Hepatic very-low-density lipoprotein and apolipoprotein B production are increased following in vivo induction of betaine-homocysteine S-methyltransferase

Biochemical Journal

Volumn 395, Issue 2, 2006, Pages 363-371

  Sparks, Janet D ^a   Collins, Heidi L ^a   Chirieac, Doru V ^a   Cianci, Joanne ^a   Jokinen, Jenny ^a   Sowden, Mark P ^a   Gallowa, Chad A ^a   Sparks, Charles E ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

1 carbon metabolism; Apolipoprotein B; Betaine homocysteine S methyltransferase; Lipoprotein secretion; Liver; Very low density lipoprotein

Indexed keywords

CELLS; ENZYME KINETICS; FATTY ACIDS; KETONES; METABOLISM; RNA;

1-CARBON METABOLISM; APOLIPOPROTEIN B; BETAINE-HOMOCYSTEINE S-METHYLTRANSFERASE; LIPOPROTEIN SECRETION; LIVER; VERY-LOW-DENSITY LIPOPROTEIN;

PROTEINS;

ALANINE AMINOTRANSFERASE; APOLIPOPROTEIN B; BETAINE HOMOCYSTEINE METHYLTRANSFERASE; GLUCOSE; HOMOCYSTEINE; INSULIN; KETONE; LIVER PROTEIN; MESSENGER RNA; METHIONINE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN; BETAINE; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; ENZYME INDUCTION; GLUCOSE BLOOD LEVEL; IN VIVO STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SECRETION; RAT; AGING; ANIMAL; BIOSYNTHESIS; DIET; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; METABOLISM; RNA STABILITY; SPRAGUE DAWLEY RAT;

ANIMALIA;

AGING; ANIMALS; APOLIPOPROTEINS B; BETAINE; BETAINE-HOMOCYSTEINE S-METHYLTRANSFERASE; DIET; ENZYME INDUCTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH AND DEVELOPMENT; LIPOPROTEINS, VLDL; LIVER; MALE; METHIONINE; RATS; RATS, SPRAGUE-DAWLEY; RNA STABILITY; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 33645755849     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051966     Document Type: Article

References (61)

1. Davidson, N. O. and Shelness, G. S. (2000) Apolipoprotein B: mRNA editing, lipoprotein assembly, and presecretory degradation, Annu. Rev. Nutr. 20, 169-193
2. Chan, L., Hung-Junn Chang, B., Liao, W., Oka, K. and Lau, P. P. (2000) Apolipoprotein B: from editosome to proteasome. Recent Prog. Horm. Res. 55, 93-125
3. Powell, L. M., Wallis, S. C., Pease, R. J., Edwards, Y. H., Knolt, T. J. and Scott, J. (1987) A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell (Cambridge, Mass.) 50, 831-840
4. Chen, S.-H., Habib, G., Yang, C.-Y., Gu, Z.-W., Lee, B. R., Weng, S.-A., Silberman, S. R., Cai, S.-J., Deslypere, J. P., Rosseneu, M. et al. (1987) Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 238, 363-366
5. Fisher, E. A., Pan, M., Chen, X., Wu, X., Wang, H., Jamil, H., Sparks, J. D. and Williams, K. J. (2001) The triple threat to nascent apolipoprotein B: evidence for multiple, distinct degradative pathways. J. Biol. Chem. 276, 27855-27863
6. Sparks, J. D., Zolfaghari, R., Sparks, C. E., Smith, H. C. and Fisher, E. A. (1992) Impaired hepatic apolipoprotein B and E translation in streptozotocin diabetic rats. J. Clin. Invest. 89, 1418-1430
7. Dashti, N. (1992) The effect of low density lipoproteins, cholesterol, and 25-hydroxycholeslerol on apolipoprotein B gene expression in HepG2 cells. J. Biol. Chem. 267, 7160-7169
8. Wang, T. W., Byrne, C. D. and Hales, C. N. (1994) Effect of ethanol on hepatic apoiipoprotein B synthesis and secretion in vitro. Biochem. Biophys. Acta 1211, 234-238
9. van't Hooft, F., Jormsjo, S., Lundahl, B., Tornvall, P., Eriksson, P. and Hamsten, A. (1999) A functional polymorphism in the apolipoprotein B promoter that influences the level of plasma low density lipoprotein. J. Lipid. Res. 40, 1686-1694
10. Singh, K., Batuman, O. A., Akman, H, O., Kedees, M. H., Vakil, V. and Hussain, M. M. (2002) Differential, tissue-specific, transcriptional regulation of apolipoprotein B secretion by translorming growth factor β. J. Biol. Chem. 277, 39515-39524
11. Sowden, M. P., Collins, H. L., Smith, H. C., Garrow, T. A., Sparks, J. D. and Sparks, C. E. (1999) Apolipoprotein B mRNA and lipoprotein secretion are increased in McArdle RH-7777 cells by expression of betaine-homocysteine S-methyltransferase. Biochem. J. 341, 639-645
12. Delgado-Reyes, C. V., Walling, M. A. and Garrow, T. A (2001) Immunohistochemical detection of betaine-homocysteine S-methyltransferase in human, pig, and rat liver and kidney. Arch. Biochem. Biophys. 393, 184-186
13. Finkelstein, J. D. (1990) Methionine metabolism in mammals. J. Nutr. Biochem. 1, 228-237
14. Finkelstein, J. D., Harris, B. J., Martin, J. J. and Kyle, W. E. (1982) Regulation of hepatic betaine-homocysteine methyltransferase by dietary methionine. Biochem. Biophys. Res. Commun. 108, 344-348
15. Finkelstein, J. D., Martin, J. J., Harris, B. J. and Kyle, W. E. (1983) Regulation of hepatic betaine-homocysteine methyltransferase by dietary betaine. J. Nutr. 113, 519-521
16. Finkelstein, J. D., Martin, J. J. and Harris, B. J. (1986) Effect of dietary cystine on methionine metabolism in rat liver. J. Nutr. 116, 985-990
17. Park, E. I., Renduchintala, M. S. and Garrow, T. A. (1997) Diet-induced changes in hepatic betaine-homocysteine methyltransferase activity are mediated by changes in the steady-state level of its mRNA. J. Nutr. Biochem. 8, 541-545
18. Park, E. I. and Garrow, T. A. (1999) Interaction between dietary methionine and methyl donor intake on rat liver betaine-homocysteine methyltransferase gene expression and organization of the human gene. J. Biol. Chem. 274, 7816-7824
19. Reeve, P. G., Nielsen, F. H. and Fahey, Jr. G. C. (1993) AIN-93 purified diets for laboratory rodents: final report ol the American Institute of Nutrition Ad Hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939-1951
20. Funk, M. A., Hortin, A. E. and Baker, D. H. (1990) Utilization of D-methionine by growing rats. Nutr. Res. 10, 1029-1034
21. Sparks, J. D., Bolognino, M., Trax, P. A. and Sparks, C. E. (1986) The production and utility of monoclonal antibodies to rat apolipoprotein B lipoproteins. Atherosclerosis 61, 205-211
22. Phung, T. L., Sowden, M., Sparks, J. D., Sparks, C. E. and Smith, H. C. (1996) Regulation of hepatic apolipoprotein B RNA editing in the genetically obese Zucker rat. Metabolism 45, 1056-1058
23. Sowden, M., Hamm, J. K., Spinelli, S. and Smith, H. C. (1996) Determinants involved in regulating the proportion of edited apolipoprotein B RNAs. RNA 2, 274-288
24. Shimomura, I., Bashmakov, Y., Ikemoto, S., Horton, J. D., Brown, M. S. and Goldstein, J, L. (1999) Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. U.S.A. 96, 13656-13661
25. Chireac, D. V., Collins, H. L., Cianci, J., Sparks, J. D. and Sparks, C. E. (2004) Altered triglyceride-ricti lipoprotein production in Zucker diabetic fatty rats. Am. J. Physiol. 287, E42-E49
26. DeHoff, J. L., Davidson, L. M. and Kritchevsky, D. (1978) An enzymatic assay for determining free and total cholesterol in tissue. Clin. Chem. 24, 433-435
27. Carr, T. P., Andresen, C. J. and Rudel, L. L. (1993) Enymatic determination of triglyceride, free cholesterol and total cholesterol in tissue lipid extracts. Clin. Biochem. 26, 39-42
28. de Waziers, I., Garlatti, M., Bouguet, J., Beaune, P. and Barouki, R. (1995) Insulin down-regulates cytochrome P450 2B and 2E expression at the post-transcriptional level in the rat hepatoma cell line. Mol. Pharmacol. 47, 474-479
29. Spector, D. L., Goldman, R. D. and Leinwand, L. A. (1998) In vitro run-on analysis of mRNA transcription. In Cells: A Laboratory Manual, pp. 25.1-25.14, Cold Spring Harbor Laboratory Press, Plainview, NY
30. Reuben, M. A., Svenson, K. L., Doolittle, M. H, Johnson, D. R. Lusis, A. J. and Elovson, J. (1988) Biosynthetic relationships between three rat apolipoprotein B peptides. J. Lipid Res. 29, 1337-1347
31. Demmer, L. A., Levin, M. S., Elovson, J., Reuben, M. A., Lusis, A. J. and Gordon, J. I. (1986) Tissue-specific expression and developmental regulation of the rat apolipoprotein B gene. Proc. Natl. Acad. Sci. U.S.A. 83, 8102-8106
32. Wu, J. H., Semenkovich, C. F., Cher, S.-H., Li, W.-H. and Chan, L. (1990) Apolipoprotein B mRNA editing. Validation of a sensitive assay and developmental biology of RNA editing in the rat. J. Biol. Chem. 265, 12312-12316
33. Horton, J. D., Shah, N. A., Warrington, J. A., Anderson, N. N., Park, S. W., Brown, M. S. and Goldstein, J. L. (2003) Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. U.S.A. 100, 12027-12032
34. Norton, J. D., Goldstein, J. L. and Brown, M. S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131
35. Pullinger, C. R., North, J. D., Teng, B.-B., Rifici, V. A., Ronhild de Brito, A. E. and Scott, J. (1989) The apoiipoprotein B gene is constitutively expressed in HepG2 cells: regulation of secretion by oleic acid, albumin, and insulin, and the measurement of the mRNA halt-life. J. Lipid Res. 30, 1065-1077
36. Patrick, L. (2002) Nonalcoholic fatty liver disease: relationship to insulin sensitivity and oxidative stress Treatment approaches using vitamin E, magnesium, and betaine. Altern. Med. Rev. 7, 276-291
37. Abdelmalek, M. F., Angulo, P., Jorgensen, R. A., Sylvestre, P. B. and Lindor, K. D. (2001) Betaine, a promising new agent for patients with nonalcoholic steatohepatitis: results of a pilot study. Am. J. Gastroenterol. 96, 2711-2717
38. Snimano, H., Horton, J. D., Hammer, R. E., Simomura, I., Brown, M. S. and Goldstein, J. I. (1996) Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J. Clin. Invest. 98, 1575-1584
39. Gillian-Daniel, D. L., Bates, P. W., Tebon, A. and Attie, A. D. (2002) Endoplasmic reticulum localization of low density lipoprotein receptor mediates pre-secretory degradation of apolipoprotein B. Proc. Natl. Acad. Sci. U.S.A. 99, 4337-4342
40. Koteish, A. and Diehl, A. M. (2001) Animal models of steatosis. Semin. Liver Dis. 21, 89-104
41. Giangreco, A., Sowden, M. P., Mikityansky, I. and Smith, H. C. (2001) Ethanol stimulates apolipoprotein B mRNA editing in the absence of de nova RNA or protein synthesis. Biochem. Biophys. Res. Commun. 289, 1162-1167
42. Wagner, R. D., Krul, E. S., Moberly, J. B., Alpers, D. H. and Schonfeld, G. (1992) Apolipoprotein expression and cellular differentiation in Caco-2 intestinal cells. Am. J. Physiol. 263, E374-E382
43. Murthy, S., Albright, E., Mathur, S. N., Davidson, N. O. and Field, F. J. (1992) Apolipoprotein B mRNA abundance is decreased by eicosapentaenoic acid in CaCo-2 cells. Arterioscler. Thromb. 12, 691-700
44. Levy-Wilson, B. (1995) Transcriptional control of the human apolipoprotein B gene in cell culture and in transgenic animals. Prog. Nucleic Acid Res. 50, 161-190
45. Wang, A.-B., Liu, D.-P. and Liang, C.-C. (2003) Regulation of human apolipoprotein B gene expression at multiple levels. Exp. Cell Res. 290, 1-12
46. Zannis, V., Kan, H.-Y., Kritis, A., Zanni, E. and Kardassis, D. (2001) Transcriptional regulation of the human apolipoprotein genes. Front. Biosci. 6, 456-504
47. Collins, H. L., Sparks, C. E. and Sparks, J. D. (2000) B48 is preferentially translated over B100 in McArdle RH-7777 cells expressing increased endogenous apo B mRNA. Biochem. Biophys. Res. Commun. 273, 1156-1160
48. Griffin, J. L., Bonney, S. A., Mann, C., Hebbachi, A. M., Gibbons, G. F., Nicholson, J. K., Shoulders, C. C. and Scott, J. (2004) An integrated reverse functional genomic and metabolic approach to understanding orotic acid-induced fatty liver. Physiol Genomics 17, 140-149
49. Barak, A. J., Beckenhauer, H. C. and Tuma, D. J. (1994) S-adenosylmethionine generation and prevention of alcoholic fatty liver by betaine. Alcohol 11, 501-503
50. Mato, J. M., Corrales, F. J., Lu, S. C. and Avila, M. A. (2002) S-adenosylmethionine: a control switch that regulates liver function. FASEB J. 16, 15-26
51. Barak, A. J., Beckenhauer, H. C, and Tuma, D. J. (2002) Methionine synthase; a possible prime site of the ethanolic lesion in liver. Alcohol 26, 65-67
52. Steenge, G. R., Verhoeff, P. and Katan, M. B. (2003) Betaine suppiementation lowers plasma homocysteine in healthy men and women. J. Nutr. 133, 1291-1295
53. Jacobs, R. L., Stead, L. M., Devlin, C., Tabas, I., Brosnan, M. E., Brosnan, J. T. and Vance, D. E. (2005) Physiological regulation of phospholipid methylation alters plasma homocysteine in mice. J. Biol. Chem. 280, 28299-28305
54. Barak, A. J., Beckenhauer, H. C., Tuma, D. J. and Badakhsh, S. (1987) Effects of prolonged ethanol feeding on methionine metabolism in rat liver. Biochem. Cell Biol. 65, 230-233
55. Halsted, C. H., Villanueva, J. A., Devlin, A. M., Niernela, O., Parkkila, S., Garrow, T. A., Wallock, L. M., Shigenaga, M. K., Melnyk, S. and James, S. J. (2002) Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig. Proc. Natl. Acad. Sci. U.S.A. 99, 10072-10077
56. Kenyon, S. H., Nicolaou, A. and Gibbons, W. A. (1998) The effect of ethanol and its metabolites upon methionine synthase activity in vitro. Alcohol 15, 305-309
57. Barak, A. J., Beckenhauer, H. C. and Tuma, D. J. (1996) Betaine effects on hepatic methionine metabolism elicited by short-term ethanol feeding. Alcohol 13, 483-486
58. Lau, P. P., Cahill, D. J., Zhu, H.-J. and Chan, L. (1995) Ethanol modulates apolipoprotein B mRNA editing in the rat. J. Lipid Res. 36, 2069-2078
59. Barak, A. J., Beckenhauer, H. C., Badakhsh, S. and Tuma, D. J. (1997) The effect of betaine in reversing alcoholic steatosis. Alcohol. Clin. Exp. Res. 21, 1100-1102
60. Browning, J. D. and Horten, J. D. (2004) Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114, 147-152
61. Pan, M., Cederbaum, A. I., Zhang, Y. L., Ginsberg, H. N., Williams, K. J. and Fisher, E. A. (2004) Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J. Clin. Invest. 113, 1277-1287