Remaining challenges in cellular flavin cofactor homeostasis and flavoprotein biogenesis

Frontiers in Chemistry

Volumn 3, Issue APR, 2015, Pages

  Giancaspero, Teresa A ^a   Colella, Matilde ^a   Brizio, Carmen ^a   Difonzo, Graziana ^a   Fiorino, Giuseppina M ^a   Leone, Piero ^a   Brandsch, Roderich ^b   Bonomi, Francesco ^c   Iametti, Stefania ^c   Barile, Maria ^a,d  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

^d CNR   (Italy)

Author keywords

Dimethylglycine dehydrogenase; FAD; FAD synthase; Flavinylation; Lysine specific demethylase 1; Mitochondria; Nucleus; Nutri epigenetics; Rat

Indexed keywords

EID: 84969533907     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2015.00030     Document Type: Article

References (56)

1. Bacher, A., Eberhardt, S., Fischer, M., Kis, K., and Richter, G. (2000). Biosynthesis of vitamin b2 (riboflavin). Annu. Rev. Nutr. 20, 153-167. doi: 10.1146/annurev.nutr.20.1.153
2. Bafunno, V., Giancaspero, T. A., Brizio, C., Bufano, D., Passarella, S., Boles, E., et al. (2004). Riboflavin uptake and FAD synthesis in Saccharomyces cerevisiae mitochondria: involvement of the Flx1p carrier in FAD export. J. Biol. Chem. 279, 95-102. doi: 10.1074/jbc.M308230200
3. Barile, M., Brizio, C., De Virgilio, C., Delfine, S., Quagliariello, E., and Passarella, S. (1997). Flavin adenine dinucleotide and flavin mononucleotide metabolism in rat liver-the occurrence of FAD pyrophosphatase and FMN phosphohydrolase in isolated mitochondria. Eur. J. Biochem. 249, 777-785. doi: 10.1111/j.1432-1033.1997.00777.x
4. Barile, M., Brizio, C., Valenti, D., De Virgilio, C., and Passarella, S. (2000). The riboflavin/FAD cycle in rat liver mitochondria. Eur. J. Biochem. 267, 4888-4900. doi: 10.1046/j.1432-1327.2000.01552.x
5. Barile, M., Giancaspero, T. A., Brizio, C., Panebianco, C., Indiveri, C., Galluccio, M., et al. (2013). Biosynthesis of flavin cofactors in man: implications in health and disease. Curr. Pharm. Des. 19, 2649-2675. doi: 10.2174/1381612811319140014
6. Barile, M., Passarella, S., Bertoldi, A., and Quagliariello, E. (1993). Flavin adenine dinucleotide synthesis in isolated rat liver mitochondria caused by imported flavin mononucleotide. Arch. Biochem. Biophys. 305, 442-447. doi: 10.1006/abbi.1993.1444
7. Bonomi, F., Iametti, S., Morleo, A., Ta, D., and Vickery, L. E. (2008). Studies on the mechanism of catalysis of iron-sulfur cluster transfer from IscU[2Fe2S] by HscA/HscB chaperones. Biochemistry 47, 12795-12801. doi: 10.1021/bi801565j
8. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
9. Brizio, C., Barile, M., and Brandsch, R. (2002). Flavinylation of the precursor of mitochondrial dimethylglycine dehydrogenase by intact and solubilised mitochondria. FEBS Lett. 522, 141-146. doi: 10.1016/S0014-5793(02)02927-7
10. Brizio, C., Brandsch, R., Bufano, D., Pochini, L., Indiveri, C., and Barile, M. (2004). Over-expression in Escherichia coli, functional characterization and refolding of rat dimethylglycine dehydrogenase. Protein Expr. Purif. 37, 434-442. doi: 10.1016/j.pep.2004.06.011
11. Brizio, C., Brandsch, R., Douka, M., Wait, R., and Barile, M. (2008). The purified recombinant precursor of rat mitochondrial dimethylglycine dehydrogenase binds FAD via an autocatalytic reaction. Int. J. Biol. Macromol. 42, 455-462. doi: 10.1016/j.ijbiomac.2008.03.001
12. Brizio, C., Galluccio, M., Wait, R., Torchetti, E. M., Bafunno, V., Accardi, R., et al. (2006). Over-expression in Escherichia coli and characterization of two recombinant isoforms of human FAD synthetase. Biochem. Biophys. Res. Commun. 344, 1008-1016. doi: 10.1016/j.bbrc.2006.04.003
13. Brizio, C., Giancaspero, T. A., Brandsch, R., and Barile, M. (2013). "Mitochondria-assisted flavinylation of recombinant rat dimethylglycine dehydrogenase, "Proceedings of 17th International Symposium on Flavins and Flavoproteins, IUMBM S3/2011, 24-29 July 2011, eds S. Miller, R. Hille, and B. Palfey (Berkeley, CA), 493-501. Publisher Lulu.com, NC.
14. Brizio, C., Otto, A., Brandsch, R., Passarella, S., and Barile, M. (2000). A protein factor of rat liver mitochondrial matrix involved in flavinylation of dimethylglycine dehydrogenase. Eur. J. Biochem. 267, 4346-4354. doi: 10.1046/j.1432-1327.2000.01464.x
15. Bruni, F., Manzari, C., Filice, M., Loguercio Polosa, P., Colella, M., Carmone, C., et al. (2012). D-MTERF5 is a novel factor modulating transcription in Drosophila mitochondria. Mitochondrion 12, 492-499. doi: 10.1016/j.mito.2012.06.010
16. Cardone, A., Lopez, F., Affortunato, F., Busco, G., Hofer, A. M., Mallamaci, R., et al. (2012). An aryleneethynylene fluorophore for cell membrane staining. Biochim. Biophys. Acta 1818, 2808-2817. doi: 10.1016/j.bbamem.2012.06.011
17. Casalin, P., Pollegioni, L., Curti, B., and Pilone Simonetta, M. (1991). A study on apoenzyme from Rhodotorula gracilis D-amino acid oxidase. Eur. J. Biochem. 197, 513-517. doi: 10.1111/j.1432-1033.1991.tb15939.x
18. Clealand, W. W. (1970). The Enzymes, 3rd Edn. Academic Press, 1-64.
19. Cook, R. J., Misono, K. S., and Wagner, C. (1985). The amino acid sequences of the flavin-peptides of dimethylglycine dehydrogenase and sarcosine dehydrogenase from rat liver mitochondria. J. Biol. Chem. 260, 12998-13002.
20. Da, G., Lenkart, J., Zhao, K., Shiekhattar, R., Cairns, B. R., and Marmorstein, R. (2006). Structure and function of the SWIRM domain, a conserved protein module found in chromatin regulatory complexes. Proc. Natl. Acad. Sci. U.S.A. 103, 2057-2062. doi: 10.1073/pnas.0510949103
21. Foley, A. R., Menezes, M. P., Pandraud, A., Gonzalez, M. A., Al-Odaib, A., Abrams, A. J., et al. (2014). Treatable childhood neuronopathy caused by mutations in riboflavin transporter RFVT2. Brain 137, 44-56. doi: 10.1093/brain/awt315
22. Galluccio, M., Brizio, C., Torchetti, E. M., Ferranti, P., Gianazza, E., Indiveri, C., et al. (2007). Over-expression in Escherichia coli, purification and characterization of isoform 2 of human FAD synthetase. Protein Expr. Purif. 52, 175-181. doi: 10.1016/j.pep.2006.09.002
23. Gerbino, A., Maiellaro, I., Carmone, C., Caroppo, R., Debellis, L., Barile, M., et al. (2012). Glucose increases extracellular [Ca2+] in rat insulinoma (INS-1E) pseudoislets as measured with Ca2+-sensitive microelectrodes. Cell Calcium 51, 393-401. doi: 10.1016/j.ceca.2012.01.002
24. Giancaspero, T. A., Busco, G., Panebianco, C., Carmone, C., Miccolis, A., Liuzzi, G. M., et al. (2013). FAD synthesis and degradation in the nucleus create a local flavin cofactor pool. J. Biol. Chem. 288, 29069-29080. doi: 10.1074/jbc.M113.500066
25. Giancaspero, T. A., Locato, V., de Pinto, M. C., De Gara, L., and Barile, M. (2009). The occurrence of riboflavin kinase and FAD synthetase ensures FAD synthesis in tobacco mitochondria and maintenance of cellular redox status. FEBS J. 276, 219-231. doi: 10.1111/j.1742-4658.2008.06775.x
26. Haack, T. B., Makowski, C., Yao, Y., Graf, E., Hempel, M., Wieland, T., et al. (2012). Impaired riboflavin transport due to missense mutations in SLC52A2 causes Brown-Vialetto-Van Laere syndrome. J. Inherit. Metab. Dis. 35, 943-948. doi: 10.1007/s10545-012-9513-y
27. Heikal, A. A. (2010). Intracellular coenzymes as natural biomarkers for metabolic activities and mitochondrial anomalies. Biomark. Med. 4, 241-263. doi: 10.2217/bmm.10.1
28. Hino, S., Sakamoto, A., Nagaoka, K., Anan, K., Wang, Y., Mimasu, S., et al. (2012). FAD-dependent lysine-specific demethylase-1 regulates cellular energy expenditure. Nat. Commun. 3:758. doi: 10.1038/ncomms1755
29. Huerta, C., Borek, D., Machius, M., Grishin, N. V., and Zhang, H. (2009). Structure and mechanism of a eukaryotic FMN adenylyltransferase. J. Mol. Biol. 389, 388-400. doi: 10.1016/j.jmb.2009.04.022
30. Joosten, V., and van Berkel, W. J. (2007). Flavoenzymes. Curr. Opin. Chem. Biol. 11, 195-202. doi: 10.1016/j.cbpa.2007.01.010
31. Kim, H. J., and Winge, D. R. (2013). Emerging concepts in the flavinylation of succinate dehydrogenase. Biochim. Biophys. Acta 1827, 627-636. doi: 10.1016/j.bbabio.2013.01.012
32. Lienhart, W. D., Gudipati, V., and Macheroux, P. (2013). The human flavoproteome. Arch. Biochem. Biophys. 535, 150-162. doi: 10.1016/j.abb.2013.02.015
33. Lin, J., Diamanduros, A., Chowdhury, S. A., Scelsa, S., Latov, N., and Sadiq, S. A. (2009). Specific electron transport chain abnormalities in amyotrophic lateral sclerosis. J. Neurol. 256, 774-782. doi: 10.1007/s00415-009-5015-8
34. Liuzzi, V. C., Giancaspero, T. A., Gianazza, E., Banfi, C., Barile, M., and De Giorgi, C. (2012). Silencing of FAD synthase gene in Caenorhabditis elegans upsets protein homeostasis and impacts on complex behavioral patterns. Biochim. Biophys. Acta 1820, 521-531. doi: 10.1016/j.bbagen.2012.01.012
35. Luka, Z., Moss, F., Loukachevitch, L. V., Bornhop, D. J., and Wagner, C. (2011). Histone demethylase LSD1 is a folate-binding protein. Biochemistry 50, 4750-4756. doi: 10.1021/bi200247b
36. Luka, Z., Pakhomova, S., Loukachevitch, L. V., Calcutt, M. W., Newcomer, M. E., and Wagner, C. (2014). Crystal structure of the histone lysine specific demethylase LSD1 complexed with tetrahydrofolate. Protein Sci. 23, 993-998. doi: 10.1002/pro.2469
37. Miccolis, A., Galluccio, M., Nitride, C., Giancaspero, T. A., Ferranti, P., Iametti, S., et al. (2014). Significance of redox-active cysteines in human FAD synthase isoform 2. Biochim. Biophys. Acta 1844, 2086-2095. doi: 10.1016/j.bbapap.2014.08.005
38. Nabokina, S. M., Subramanian, V. S., and Said, H. M. (2012). Effect of clinical mutations on functionality of the human riboflavin transporter-2 (hRFT-2). Mol. Genet. Metab. 105, 652-657. doi: 10.1016/j.ymgme.2011.12.021
39. Oka, M., and McCormick, D. B. (1987). Complete purification and general characterization of FAD synthetase from rat liver. J. Biol. Chem. 262, 7418-7422.
40. Orsomando, G., Cialabrini, L., Amici, A., Mazzola, F., Ruggieri, S., Conforti, L., et al. (2012). Simultaneous single-sample determination of NMNAT isozyme activities in mouse tissues. PLoS ONE 7:e53271. doi: 10.1371/journal.pone.0053271
41. Otto, A., Stoltz, M., Sailer, H. P., and Brandsch, R. (1996). Biogenesis of the covalently flavinylated mitochondrial enzyme dimethylglycine dehydrogenase. J. Biol. Chem. 271, 9823-9829. doi: 10.1074/jbc.271.16.9823
42. Padovani, D., and Banerjee, R. (2009). A rotary mechanism for coenzyme B(12) synthesis by adenosyltransferase. Biochemistry 48, 5350-5357. doi: 10.1021/bi900454s
43. Pallotta, M. L., Brizio, C., Fratianni, A., De Virgilio, C., Barile, M., and Passarella, S. (1998). Saccharomyces cerevisiae mitochondria can synthesise FMN and FAD from externally added riboflavin and export them to the extramitochondrial phase. FEBS Lett. 428, 245-249. doi: 10.1016/S0014-5793(98)00544-4
44. Patel, M., Vadlapatla, R. K., Pal, D., and Mitra, A. K. (2012). Molecular and functional characterization of riboflavin specific transport system in rat brain capillary endothelial cells. Brain Res. 1468, 1-10. doi: 10.1016/j.brainres.2012.05.052
45. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. doi: 10.1038/nmeth.2019
46. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., et al. (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953. doi: 10.1016/j.cell.2004.12.012
47. Srour, M., Putorti, M. L., Schwartzentruber, J., Bolduc, V., Shevell, M. I., Poulin, C., et al. (2014). Mutations in riboflavin transporter present with severe sensory loss and deafness in childhood. Muscle Nerve 50, 775-779. doi: 10.1002/mus.24224
48. Stojanovski, D., Muller, J. M., Milenkovic, D., Guiard, B., Pfanner, N., and Chacinska, A. (2008). The MIA system for protein import into the mitochondrial intermembrane space. Biochim. Biophys. Acta 1783, 610-617. doi: 10.1016/j.bbamcr.2007.10.004
49. Thorpe, C., Hoober, K. L., Raje, S., Glynn, N. M., Burnside, J., Turi, G. K., et al. (2002). Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch. Biochem. Biophys. 405, 1-12. doi: 10.1016/S0003-9861(02)00337-5
50. Tonazzi, A., Mantovani, C., Colella, M., Terenghi, G., and Indiveri, C. (2013). Localization of mitochondrial carnitine/acylcarnitine translocase in sensory neurons from rat dorsal root ganglia. Neurochem. Res. 38, 2535-2541. doi: 10.1007/s11064-013-1168-z
51. Torchetti, E. M., Bonomi, F., Galluccio, M., Gianazza, E., Giancaspero, T. A., Iametti, S., et al. (2011). Human FAD synthase (isoform 2): a component of the machinery that delivers FAD to apo-flavoproteins. FEBS J. 278, 4434-4449. doi: 10.1111/j.1742-4658.2011.08368.x
52. Torchetti, E. M., Brizio, C., Colella, M., Galluccio, M., Giancaspero, T. A., Indiveri, C., et al. (2010). Mitochondrial localization of human FAD synthetase isoform 1. Mitochondrion 10, 263-273. doi: 10.1016/j.mito.2009.12.149
53. Tu, B. P., Ho-Schleyer, S. C., Travers, K. J., and Weissman, J. S. (2000). Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290, 1571-1574. doi: 10.1126/science.290.5496.1571
54. Tyihak, E., Albert, L., Nemeth, Z. I., Katay, G., Kiraly-Veghely, Z., and Szende, B. (1998). Formaldehyde cycle and the natural formaldehyde generators and capturers. Acta Biol. Hung. 49, 225-238.
55. Yao, Y., Yonezawa, A., Yoshimatsu, H., Masuda, S., Katsura, T., and Inui, K. (2010). Identification and comparative functional characterization of a new human riboflavin transporter hRFT3 expressed in the brain. J. Nutr. 140, 1220-1226. doi: 10.3945/jn.110.122911
56. Ye, H., and Rouault, T. A. (2010). Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry 49, 4945-4956. doi: 10.1021/bi1004798