Novel insights on interactions between folate and lipid metabolism

BioFactors

Volumn 40, Issue 3, 2014, Pages 277-283

  da Silva, Robin P ^a   Kelly, Karen B ^a   Al Rajabi, Ala ^a   Jacobs, René L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Choline; Folate; NASH; One carbon metabolism; Phospholipids; Steatosis; Triacylglycerol

Indexed keywords

CARBON; CARNITINE; CREATINE; FOLIC ACID; LIPID; PHOSPHATIDYLCHOLINE;

ATHEROSCLEROSIS; CARBON METABOLISM; DNA METHYLATION; EPIGENETICS; FOLATE METABOLISM; FOLIC ACID DEFICIENCY; HORMONE SYNTHESIS; HUMAN; LIPID LIVER LEVEL; LIPID METABOLISM; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVIEW; ANIMAL; BLOOD; DIET SUPPLEMENTATION; DRUG EFFECTS; GENETIC EPIGENESIS; LIVER; METABOLISM; PHYSIOLOGY;

ANIMALS; ATHEROSCLEROSIS; DIETARY SUPPLEMENTS; EPIGENESIS, GENETIC; FOLIC ACID; HUMANS; LIPID METABOLISM; LIVER; OBESITY;

EID: 84902544544     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1154     Document Type: Review

References (76)

1. Brosnan, J. T. and Brosnan, M. E. (2006) The sulfur-containing amino acids: an overview. J. Nutr. 136, 1636S-1640S.
2. Tibbetts, A. S. and Appling, D. R. (2010) Compartmentalization of Mammalian folate-mediated one-carbon metabolism. Annu. Rev. Nutr. 30, 57-81.
3. Stover, P. J. and Field, M. S. (2011) Trafficking of intracellular folates. Adv. Nutr. 2, 325-331.
4. Clarke, S. and Banfield, K. (2001) S-adenosylmethionine-dependent methyltransferases. In Homocysteine in Health and Disease (Carmel, R. and Jacobsen, D. W., eds.). pp 63-78, Cambridge University Press, Cambridge.
5. Akesson, B., Fehling, C., Jagerstad, M., and Stenram, U. (1982) Effect of experimental folate deficiency on lipid metabolism in liver and brain. Br. J. Nutr. 47, 505-520.
6. Koteish, A. and Diehl, A. M. (2001) Animal models of steatosis. Semin. Liver Dis. 21, 89-104.
7. Rinella, M. E. and Green, R. M. (2004) The methionine-choline deficient dietary model of steatohepatitis does not exhibit insulin resistance. J. Hepatol. 40, 47-51.
8. Henkel, A. S., Dewey, A. M., Anderson, K. A., Olivares, S., and Green, R. M. (2012) Reducing endoplasmic reticulum stress does not improve steatohepatitis in mice fed a methionine- and choline-deficient diet. Am. J. Physiol. Gastrointest. Liver Physiol. 303, G54-59.
9. Pogribny, I. P., Kutanzi, K., Melnyk, S., de Conti, A., Tryndyak, V., et al. (2013) Strain-dependent dysregulation of one-carbon metabolism in male mice is associated with choline- and folate-deficient diet-induced liver injury. FASEB J. 27, 2233-2243.
10. Christensen, K. E., Wu, Q., Wang, X., Deng, L., Caudill, M. A., and Rozen, R. (2010) Steatosis in mice is associated with gender, folate intake, and expression of genes of one-carbon metabolism. J. Nutr. 140, 1736-1741.
11. Chew, T. W., Jiang, X., Yan, J., Wang, W., Lusa, A. L., et al. (2011) Folate intake, MTHFR genotype, and sex modulate choline metabolism in mice. J. Nutr. 141, 1475-1481.
12. Stead, L. M., Brosnan, J. T., Brosnan, M. E., Vance, D. E., and Jacobs, R. L. (2006) Is it time to reevaluate methyl balance in humans? Am. J. Clin. Nutr. 83, 5-10.
13. Vance, D. E., Li, Z., and Jacobs, R. L. (2007) Hepatic phosphatidylethanolamine N-methyltransferase, unexpected roles in animal biochemistry and physiology. J. Biol. Chem. 282, 33237-33241.
14. Guo, Y., Walther, T. C., Rao, M., Stuurman, N., Goshima, G., et al. (2008) Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453, 657-661.
15. Jacobs, R. L., Lingrell, S., Zhao, Y., Francis, G. A., and Vance, D. E. (2008) Hepatic CTP:phosphocholine cytidylyltransferase-alpha is a critical predictor of plasma high density lipoprotein and very low density lipoprotein. J. Biol. Chem. 283, 2147-2155.
16. Noga, A. A. and Vance, D. E. (2003) A gender-specific role for phosphatidylethanolamine N-methyltransferase-derived phosphatidylcholine in the regulation of plasma high density and very low density lipoproteins in mice. J. Biol. Chem. 278, 21851-21859.
17. Jacobs, R. L., Devlin, C., Tabas, I., and Vance, D. E. (2004) Targeted deletion of hepatic CTP:phosphocholine cytidylyltransferase alpha in mice decreases plasma high density and very low density lipoproteins. J. Biol. Chem. 279, 47402-47410.
18. Niebergall, L. J., Jacobs, R. L., Chaba, T., and Vance, D. E. (2011) Phosphatidylcholine protects against steatosis in mice but not non-alcoholic steatohepatitis. Biochim. Biophys. Acta 1811, 1177-1185.
19. Teng, Y. W., Mehedint, M. G., Garrow, T. A., and Zeisel, S. H. (2011) Deletion of betaine-homocysteine S-methyltransferase in mice perturbs choline and 1-carbon metabolism, resulting in fatty liver and hepatocellular carcinomas. J. Biol. Chem. 286, 36258-36267.
20. Teng, Y. W., Cerdena, I., and Zeisel, S. H. (2012) Homocysteinemia in mice with genetic betaine homocysteine S-methyltransferase deficiency is independent of dietary folate intake. J. Nutr. 142, 1964-1967.
21. Martinez-Chantar, M. L., Vazquez-Chantada, M., Ariz, U., Martinez, N., Varela, M., et al. (2008) Loss of the glycine N-methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice. Hepatology 47, 1191-1199.
22. Luka, Z. (2008) Methyltetrahydrofolate in folate-binding protein glycine N-methyltransferase. Vitam. Horm. 79, 325-345.
23. Jencks, D. A. and Mathews, R. G. (1987) Allosteric inhibition of methylenetetrahydrofolate reductase by adenosylmethionine. Effects of adenosylmethionine and NADPH on the equilibrium between active and inactive forms of the enzyme and on the kinetics of approach to equilibrium. J. Biol. Chem. 262, 2485-2493.
24. Varela-Rey, M., Martinez-Lopez, N., Fernandez-Ramos, D., Embade, N., Calvisi, D. F., et al. (2010) Fatty liver and fibrosis in glycine N-methyltransferase knockout mice is prevented by nicotinamide. Hepatology 52, 105-114.
25. Martinez-Una, M., Varela-Rey, M., Cano, A., Fernandez-Ares, L., Beraza, N., et al. (2013) Excess S-adenosylmethionine reroutes phosphatidylethanolamine towards phosphatidylcholine and triglyceride synthesis. Hepatology 58, 1296-1305.
26. Mudd, S. H., Brosnan, J. T., Brosnan, M. E., Jacobs, R. L., Stabler, S. P., et al. (2007) Methyl balance and transmethylation fluxes in humans. Am. J. Clin. Nutr. 85, 19-25.
27. Mavrelis, P. G., Ammon, H. V., Gleysteen, J. J., Komorowski, R. A., and Charaf, U. K. (1983) Hepatic free fatty acids in alcoholic liver disease and morbid obesity. Hepatology 3, 226-231.
28. Farquhar, J. W., Gross, R. C., Wagner, R. M., and Reaven, G. M. (1965) Validation of an incompletely coupled two-compartment nonrecycling catenary model for turnover of liver and plasma triglyceride in man. J. Lipid Res. 6, 119-134.
29. Magoulas, P. L. and El-Hattab, A. W. (2012) Systemic primary carnitine deficiency: an overview of clinical manifestations, diagnosis, and management. Orphanet J. Rare Dis. 7, 68.
30. Strijbis, K., Vaz, F. M., and Distel, B. (2010) Enzymology of the carnitine biosynthesis pathway. IUBMB Life 62, 357-362.
31. Malaguarnera, M., Gargante, M. P., Russo, C., Antic, T., Vacante, M., et al. (2010) L-carnitine supplementation to diet: a new tool in treatment of nonalcoholic steatohepatitis-a randomized and controlled clinical trial. Am. J. Gastroenterol. 105, 1338-1345.
32. Cox, R. A. and Hoppel, C. L. (1973) Biosynthesis of carnitine and 4-N-trimethylaminobutyrate from lysine. Biochem. J. 136, 1075-1082.
33. Mehlman, M. A., Therriault, D. G., and Tobin, R. B. (1971) Carnitine-14C metabolism in choline-deficient, alloxan-diabetic choline-deficient and insulin-treated rats. Metabolism 20, 100-107.
34. Kim, Y. I., Miller, J. W., da Costa, K. A., Nadeau, M., Smith, D., et al. (1994) Severe folate deficiency causes secondary depletion of choline and phosphocholine in rat liver. J. Nutr. 124, 2197-2203.
35. Champier, J., Claustrat, F., Nazaret, N., Fevre Montange, M., and Claustrat, B. (2012) Folate depletion changes gene expression of fatty acid metabolism, DNA synthesis, and circadian cycle in male mice. Nutr. Res. 32, 124-132.
36. Zhao, Y., Su, B., Jacobs, R. L., Kennedy, B., Francis, G. A., et al. (2009) Lack of phosphatidylethanolamine N-methyltransferase alters plasma VLDL phospholipids and attenuates atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 29, 1349-1355.
37. Walker, A. K., Jacobs, R. L., Watts, J. L., Rottiers, V., Jiang, K., et al. (2011) A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell 147, 840-852.
38. McNeil, C. J., Hay, S. M., Rucklidge, G. J., Reid, M. D., Duncan, G. J., et al. (2009) Maternal diets deficient in folic acid and related methyl donors modify mechanisms associated with lipid metabolism in the fetal liver of the rat. Br. J. Nutr. 102, 1445-1452.
39. Tryndyak, V. P., Latendresse, J. R., Montgomery, B., Ross, S. A., Beland, F. A., et al. (2012) Plasma microRNAs are sensitive indicators of inter-strain differences in the severity of liver injury induced in mice by a choline- and folate-deficient diet. Toxicol. Appl. Pharmacol. 262, 52-59.
40. Lewis, C. J., Crane, N. T., Wilson, D. B., and Yetley, E. A. (1999) Estimated folate intakes: data updated to reflect food fortification, increased bioavailability, and dietary supplement use. Am. J. Clin. Nutr. 70, 198-207.
41. Choumenkovitch, S. F., Selhub, J., Wilson, P. W., Rader, J. I., Rosenberg, I. H., et al. (2002) Folic acid intake from fortification in United States exceeds predictions. J. Nutr. 132, 2792-2798.
42. Matthews, R. G. and Daubner, S. C. (1982) Modulation of methylenetetrahydrofolate reductase activity by S-adenosylmethionine and by dihydrofolate and its polyglutamate analogues. Adv. Enzyme Regul. 20, 123-131.
43. Smith, A. D., Kim, Y. I., and Refsum, H. (2008) Is folic acid good for everyone? Am. J. Clin. Nutr. 87, 517-533.
44. Ulrich, C. M. and Potter, J. D. (2006) Folate supplementation: too much of a good thing? Cancer Epidemiol. Biomarkers Prev. 15, 189-193.
45. Prinz-Langenohl, R., Bramswig, S., Tobolski, O., Smulders, Y. M., Smith, D. E., et al. (2009) [6S]-5-Methyltetrahydrofolate increases plasma folate more effectively than folic acid in women with the homozygous or wild-type 677C->T polymorphism of methylenetetrahydrofolate reductase. Br. J. Pharmacol. 158, 2014-2021.
46. Fohr, I. P., Prinz-Langenohl, R., Bronstrup, A., Bohlmann, A. M., Nau, H., et al. (2002) 5, 10-Methylenetetrahydrofolate reductase genotype determines the plasma homocysteine-lowering effect of supplementation with 5-methyltetrahydrofolate or folic acid in healthy young women. Am. J. Clin. Nutr. 75, 275-282.
47. Kelley, B., Totter, J. R., and Day, P. L. (1950) The lipotropic effect of folic acid on rats receiving various purified diets. J. Biol. Chem. 187, 529-535.
48. Burdge, G. C., Lillycrop, K. A., Phillips, E. S., Slater-Jefferies, J. L., Jackson, A. A., et al. (2009) Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J. Nutr. 139, 1054-1060.
49. McNeil, C. J., Hay, S. M., Rucklidge, G. J., Reid, M., Duncan, G., et al. (2008) Disruption of lipid metabolism in the liver of the pregnant rat fed folate-deficient and methyl donor-deficient diets. Br. J. Nutr. 99, 262-271.
50. Mojtabai, R. (2004) Body mass index and serum folate in childbearing age women. Eur. J. Epidemiol. 19, 1029-1036.
51. Gallistl, S., Sudi, K., Mangge, H., Erwa, W., and Borkenstein, M. (2000) Insulin is an independent correlate of plasma homocysteine levels in obese children and adolescents. Diabetes Care 23, 1348-1352.
52. Mahabir, S., Ettinger, S., Johnson, L., Baer, D. J., Clevidence, B. A., et al. (2008) Measures of adiposity and body fat distribution in relation to serum folate levels in postmenopausal women in a feeding study. Eur. J. Clin. Nutr. 62, 644-650.
53. Tungtrongchitr, R., Pongpaew, P., Tongboonchoo, C., Vudhivai, N., Changbumrung, S., et al. (2003) Serum homocysteine, B12 and folic acid concentration in Thai overweight and obese subjects. Int. J. Vitam. Nutr. Res. 73, 8-14.
54. Furness, D. L., Yasin, N., Dekker, G. A., Thompson, S. D., and Roberts, C. T. (2012) Maternal red blood cell folate concentration at 10-12 weeks gestation and pregnancy outcome. J. Matern. Fetal Neonatal Med 25, 1423-1427.
55. Engeham, S. F., Haase, A., and Langley-Evans, S. C. (2010) Supplementation of a maternal low-protein diet in rat pregnancy with folic acid ameliorates programming effects upon feeding behaviour in the absence of disturbances to the methionine-homocysteine cycle. Br. J. Nutr. 103, 996-1007.
56. Yajnik, C. S., Joglekar, C. V., Lubree, H. G., Rege, S. S., Naik, S. S., et al. (2008) Adiposity, inflammation and hyperglycaemia in rural and urban Indian men: coronary risk of insulin sensitivity in Indian subjects (CRISIS) study. Diabetologia 51, 39-46.
57. Lewis, S. J., Leary, S., Davey Smith, G., and Ness, A. (2009) Body composition at age 9 years, maternal folate intake during pregnancy and methyltetrahydrofolate reductase (MTHFR) C677T genotype. Br. J. Nutr. 102, 493-496.
58. Boushey, C. J., Beresford, S. A., Omenn, G. S., and Motulsky, A. G. (1995) A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA 274, 1049-1057.
59. Verhaar, M. C., Stroes, E., and Rabelink, T. J. (2002) Folates and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 22, 6-13.
60. Robinson, K., Arheart, K., Refsum, H., Brattstrom, L., Boers, G., et al. (1998) Low circulating folate and vitamin B6 concentrations: risk factors for stroke, peripheral vascular disease, and coronary artery disease. European COMAC Group. Circulation 97, 437-443.
61. Morrison, H. I., Schaubel, D., Desmeules, M., and Wigle, D. T. (1996) Serum folate and risk of fatal coronary heart disease. JAMA 275, 1893-1896.
62. Alessio, A. C., Santos, C. X., Debbas, V., Oliveira, L. C., Haddad, R., et al. (2011) Evaluation of mild hyperhomocysteinemia during the development of atherosclerosis in apolipoprotein E-deficient and normal mice. Exp. Mol. Pathol. 90, 45-50.
63. Hofmann, M. A., Lalla, E., Lu, Y., Gleason, M. R., Wolf, B. M., et al. (2001) Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J. Clin. Invest. 107, 675-683.
64. McNeil, C. J., Beattie, J. H., Gordon, M. J., Pirie, L. P., and Duthie, S. J. (2012) Nutritional B vitamin deficiency disrupts lipid metabolism causing accumulation of proatherogenic lipoproteins in the aorta adventitia of ApoE null mice. Mol. Nutr. Food Res. 56, 1122-1130.
65. McNeil, C. J., Beattie, J. H., Gordon, M. J., Pirie, L. P., and Duthie, S. J. (2011) Differential effects of nutritional folic acid deficiency and moderate hyperhomocysteinemia on aortic plaque formation and genome-wide DNA methylation in vascular tissue from ApoE-/- mice. Clin. Epigenetics 2, 361-368.
66. Carnicer, R., Navarro, M. A., Arbones-Mainar, J. M., Acin, S., Guzman, M. A., et al. (2007) Folic acid supplementation delays atherosclerotic lesion development in apoE-deficient mice. Life Sci. 80, 638-643.
67. Toole, J. F., Malinow, M. R., Chambless, L. E., Spence, J. D., Pettigrew, L. C., et al. (2004) Lowering homocysteine in patients with ischemic stroke to prevent recurrent stroke, myocardial infarction, and death: the Vitamin Intervention for Stroke Prevention (VISP) randomized controlled trial. JAMA 291, 565-575.
68. Bonaa, K. H., Njolstad, I., Ueland, P. M., Schirmer, H., Tverdal, A., et al. (2006) Homocysteine lowering and cardiovascular events after acute myocardial infarction. N. Engl. J. Med. 354, 1578-1588.
69. Lonn, E., Yusuf, S., Arnold, M. J., Sheridan, P., Pogue, J., et al. (2006) Homocysteine lowering with folic acid and B vitamins in vascular disease. N. Engl. J. Med. 354, 1567-1577.
70. Bazzano, L. A., Reynolds, K., Holder, K. N., and He, J. (2006) Effect of folic acid supplementation on risk of cardiovascular diseases: a meta-analysis of randomized controlled trials. JAMA 296, 2720-2726.
71. Ebbing, M., Bleie, O., Ueland, P. M., Nordrehaug, J. E., Nilsen, D. W., et al. (2008) Mortality and cardiovascular events in patients treated with homocysteine-lowering B vitamins after coronary angiography: a randomized controlled trial. JAMA 300, 795-804.
72. Yang, Q., Cogswell, M. E., Hamner, H. C., Carriquiry, A., Bailey, L. B., et al. (2010) Folic acid source, usual intake, and folate and vitamin B-12 status in US adults: National Health and Nutrition Examination Survey (NHANES) 2003-2006. Am. J. Clin. Nutr. 91, 64-72.
73. Devlin, A. M., Singh, R., Wade, R. E., Innis, S. M., Bottiglieri, T., et al. (2007) Hypermethylation of Fads2 and altered hepatic fatty acid and phospholipid metabolism in mice with hyperhomocysteinemia. J. Biol. Chem. 282, 37082-37090.
74. Gavrilova, O., Haluzik, M., Matsusue, K., Cutson, J. J., Johnson, L., et al. (2003) Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J. Biol. Chem. 278, 34268-34276.
75. Sie, K. K., Li, J., Ly, A., Sohn, K. J., Croxford, R., et al. (2013) Effect of maternal and postweaning folic acid supplementation on global and gene-specific DNA methylation in the liver of the rat offspring. Mol. Nutr. Food Res. 57, 677-685.
76. Iizuka, K. and Horikawa, Y. (2008) ChREBP: a glucose-activated transcription factor involved in the development of metabolic syndrome. Endocr. J. 55, 617-624.