Methionine metabolism and liver disease.

In the early 1930s, Banting and Best, the discoverers of insulin, found that choline could prevent the development of fatty liver disease (steatosis) in pancreatectomized dogs treated with insulin. Later work indicated that in rats and mice, diets deficient in labile methyl groups (choline, methionine, betaine, folate) produced fatty liver and that long-term administration of diets deficient in choline and methionine also caused hepatocellular carcinoma. These experiments not only linked steatosis and diabetes but also provided evidence, for the first time, of the importance of labile methyl group balance to maintain normal liver function. This conclusion is now amply supported by the observation of mice devoid of key enzymes of methionine and folate metabolism and in patients with severe deficiencies in these enzymes. Moreover, treatments with various methionine metabolites in experimental animal models of liver disease show hepatoprotective properties.

[1]  D. Virshup,et al.  Protein phosphatase 2A: a panoply of enzymes. , 2000, Current opinion in cell biology.

[2]  H. Jakubowski Protein homocysteinylation: possible mechanism underlying pathological consequences of elevated homocysteine levels , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  M. Young,et al.  The small leucine‐rich proteoglycan biglycan modulates BMP‐4‐induced osteoblast differentiation , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  T. Drake,et al.  Pathology of atheromatous lesions in inbred and genetically engineered mice. Genetic determination of arterial calcification. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[5]  F. Corrales,et al.  Methionine adenosyltransferase I/III deficiency: two Korean compound heterozygous siblings with a novel mutation , 2003, Journal of Inherited Metabolic Disease.

[6]  N. Reo,et al.  Kinetic analyses of liver phosphatidylcholine and phosphatidylethanolamine biosynthesis using (13)C NMR spectroscopy. , 2002, Biochimica et biophysica acta.

[7]  S. J. James,et al.  Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Hardie,et al.  AMP‐activated protein kinase: the energy charge hypothesis revisited , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[9]  M. Avila,et al.  S‐Adenosylmethionine regulates MAT1A and MAT2A gene expression in cultured rat hepatocytes: a new role for S‐adenosylmethionine in the maintenance of the differentiated status of the liver , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[10]  R. Matthews,et al.  Human methylenetetrahydrofolate reductase: isolation of cDNA, mapping and mutation identification , 1994, Nature Genetics.

[11]  M. Esteller Cancer epigenomics: DNA methylomes and histone-modification maps , 2007, Nature Reviews Genetics.

[12]  J. Rodés,et al.  S-adenosylmethionine in alcoholic liver cirrhosis: a randomized, placebo-controlled, double-blind, multicenter clinical trial. , 1999, Journal of hepatology.

[13]  Shelly C. Lu,et al.  Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Pick,et al.  Activation of cystathionine synthase by adenosylmethionine and adenosylethionine. , 1975, Biochemical and biophysical research communications.

[15]  G. Barsh,et al.  The mouse lethal nonagouti (a(x)) mutation deletes the S‐adenosylhomocysteine hydrolase (Ahcy) gene. , 1994, The EMBO journal.

[16]  J. Henderson,et al.  Evidence for impairment of transsulfuration pathway in cirrhosis , 1981 .

[17]  J. Finkelstein,et al.  Homocystinuria due to cystathionine synthase deficiency: the metabolism of L-methionine. , 1965, The Journal of clinical investigation.

[18]  Jens Frahm,et al.  Creatine replacement therapy in guanidineoacetate methyltransferase deficiency, a novel inborn error of metabolism , 1996, The Lancet.

[19]  M. D. De Miglio,et al.  Chemoprevention of hepatocarcinogenesis: S-adenosyl-L-methionine. , 2002, Alcohol.

[20]  N. Maeda,et al.  Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Matthews,et al.  Cobalamin‐dependent methionine synthase , 1990, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[22]  S. Alemany,et al.  Purification and comparison of two forms of S-adenosyl-L-methionine synthetase from rat liver. , 1987, European journal of biochemistry.

[23]  H Ogawa,et al.  Purification and properties of glycine N-methyltransferase from rat liver. , 1982, The Journal of biological chemistry.

[24]  Sierra Ee,et al.  Recent advances in the understanding of the mechanism of membrane transport of folates and antifolates , 1999 .

[25]  Shelly C. Lu,et al.  Spontaneous oxidative stress and liver tumors in mice lacking methionine adenosyltransferase 1A , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[26]  L. Glória,et al.  Hyperhomocysteinemia in chronic alcoholism: correlation with folate, vitamin B-12, and vitamin B-6 status. , 1996, The American journal of clinical nutrition.

[27]  Zhoutao Chen,et al.  Homocysteine‐betaine interactions in a murine model of 5,10‐methylenetetrahydrofolate reductase deficiency , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[28]  J. Belmont,et al.  Disruption of the adenosine deaminase gene causes hepatocellular impairment and perinatal lethality in mice. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Richard G. W. Anderson,et al.  Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development , 1999, Nature Genetics.

[30]  T. Garrow,et al.  Interaction between Dietary Methionine and Methyl Donor Intake on Rat Liver Betaine-homocysteine Methyltransferase Gene Expression and Organization of the Human Gene* , 1999, The Journal of Biological Chemistry.

[31]  K. Lindor,et al.  Betaine, a promising new agent for patients with nonalcoholic steatohepatitis: results of a pilot study , 2001 .

[32]  M. Brosnan,et al.  Is it time to reevaluate methyl balance in humans? , 2006, The American journal of clinical nutrition.

[33]  I. Pogribny,et al.  S-adenosylhomocysteine hydrolase deficiency in a human: A genetic disorder of methionine metabolism , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  R. Green,et al.  Update on cobalamin, folate, and homocysteine. , 2003, Hematology. American Society of Hematology. Education Program.

[35]  M. Stitzel,et al.  Targeted Disruption of the Methionine Synthase Gene in Mice , 2001, Molecular and Cellular Biology.

[36]  N. Kaplowitz,et al.  Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. , 2003, Gastroenterology.

[37]  Shelly C. Lu,et al.  Role of S-adenosylmethionine, folate, and betaine in the treatment of alcoholic liver disease: summary of a symposium. , 2007, The American journal of clinical nutrition.

[38]  R. Bronson,et al.  Disruption of the murine gene encoding phosphatidylethanolamine N-methyltransferase. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D. Vance,et al.  The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. , 2006, Cell metabolism.

[40]  Shelly C. Lu,et al.  Genetic polymorphisms in the methylenetetrahydrofolate reductase and thymidylate synthase genes and risk of hepatocellular carcinoma , 2007, Hepatology.

[41]  I. Pogribny,et al.  S-Adenosylhomocysteine hydrolase deficiency in a 26-year-old man , 2006, Journal of Inherited Metabolic Disease.

[42]  Yuan-Yuan Shi,et al.  Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. , 2001, The Journal of clinical investigation.

[43]  Yi-Jen Chen,et al.  Characterization of glycine‐N‐methyltransferase‐gene expression in human hepatocellular carcinoma , 1998, International journal of cancer.

[44]  W. Willett,et al.  Methylenetetrahydrofolate reductase polymorphism, dietary interactions, and risk of colorectal cancer. , 1997, Cancer research.

[45]  R. Banerjee,et al.  Human Methionine Synthase Reductase, a Soluble P-450 Reductase-like Dual Flavoprotein, Is Sufficient for NADPH-dependent Methionine Synthase Activation* , 2001, The Journal of Biological Chemistry.

[46]  K. Robert,et al.  Altered Gene Expression in Liver from a Murine Model of Hyperhomocysteinemia* , 2003, Journal of Biological Chemistry.

[47]  R. Gordon,et al.  Cystathionine β‐synthase mutations in homocystinuria , 1999 .

[48]  R. Matthews,et al.  A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase , 1995, Nature Genetics.

[49]  R. Matthews,et al.  Human methionine synthase reductase is a molecular chaperone for human methionine synthase. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  J. Eggermont,et al.  CBS domains: structure, function, and pathology in human proteins. , 2005, American journal of physiology. Cell physiology.

[51]  J. Finkelstein,et al.  Methionine metabolism in mammals. Distribution of homocysteine between competing pathways. , 1984, The Journal of biological chemistry.

[52]  L. Edwards,et al.  Phosphatidylethanolamine N-methyltransferase (PEMT) knockout mice have hepatic steatosis and abnormal hepatic choline metabolite concentrations despite ingesting a recommended dietary intake of choline. , 2003, The Biochemical journal.

[53]  A. Barrier,et al.  The MTHFR 677C > T polymorphism is associated with an increased risk of hepatocellular carcinoma in patients with alcoholic cirrhosis. , 2004, Carcinogenesis.

[54]  A. Cederbaum,et al.  S-Adenosylmethionine Blocks Collagen I Production by Preventing Transforming Growth Factor-β Induction of the COL1A2 Promoter* , 2005, Journal of Biological Chemistry.

[55]  J. Leonard,et al.  Demyelination of the brain is associated with methionine adenosyltransferase I/III deficiency. , 1996, The Journal of clinical investigation.

[56]  Michael J. Thomas,et al.  Molecular Distinction of Phosphatidylcholine Synthesis between the CDP-Choline Pathway and Phosphatidylethanolamine Methylation Pathway* , 1999, The Journal of Biological Chemistry.

[57]  Shelly C. Lu,et al.  Differential expression of methionine adenosyltransferase genes influences the rate of growth of human hepatocellular carcinoma cells. , 1998, Cancer research.

[58]  L. Poirier The effects of diet, genetics and chemicals on toxicity and aberrant DNA methylation: an introduction. , 2002, The Journal of nutrition.

[59]  C. W. Tabor,et al.  1,4-Diaminobutane (putrescine), spermidine, and spermine. , 1976, Annual review of biochemistry.

[60]  Shelly C. Lu,et al.  S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[61]  D. Sullivan,et al.  Fractionation and kinetic properties of rat liver and kidney methionine adenosyltransferase isozymes. , 1983, Biochemistry.

[62]  E. Stokstad,et al.  Feedback inhibition of methylene-tetrahydrofolate reductase in rat liver by S-adenosylmethionine. , 1967, Biochimica et biophysica acta.

[63]  J. Mato,et al.  A Glycine N-methyltransferase Knockout Mouse Model for Humans with Deficiency of this Enzyme , 2006, Transgenic Research.

[64]  Stefan Neubauer,et al.  Severely altered guanidino compound levels, disturbed body weight homeostasis and impaired fertility in a mouse model of guanidinoacetate N-methyltransferase (GAMT) deficiency. , 2004, Human molecular genetics.

[65]  R. Finnell,et al.  Identification of two putative novel folate receptor genes in humans and mouse. , 2000, Gene.

[66]  Fernando J. Corrales,et al.  Reduced mRNA abundance of the main enzymes involved in methionine metabolism in human liver cirrhosis and hepatocellular carcinoma. , 2000 .

[67]  Shelly C. Lu,et al.  Role of S‐adenosyl‐L‐methionine in liver health and injury , 2007, Hepatology.

[68]  D. A. Jencks,et al.  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. , 1987, The Journal of biological chemistry.

[69]  M. Martínez-Chantar,et al.  NO sensitizes rat hepatocytes to proliferation by modifying S-adenosylmethionine levels. , 2002, Gastroenterology.

[70]  Jonathan E Katz,et al.  Automated Identification of Putative Methyltransferases from Genomic Open Reading Frames*S , 2003, Molecular & Cellular Proteomics.

[71]  M. Houweling,et al.  Stimulation of CTP:Phosphocholine Cytidylyltransferase by Free Cholesterol Loading of Macrophages Involves Signaling through Protein Dephosphorylation (*) , 1995, The Journal of Biological Chemistry.

[72]  Shelly C. Lu,et al.  Inhibition of human betaine-homocysteine methyltransferase expression by S-adenosylmethionine and methylthioadenosine. , 2007, The Biochemical journal.

[73]  D. Vance,et al.  Expression of Phosphatidylethanolamine N-Methyltransferase-2 Cannot Compensate for an Impaired CDP-choline Pathway in Mutant Chinese Hamster Ovary Cells (*) , 1995, The Journal of Biological Chemistry.

[74]  C. Wagner,et al.  Glycine N-methyltransferase deficiency: A new patient with a novel mutation , 2003, Journal of Inherited Metabolic Disease.

[75]  D. Vance,et al.  Biochemical and Evolutionary Significance of Phospholipid Methylation* , 1998, The Journal of Biological Chemistry.

[76]  Shelly C. Lu,et al.  S‐adenosylmethionine and its metabolite induce apoptosis in HepG2 cells: Role of protein phosphatase 1 and Bcl‐xS , 2004, Hepatology.

[77]  J. Mato,et al.  S‐adenosyl‐L‐methionine synthetase and phospholipid methyltransferase are inhibited in human cirrhosis , 1988, Hepatology.

[78]  J. Janin,et al.  Structure of Protein Phosphatase Methyltransferase 1 (PPM1), a Leucine Carboxyl Methyltransferase Involved in the Regulation of Protein Phosphatase 2A Activity* , 2003, Journal of Biological Chemistry.

[79]  Shelly C. Lu,et al.  S‐adenosylmethionine and methylthioadenosine are antiapoptotic in cultured rat hepatocytes but proapoptotic in human hepatoma cells , 2002, Hepatology.

[80]  M. Stipanuk Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. , 2004, Annual review of nutrition.

[81]  S. Craig,et al.  Betaine in human nutrition. , 2004, The American journal of clinical nutrition.

[82]  K. Buetow,et al.  Genotypic and phenotypic characterization of a putative tumor susceptibility gene, GNMT, in liver cancer. , 2003, Cancer research.

[83]  Dong Hwan Lee,et al.  Identification and functional analysis of cystathionine beta-synthase gene mutations in patients with homocystinuria , 2005, Journal of Human Genetics.

[84]  D. Rosenblatt Inherited disorders of folate transport and metabolism , 1989 .

[85]  J. Chou,et al.  Molecular mechanisms of an inborn error of methionine pathway. Methionine adenosyltransferase deficiency. , 1995, The Journal of clinical investigation.

[86]  Shelly C. Lu,et al.  Loss of the glycine N‐methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice , 2007, Hepatology.

[87]  R. Rozen,et al.  A second genetic polymorphism in methylenetetrahydrofolate reductase (MTHFR) associated with decreased enzyme activity. , 1998, Molecular genetics and metabolism.

[88]  J. Finkelstein,et al.  Methionine metabolism in mammals. , 1990, The Journal of nutritional biochemistry.

[89]  M. Pajares,et al.  Modulation of rat liver S-adenosylmethionine synthetase activity by glutathione. , 1992, The Journal of biological chemistry.

[90]  J. Finkelstein,et al.  Homocystinuria: An Enzymatic Defect , 1964, Science.

[91]  A. Cimmino,et al.  Hyperhomocysteinemia and the MTHFR C677T polymorphism promote steatosis and fibrosis in chronic hepatitis C patients , 2005, Hepatology.

[92]  F. Corrales,et al.  Hysteretic Behavior of Methionine Adenosyltransferase III , 2000, The Journal of Biological Chemistry.

[93]  Conrad Wagner,et al.  Methyl balance and transmethylation fluxes in humans. , 2007, The American journal of clinical nutrition.

[94]  M. Brosnan,et al.  Plasma Homocysteine Is Regulated by Phospholipid Methylation* , 2003, The Journal of Biological Chemistry.

[95]  J. Loscalzo,et al.  Homocyst(e)ine Decreases Bioavailable Nitric Oxide by a Mechanism Involving Glutathione Peroxidase* , 1997, The Journal of Biological Chemistry.

[96]  M. Rudnicki,et al.  Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. , 2001, Human molecular genetics.

[97]  L. Tessitore,et al.  Induction of hepatocyte proliferation after partial hepatectomy is accompanied by a markedly reduced expression of phosphatidylethanolamine N-methyltransferase-2. , 1997, Biochimica et biophysica acta.

[98]  Shuli Wang,et al.  Polymorphism of the PEMT gene and susceptibility to nonalcoholic fatty liver disease (NAFLD) , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[99]  Shelly C. Lu,et al.  S-adenosylmethionine regulates cytoplasmic HuR via AMP-activated kinase. , 2006, Gastroenterology.

[100]  W. Loenen S-adenosylmethionine: jack of all trades and master of everything? , 2006 .

[101]  A. Berns,et al.  Adenosine–deaminase–deficient mice die perinatally and exhibit liver–cell degeneration, atelectasis and small intestinal cell death , 1995, Nature Genetics.

[102]  K. Namekata,et al.  Abnormal Lipid Metabolism in Cystathionine β-Synthase-deficient Mice, an Animal Model for Hyperhomocysteinemia* , 2004, Journal of Biological Chemistry.

[103]  J. Finkelstein,et al.  Homocystinuria due to Cystathionine Synthetase Deficiency: The Mode of Inheritance , 1964, Science.

[104]  C. Allis,et al.  The language of covalent histone modifications , 2000, Nature.

[105]  R. Matthews,et al.  Metabolic derangement of methionine and folate metabolism in mice deficient in methionine synthase reductase. , 2007, Molecular genetics and metabolism.

[106]  I. Pogribny,et al.  S-Adenosylhomocysteine hydrolase deficiency: A second patient, the younger brother of the index patient, and outcomes during therapy , 2005, Journal of Inherited Metabolic Disease.

[107]  K. Robert,et al.  Cystathionine beta synthase deficiency promotes oxidative stress, fibrosis, and steatosis in mice liver. , 2005, Gastroenterology.

[108]  M. Kotb,et al.  Consensus nomenclature for the mammalian methionine adenosyltransferase genes and gene products. , 1997, Trends in genetics : TIG.

[109]  S. Clarke 16 Inhibition of mammalian protein methyltransferases by 5'-methylthioadenosine (MTA): A mechanism of action of dietary same? , 2006, The Enzymes.

[110]  Shelly C. Lu,et al.  S‐Adenosylmethionine: a control switch that regulates liver function , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[111]  N. Kaplowitz,et al.  Hyperhomocysteinemia, endoplasmic reticulum stress, and alcoholic liver injury. , 2004, World journal of gastroenterology.

[112]  E. Stokstad,et al.  Mammalian methylenetetrahydrofolate reductase. Partial purification, properties, and inhibition by S-adenosylmethionine. , 1971, Biochimica et biophysica acta.

[113]  Shelly C. Lu,et al.  Impaired liver regeneration in mice lacking methionine adenosyltransferase 1A , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[114]  Shelly C. Lu,et al.  5′‐methylthioadenosine modulates the inflammatory response to endotoxin in mice and in rat hepatocytes , 2004, Hepatology.

[115]  R. Lorini,et al.  Glycine N-methyltransferase deficiency: A novel inborn error causing persistent isolated hypermethioninaemia , 2001, Journal of Inherited Metabolic Disease.

[116]  B. Fowler,et al.  Neonatal hepatic steatosis by disruption of the adenosine kinase gene , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[117]  J. Straková,et al.  Inhibition of betaine-homocysteine S-methyltransferase causes hyperhomocysteinemia in mice. , 2006, The Journal of nutrition.

[118]  M. Hsiao,et al.  Glycine N‐methyltransferase−/− mice develop chronic hepatitis and glycogen storage disease in the liver , 2007, Hepatology.

[119]  D. Vance,et al.  Suppression of rat hepatoma cell growth by expression of phosphatidylethanolamine N-methyltransferase-2. , 1994, The Journal of biological chemistry.

[120]  Zhoutao Chen,et al.  Mice deficient in methylenetetrahydrofolate reductase exhibit tissue-specific distribution of folates. , 2004, The Journal of nutrition.