Intestinal transcription and synthesis of apolipoprotein AI is regulated by five natural polymorphisms upstream of the apolipoprotein CIII gene

Journal of Clinical Investigation

Volumn 99, Issue 8, 1997, Pages 1958-1965

  Naganawa, Satoshi ^a   Ginsberg, Henry N ^b   Glickman, Robert M ^a   Ginsburg, Geoffrey S ^a,b,c,d  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c Columbia Physicians and Surgeons ^*  (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

apolipoproteins; enhancer; high density lipoprotein; intestine; mutation; transcription factor

Indexed keywords

APOLIPOPROTEIN A1;

ADULT; ARTICLE; ATHEROSCLEROSIS; ENHANCER REGION; GENETIC POLYMORPHISM; HUMAN; HUMAN TISSUE; ISCHEMIC HEART DISEASE; LIPOPROTEIN SYNTHESIS; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TISSUE DISTRIBUTION;

EID: 0030964911     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119363     Document Type: Article

References (55)

1. Castelli, W.P., J.T. Doyle, T. Gordon, C.G. Hames, M.C. Hjortland, S.B. Hulley, A. Kagan, and W.J. Zukel. 1977. HDL cholesterol and other lipids in coronary heart disease: the cooperative lipoprotein phenotyping study. Circulation. 55:767-772.
2. Glueck, C.J., P. Gartside, R.W. Fallat, J. Sielski, and P.M. Steiner. 1976. Longevity syndromes: familial hypoheta and familial hypoalpha lipoproteinemia. J. Lab. Clin. Med. 88:941-957.
3. Karathanasis, S.K., J. McPherson, V.I. Zannis, and J.L. Breslow. 1983. Linkage of human apolipoproteins A-I and C-III genes. Nature (Lond.). 304: 371-373.
4. Ginsburg, G.S., J. Ozer, and S.K. Karathanasis. 1995. Intestinal apolipoprotein AI gene transcription is regulated by multiple distinct DNA elements and is synergistically activated by the orphan nuclear receptor, hepatocyte nuclear factor 4. J. Clin. Invest. 96:528-538.
5. Widom, R.L., J.A.A. Ladias, S. Kouidou, and S.K. Karathanasis. 1991. Synergistic interactions between transcription factors control expression of the apolipoprotein AI gene in liver cells. Mol. Cell. Biol. 11:677-687.
6. Sastry, K.N., U. Seedorf, and S.K. Karathanasis. 1988. Different cis-acting DNA elements control expression of the human apolipoprotein AI gene in different cell types. Mol. Cell. Biol. 8:605-614.
7. Walsh, A., N. Azrolan, K. Wang, A. Marcigliano, A. O'Connell, and J.L. Breslow. 1993. Intestinal expression of the human apoA-I gene in transgenic mice is controlled by a DNA region 3′ to the gene in the promoter of the adjacent convergently transcribed apoC-III gene. J. Lipid Res. 34:617-623.
8. Davidson, N.O., and R.M. Glickman. 1985. Apolipoprotein A-I synthesis in rat small intestine: regulation by dietary triglyceride and biliary lipid. J. Lipid Res. 26:368-379.
9. Apfelbaum, T.F., N.O. Davidson, and R.M. Glickman. 1987. Apolipoprotein A-IV synthesis in rat intestine: regulation by dietary triglyceride. Am. J. Physiol. 252:G662-G666.
10. Davidson, N.O., M.E. Kollmer, and R.M. Glickman. 1986. Apolipoprotein B synthesis in rat small intestine: regulation by dietary triglyceride and biliary lipid. J. Lipid Res. 27:30-39.
11. Chirgwin, J.M., A.E. Przybyla, R.J. MacDonald, and W.J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 18:5294-5299.
12. Kunkel, L.M., K.D. Smith, S.H. Boyer, D.S. Borgaonkar, S.S. Wachtel, O.J. Miller, W.R. Breg, H.W. Jones, Jr., and J.M. Rary. 1977. Analysis of human Y-chromosome-specific reiterated DNA in chromosome variants. Proc. Natl. Acad. Sci. USA. 74:1245-1249.
13. Ogami, K., M. Hadzopoulou-Cladaras, C. Cladaras, and V.I. Zannis. 1990. Promoter elements and factors required for hepatic and intestinal transcription of the human apoCIII gene. J. Biol. Chem. 265:9808-9815.
14. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
15. Luckow, B., and G. Schutz. 1987. CAT constructions with multiple unique restriction sites for functional analysis of eukaryotic promoter and regulatory elements. Nucleic Acids Res. 15:5490.
16. Edlund, T., M.D. Walker, P.J. Barr, and W.J. Rutter. 1985. Cell-specific expression of the rat insulin gene: evidence for role of two distinct 5′ flanking elements. Science (Wash. DC). 230:912-916.
17. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 11-20.
18. Graham, F.L., and A.J. Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 52:456-467.
19. Dignam, J.D., R.M. Lebovitz, and R.G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
20. Lowry, O.H., N.J. Rosenbrough, A.L. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
21. Dammerman, M., L.A. Sandkuijl, J.L. Halaas, W. Chung, and J.L. Breslow. 1993. An apolipoprotein CIII haplotype protective against hypertriglyceridemia is specified by promoter and 3′ untranslated region polymorphisms. Proc. Natl. Acad. Sci. USA. 90:4562-4566.
22. Green, P.H.R., R.M. Glickman, C.D. Saudek, C.B. Blum, and A.R. Tall. 1979. Human intestinal lipoproteins. Studies in chyluric subjects. J. Clin. Invest. 64:233-242.
23. Wu, A.L., and H.G. Windmueller. 1979. Relative contributions by liver and intestine to individual plasma apolipoproteins in the rat. J. Biol. Chem. 254: 7316-7322.
24. Windmueller, H.G., P.N. Herbert, and R.I. Levy. 1973. Biosynthesis of lymph and plasma lipoprotein apoproteins by isolated perfused rat liver and intestine. J. Lipid Res. 14:215-223.
25. Windmueller, H.G., and A.L. Wu. 1981. Biosynthesis of plasma apolipoproteins by rat small intestine without dietary or biliary fat. J. Biol. Chem. 256: 3012-3016.
26. Glickman, R.M., and A.M. Magun. 1986. High-density lipoprotein formation by the intestine. Methods Enzymol. 129:519-536.
27. Rubin, E.M., B.Y. Ishida, S.M. Clift, and R.M. Krauss. 1991. Expression of human apolipoprotein A-I in transgenic mice results in reduced plasma levels of murine apolipoprotein A-I and the appearance of two new high density lipoprotein size subclasses. Proc. Natl. Acad. Sci. USA. 88:434-438.
28. Walsh, A., Y. Ito, and J.L. Breslow. 1989. High levels of human apolipoprotein A-I in transgenic mice result in increased plasma levels of small high density lipoprotein (HDL) particles comparable to human HDL3. J. Biol. Chem. 264:6488-6494.
29. Kilbourne, E.J., R. Widom, D.C. Harnish, S. Malik, and S.K. Karathanasis. 1995. Involvement of early growth response factor Egr-1 in apolipoprotein AI gene transcription. J. Biol. Chem. 270:7004-7010.
30. Rottman, J.N., R.L. Widom, D. Nadal-Ginard, V. Mahdavi, and S.K. Karathanasis. 1991. A retinoic acid-responsive element in the apolipoprotein AI gene distinguishes between two different retinoic acid response pathways. Mol. Cell. Biol. 11:3814-3820.
31. Harnish, D.C., S. Malik, and S.K. Karathanasis. 1994. Activation of apolipoprotein AI gene transcription by the liver-enriched factor HNF-3. J. Biol. Chem. 269:28220-28226.
32. Reisher, S.R., T.E. Hughes, J.M. Ordovas, E.J. Schaefer, and S.I. Feinstein. 1993. Increased expression of apolipoprotein genes accompanies differentiation in the intestinal cell line Caco-2. Proc. Natl. Acad. Sci. USA. 90:5757-5761.
33. Bisaha, J.G., T.C. Simon, J.I. Gordon, and J.L. Breslow. 1995. Characterization of an enhancer element in the human apolipoprotein C-III gene that regulates human apolipoprotein A-I gene expression in the intestinal epithelium. J. Biol. Chem. 270:19979-19988.
34. Sorci-Thomas, M., M.M. Prack, N. Dashti, F. Johnson, L.L. Rudel, and D.L. Williams. 1988. Apolipoprotein (apo) AI production and mRNA abundance explain plasma apoAI and high density lipoprotein differences between two nonhuman primate species with high and low susceptibilities to diet-induced hypercholesterolemia. J. Biol. Chem. 263:5183-5189.
35. Sorci-Thomas, M., and M.W. Kearns. 1991. Transcriptional regulation of the apolipoprotein AI gene. J. Biol. Chem. 266:18045-18050.
36. Sorci-Thomas, M., M.M. Prack, N. Dashti, F. Johnson, L.L. Rudel, and D.L. Williams. 1989. Differential effects of dietary fat on the tissue-specific expression of the apolipoprotein AI gene: relationships to plasma concentration of high density lipoproteins. J. Lipid Res. 30:1397-1403.
37. Tam, S.P., T.K. Archer, and R.G. Deeley. 1986. Biphasic effects of estrogen on apolipoprotein synthesis in human hepatoma cells: mechanisms of antagonism by testosterone. Proc. Natl. Acad. Sci. USA. 83:3111-3115.
38. Elshourbagy, N.A., M.S. Boguski, W.S. Liao, L.S. Jefferson, J.I. Gordon, and J.M. Taylor. 1985. Expression of rat apolipoprotein A-IV and A-I genes: mRNA induction during development and in response to glucocorticoids and insulin. Proc. Natl. Acad. Sci. USA. 82:8242-8246.
39. Smith, J.D., E.A. Brinton, and J.L. Breslow. 1992. Polymorphism in the human apolipoprotein A-I gene promoter region. J. Clin. Invest. 89:1796-1800.
40. Hayek, T., Y. Ito, N. Azrolan, R.B. Verdery, K. Aalto-Setala, A. Walsh. and J.L. Breslow. 1993. Dietary fat increases high density lipoprotein (HDL) levels both by increasing the transport rates and decreasing the fractional catabolic rates of HDL cholesterol ester and apolipoprotein (apo) AI. J. Clin. Invest. 91:1665-1671.
41. Panduro, A., Y.C. Lin-Lee, L. Chanand, and D. A. Shafritz. 1990. Transcriptional and post-transcriptional regulation of apolipoprotein E, A-I, and A-II gene expression in normal rat liver and during several pathophysiologic states. Biochemistry. 29:8430-8435.
42. Golder-Novoselsky, E., T.M. Forte, A.V. Nichols, and E.M. Rubin. 1992. Apolipoprotein AI expression and high density lipoprotein distribution in transgenic mice during development. J. Biol. Chem. 267:20787-20790.
43. Surguchov, A.P., G.P. Page, L. Smith, W. Patsche, and E. Boerwinkle. 1996. Polymorphic markers in apolipoprotein CIII flanking regions and hypertriglyceridemia. Arterioscler. Throm. Vasc. Biol. 16:941-947.
44. Li, W.W., M.M. Dammerman, J.D. Smith, S. Metzger, J.L. Breslow, and T. Leff. 1995. Common genetic variation in the promoter of the human apoCIII gene abolishes regulation by insulin and may contribute to hypertriglyceridemia. J. Clin. Invest. 96:2601-2605.
45. Reaven, G.M. 1988. Role of insulin resistance in human disease. Diabetes. 37:1595-1607.
46. Ito, Y., N. Azrolan, A. O'Connell, A. Walsh, and J.L. Breslow. 1990. Hypertriglyceridemia as a result of human apoCIII gene expression in transgenic mice. Science (Wash. DC). 249:790-793.
47. Koivisto, U.M., J.J. Palvimo, O.A. Jaennem, and K. Kontula. 1994. A single-base substitution in the proximal Sp1 site of the human low density lipoprotein receptor promoter as a cause of heterozygous familial hypercholesterolemia. Proc. Natl. Acad. Sci. USA. 91:10526-10530.
48. Yang, W., D.N. Nevin, R. Peng, J.D. Brunzell, and S.R. Deeb. 1995. A mutation in the promoter of the lipoprotein lipase (LPL) gene in a patient with familial combined hyperlipidemia and low LPL activity. Proc. Natl. Acad. Sci. USA. 92:4462-4466.
49. Eriksson, P., B. Kallin, P.M. van't hooft, P. Bavenholm, and A. Hamsten. 1995. Allele-specific increase in basal transcription of the plasminogen-activator inhibitor 1 gene is associated with myocardial infarction. Proc. Natl. Acad. Sci. USA. 92:1851-1855.
50. Beaty, J.S., K.A. West, and G.T. Nepom. 1995. Functional effects of a natural polymorphism in the transcriptional regulatory sequence of HLA-DQB1. Mol. Cell. Biol. 15:4771-4782.
51. Louis, P., R. Vincent, P. Cavadore, J. Clot, and J.F. Eliaou. 1994. Differential transcriptional activities of HLA-DR genes in the various haplotypes. J. Immunol. 153:5059-5067.
52. s mutation. Blood. 79:787-792.
53. Efremov, D.G., A.J. Dimovoski, and T.H.J. Huisman. 1994. The -158 (C→T) promoter mutation is responsible for the increased transcription of the 3′ gamma gene in the Atlanta type of hereditary persistence of fetal hemoglobin. Blood. 83:3350-3355.
54. Crossley, M., and G.G. Brownlee. 1990. Distribution of a C/EBP binding site in the factor IX promoter is associated with haemophilia B. Nature (Lond.). 345:444-446.
55. Bienvenu, T., V. Lacronique, M. Raymondjean, C. Cazeneuve, D. Hubert, J.C. Kaplan, and C. Beldjord. 1995. Three novel sequence variations in the 5′ upstream region of the cystic fibrosis transmembrane conductance regulator (CFTR) gene: two polymorphisms and one putative molecular defect. Hum. Genet. 95:698-702.