Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery

Journal of Clinical Investigation

Volumn 92, Issue 2, 1993, Pages 883-893

  Ishibashi, Shun ^a   Brown, Michael S ^a   Goldstein, Joseph L ^a   Gerard, Robert D ^a   Hammer, Robert E ^a,b   Herz, Joachim ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Gene therapy; Homologous recombination; Lipoprotein metabolism; Liver receptors; Very low density lipoprotein

Indexed keywords

CHOLESTEROL; INTERMEDIATE DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; VERY LOW DENSITY LIPOPROTEIN;

ADENOVIRUS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CHOLESTEROL INTAKE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE THERAPY; GENETIC RECOMBINATION; HYPERCHOLESTEROLEMIA; LIPOPROTEIN METABOLISM; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ALLELES; ANIMAL; BASE SEQUENCE; CHOLESTEROL; CHOLESTEROL, DIETARY; CHROMOSOME MAPPING; CROSSES, GENETIC; EMBRYO; FEMALE; GENE THERAPY; HUMAN; HYPERCHOLESTEROLEMIA; LIPOPROTEINS; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; LIVER; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES; RECEPTORS, LDL; RECOMBINATION, GENETIC; RESTRICTION MAPPING; STEM CELLS; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0027258140     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI116663     Document Type: Article

References (52)

1. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science (Wash. DC). 232:34-47.
2. Goldstein, J. L., and M. S. Brown. 1989. Familial hypercholesterolemia. In The Metabolic Basis of Inherited Disease. C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill Publishing Co., New York, 1215-1250.
3. Mahley, R. W. 1988. Apolipoprotein E: Cholesterol transport protein with expanding role in cell biology. Science (Wash. DC). 240:622-630.
4. Brown, M. S., J. Herz, R. C. Kowal, and J. L. Goldstein. 1991. The low-density lipoprotein receptor-related protein: double agent or decoy? Curr. Opin. in Lipidol. 2:65-72.
5. Ji, Z.-S., W. J. Brecht, D. Miranda, M. M. Hussain, T. L. Innerarity, and R. W. Mahley. 1993. Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells. J. Biol. Chem. 268:10160-10167.
6. Hobbs, H. H., M. S. Brown, and J. L. Goldstein. 1992. Molecular genetics of the LDL receptor gene in familial hypercholesterolemia. Hum. Mutat. 1:445-466.
7. Watanabe, Y., T. Ito, and M. Shiomi. 1985. The effect of selective breeding on the development of coronary atherosclerosis in WHHL rabbits. An animal model for familial hypercholesterolemia. Atherosclerosis. 56:71-97.
8. Scanu, A. M., A. Khalil, L. Neven, M. Tidore, G. Dawson, D. Pfaffinger, E. Jackson, K. D. Carey, H. C. McGill, and G. M. Hess. 1988. Genetically determined hypercholesterolemia in a rhesus monkey family due to a deficiency of the LDL receptor. J. Lipid Res. 29:1671-1681.
9. Soutar, A. K., N. B. Myant, and G. R. Thompson. 1982. The metabolism of very low density and intermediate density lipoproteins in patients with familial hypercholesterolaemia. Atherosclerosis. 43:217-231.
10. Kita, T., M. S. Brown, D. W. Bilheimer, and J. L. Goldstein. 1982. Delayed clearance of very low density and intermediate density lipoproteins with enhanced conversion to low density lipoprotein in WHHL rabbits. Proc. Natl. Acad. Sci. USA. 79:5693-5697.
11. Hobos, H. H., E. Leitersdorf, C. C. Leffert, D. R. Cryer, M. S. Brown, and J. L. Goldstein. 1989. Evidence for a dominant gene that suppresses hypercholesterolemia in a family with defective low density lipoprotein receptors. J. Clin. Invest. 84:656-664.
12. Lamon-Fava, S., D. Jimenez, J. C. Christian, R. R. Fabsitz, T. Reed, D. Carmelli, W. P. Castelli, J. M. Ordovas, P. W. F. Wilson, and E. J. Schaefer. 1991. The NHLBI twin study: heritability of apolipoprotein A-I, B, and low density lipoprotein subclasses and concordance for lipoprotein(a). Atherosclerosis. 91:97-106.
13. Spady, D. K., L. A. Woollett, and J. M. Dietschy. 1993. Regulation of plasma LDL-cholesterol levels by dietary cholesterol and fatty acids. Annu. Rev. Nutr. 13:355-381.
14. Higuchi, K., K. Kitagawa, K. Kogishi, and T. Takeda. 1992. Developmental and age-related changes in apolipoprotein B mRNA editing in mice. J. Lipid Res. 33:1753-1764.
15. Scott, J. 1989. The molecular and cell biology of apolipoprotein-B. Mol. Biol. Med. 6:65-80.
16. Chan, L. 1992. Apolipoprotein B, the major protein component of triglyceride-rich and low density lipoproteins. J. Biol. Chem. 267:25621-25624.
17. Van't Hooft, F. M., D. A. Hardman, J. P. Kane, and R. J. Havel. 1982. Apolipoprotein B (B-48) of rat chylomicrons is not a precursor of the apolipoprotein of low density lipoproteins. Proc. Natl. Acad. Sci. USA. 79:179-182.
18. Chowdhury, J. R., M. Grossman, S. Gupta, N. R. Chowdhury, J. R. Baker, Jr., and J. M. Wilson. 1991. Long-term improvement of hypercholesterolemia after ex vivo gene therapy in LDLR-deficient rabbits. Science (Wash. DC). 254:1802-1805.
19. Wilson, J. M., M. Grossman, C. H. Wu, N. R. Chowdhury, G. Y. Wu, and J. R. Chowdhury. 1992. Hepatocyte-directed gene transfer in vivo leads to transient improvement of hypercholesterolemia in low density lipoprotein receptor-deficient rabbits. J. Biol. Chem. 267:963-967.
20. Hofmann, S. L., D. W. Russell, M. S. Brown, J. L. Goldstein, and R. E. Hammer. 1988. Overexpression of low density lipoprotein (LDL) receptor eliminates LDL from plasma in transgenic mice. Science (Wash. DC). 239:1277-1281.
21. Pathak, R. K., M. Yokode, R. E. Hammer, S. L. Hofmann, M. S. Brown, J. L. Goldstein, and R. G. W. Anderson. 1990. Tissue-specific sorting of the human LDL receptor in polarized epithelia of transgenic mice. J. Cell Biol. 111:347-359.
22. Yokode, M., R. E. Hammer, S. Ishibashi, M. S. Brown, and J. L. Goldstein. 1990. Diet-induced hypercholesterolemia in mice: Prevention by overexpression of LDL receptors. Science (Wash. DC). 250:1273-1275.
23. Herz, J., and R. D. Gerard. 1993. Adenovirus-mediated low density lipoprotein receptor gene transfer accelerates cholesterol clearance in normal mice. Proc. Natl. Acad. Sci. USA. 90:2812-2816.
24. Stratford-Perricaudet, L. D., M. Levrero, J.-F. Chasse, M. Perricaudet, and P. Briand. 1990. Evaluation of the transfer and expression in mice of an enzyme-encoding gene using a human adenovirus vector. Hum. Gene Ther. 1:241-256.
25. Capecchi, M. R. 1989. Altering the genome by homologous recombination. Science (Wash. DC). 244:1288-1292.
26. Smithies, O. 1991. Altering genes in animals and humans. In Etiology of Human Disease at the DNA Level. J. Lindsten and U. Pettersson, editors. Raven Press, New York. 221-259.
27. Bradley, A. 1987. Production and analysis of chimaeric mice. In Teratocarcinomas and Embryonic Stem Cells: A Practical Approach. E. J. Robertson, editor. IRL Press, Oxford, UK/Washington, DC. 113-151.
28. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
29. Yokode, M., R. K. Pathak, R. E. Hammer, M. S. Brown, J. L. Goldstein, and R. G. W. Anderson. 1992. Cytoplasmic sequence required for basolateral targeting of LDL receptor in livers of transgenic mice. J. Cell Biol. 117:39-46.
30. Willnow, T. F., J. L. Goldstein, K. Orth, M. S. Brown, and J. Herz. 1992. Low density lipoprotein receptor-related protein (LRP) and gp330 bind similar ligands, including plasminogen activator-inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance. J. Biol. Chem. 267:26172-26180.
31. Goldstein, J. L., S. K. Basu, and M. S. Brown. 1983. Receptor-mediated endocytosis of LDL in cultured cells. Methods Enzymol. 98:241-260.
32. Yamamoto, T., C. G. Davis, M. S. Brown, W. J. Schneider, M. L. Casey, J. L. Goldstein, and D. W. Russell. 1984. The human LDL receptor A cysteinerich protein with multiple Alu sequences in its mRNA. Cell. 39:27-38.
33. Mehta, K. D., W.-J. Chen, J. L. Goldstein, and M. S. Brown. 1991. The low density lipoprotein receptor in Xenopus laevis. I. Five domains that resemble the human receptor. J. Biol. Chem. 266:10406-10414.
34. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell. 64:693-702.
35. Mansour, S. L., K. R. Thomas, and M. R. Capecchi. 1988. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature (Lond.). 336:348-352.
36. McMahon, A. P., and A. Bradley. 1990. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell. 62:1073-1085.
37. Russell, D. W., W. J. Schneider, T. Yamamoto, K. L. Luskey, M. S. Brown, and J. L. Goldstein. 1984. Domain map of the LDL receptor: sequence homology with the epidermal growth factor precursor. Cell. 37:577-585.
38. Yamada, N., D. M. Shames, K., Takahashi, and R. J. Havel. 1988. Metabolism of apolipoprotein B-100 in large very low density lipoproteins of blood plasma. J. Clin. Invest. 82:2106-2113.
39. Yamada, N., D. M. Shames, and R. J. Havel. 1987. Effect of LDL receptor deficiency on the metabolism of apolipoprotein B-100 in blood plasma: kinetic studies in normal and Watanabe heritable hyperlipidemic rabbits. J. Clin. Invest. 80:507-515.
40. Pittman, R. C., T. E. Carew, A. D. Attie, J. L. Witztum, Y. Watanabe, and D. Steinberg. 1982. Receptor-dependent and receptor-independent degradation of low density lipoprotein in normal rabbits and in receptor-deficient mutant rabbits. J. Biol. Chem. 257:7994-8000.
41. Spady, D. K., M. Huettinger, D. W. Bilheimer, and J. M. Dietschy. 1987. Role of receptor-independent low density lipoprotein transport in the maintenance of tissue cholesterol balance in the normal and WHHL rabbit. J. Lipid Res. 28:32-41.
42. Bilheimer, D. W., N. J. Stone, and S. M. Grundy. 1979. Metabolic studies in familial hypercholesterolemia: evidence for a gene-dosage effect in vivo. J. Clin. Invest. 64:524-533.
43. James, R. W., B. Martin, D. Pometta, J. C. Fruchart, P. Duriez, P. Fuchois, J. P. Farriaux, A. Tacquet, T. Demant, R. J. Clegg, A. Munro, M. F. Oliver et al. 1989. Apolipoprotein B metabolism in homozygous familial hypercholesterolemia. J. Lipid Res. 30:159-169.
44. Havel, R. J., T. Kita, L. Kotite, J. P. Kane, R. L. Hamilton, J. L. Goldstein, and M. S. Brown. 1982. Concentration and composition of lipoproteins in blood plasma of WHHL rabbits. Arteriosclerosis. 3:467-474.
45. Zhang, S. H., R. L. Reddick, J. A. Piedrahita, and N. Maeda. 1992. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science (Wash. DC). 258:468-471.
46. Plump, A. S., J. D. Smith, T. Hayek, K. Aalto-Setälä, A. Walsh, J. G. Verstuyft, E. M. Rubin, and J. L. Breslow. 1992. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E deficient mice created by homologous recombination in ES cells. Cell. 71:343-353.
47. Schaefer, E. J., R. E. Gregg, G. Ghiselli, T. M. Forte, J. M. Ordovas, L. A. Zech, and H. B. Brewer, Jr. 1986. Familial apolipoprotein E deficiency. J. Clin. Invest. 78:1206-1219.
48. Kovanen, P. T., M. S. Brown, S. K. Basu, D. W. Bilheimer, and J. L. Goldstein. 1981. Saturation and suppression of hepatic lipoprotein receptors: a mechanism for the hypercholesterolemia of cholesterol-fed rabbits. Proc. Natl. Acad. Sci. USA. 78:1396-1400.
49. Spady, D. K., and J. M. Dietschy. 1988. Interaction of dietary cholesterol and triglycerides in the regulation of hepatic low density lipoprotein transport in the hamster. J Clin. Invest. 81:300-309.
50. Ginsberg, H. S., L. L. Moldawer, P. B. Sehgal, M. Redington, P. L. Kilian, R. M. Chanock, and G. A. Prince. 1991. A mouse model for investigating the molecular pathogenesis of adenoviras pneumonia. Proc. Nail. Acad. Sci. USA. 88:1651-1655.
51. Kowal, R. C., J. Herz, J. L. Goldstein, V. Esser, and M. S. Brown. 1989. Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotem E-enriched lipoproteins. Proc. Natl. Acad. Sci. USA. 86:5810-5814.
52. Holmquist, L., K. Carlson, and L. A. Carlson. 1978. Comparison between the use of isopropanol and tetramethylurea for the solubilisation and quantitation of human serum very low density apolipoprotems. Anal. Biochem. 88:457-460.