Hypomorphic sialidase expression decreases serum cholesterol by downregulation of VLDL production in mice

Journal of Lipid Research

Volumn 53, Issue 12, 2012, Pages 2573-2585

  Yang, Abraham ^a   Gyulay, Gabriel ^a   Mitchell, Mark ^a   White, Elizabeth ^a   Trigatti, Bernardo L ^a,b   Igdoura, Suleiman A ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Adenovirus; Cholesterol metabolism; Neu1; Very low density lipoprotein

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 2; LOW DENSITY LIPOPROTEIN RECEPTOR; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; SIALIDASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL LIVER LEVEL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIPID STORAGE; LIPOPROTEIN SECRETION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOVIRIDAE; ANIMALS; CELL LINE; CHOLESTEROL; DOWN-REGULATION; HUMANS; LIPOPROTEINS, VLDL; MICE; MICE, INBRED STRAINS; NEURAMINIDASE; REAL-TIME POLYMERASE CHAIN REACTION; TRIGLYCERIDES;

EID: 84869013855     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M027300     Document Type: Article

References (86)

1. Hegele, R. A. 2009. Plasma lipoproteins: genetic influences and clinical implications. Nat. Rev. Genet. 10: 109-121.
2. Glass, C. K., and J. L. Witztum. 2001. Atherosclerosis: the road ahead. Cell. 104: 503-516. (Pubitemid 32201946)
3. Reuter, G., and H. J. Gabius. 1996. Sialic acids structure-analysis- metabolism-occurrence-recognition. Biol. Chem. Hoppe Seyler. 377: 325-342.
4. Collard, J. G., J. F. Schijven, A. Bikker, R. G. La, J. G. Bolscher, and E. Roos. 1986. Cell surface sialic acid and the invasive and metastatic potential of T-cell hybridomas. Cancer Res. 46: 3521-3527. (Pubitemid 16096901)
5. Pilatte, Y., J. Bignon, and C. R. Lambre. 1993. Sialic acids as important molecules in the regulation of the immune system: pathophysiological implications of sialidases in immunity. Glycobiology. 3: 201-218.
6. Varki, A. 1997. Sialic acids as ligands in recognition phenomena. FASEB J. 11: 248-255. (Pubitemid 27118325)
7. Bonten, E., A. van der Spoel, M. Fornerod, G. Grosveld, and A. d'Azzo. 1996. Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis. Genes Dev. 10: 3156-3169. (Pubitemid 27020543)
8. Varki, A. 2008. Sialic acids in human health and disease. Trends Mol. Med. 14: 351-360.
9. Abdulkhalek, S., S. R. Amith, S. L. Franchuk, P. Jayanth, M. Guo, T. Finlay, A. Gilmour, C. Guzzo, K. Gee, R. Beyaert, et al. 2011. Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for Toll-like receptor activation and cellular signaling. J. Biol. Chem. 286: 36532-36549.
10. Katoh, S., T. Miyagi, H. Taniguchi, Y. Matsubara, J. Kadota, A. Tominaga, P. W. Kincade, S. Matsukura, and S. Kohno. 1999. Cutting edge: an inducible sialidase regulates the hyaluronic acid binding ability of CD44-bearing human monocytes. J. Immunol. 162: 5058-5061. (Pubitemid 29307104)
11. Cuff, C. A., D. Kothapalli, I. Azonobi, S. Chun, Y. Zhang, R. Belkin, C. Yeh, A. Secreto, R. K. Assoian, D. J. Rader, et al. 2001. The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Invest. 108: 1031-1040. (Pubitemid 32946077)
12. Gee, K., M. Kozlowski, and A. Kumar. 2003. Tumor necrosis factor-alpha induces functionally active hyaluronan-adhesive CD44 by activating sialidase through p38 mitogen-activated protein kinase in lipopolysaccharide-stimulated human monocytic cells. J. Biol. Chem. 278: 37275-37287. (Pubitemid 37175244)
13. Khan, A. I., S. M. Kerfoot, B. Heit, L. Liu, G. Andonegui, B. Ruffell, P. Johnson, and P. Kubes. 2004. Role of CD44 and hyaluronan in neutrophil recruitment. J. Immunol. 173: 7594-7601. (Pubitemid 39628201)
14. Gadhoum, S. Z., and R. Sackstein. 2008. CD15 expression in human myeloid cell differentiation is regulated by sialidase activity. Nat. Chem. Biol. 4: 751-757.
15. Katoh, S., S. Maeda, H. Fukuoka, T. Wada, S. Moriya, A. Mori, K. Yamaguchi, S. Senda, and T. Miyagi. 2010. A crucial role of sialidase Neu1 in hyaluronan receptor function of CD44 in T helper type 2-mediated airway inflammation of murine acute asthmatic model. Clin. Exp. Immunol. 161: 233-241.
16. Katoh, S., O. Kaminuma, T. Hiroi, A. Mori, T. Ohtomo, S. Maeda, H. Shimizu, Y. Obase, and M. Oka. 2011. CD44 is critical for airway accumulation of antigen-specific Th2, but not Th1, cells induced by antigen challenge in mice. Eur. J. Immunol. 41: 3198-3207.
17. Feng, C., L. Zhang, L. Almulki, S. Faez, M. Whitford, A. Hafezi- Moghadam, and A. S. Cross. 2011. Endogenous PMN sialidase activity exposes activation epitope on CD11b/CD18 which enhances its binding interaction with ICAM-1. J. Leukoc. Biol. 90: 313-321.
18. Lambré, C. R., A. Greffard, L. Gattegno, and L. Saffar. 1990. Modifications of sialidase activity during the monocyte-macrophage differentiation in vitro. Immunol. Lett. 23: 179-182. (Pubitemid 20058776)
19. Liang, F., V. Seyrantepe, K. Landry, R. Ahmad, A. Ahmad, N. M. Stamatos, and A. V. Pshezhetsky. 2006. Monocyte differentiation up-regulates the expression of the lysosomal sialidase, Neu1, and triggers its targeting to the plasma membrane via major histocompatibility complex class II-positive compartments. J. Biol. Chem. 281: 27526-27538. (Pubitemid 44401779)
20. Stamatos, N. M., F. Liang, X. Nan, K. Landry, A. S. Cross, L. X. Wang, and A. V. Pshezhetsky. 2005. Differential expression of endogenous sialidases of human monocytes during cellular differentiation into macrophages. FEBS J. 272: 2545-2556. (Pubitemid 40705074)
21. Pappu, B. P., and P. A. Shrikant. 2004. Alteration of cell surface sialylation regulates antigen-induced naive CD8+ T cell responses. J. Immunol. 173: 275-284. (Pubitemid 38797352)
22. Xu, Z., and A. Weiss. 2002. Negative regulation of CD45 by differential homodimerization of the alternatively spliced isoforms. Nat. Immunol. 3: 764-771.
23. Chen, X. P., E. Y. Enioutina, and R. A. Daynes. 1997. The control of IL-4 gene expression in activated murine T lymphocytes: a novel role for neu-1 sialidase. J. Immunol. 158: 3070-3080.
24. Cross, A. S., and D. G. Wright. 1991. Mobilization of sialidase from intracellular stores to the surface of human neutrophils and its role in stimulated adhesion responses of these cells. J. Clin. Invest. 88: 2067-2076.
25. Cross, A. S., S. Sakarya, S. Rifat, T. K. Held, B. E. Drysdale, P. A. Grange, F. J. Cassels, L. X. Wang, N. Stamatos, A. Farese, et al. 2003. Recruitment of murine neutrophils in vivo through endogenous sialidase activity. J. Biol. Chem. 278: 4112-4120. (Pubitemid 36801147)
26. Sakarya, S., S. Rifat, J. Zhou, D. D. Bannerman, N. M. Stamatos, A. S. Cross, and S. E. Goldblum. 2004. Mobilization of neutrophil sialidase activity desialylates the pulmonary vascular endothelial surface and increases resting neutrophil adhesion to and migration across the endothelium. Glycobiology. 14: 481-494. (Pubitemid 38868263)
27. Igdoura, S. A., C. Gafuik, C. Mertineit, F. Saberi, A. V. Pshezhetsky, M. Potier, J. M. Trasler, and R. A. Gravel. 1998. Cloning of the cDNA and gene encoding mouse lysosomal sialidase and correction of sialidase deficiency in human sialidosis and mouse SM/J fibroblasts. Hum. Mol. Genet. 7: 115-121.
28. Carrillo, M. B., C. M. Milner, S. T. Ball, M. Snoek, and R. D. Campbell. 1997. Cloning and characterization of a sialidase from the murine histocompatibility-2 complex: low levels of mRNA and a single amino acid mutation are responsible for reduced sialidase activity in mice carrying the Neu1a allele. Glycobiology. 7: 975-986.
29. Pshezhetsky, A. V., C. Richard, L. Michaud, S. Igdoura, S. Wang, M. A. Elsliger, J. Qu, D. Leclerc, R. Gravel, L. Dallaire, et al. 1997. Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis. Nat. Genet. 15: 316-320. (Pubitemid 27098731)
30. Monti, E., A. Preti, E. Rossi, A. Ballabio, and G. Borsani. 1999. Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases. Genomics. 57: 137-143. (Pubitemid 29187946)
31. Ferrari, J., R. Harris, and T. G. Warner. 1994. Cloning and expression of a soluble sialidase from Chinese hamster ovary cells: sequence alignment similarities to bacterial sialidases. Glycobiology. 4: 367-373. (Pubitemid 24217253)
32. Miyagi, T., T. Wada, A. Iwamatsu, K. Hata, Y. Yoshikawa, S. Tokuyama, and M. Sawada. 1999. Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J. Biol. Chem. 274: 5004-5011.
33. Wada, T., Y. Yoshikawa, S. Tokuyama, M. Kuwabara, H. Akita, and T. Miyagi. 1999. Cloning, expression, and chromosomal mapping of a human ganglioside sialidase. Biochem. Biophys. Res. Commun. 261: 21-27. (Pubitemid 29371612)
34. Comelli, E. M., M. Amado, S. R. Lustig, and J. C. Paulson. 2003. Identification and expression of Neu4, a novel murine sialidase. Gene. 321: 155-161. (Pubitemid 37421406)
35. Monti, E., M. T. Bassi, R. Bresciani, S. Civini, G. L. Croci, N. Papini, M. Riboni, G. Zanchetti, A. Ballabio, A. Preti, et al. 2004. Molecular cloning and characterization of NEU4, the fourth member of the human sialidase gene family. Genomics. 83: 445-453. (Pubitemid 38220849)
36. Seyrantepe, V., A. Hinek, J. Peng, M. Fedjaev, S. Ernest, Y. Kadota, M. Canuel, K. Itoh, C. R. Morales, J. Lavoie, et al. 2008. Enzymatic activity of lysosomal carboxypeptidase (cathepsin) A is required for proper elastic fiber formation and inactivation of endothelin-1. Circulation. 117: 1973-1981. (Pubitemid 351543473)
37. O'Brien, J. S., and T. G. Warner. 1980. Sialidosis: delineation of subtypes by neuraminidase assay. Clin. Genet. 17: 35-38. (Pubitemid 10187588)
38. Sprague, E. A., M. Moser, E. H. Edwards, and C. J. Schwartz. 1988. Stimulation of receptor-mediated low density lipoprotein endocytosis in neuraminidase-treated cultured bovine aortic endothelial cells. J. Cell. Physiol. 137: 251-262. (Pubitemid 19009021)
39. Afzali, B., R. S. Bakri, P. Bharma-Ariza, P. J. Lumb, N. Dalton, N. C. Turner, A. S. Wierzbicki, M. A. Crook, and D. J. Goldsmith. 2003. Raised plasma total sialic acid levels are markers of cardiovascular disease in renal dialysis patients. J. Nephrol. 16: 540-545. (Pubitemid 38120463)
40. Gokmen, S. S., G. Kilicli, F. Ozcelik, M. Ture, and S. Gulen. 2002. Association between serum total and lipid-bound sialic acid concentration and the severity of coronary atherosclerosis. J. Lab. Clin. Med. 140: 110-118. (Pubitemid 35028785)
41. Sathiyapriya, V., N. Selvaraj, H. Nandeesha, Z. Bobby, A. Aparna, and P. Pavithran. 2008. Association between protein bound sialic acid and high sensitivity C-reactive protein in prehypertension: a possible indication of underlying cardiovascular risk. Clin. Exp. Hypertens. 30: 367-374. (Pubitemid 352009294)
42. Orekhov, A. N., V. V. Tertov, I. A. Sobenin, V. N. Smirnov, D. P. Via, J. Guevara, Jr., A. M. Gotto, Jr., and J. D. Morrisett. 1992. Sialic acid content of human low density lipoproteins affects their interaction with cell receptors and intracellular lipid accumulation. J. Lipid Res. 33: 805-817.
43. Goldstein, J. L., M. S. Brown, R. G. Anderson, D. W. Russell, and W. J. Schneider. 1985. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1: 1-39.
44. Davis, C. G., A. Elhammer, D. W. Russell, W. J. Schneider, S. Kornfeld, M. S. Brown, and J. L. Goldstein. 1986. Deletion of clustered O-linked carbohydrates does not impair function of low density lipoprotein receptor in transfected fibroblasts. J. Biol. Chem. 261: 2828-2838. (Pubitemid 17218299)
45. Kozarsky, K., D. Kingsley, and M. Krieger. 1988. Use of a mutant cell line to study the kinetics and function of O-linked glycosylation of low density lipoprotein receptors. Proc. Natl. Acad. Sci. USA. 85: 4335-4339.
46. Kingsley, D. M., K. F. Kozarsky, L. Hobbie, and M. Krieger. 1986. Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase deficient mutant. Cell. 44: 749-759. (Pubitemid 16073971)
47. Cummings, R. D., S. Kornfeld, W. J. Schneider, K. K. Hobgood, H. Tolleshaug, M. S. Brown, and J. L. Goldstein. 1983. Biosynthesis of N- and O-linked oligosaccharides of the low density lipoprotein receptor. J. Biol. Chem. 258: 15261-15273. (Pubitemid 14178957)
48. Filipovic, I. 1989. Effect of inhibiting N-glycosylation on the stability and binding activity of the low density lipoprotein receptor. J. Biol. Chem. 264: 8815-8820. (Pubitemid 19151604)
49. Millar, J. S. 2001. The sialylation of plasma lipoproteins. Atherosclerosis 154: 1-13. (Pubitemid 32008558)
50. Stoline, A. M., K. Saku, B. A. Hynd, and M. L. Kashyap. 1985. Effect of desialylation of very low-density lipoproteins on their catabolism by lipoprotein lipase. Metabolism. 34: 30-35. (Pubitemid 15150412)
51. Lee, Y., M. Kockx, M. J. Raftery, W. Jessup, R. Griffith, and L. Kritharides. 2010. Glycosylation and sialylation of macrophage-derived human apolipoprotein E analyzed by SDS-PAGE and mass spectrometry: evidence for a novel site of glycosylation on Ser290. Mol. Cell. Proteomics. 9: 1968-1981.
52. Kawakami, A., M. Aikawa, P. Libby, P. Alcaide, F. W. Luscinskas, and F. M. Sacks. 2006. Apolipoprotein CIII in apolipoprotein B lipoproteins enhances the adhesion of human monocytic cells to endothelial cells. Circulation. 113: 691-700.
53. Potier, M., Y. D. Lu Shun, and J. E. Womack. 1979. Neuraminidase deficiency in the mouse. FEBS Lett. 108: 345-348. (Pubitemid 10126512)
54. Womack, J. E., D. L. Yan, and M. Potier. 1981. Gene for neuraminidase activity on mouse chromosome 17 near h-2: pleiotropic effects on multiple hydrolases. Science. 212: 63-65. (Pubitemid 11114681)
55. Clark, E. A., D. Engel, and N. T. Windsor. 1981. Immune responsiveness of SM/J mice: hyper NK cell activity mediated by NK 1+ Qa 5- cells. J. Immunol. 127: 2391-2395. (Pubitemid 12245826)
56. Champigny, M. J., M. Mitchell, A. Fox-Robichaud, B. L. Trigatti, and S. A. Igdoura. 2009. A point mutation in the neu1 promoter recruits an ectopic repressor, Nkx3.2 and results in a mouse model of sialidase deficiency. Mol. Genet. Metab. 97: 43-52.
57. Hara, T., M. Ichihara, M. Takagi, and A. Miyajima. 1995. Interleukin-3 (IL-3) poor-responsive inbred mouse strains carry the identical deletion of a branch point in the IL-3 receptor alpha subunit gene. Blood. 85: 2331-2336.
58. Blankenhorn, E. P., G. Bryan, A. V. Kossenkov, L. D. Clark, X. M. Zhang, C. Chang, W. Horng, L. S. Pletscher, J. M. Cheverud, L. C. Showe, et al. 2009. Genetic loci that regulate healing and regeneration in LG/J and SM/J mice. Mamm. Genome. 20: 720-733.
59. Pattison, S., M. Pankarican, C. A. Rupar, F. L. Graham, and S. A. Igdoura. 2004. Five novel mutations in the lysosomal sialidase gene (NEU1) in type II sialidosis patients and assessment of their impact on enzyme activity and intracellular targeting using adenovirus-mediated expression. Hum. Mutat. 23: 32-39. (Pubitemid 38056099)
60. Champigny, M. J., M. Johnson, and S. A. Igdoura. 2003. Characterization of the mouse lysosomal sialidase promoter. Gene. 319: 177-187. (Pubitemid 37346212)
61. Hitt, M. M., and F. L. Graham. 2000. Adenovirus vectors for human gene therapy. Adv. Virus Res. 55: 479-505.
62. Kaboord, B., and M. Perr. 2008. Isolation of proteins and protein complexes by immunoprecipitation. Methods Mol. Biol. 424: 349-364.
63. Knibbs, R. N., I. J. Goldstein, R. M. Ratcliffe, and N. Shibuya. 1991. Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266: 83-88. (Pubitemid 21906093)
64. Rigotti, A., B. L. Trigatti, M. Penman, H. Rayburn, J. Herz, and M. Krieger. 1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc. Natl. Acad. Sci. USA. 94: 12610-12615. (Pubitemid 27492576)
65. Vaisman, B. L., H. G. Klein, M. Rouis, A. M. Berard, M. R. Kindt, G. D. Talley, S. M. Meyn, R. F. Hoyt, Jr., S. M. Marcovina, and J. J. Albers. 1995. Overexpression of human lecithin cholesterol acyltransferase leads to hyperalphalipoproteinemia in transgenic mice. J. Biol. Chem. 270: 12269-12275.
66. de Silva, H. V., J. Mas-Oliva, J. M. Taylor, and R. W. Mahley. 1994. Identification of apolipoprotein B-100 low density lipoproteins, apolipoprotein B-48 remnants, and apolipoprotein E-rich high density lipoproteins in the mouse. J. Lipid Res. 35: 1297-1310. (Pubitemid 24209404)
67. Gordon, D. A., J. R. Wetterau, and R. E. Gregg. 1995. Microsomal triglyceride transfer protein: a protein complex required for the assembly of lipoprotein particles. Trends Cell Biol. 5: 317-321.
68. Wetterau, J. R., R. E. Gregg, T. W. Harrity, C. Arbeeny, M. Cap, F. Connolly, C. H. Chu, R. J. George, D. A. Gordon, H. Jamil, et al. 1998. An MTP inhibitor that normalizes atherogenic lipoprotein levels in WHHL rabbits. Science. 282: 751-754. (Pubitemid 28489389)
69. Gordon, D. A., H. Jamil, R. E. Gregg, S. O. Olofsson, and J. Boren. 1996. Inhibition of the microsomal triglyceride transfer protein blocks the first step of apolipoprotein B lipoprotein assembly but not the addition of bulk core lipids in the second step. J. Biol. Chem. 271: 33047-33053. (Pubitemid 27008743)
70. Rubin, D., A. Schneider-Muntau, M. Klapper, I. Nitz, U. Helwig, U. R. Folsch, J. Schrezenmeir, and F. Doring. 2008. Functional analysis of promoter variants in the microsomal triglyceride transfer protein (MTTP) gene. Hum. Mutat. 29: 123-129.
71. Horton, J. D., I. Shimomura, M. S. Brown, R. E. Hammer, J. L. Goldstein, and H. Shimano. 1998. Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2. J. Clin. Invest. 101: 2331-2339. (Pubitemid 28270427)
72. Cases, S., S. Novak, Y. W. Zheng, H. M. Myers, S. R. Lear, E. Sande, C. B. Welch, A. J. Lusis, T. A. Spencer, B. R. Krause, et al. 1998. ACAT-2, a second mammalian acyl-CoA:cholesterol acyltransferase. Its cloning, expression, and characterization. J. Biol. Chem. 273: 26755-26764. (Pubitemid 28471692)
73. Yen, C. L., S. J. Stone, S. Koliwad, C. Harris, and R. V. Farese, Jr. 2008. Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J. Lipid Res. 49: 2283-2301.
74. Abifadel, M., M. Varret, J. P. Rabes, D. Allard, K. Ouguerram, M. Devillers, C. Cruaud, S. Benjannet, L. Wickham, D. Erlich, et al. 2003. Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat. Genet. 34: 154-156. (Pubitemid 36666925)
75. Cohen, J., A. Pertsemlidis, I. K. Kotowski, R. Graham, C. K. Garcia, and H. H. Hobbs. 2005. Low LDL cholesterol in individuals of African descent resulting from frequent nonsense mutations in PCSK9. Nat. Genet. 37: 161-165.
76. Maxwell, K. N., R. E. Soccio, E. M. Duncan, E. Sehayek, and J. L. Breslow. 2003. Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice. J. Lipid Res. 44: 2109-2119. (Pubitemid 37509626)
77. Park, S. W., Y. A. Moon, and J. D. Horton. 2004. Post-transcriptional regulation of low density lipoprotein receptor protein by proprotein convertase subtilisin/kexin type 9a in mouse liver. J. Biol. Chem. 279: 50630-50638.
78. Horton, J. D., J. C. Cohen, and H. H. Hobbs. 2007. Molecular biology of PCSK9: its role in LDL metabolism. Trends Biochem. Sci. 32: 71-77. (Pubitemid 46199197)
79. Horton, J. D., N. A. Shah, J. A. Warrington, N. N. Anderson, S. W. Park, M. S. Brown, and J. L. Goldstein. 2003. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA. 100: 12027-12032. (Pubitemid 37271509)
80. Horton, J. D., J. L. Goldstein, and M. S. Brown. 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109: 1125-1131. (Pubitemid 34496588)
81. Brown, M. S., and J. L. Goldstein. 1997. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 89: 331-340. (Pubitemid 27220877)
82. Sun, L. P., L. Li, J. L. Goldstein, and M. S. Brown. 2005. Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro. J. Biol. Chem. 280: 26483-26490. (Pubitemid 41022245)
83. Horton, J. D., H. Shimano, R. L. Hamilton, M. S. Brown, and J. L. Goldstein. 1999. Disruption of LDL receptor gene in transgenic SREBP-1a mice unmasks hyperlipidemia resulting from production of lipid-rich VLDL. J. Clin. Invest. 103: 1067-1076. (Pubitemid 29169615)
84. Sato, R., W. Miyamoto, J. Inoue, T. Terada, T. Imanaka, and M. Maeda. 1999. Sterol regulatory element-binding protein negatively regulates microsomal triglyceride transfer protein gene transcription. J. Biol. Chem. 274: 24714-24720.
85. Chang, T. Y., B. L. Li, C. C. Chang, and Y. Urano. 2009. Acylcoenzyme A:cholesterol acyltransferases. Am. J. Physiol. Endocrinol. Metab. 297: E1-E9.
86. Millar, J. S., S. J. Stone, U. J. Tietge, B. Tow, J. T. Billheimer, J. S. Wong, R. L. Hamilton, R. V. Farese, Jr., and D. J. Rader. 2006. Short-term overexpression of DGAT1 or DGAT2 increases hepatic triglyceride but not VLDL triglyceride or apoB production. J. Lipid Res. 47: 2297-2305. (Pubitemid 44936140)