet J Rare Dis. 2012;7:83.

Article  PubMed  PubMed Central  Google Scholar 

Carreau C, Lenglet T, Mosnier I, Lahlou G, Fargeot G, Weiss N, Demeret S, Salachas F, Veauville-Merllie A, Acquaviva C, Nadjar Y. A juvenile ALS-like phenotype dramatically improved after high-dose riboflavin treatment. Ann Clin Transl Neurol. 2020;7:250–3.

Article  PubMed  PubMed Central  Google Scholar 

Foley AR, Menezes MP, Pandraud A, Gonzalez MA, Al-Odaib A, Abrams AJ, Sugano K, Yonezawa A, Manzur AY, Burns J, et al. Treatable childhood neuronopathy caused by mutations in riboflavin transporter RFVT2. Brain. 2014;137:44–56.

Article  PubMed  Google Scholar 

Carreau C, Benoit C, Ahle G, Cauquil C, Roubertie A, Lenglet T, Cosgrove J, Meunier I, Veauville-Merllié A, Acquaviva-Bourdain C, Nadjar Y. Late-onset riboflavin transporter deficiency: a treatable mimic of various motor neuropathy aetiologies. J Neurol Neurosurg Psychiatry. 2021;92(1):27–35.

Article  Google Scholar 

Cosgrove J, Datta S, Busby M. Adult onset Brown–Vialetto–Van Laere syndrome with opsoclonus and a novel heterozygous mutation: a case report. Clin Neurol Neurosurg. 2015;128:1–3.

Article  PubMed  Google Scholar 

Camargos S, Guerreiro R, Bras J, Mageste LS. Late-onset and acute presentation of Brown–Vialetto–Van Laere syndrome in a Brazilian family. Neurol Genet. 2018;4:e215.

Article  PubMed  PubMed Central  Google Scholar 

Udhayabanu T, Subramanian VS, Teafatiller T, Gowda VK, Raghavan VS, Varalakshmi P, Said HM, Ashokkumar B. SLC52A2 [p.P141T] and SLC52A3 [p.N21S] causing Brown–Vialetto–Van Laere syndrome in an indian patient: first genetically proven case with mutations in two riboflavin transporters. Clin Chim Acta. 2016;462:210–4.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bashford JA, Chowdhury FA, Shaw CE. Remarkable motor recovery after riboflavin therapy in adult-onset Brown–Vialetto–Van Laere syndrome. Pract Neurol. 2017;17:53–6.

Article  PubMed  Google Scholar 

Spaan AN, Ijlst L, van Roermund CW, Wijburg FA, Wanders RJ, Waterham HR. Identification of the human mitochondrial FAD transporter and its potential role in multiple acyl-CoA dehydrogenase deficiency. Mol Genet Metab. 2005;86:441–7.

Article  CAS  PubMed  Google Scholar 

Peng MZ, Shao YX, Li XZ, Zhang KD, Cai YN, Lin YT, Jiang MY, Liu ZC, Su XY, Zhang W, et al. Mitochondrial FAD shortage in SLC25A32 deficiency affects folate-mediated one-carbon metabolism. Cell Mol Life Sci. 2022;79:375.

Article  CAS  PubMed  Google Scholar 

Schiff M, Veauville-Merllie A, Su CH, Tzagoloff A, Rak M, Ogier de Baulny H, Boutron A, Smedts-Walters H, Romero NB, Rigal O, et al. SLC25A32 mutations and riboflavin-responsive exercise intolerance. N Engl J Med. 2016;374:795–7.

Article  PubMed  PubMed Central  Google Scholar 

Al Shamsi B, Al Murshedi F, Al Habsi A, Al-Thihli K. Hypoketotic hypoglycemia without neuromuscular complications in patients with SLC25A32 deficiency. Eur J Hum Genet. 2022;30(8):976–9.

Article  CAS  PubMed  Google Scholar 

Yonezawa A, Inui K. Novel riboflavin transporter family RFVT/SLC52: identification, nomenclature, functional characterization and genetic diseases of RFVT/SLC52. Mol Aspects Med. 2013;34:693–701.

Article  CAS  PubMed  Google Scholar 

Miccolis A, Galluccio M, Giancaspero TA, Indiveri C, Barile M. 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;13:16880–98.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Giancaspero TA, Galluccio M, Miccolis A, Leone P, Eberini I, Iametti S, Indiveri C, Barile M. Human FAD synthase is a bi-functional enzyme with a FAD hydrolase activity in the molybdopterin binding domain. Biochem Biophys Res Commun. 2015;465:443–9.

Article  CAS  PubMed  Google Scholar 

Olsen RKJ, Konarikova E, Giancaspero TA, Mosegaard S, Boczonadi V, Matakovic L, Veauville-Merllie A, Terrile C, Schwarzmayr T, Haack TB, 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;98:1130–45.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Torchetti EM, Bonomi F, Galluccio M, Gianazza E, Giancaspero TA, Iametti S, Indiveri C, Barile M. Human FAD synthase (isoform 2): a component of the machinery that delivers FAD to apo-flavoproteins. FEBS J. 2011;278:4434–49.

Comments (0)

No login
gif