Mutations in genes encoding the glycine cleavage system predispose to neural tube defects in mice and humans

Human Molecular Genetics

Volumn 21, Issue 7, 2012, Pages 1496-1503

  Narisawa, Ayumi ^a   Komatsuzaki, Shoko ^a   Kikuchi, Atsuo ^a   Niihori, Tetsuya ^a   Aoki, Yoko ^a   Fujiwara, Kazuko ^b   Tanemura, Mitsuyo ^c   Hata, Akira ^d   Suzuki, Yoichi ^d   Relton, Caroline L ^e   Grinham, James ^f   Leung, Kit Yi ^f   Partridge, Darren ^f   Robinson, Alexis ^f   Stone, Victoria ^f   Gustavsson, Peter ^g   Stanier, Philip ^f   Copp, Andrew J ^f   Greene, Nicholas D E ^f   Tominaga, Teiji ^a   Matsubara, Yoichi ^a   Kure, Shigeo ^a   more..

^a TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c Tanemura Women's Clinic   (Japan)

^d CHIBA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOMETHLYLTRANSFERASE; FOLIC ACID; GLYCINE CLEAVAGE SYSTEM; GLYCINE CLEAVAGE SYSTEM PROTEIN H; GLYCINE DEHYDROGENASE (DECARBOXYLATING); METHIONINE; UNCLASSIFIED DRUG;

ANENCEPHALUS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRANIORACHISCHISIS; DISEASE PREDISPOSITION; EMBRYO DEVELOPMENT; ENZYMATIC ASSAY; FOLATE METABOLISM; GENE MUTATION; HUMAN; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MOUSE; NEURAL TUBE DEFECT; NONHUMAN; PRIORITY JOURNAL; SPINA BIFIDA;

AMINOMETHYLTRANSFERASE; ANIMALS; GLYCINE DECARBOXYLASE COMPLEX; GLYCINE DECARBOXYLASE COMPLEX H-PROTEIN; GLYCINE DEHYDROGENASE (DECARBOXYLATING); HUMANS; MICE; MICE, KNOCKOUT; MUTATION; MUTATION, MISSENSE; NEURAL TUBE DEFECTS;

MUS;

EID: 84858189393     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr585     Document Type: Article

References (49)

1. Greene, N.D. and Copp, A.J. (2009) Development of the vertebrate central nervous system: formation of the neural tube. Prenatal Diag., 29, 303-311.
2. Harris, M.J. and Juriloff, D.M. (2007) Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects. Birth Defects Res. A Clin. Mol. Teratol., 79, 187-210.
3. Greene, N.D.E., Stanier, P. and Copp, A.J. (2009) Genetics of human neural tube defects. Hum. Mol. Genet., 18, R113-R129.
4. Au, K.S., Ashley-Koch, A. and Northrup, H. (2010) Epidemiologic and genetic aspects of spina bifida and other neural tube defects. Dev. Disabil. Res. Rev., 16, 6-15.
5. Harris, M.J. and Juriloff, D.M. (2010) An update to the list of mouse mutants with neural tube closure defects and advances toward a complete genetic perspective of neural tube closure. Birth Defects Res. A Clin. Mol. Teratol., 88, 653-669.
6. Copp, A.J. and Greene, N.D.E. (2010) Genetics and development of neural tube defects. J. Pathol., 220, 217-230.
7. Blom, H.J., Shaw, G.M., Den Heijer, M. and Finnell, R.H. (2006) Neural tube defects and folate: case far from closed. Nat. Rev. Neurosci., 7, 724-731.
8. Molloy, A.M., Brody, L.C., Mills, J.L., Scott, J.M. and Kirke, P.N. (2009) The search for genetic polymorphisms in the homocysteine/folate pathway that contribute to the etiology of human neural tube defects. Birth Defects Res. A Clin. Mol. Teratol., 85, 285-294.
9. Beaudin, A.E. and Stover, P.J. (2009) Insights into metabolic mechanisms underlying folate-responsive neural tube defects: a mini review. Birth Defects Res. A Clin. Mol. Teratol., 85, 274-284.
10. Tibbetts, A.S. and Appling, D.R. (2010) Compartmentalization of mammalian folate-mediated one-carbon metabolism. Annu. Rev. Nutr., 30, 57-81.
11. Boyles, A.L., Hammock, P. and Speer, M.C. (2005) Candidate gene analysis in human neural tube defects. Am. J. Med. Genet. C Semin. Med. Genet., 135, 9-23.
12. Shaw, G.M., Lu, W., Zhu, H., Yang, W., Briggs, F.B., Carmichael, S.L., Barcellos, L.F., Lammer, E.J. and Finnell, R.H. (2009) 118 SNPs of folate-related genes and risks of spina bifida and conotruncal heart defects. BMC Med. Genet., 10, 49.
13. Martinez, C.A., Northrup, H., Lin, J.I., Morrison, A.C., Fletcher, J.M., Tyerman, G.H. and Au, K.S. (2009) Genetic association study of putative functional single nucleotide polymorphisms of genes in folate metabolism and spina bifida. Am. J. Obstet. Gynecol., 201, 394-411.
14. Dunlevy, L.P.E., Chitty, L.S., Doudney, K., Burren, K.A., Stojilkovic-Mikic, T., Stanier, P., Scott, R., Copp, A.J. and Greene, N.D.E. (2007) Abnormal folate metabolism in foetuses affected by neural tube defects. Brain, 130, 1043-1049.
15. Parle-McDermott, A., Pangilinan, F., O'Brien, K.K., Mills, J.L., Magee, A.M., Troendle, J., Sutton, M., Scott, J.M., Kirke, P.N., Molloy, A.M. and Brody, L.C. (2009) A common variant in MTHFD1L is associated with neural tube defects and mRNA splicing efficiency. Hum. Mutat., 30, 1650-1656.
16. Kikuchi, G. (1973) The glycine cleavage system: composition, reaction mechanism, and physiological significance. Mol. Cell. Biochem., 1, 169-187.
17. Kure, S., Tada, K. and Narisawa, K. (1997) Nonketotic hyperglycinemia: biochemical, molecular, and neurological aspects. Jpn J. Hum. Genet, 42, 13-22.
18. Kure, S., Narisawa, K. and Tada, K. (1992) Enzymatic diagnosis of nonketotic hyperglycinemia with lymphoblasts. J. Pediatr., 120, 95-98.
19. Hayasaka, K., Tada, K., Kikuchi, G., Winter, S. and Nyhan, W.L. (1983) Nonketotic hyperglycinemia: two patients with primary defects of P-protein and T-protein, respectively, in the glycine cleavage system. Pediatr. Res., 17, 967-970.
20. Ichinohe, A., Kure, S., Mikawa, S., Ueki, T., Kojima, K., Fujiwara, K., Iinuma, K., Matsubara, Y. and Sato, K. (2004) Glycine cleavage system in neurogenic regions. Eur. J. Neurosci., 19, 2365-2370.
21. Toone, J.R., Applegarth, D.A., Kure, S., Coulter-Mackie, M.B., Sazegar, P., Kojima, K. and Ichinohe, A. (2002) Novel mutations in the P-protein (glycine decarboxylase) gene in patients with glycine encephalopathy (non-ketotic hyperglycinemia). Mol. Genet. Metab., 76, 243-249.
22. Sakata, Y., Owada, Y., Sato, K., Kojima, K., Hisanaga, K., Shinka, T., Suzuki, Y., Aoki, Y., Satoh, J., Kondo, H. et al. (2001) Structure and expression of the glycine cleavage system in rat central nervous system. Brain Res. Mol. Brain Res., 94, 119-130.
23. Fleming, A. and Copp, A.J. (1998) Embryonic folate metabolism and mouse neural tube defects. Science, 280, 2107-2109.
24. Applegarth, D.A., Toone, J.R. and Lowry, R.B. (2000) Incidence of inborn errors of metabolism in British Columbia, 1969-1996. Pediatrics, 105, e10.
25. Nyhan, W.L. (1989) Nonketotic hyperglycinemia. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic Basis of Inherited Disease. McGraw-Hill, Inc., New York, 743-753.
26. Kure, S., Kato, K., Dinopoulos, A., Gail, C., DeGrauw, T.J., Christodoulou, J., Bzduch, V., Kalmanchey, R., Fekete, G., Trojovsky, A. et al. (2006) Comprehensive mutation analysis of GLDC, AMT, and GCSH in nonketotic hyperglycinemia. Hum. Mutat., 27, 343-352.
27. Harris, M.J. (2008) Insights into prevention of human neural tube defects by folic acid arising from consideration of mouse mutants. Birth Defects Res. A Clin. Mol. Teratol., 85, 331-339.
28. Watanabe, M., Osada, J., Aratani, Y., Kluckman, K., Reddick, R., Malinow, M.R. and Maeda, N. (1995) Mice deficient in cystathionine b-synthase: animal models for mild and severe homocyst(e)inemia. Proc. Natl Acad. Sci. USA, 92, 1585-1589.
29. Champion, K.M., Cook, R.J., Tollaksen, S.L. and Giometti, C.S. (1994) Identification of a heritable deficiency of the folate-dependent enzyme 10-formyltetrahydrofolate dehydrogenase in mice. Proc. Natl Acad. Sci. USA, 91, 11338-11342.
30. Chen, Z., Karaplis, A.C., Ackerman, S.L., Pogribny, I.P., Melnyk, S., Lussier-Cacan, S., Chen, M.F., Pai, A., John, S.W., Smith, R.S. et al. (2001) Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum. Mol. Genet., 10, 433-443.
31. MacFarlane, A.J., Liu, X., Perry, C.A., Flodby, P., Allen, R.H., Stabler, S.P. and Stover, P.J. (2008) Cytoplasmic serine hydroxymethyltransferase regulates the metabolic partitioning of methylenetetrahydrofolate but is not essential in mice. J. Biol. Chem., 283, 25846-25853.
32. Di, P.E., Sirois, J., Tremblay, M.L. and Mackenzie, R.E. (2002) Mitochondrial NAD-dependent methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase is essential for embryonic development. Mol. Cell. Biol., 22, 4158-4166.
33. Swanson, D.A., Liu, M.L., Baker, P.J., Garrett, L., Stitzel, M., Wu, J.M., Harris, M., Banerjee, R., Shane, B. and Brody, L.C. (2001) Targeted disruption of the methionine synthase gene in mice. Mol. Cell. Biol., 21, 1058-1065.
34. Elmore, C.L., Wu, X., Leclerc, D., Watson, E.D., Bottiglieri, T., Krupenko, N.I., Krupenko, S.A., Cross, J.C., Rozen, R., Gravel, R.A. and Matthews, R.G. (2007) Metabolic derangement of methionine and folate metabolism in mice deficient in methionine synthase reductase. Mol. Genet. Metab., 91, 85-97.
35. Field, M.S., Anderson, D.D. and Stover, P.J. Mthfs is an essential gene in mice and a component of the purinosome. Front. Genet. http://www.frontiersin.org/nutrigenomics/10.3389/fgene.2011.00036/abstract.
36. Spiegelstein, O., Mitchell, L.E., Merriweather, M.Y., Wicker, N.J., Zhang, Q., Lammer, E.J. and Finnell, R.H. (2004) Embryonic development of folate binding protein-1 (Folbp1) knockout mice: effects of the chemical form, dose, and timing of maternal folate supplementation. Dev. Dyn., 231, 221-231.
37. Burren, K.A., Savery, D., Massa, V., Kok, R.M., Scott, J.M., Blom, H.J., Copp, A.J. and Greene, N.D.E. (2008) Gene-environment interactions in the causation of neural tube defects: folate deficiency increases susceptibility conferred by loss of Pax3 function. Hum. Mol. Genet., 17, 3675-3685.
38. Beaudin, A.E., Abarinov, E.V., Noden, D.M., Perry, C.A., Chu, S., Stabler, S.P., Allen, R.H. and Stover, P.J. (2011) Shmt1 and de novo thymidylate biosynthesis underlie folate-responsive neural tube defects in mice. Am. J. Clin. Nutr., 93, 789-798.
39. Nijhout, H.F., Reed, M.C., Lam, S.L., Shane, B., Gregory, J.F. III and Ulrich, C.M. (2006) In silico experimentation with a model of hepatic mitochondrial folate metabolism. Theor. Biol. Med. Model., 3, 40.
40. Pike, S.T., Rajendra, R., Artzt, K. and Appling, D.R. (2010) Mitochondrial C1-tetrahydrofolate synthase (MTHFD1L) supports the flow of mitochondrial one-carbon units into the methyl cycle in embryos. J. Biol. Chem., 285, 4612-4620.
41. Dunlevy, L.P.E., Burren, K.A., Mills, K., Chitty, L.S., Copp, A.J. and Greene, N.D.E. (2006) Integrity of the methylation cycle is essential for mammalian neural tube closure. Birth Defects Res. A, 76, 544-552.
42. Greene, N.D., Stanier, P. and Moore, G.E. (2011) The emerging role of epigenetic mechanisms in the aetiology of neural tube defects. Epigenetics, 6, 875-893.
43. Apostolidou, S., Abu-Amero, S., O'Donoghue, K., Frost, J., Olafsdottir, O., Chavele, K.M., Whittaker, J.C., Loughna, P., Stanier, P. and Moore, G.E. (2007) Elevated placental expression of the imprinted PHLDA2 gene is associated with low birth weight. J. Mol. Med., 85, 379-387.
44. Niwa, H., Yamamura, K. and Miyazaki, J. (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene, 108, 193-199.
45. Oda, M., Kure, S., Sugawara, T., Yamaguchi, S., Kojima, K., Shinka, T., Sato, K., Narisawa, A., Aoki, Y., Matsubara, Y. et al. (2007) Direct correlation between ischemic injury and extracellular glycine concentration in mice with genetically altered activities of the glycine cleavage multienzyme system. Stroke, 38, 2157-2164.
46. Fujiwara, K., Okamura-Ikeda, K. and Motokawa, Y. (1991) Lipoylation of H-protein of the glycine cleavage system. The effect of site-directed mutagenesis of amino acid residues around the lipoyllysine residue on the lipoate attachment. FEBS Lett., 293, 115-118.
47. Wlodarczyk, B.J., Tang, L.S., Triplett, A., Aleman, F. and Finnell, R.H. (2006) Spontaneous neural tube defects in splotch mice supplemented with selected micronutrients. Toxicol. Appl. Pharmacol., 213, 55-63.
48. Essien, F.B. and Wannberg, S.L. (1993) Methionine but not folinic acid or vitamin B-12 alters the frequency of neural tube defects in Axd mutant mice. J. Nutr., 123, 27-34.
49. Nakai, T., Nakagawa, N., Maoka, N., Masui, R., Kuramitsu, S. and Kamiya, N. (2005) Structure of P-protein of the glycine cleavage system: implications for nonketotic hyperglycinemia. EMBO J., 24, 1523-1536.