Mitochondrial MTHFD2L is a dual redox cofactor-specific methylenetetrahydrofolate dehydrogenase/methenyltetrahydrofolate cyclohydrolase expressed in both adult and embryonic tissues

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15507-15517

  Shin, Minhye ^a   Bryant, Joshua D ^a   Momb, Jessica ^a   Appling, Dean R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNCTIONAL GROUPS; TUBES (COMPONENTS);

COFACTOR SPECIFICITY; CYCLOHYDROLASE; EMBRYONIC TISSUE; METABOLIC CONDITIONS; METHYL GROUP; ONE-CARBON UNITS; RAPID RESPONSE;

MITOCHONDRIA;

METHENYLTETRAHYDROFOLATE CYCLOHYDROLASE; METHYLENETETRAHYDROFOLATE DEHYDROGENASE; METHYLENETETRAHYDROFOLATE DEHYDROGENASE 2 LIKE; PHOSPHATE; UNCLASSIFIED DRUG;

ADULT; ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SPECIFICITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; LUNG; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE;

FOLATE METABOLISM; MITOCHONDRIAL METABOLISM; MULTIFUNCTIONAL ENZYMES; NAD; NEURODEVELOPMENT;

AGE FACTORS; ALTERNATIVE SPLICING; AMINOHYDROLASES; ANIMALS; FEMALE; FOLIC ACID; FORMATE-TETRAHYDROFOLATE LIGASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ISOENZYMES; MALE; METHYLENETETRAHYDROFOLATE DEHYDROGENASE (NADP); MICE; MICE, INBRED C57BL; MITOCHONDRIA; MULTIENZYME COMPLEXES; NAD; NADP; NEURAL TUBE; OXIDATION-REDUCTION; PREGNANCY; RATS; SUBSTRATE SPECIFICITY;

EID: 84901697497     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.555573     Document Type: Article

References (49)

1. Tibbetts, A. S., and Appling, D. R. (2010) Compartmentalization of mammalian folate-mediated one-carbon metabolism. Annu. Rev. Nutr. 30, 57-81
2. Walkup, A. S., and Appling, D. R. (2005) Enzymatic characterization of human mitochondrial C1-tetrahydrofolate synthase. Arch. Biochem. Biophys. 442, 196-205
3. Mejia, N. R., and MacKenzie, R. E. (1985) NAD-dependent methylenetetrahydrofolate dehydrogenase is expressed by immortal cells. J. Biol. Chem. 260, 14616-14620
4. Mejia, N. R., Rios-Orlandi, E. M., and MacKenzie, R. E. (1986) NAD-dependent methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase from ascites tumor cells: purification and properties. J. Biol. Chem. 261, 9509-9513
5. Mejia, N. R., and MacKenzie, R. E. (1988) NAD-dependent methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase in transformed cells is a mitochondrial enzyme. Biochem. Biophys. Res. Comm. 155, 1-6
6. Yang, X. M., and MacKenzie, R. E. (1993) NAD-dependent methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase is the mammalian homolog of the mitochondrial enzyme encoded by the yeast MIS1 gene. Biochemistry 32, 11118-11123
7. Pelletier, J. N., and MacKenzie, R. E. (1995) Binding and interconversion of tetrahydrofolates at a single site in the bifunctional methylenetetrahydrofolate dehydrogenase/cyclohydrolase. Biochemistry 34, 12673-12680
8. Pawelek, P. D., and MacKenzie, R. E. (1998) Methenyltetrahydrofolate cyclohydrolase is rate limiting for the enzymatic conversion of 10-formyltetrahydrofolate to 5,10- methylenetetrahydrofolate in bifunctional dehydrogenase- cyclohydrolase enzymes. Biochemistry 37, 1109-1115
9. Di Pietro, E., Wang, X. L., and MacKenzie, R. E. (2004) The expression of mitochondrial methylenetetrahydrofolate dehydrogenase-cyclohydrolase supports a role in rapid cell growth. Biochim. Biophys. Acta 1674, 78-84
10. Christensen, K. E., Mirza, I. A., Berghuis, A. M., and Mackenzie, R. E. (2005) Magnesium and phosphate ions enable NAD binding to methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase. J. Biol. Chem. 280, 34316-34323
11. Bolusani, S., Young, B. A., Cole, N. A., Tibbetts, A. S., Momb, J., Bryant, J. D., Solmonson, A., and Appling, D. R. (2011) Mammalian MTHFD2L Encodes a mitochondrial methylenetetrahydrofolate dehydrogenase isozyme expressed in adult tissues. J. Biol. Chem. 286, 5166-5174
12. Blakley, R. L. (1957) The interconversion of serine and glycine: preparation and properties of catalytic derivatives of pteroylglutamic acid. Biochem. J. 65, 331-342
13. Curthoys, N. P., and Rabinowitz, J. C. (1971) Formyltetrahydrofolate synthetase: binding of adenosine triphosphate and related ligands determined by partition equilibrium. J. Biol. Chem. 246, 6942-6952
14. Appling, D. R., and West, M. G. (1997) Monofunctional NAD-dependent, 5,10-methylenetetrahydrofolate dehydrogenase from Saccharomyces cerevisiae. Methods Enzymol. 281, 178-188
15. Kallen, R. G., and Jencks, W. P. (1966) The mechanism of the condensation of formaldehyde with tetrahydrofolic acid. J. Biol. Chem. 241, 5851-5863
16. Rabinowitz, J. C. (1963) Preparation and properties of 5,10-methenyltetrahydrofolic acid and 10-formyltetrahydrofolic acid. Methods Enzymol. 6, 814-815
17. Suliman, H. S., Sawyer, G. M., Appling, D. R., and Robertus, J. D. (2005) Purification and properties of cobalamin-independent methionine synthase from Candida albicans and Saccharomyces cerevisiae. Arch. Biochem. Biophys. 441, 56-63
18. Claros, M. G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786
19. Li, M. Z., and Elledge, S. J. (2007) Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4, 251-256
20. West, M. G., Barlowe, C. K., and Appling, D. R. (1993) Cloning and characterization of the Saccharomyces cerevisiae gene encoding NAD-dependent 5,10-methylenetetrahydrofolate dehydrogenase. J. Biol. Chem. 268, 153-160
21. Gietz, R. D., and Woods, R. A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96
22. Wagner, W., Breksa, A. P., 3rd, Monzingo, A. F., Appling, D. R., and Robertus, J. D. (2005) Kinetic and structural analysis of active site mutants of monofunctional NAD-dependent 5,10-methylenetetrahydrofolate dehydrogenase from Saccharomyces cerevisiae. Biochemistry 44, 13163-13171
23. Palmer, K. F., and Williams, D. (1974) Optical properties of water in the near infrared. J. Opt. Soc. Am. 64, 1107-1110
24. Barlowe, C. K., and Appling, D. R. (1990) Isolation and characterization of a novel eukaryotic monofunctionalNAD+-dependent 5,10- methylenetetrahydrofolate dehydrogenase. Biochemistry 29, 7089-7094
25. Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., and Madden, T. L. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134
26. Willems, E., Mateizel, I., Kemp, C., Cauffman, G., Sermon, K., and Leyns, L. (2006) Selection of reference genes in mouse embryos and in differentiating human and mouse ES cells. Int. J. Dev. Biol. 50, 627-635
27. Kouadjo, K. E., Nishida, Y., Cadrin-Girard, J. F., Yoshioka, M., and St- Amand, J. (2007) Housekeeping and tissue-specific genes in mouse tissues. BMC Genomics 8, 127
28. Pike, S. T., Rajendra, R., Artzt, K., and Appling, D. R. (2010) Mitochondrial C1-THF synthase (MTHFD1L) supports flow of mitochondrial one-carbon units into the methyl cycle in embryos. J. Biol. Chem. 285, 4612-4620
29. Kawai, J., Shinagawa, A., Shibata, K., Yoshinom M., Itoh, M., Ishii, Y., Arakawa, T., Hara, A., Fukunishi, Y., Konno, H., Adachi, J., Fukuda, S., Aizawa, K., Izawa, M., Nishi, K., Kiyosawa, H., Kondo, S., Yamanaka, I., Saito, T., Okazaki, Y., Gojobori, T., Bono, H., Kasukawa, T., Saito, R., Kadota, K., Matsuda, H., Ashburner, M., Batalov, S., Casavant, T., Fleischmann, W., Gaasterland, T., Gissi, C., King, B., Kochiwa, H., Kuehl, P., Lewis, S., Matsuo, Y., Nikaido, I., Pesole, G., Quackenbush, J., Schriml, L. M., Staubli, F., Suzuki, R., Tomita, M., Wagner, L., Washio, T., Sakai, K., Okido, T., Furuno, M., Aono, H., Baldarelli, R., Barsh, G., Blake, J., Boffelli, D., Bojunga, N., Carninci, P., de Bonaldo, M. F., Brownstein, M. J., Bult, C., Fletcher, C., Fujita, M., Gariboldi, M., Gustincich, S., Hill, D., Hofmann, M., Hume, D. A., Kamiya, M., Lee, N. H., Lyons, P., Marchionni, L., Mashima, J., Mazzarelli, J., Mombaerts, P., Nordone, P., Ring, B., Ringwald, M., Rodriguez, I., Sakamoto, N., Sasaki, H., Sato, K., Schönbach, C., Seya, T., Shibata, Y., Storch, K. F., Suzuki, H., Toyo-oka, K., Wang, K. H., Weitz, C., Whittaker, C., Wilming, L., Wynshaw-Boris, A., Yoshida, K., Hasegawa, Y., Kawaji, H., Kohtsuki, S., Hayashizaki, Y, RIKEN Genome Exploration Research Group Phase II Team, and the FANTOM Consortium (2001) Functional annotation of a full-length mouse cDNA collection. Nature 409, 685-690
30. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J.K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77, 51-59
31. Zhang, L., Joshi, A. K., and Smith, S. (2003) Cloning, expression, characterization, and interaction of two components of a human mitochondrial fatty acid synthase: malonyltransferase and acyl carrier protein. J. Biol. Chem. 278, 40067-40074
32. Prasannan, P., and Appling, D. R. (2009) Human mitochondrial C1-tetrahydrofolate synthase: submitochondrial localization of the full-length enzyme and characterization of a short isoform. Arch. Biochem. Biophys. 481, 86-93
33. Dihazi, H., Kessler, R., and Eschrich, K. (2001) One-step purification of recombinant yeast 6-phosphofructo-2-kinase after the identification of contaminants by MALDI-TOF MS. Protein Expr. Purif. 21, 201-209
34. Thigpen, A. E., West, M. G., and Appling, D. R. (1990) Rat C1-tetrahydrofolate synthase: cDNA isolation, tissue-specific levels of the mRNA, and expression of the protein in yeast. J. Biol. Chem. 265, 7907-7913
35. West, M. G., Horne, D. W., and Appling, D. R. (1996) Metabolic role of cytoplasmic isozymes of 5,10-methylenetetrahydrofolate dehydrogenase in Saccharomyces cerevisiae. Biochemistry 35, 3122-3132
36. Barlowe, C. K., and Appling, D. R. (1990) Molecular genetic analysis of Saccharomyces cerevisiae C1-tetrahydrofolate synthase mutants reveals a noncatalytic function of the ADE3 gene product and an additional folatedependent enzyme. Mol. Cell. Biol. 10, 5679-5687
37. Nijhout, H. F., Reed, M. C., Lam, S. L., Shane, B., Gregory, J. F., 3rd, and Ulrich, C. M. (2006) In silico experimentation with a model of hepatic mitochondrial folate metabolism. Theor. Biol. Med. Model. 3, 40
38. Seither, R. L., Trent, D. F., Mikulecky, D. C., Rape, T. J., and Goldman, I. D. (1989) Folate-pool interconversions and inhibition of biosynthetic processes after exposure of L1210 leukemia cells to antifolates: experimental and network thermodynamic analyses of the role of dihydrofolate polyglutamates in antifolate action in cells. J. Biol. Chem. 264, 17016-17023
39. Horne, D. W., Patterson, D., and Cook, R. (1989) Effect of nitrous oxide inactivation of vitamin B12-dependent methionine synthetase on the subcellular distribution of folate coenzymes in rat liver. Arch. Biochem. Biophys. 270, 729-733
40. Eto, I., and Krumdieck, C. L. (1982) Determination of three different pools of reduced one-carbon-substituted folates. III. Reversed-phase high-performance liquid chromatography of the azo dye derivatives of p-aminobenzoylpoly-γ-glutamates and its application to the study of unlabeled endogenous pteroylpolyglutamates of rat liver. Anal. Biochem. 120, 323-329
41. Veech, R. L. (1987) Pyridine nucleotides and control of metabolic processes, in Pyridine Nucleotide Coenzymes: Chemical, Biochemical, and Medical Aspects, Part B (Dolphin, D., Poulson, R., and Avramovic, O., eds) pp. 79-105, John Wiley & Sons, New York
42. Yang, H., Yang, T., Baur, J. A., Perez, E., Matsui, T., Carmona, J. J., Lamming, D. W., Souza-Pinto, N. C., Bohr, V. A., Rosenzweig, A., de Cabo, R., Sauve, A. A., and Sinclair, D. A. (2007) Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 130, 1095-1107
43. Sies, H. (1982) Nicotinamide nucleotide compartmentation, in Metabolic Compartmentation (Sies, H., ed) pp. 205-231, Academic Press, New York
44. Christensen, K. E., and MacKenzie, R. E. (2006) Mitochondrial one-carbon metabolism is adapted to the specific needs of yeast, plants and mammals. Bioessays 28, 595-605
45. Momb, J., Lewandowski, J. P., Bryant, J. D., Fitch, R., Surman, D. R., Vokes, S. A., and Appling, D. R. (2013) Deletion of Mthfd1l causes embryonic lethality and neural tube and craniofacial defects in mice. Proc. Natl. Acad. Sci. U.S.A. 110, 549-554
46. Alexiou, M., and Leese, H. J. (1992) Purine utilisation, de novo synthesis and degradation in mouse preimplantation embryos. Development 114, 185-192
47. Albe, K. R., Butler, M. H., and Wright, B. E. (1990) Cellular concentrations of enzymes and their substrates. J. Theor. Biol. 143, 163-195
48. Corkey, B. E., Duszynski, J., Rich, T. L., Matschinsky, B., and Williamson, J. R. (1986) Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J. Biol. Chem. 261, 2567-2574
49. Saleet Jafri, M., and Kotulska, M. (2006) Modeling the mechanism of metabolic oscillations in ischemic cardiac myocytes. J. Theor. Biol. 242, 801-817