The MMACHC proteome: Hallmarks of functional cobalamin deficiency in humans

Molecular Genetics and Metabolism

Volumn 103, Issue 3, 2011, Pages 226-239

  Hannibal, Luciana ^a,b   DiBello, Patricia M ^a   Yu, Michelle ^a   Miller, Abby ^a   Wang, Sihe ^a   Willard, Belinda ^a   Rosenblatt, David S ^c   Jacobsen, Donald W ^a,b,d  

^a LERNER RESEARCH INSTITUTE   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CblC complementation group; Cobalamin deficiency; Cobalamin processing; Homocystinuria; Methylmalonic aciduria; MMACHC proteome

Indexed keywords

COBALAMIN; FOLIC ACID; HOMOCYSTEINE; HYDROXOCOBALAMIN; METHYLMALONIC ACID; PROTEOME;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYANOCOBALAMIN DEFICIENCY; CYTOSKELETON; ELECTROSPRAY MASS SPECTROMETRY; GENETIC ASSOCIATION; HOMOCYSTINURIA; HUMAN; HUMAN CELL; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; METHYLMALONIC ACIDURIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROBLAST; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

AMINO ACID METABOLISM, INBORN ERRORS; CARRIER PROTEINS; CELL LINE; CELLS, CULTURED; FIBROBLASTS; FOLIC ACID; HOMOCYSTEINE; HUMANS; HYDROXOCOBALAMIN; INTRACELLULAR SPACE; METABOLIC NETWORKS AND PATHWAYS; METHYLMALONIC ACID; MUTATION; PHENOTYPE; PROTEOME; VIMENTIN; VITAMIN B 12; VITAMIN B 12 DEFICIENCY; VITAMIN B COMPLEX;

EID: 79958039796     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2011.03.008     Document Type: Article

References (59)

1. Banerjee R., Chowdhury S. Methylmalonyl-CoA mutase. Chemistry and Biochemistry of B12 1999, 707-729. John Wiley & Sons, Inc., New York. R. Banerjee (Ed.).
2. Matthews R.G. Cobalamin-dependent methionine synthase. Chemistry and Biochemistry of B12 1999, 681-706. John Wiley & Sons, Inc., New York. R. Banerjee (Ed.).
3. Lerner-Ellis J.P., Tirone J.C., Pawelek P.D., Dore C., Atkinson J.L., Watkins D., Morel C.F., Fujiwara T.M., Moras E., Hosack A.R., Dunbar G.V., Antonicka H., Forgetta V., Dobson C.M., Leclerc D., Gravel R.A., Shoubridge E.A., Coulton J.W., Lepage P., Rommens J.M., Morgan K., Rosenblatt D.S. Identification of the gene responsible for methylmalonic aciduria and homocystinuria, cblC type. Nat. Genet. 2006, 38:93-100.
4. Kim J., Gherasim C., Banerjee R. Decyanation of vitamin B12 by a trafficking chaperone. Proc. Natl Acad. Sci. U. S. A. 2008, 105:14551-14554.
5. Hannibal L., Kim J., Brasch N.E., Wang S., Rosenblatt D.S., Banerjee R., Jacobsen D.W. Processing of alkylcobalamins in mammalian cells: A role for the MMACHC (cblC) gene product. Mol. Genet. Metab. 2009, 97:260-266.
6. Kim J., Hannibal L., Gherasim C., Jacobsen D.W., Banerjee R. A human vitamin B12 trafficking protein uses glutathione transferase activity for processing alkylcobalamins. J. Biol. Chem. 2009, 284:33418-33424.
7. Andersson H.C., Marble M., Shapira E. Long-term outcome in treated combined methylmalonic acidemia and homocystinemia. Genet. Med. 1999, 1:146-150.
8. Rosenblatt D.S., Fenton W.A. Inherited disorders of folate and cobalamin transport and metabolism. The Metabolic and Molecular Bases of Inherited Disease 2001, 3897-3933. Mc-Graw Hill, New York. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, B. Childs, K.W. Kinzler, B. Vogelstein (Eds.).
9. Shinnar S., Singer H.S. Cobalamin C mutation (methylmalonic aciduria and homocystinuria) in adolescence: A treatable cause of dementia and myelopathy. N. Engl. J. Med. 1984, 311:451-454.
10. Rosenblatt D.S., Aspler A.L., Shevell M.I., Pletcher B.A., Fenton W.A., Seashore M.R. Clinical heterogeneity and prognosis in combined methylmalonic aciduria and homocystinuria (cblC). J. Inherit. Metab. Dis. 1997, 20:528-538.
11. Lerner-Ellis J.P., Anastasio N., Liu J., Coelho D., Suormala T., Stucki M., Loewy A.D., Gurd S., Grundberg E., Morel C.F., Watkins D., Baumgartner M.R., Pastinen T., Rosenblatt D.S., Fowler B. Spectrum of mutations in MMACHC, allelic expression, and evidence for genotype-phenotype correlations. Hum. Mutat. 2009, 30:1072-1081.
12. Hannibal L., Axhemi A., Glushchenko A.V., Moreira E.S., Brasch N.E., Jacobsen D.W. Accurate assessment and identification of naturally occurring cellular cobalamins. Clin. Chem. Lab. Med. 2008, 46:1739-1746.
13. Jacobsen D.W., Gatautis V.J., Green R., Robinson K., Savon S.R., Secic M., Ji J., Otto J.M., Taylor L.M. Rapid HPLC determination of total homocysteine and other thiols in serum and plasma: Sex differences and correlation with cobalamin and folate levels in normal subjects. Clin. Chem. 1994, 40:873-881.
14. Hoffmann G., Aramaki S., Blum-Hoffmann E., Nyhan W.L., Sweetman L. Quantitative analysis for organic acids in biological samples: Batch isolation followed by gas chromatographic-mass spectrometric analysis. Clin. Chem. 1989, 35:587-595.
15. Marouga R., David S., Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382:669-678.
16. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
17. Karp N.A., Kreil D.P., Lilley K.S. Determining a significant change in protein expression with DeCyder during a pair-wise comparison using two-dimensional difference gel electrophoresis. Proteomics 2004, 4:1421-1432.
18. Suormala T., Baumgartner M.R., Coelho D., Zavadakova P., Kozich V., Koch H.G., Berghauser M., Wraith J.E., Burlina A., Sewell A., Herwig J., Fowler B. The cblD defect causes either isolated or combined deficiency of methylcobalamin and adenosylcobalamin synthesis. J. Biol. Chem. 2004, 279:42742-42749.
19. Mellman I., Willard H.F., Youngdahl-Turner P., Rosenberg L.E. Cobalamin coenzyme synthesis in normal and mutant human fibroblasts. J. Biol. Chem. 1979, 254:11847-11853.
20. Fenton W.A., Ambani L.M., Rosenberg L.E. Uptake of hydroxocobalamin by rat liver mitochondria. Binding to a mitochondrial protein. J. Biol. Chem. 1976, 251:6616-6623.
21. Fenton W.A., Rosenberg L.E. Mitochondrial metabolism of hydroxocobalamin: Synthesis of adenosylcobalamin by intact rat liver mitochondria. Arch. Biochem. Biophys. 1978, 189:441-447.
22. Loewy A.D., Niles K.M., Anastasio N., Watkins D., Lavoie J., Lerner-Ellis J.P., Pastinen T., Trasler J.M., Rosenblatt D.S. Epigenetic modification of the gene for the vitamin B12 chaperone MMACHC can result in increased tumorigenicity and methionine dependence. Mol. Genet. Metab. 2009, 96:261-267.
23. Tsai A.C., Morel C.F., Scharer G., Yang M., Lerner-Ellis J.P., Rosenblatt D.S., Thomas J.A. Late-onset combined homocystinuria and methylmalonic aciduria (cblC) and neuropsychiatric disturbance. Am. J. Med. Genet. A 2007, 143A:2430-2434.
24. Morel C.F., Lerner-Ellis J.P., Rosenblatt D.S. Combined methylmalonic aciduria and homocystinuria (cblC): Phenotype-genotype correlations and ethnic-specific observations. Mol. Genet. Metab. 2006, 88:315-321.
25. Guigonis V., Fremeaux-Bacchi V., Giraudier S., Favier R., Borderie D., Massy Z., Mougenot B., Rosenblatt D.S., Deschenes G. Late-onset thrombocytic microangiopathy caused by cblC disease: Association with a factor H mutation. Am. J. Kidney Dis. 2005, 45:588-595.
26. Harding C.O., Pillers D.A., Steiner R.D., Bottiglieri T., Rosenblatt D.S., Debley J., Michael Gibson K. Potential for misdiagnosis due to lack of metabolic derangement in combined methylmalonic aciduria/hyperhomocysteinemia (cblC) in the neonate. J. Perinatol. 2003, 23:384-386.
27. Bodamer O.A., Rosenblatt D.S., Appel S.H., Beaudet A.L. Adult-onset combined methylmalonic aciduria and homocystinuria (cblC). Neurology 2001, 56:1113.
28. Augoustides-Savvopoulou P., Mylonas I., Sewell A.C., Rosenblatt D.S. Reversible dementia in an adolescent with cblC disease: Clinical heterogeneity within the same family. J. Inherit. Metab. Dis. 1999, 22:756-758.
29. Enns G.M., Barkovich A.J., Rosenblatt D.S., Fredrick D.R., Weisiger K., Ohnstad C., Packman S. Progressive neurological deterioration and MRI changes in cblC methylmalonic acidaemia treated with hydroxocobalamin. J. Inherit. Metab. Dis. 1999, 22:599-607.
30. Rosenblatt D.S., Aspler A.L., Shevell M.I., Pletcher B.A., Fenton W.A., Seashore M.R. Clinical heterogeneity and prognosis in combined methylmalonic aciduria and homocystinuria (cblC). J. Inherit. Metab. Dis. 1997, 20:528-538.
31. Froese D.S., Zhang J., Healy S., Gravel R.A. Mechanism of vitamin B12-responsiveness in cblC methylmalonic aciduria with homocystinuria. Mol. Genet. Metab. 2009, 98:338-343.
32. Herbert V., Zalusky R. Interrelations of vitamin B12 and folic acid metabolism: Folic acid clearance studies. J. Clin. Investig. 1962, 41:1263-1276.
33. Richard E., Monteoliva L., Juarez S., Perez B., Desviat L.R., Ugarte M., Albar J.P. Quantitative analysis of mitochondrial protein expression in methylmalonic acidemia by two-dimensional difference gel electrophoresis. J. Proteome Res. 2006, 5:1602-1610.
34. Katula K.S., Heinloth A.N., Paules R.S. Folate deficiency in normal human fibroblasts leads to altered expression of genes primarily linked to cell signaling, the cytoskeleton and extracellular matrix. J. Nutr. Biochem. 2007, 18:541-552.
35. Majors A.K., Sengupta S., Jacobsen D.W., Pyeritz R.E. Upregulation of smooth muscle cell collagen production by homocysteine-insight into the pathogenesis of homocystinuria. Mol. Genet. Metab. 2002, 76:92-99.
36. Majors A., Ehrhart L.A., Pezacka E.H. Homocysteine as a risk factor for vascular disease. Enhanced collagen production and accumulation by smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 1997, 17:2074-2081.
37. Andersson H.C., Shapira E. Biochemical and clinical response to hydroxocobalamin versus cyanocobalamin treatment in patients with methylmalonic acidemia and homocystinuria (cblC). J. Pediatr. 1998, 132:121-124.
38. Perreau J., Lilienbaum A., Vasseur M., Paulin D. Nucleotide sequence of the human vimentin gene and regulation of its transcription in tissues and cultured cells. Gene 1988, 62:7-16.
39. Isoda K., Kagaya N., Akamatsu S., Hayashi S., Tamesada M., Watanabe A., Kobayashi M., Tagawa Y., Kondoh M., Kawase M., Yagi K. Hepatoprotective effect of vitamin B12 on dimethylnitrosamine-induced liver injury. Biol. Pharm. Bull. 2008, 31:309-311.
40. Wilson P.O., Barber P.C., Hamid Q.A., Power B.F., Dhillon A.P., Rode J., Day I.N., Thompson R.J., Polak J.M. The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Pathol. 1988, 69:91-104.
41. Doran J.F., Jackson P., Kynoch P.A., Thompson R.J. Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J. Neurochem. 1983, 40:1542-1547.
42. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: Dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 2002, 82:1524-1532.
43. Choi J., Levey A.I., Weintraub S.T., Rees H.D., Gearing M., Chin L.S., Li L. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 2004, 279:13256-13264.
44. Butterfield D.A., Gnjec A., Poon H.F., Castegna A., Pierce W.M., Klein J.B., Martins R.N. Redox proteomics identification of oxidatively modified brain proteins in inherited Alzheimer's disease: An initial assessment. J. Alzheimers Dis. 2006, 10:391-397.
45. Abou-Sleiman P.M., Healy D.G., Quinn N., Lees A.J., Wood N.W. The role of pathogenic DJ-1 mutations in Parkinson's disease. Ann. Neurol. 2003, 54:283-286.
46. Annesi G., Savettieri G., Pugliese P., D'Amelio M., Tarantino P., Ragonese P., La Bella V., Piccoli T., Civitelli D., Annesi F., Fierro B., Piccoli F., Arabia G., Caracciolo M., Ciro Candiano I.C., Quattrone A. DJ-1 mutations and parkinsonism-dementia-amyotrophic lateral sclerosis complex. Ann. Neurol. 2005, 58:803-807.
47. Kitamura K., Takayama M., Hamajima N., Nakanishi M., Sasaki M., Endo Y., Takemoto T., Kimura H., Iwaki M., Nonaka M. Characterization of the human dihydropyrimidinase-related protein 2 (DRP-2) gene. DNA Res. 1999, 6:291-297.
48. Appenzeller-Herzog C., Ellgaard L. The human PDI family: Versatility packed into a single fold. Biochim. Biophys. Acta 2008, 1783:535-548.
49. Gregersen N. Protein misfolding disorders: Pathogenesis and intervention. J. Inherit. Metab. Dis. 2006, 29:456-470.
50. Raynal P., Pollard H.B. Annexins: The problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1994, 1197:63-93.
51. Gerke V., Creutz C.E., Moss S.E. Annexins: Linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:449-461.
52. Grewal T., Enrich C. Molecular mechanisms involved in Ras inactivation: The annexin A6-p120GAP complex. Bioessays 2006, 28:1211-1220.
53. Stevens T.H., Forgac M. Structure, function and regulation of the vacuolar (H+)-ATPase. Annu. Rev. Cell Dev. Biol. 1997, 13:779-808.
54. Matus S., Glimcher L.H., Hetz C. Protein folding stress in neurodegenerative diseases: A glimpse into the ER. Curr. Opin. Cell Biol. 2011, 23:239-252.
55. Vidal R., Caballero B., Couve A., Hetz C. Converging pathways in the occurrence of endoplasmic reticulum (ER) stress in Huntington's disease. Curr. Mol. Med. 2011, 11:1-12.
56. Plenz G., Kugler S., Schnittger S., Rieder H., Fonatsch C., Muller P.K. The human vigilin gene: Identification, chromosomal localization and expression pattern. Hum. Genet. 1994, 93:575-582.
57. Takeshita H., Fujihara J., Takastuka H., Agusa T., Yasuda T., Kunito T. Diversity of glutathione S-transferase omega 1 (a140d) and 2 (n142d) gene polymorphisms in worldwide populations. Clin. Exp. Pharmacol. Physiol. 2009, 36:283-286.
58. Knoops B., Loumaye E., Van Der Eecken V. Evolution of the peroxiredoxins. Subcell. Biochem. 2007, 44:27-40.
59. Duthie S.J., Mavrommatis Y., Rucklidge G., Reid M., Duncan G., Moyer M.P., Pirie L.P., Bestwick C.S. The response of human colonocytes to folate deficiency in vitro: Functional and proteomic analyses. J. Proteome Res. 2008, 7:3254-3266.