Apolipoprotein B-containing lipoprotein assembly in microsomal triglyceride transfer protein-deficient McA-RH7777 cells

Journal of Lipid Research

Volumn 51, Issue 8, 2010, Pages 2253-2264

  Liu, Yanwen ^a   Manchekar, Medha ^a   Sun, Zhihuan ^a   Richardson, Paul E ^a   Dashti, Nassrin ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b Wall College of Business   (United States)

Author keywords

Atherosclerosis; Hepatic lipoproteins; Liver; Triglyceride rich lipoprotein biosynthesis; VLDL secretion

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN B48; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; APOLIPOPROTEIN B100; CARRIER PROTEIN; PHOSPHOLIPID;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL STRAIN MCA RH7777; CELL TRANSFORMATION; CONTROLLED STUDY; GENE CASSETTE; GENE SILENCING; IMMUNOPRECIPITATION; LIPID ANALYSIS; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RAT; ANIMAL; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC TRANSFORMATION; GENETICS; HUMAN; METABOLISM; RNA INTERFERENCE; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; APOLIPOPROTEIN B-100; APOLIPOPROTEIN B-48; APOLIPOPROTEINS B; CARRIER PROTEINS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; PHOSPHOLIPIDS; RATS; RNA INTERFERENCE; TRANSFORMATION, GENETIC;

EID: 77956821591     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M005371     Document Type: Article

References (62)

1. Blasiole, D. A., R. A. Davis, and A. D. Attie. 2007. The physiological and molecular regulation of lipoprotein assembly and secretion. Mol. Biosyst. 3: 608-619.
2. Schumaker, V. N., M. L. Phillips, and J. E. Chatterton. 1994. Apolipoprotein B and low-density lipoprotein structure: implications for biosynthesis of triglyceride-rich lipoproteins. Adv. Protein Chem. 45: 205-248.
3. Fisher, E. A., and H. N. Ginsberg. 2002. Complexity in the secretory pathway: the assembly and secretion of apolipoprotein B-containing lipoproteins. J. Biol. Chem. 277: 17377-17380.
4. Elovson, J., J. E. Chatterton, G. T. Bell, V. N. Schumaker, M. A. Reuben, D. L. Puppione, J. R. Reeve, Jr., and N. L. Young. 1988. Plasma very low density lipoproteins contain a single molecule of apolipoprotein B. J. Lipid Res. 29: 1461-1473.
5. Chan, L. 1992. Apolipoprotein B, the major protein component of triglyceride-rich and low density lipoproteins. J. Biol. Chem. 267: 25621-25624.
6. Xie, Y., J. Luo, S. Kennedy, and N. O. Davidson. 2007. Conditional intestinal lipotoxicity in Apobec-1-/- Mttp-IKO mice: a survival advantage for mammalian intestinal apolipoprotein B mRNA editing. J. Biol. Chem. 282: 33043-33051.
7. Knott, T. J., R. J. Pease, L. M. Powell, S. C. Wallis, S. C. Rall, Jr., T. L. Innerarity, B. Blackhart, W. H. Taylor, Y. Marcel, R. Milne, et al. 1986. Complete protein sequence and identification of structural domains of human apolipoprotein B. Nature. 323: 734-738.
8. Yang, C. Y., S. H. Chen, S. H. Gianturco, W. A. Bradley, J. T. Sparrow, M. Tanimura, W. H. Li, D. A. Sparrow, H. DeLoof, M. Rosseneu, et al. 1986. Sequence, structure, receptor-binding domains and internal repeats of human apolipoprotein B-100. Nature. 323: 738-742.
9. Bell-Quint, J., T. Forte, and P. Graham. 1981. Synthesis of two forms of apolipoprotein B by cultured rat hepatocytes. Biochem. Biophys. Res. Commun. 99: 700-706.
10. Alexander, C. A., R. L. Hamilton, and R. J. Havel. 1976. Subcellular localization of B apoprotein of plasma lipoproteins in rat liver. J. Cell Biol. 69: 241-263.
11. Olofsson, S. O., P. Stillemark-Billton, and L. Asp. 2000. Intracellular assembly of VLDL: two major steps in separate cell compartments. Trends Cardiovasc. Med. 10: 338-345.
12. Davis, R. A. 1999. Cell and molecular biology of the assembly and secretion of apolipoprotein B-containing lipoproteins by the liver. Biochim. Biophys. Acta. 1440: 1-31.
13. Hamilton, R. L., J. S. Wong, C. M. Cham, L. B. Nielsen, and S. G. Young. 1998. Chylomicron-sized lipid particles are formed in the setting of apolipoprotein B deficiency. J. Lipid Res. 39: 1543-1557.
14. Boren, J., S. Rustaeus, and S. O. Olofsson. 1994. Studies on the assembly of apolipoprotein B-100- and B-48-containing very low density lipoproteins in McA-RH7777 cells. J. Biol. Chem. 269: 25879-25888.
15. Wetterau, J. R., L. P. Aggerbeck, M. E. Bouma, C. Eisenberg, A. Munck, M. Hermier, J. Schmitz, G. Gay, D. J. Rader, and R. E. Gregg. 1992. Absence of microsomal triglyceride transfer protein in individuals with abetalipoproteinemia. Science. 258: 999-1001.
16. Gordon, D. A. 1997. Recent advances in elucidating the role of the microsomal triglyceride transfer protein in apolipoprotein B lipoprotein assembly. Curr. Opin. Lipidol. 8: 131-137.
17. Hussain, M. M., J. Shi, and P. Dreizen. 2003. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res. 44: 22-32.
18. Xie, Y., E. P. Newberry, S. G. Young, S. Robine, R. L. Hamilton, J. S. Wong, J. Luo, S. Kennedy, and N. O. Davidson. 2006. Compensatory increase in hepatic lipogenesis in mice with conditional intestine-specific Mttp deficiency. J. Biol. Chem. 281: 4075-4086.
19. Du, E. Z., S. L. Wang, H. J. Kayden, R. Sokol, L. K. Curtiss, and R. A. Davis. 1996. Translocation of apolipoprotein B across the endoplasmic reticulum is blocked in abetalipoproteinemia. J. Lipid Res. 37: 1309-1315.
20. 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.
21. Benoist, F., and T. Grand-Perret. 1997. Co-translational degradation of apolipoprotein B100 by the proteasome is prevented by microsomal triglyceride transfer protein. Synchronized translation studies on HepG2 cells treated with an inhibitor of microsomal triglyceride transfer protein. J. Biol. Chem. 272: 20435-20442.
22. Mitchell, D. M., M. Zhou, R. Pariyarath, H. Wang, J. D. Aitchison, H. N. Ginsberg, and E. A. Fisher. 1998. Apoprotein B100 has a prolonged interaction with the translocon during which its lipidation and translocation change from dependence on the microsomal triglyceride transfer protein to independence. Proc. Natl. Acad. Sci. USA. 95: 14733-14738.
23. Rustaeus, S., P. Stillemark, K. Lindberg, D. Gordon, and S. O. Olofsson. 1998. The microsomal triglyceride transfer protein catalyzes the post-translational assembly of apolipoprotein B-100 very low density lipoprotein in McA-RH7777 cells. J. Biol. Chem. 273: 5196-5203.
24. Pan, M., J. S. Liang Js, E. A. Fisher, and H. N. Ginsberg. 2002. The late addition of core lipids to nascent apolipoprotein B100, resulting in the assembly and secretion of triglyceride-rich lipoproteins, is independent of both microsomal triglyceride transfer protein activity and new triglyceride synthesis. J. Biol. Chem. 277: 4413-4421.
25. Kulinski, A., S. Rustaeus, and J. E. Vance. 2002. Microsomal triacylglycerol transfer protein is required for lumenal accretion of triacylglycerol not associated with ApoB, as well as for ApoB lipidation. J. Biol. Chem. 277: 31516-31525.
26. Wang, Y., R. S. McLeod, and Z. Yao. 1997. Normal activity of microsomal triglyceride transfer protein is required for the oleate-induced secretion of very low density lipoproteins containing apolipoprotein B from McA-RH7777 cells. J. Biol. Chem. 272: 12272-12278.
27. Wang, Y., K. Tran, and Z. Yao. 1999. The activity of microsomal triglyceride transfer protein is essential for accumulation of triglyceride within microsomes in McA-RH7777 cells. A unified model for the assembly of very low density lipoproteins. J. Biol. Chem. 274: 27793-27800.
28. Raabe, M., M. M. Veniant, M. A. Sullivan, C. H. Zlot, J. Bjorkegren, L. B. Nielsen, J. S. Wong, R. L. Hamilton, and S. G. Young. 1999. Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice. J. Clin. Invest. 103: 1287-1298.
29. Larsson, S. L., J. Skogsberg, and J. Bjorkegren. 2004. The low density lipoprotein receptor prevents secretion of dense apoB100-containing lipoproteins from the liver. J. Biol. Chem. 279: 831-836.
30. Levy, E., S. Stan, E. Delvin, D. Menard, C. Shoulders, C. Garofalo, I. Slight, E. Seidman, G. Mayer, and M. Bendayan. 2002. Localization of microsomal triglyceride transfer protein in the Golgi: possible role in the assembly of chylomicrons. J. Biol. Chem. 277: 16470-16477.
31. Manchekar, M., P. E. Richardson, T. M. Forte, G. Datta, J. P. Segrest, and N. Dashti. 2004. Apolipoprotein B-containing lipoprotein particle assembly: lipid capacity of the nascent lipoprotein particle. J. Biol. Chem. 279: 39757-39766.
32. Richardson, P. E., M. Manchekar, N. Dashti, M. K. Jones, A. Beigneux, S. G. Young, S. C. Harvey, and J. P. Segrest. 2005. Assembly of lipoprotein particles containing apolipoprotein-B: structural model for the nascent lipoprotein particle. Biophys. J. 88: 2789-2800.
33. Segrest, J. P., M. K. Jones, and N. Dashti. 1999. N-terminal domain of apolipoprotein B has structural homology to lipovitellin and microsomal triglyceride transfer protein: a "lipid pocket" model for self-assembly of apob-containing lipoprotein particles. J. Lipid Res. 40: 1401-1416.
34. Segrest, J. P., M. K. Jones, H. De Loof, and N. Dashti. 2001. Structure of apolipoprotein B-100 in low density lipoproteins. J. Lipid Res. 42: 1346-1367.
35. Dashti, N., M. Manchekar, Y. Liu, Z. Sun, and J. P. Segrest. 2007. Microsomal triglyceride transfer protein activity is not required for the initiation of apolipoprotein B-containing lipoprotein assembly in McA-RH7777 cells. J. Biol. Chem. 282: 28597-28608.
36. 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.
37. Rava, P., H. Athar, C. Johnson, and M. M. Hussain. 2005. Transfer of cholesteryl esters and phospholipids as well as net deposition by microsomal triglyceride transfer protein. J. Lipid Res. 46: 1779-1785.
38. Jiang, Z. G., Y. Liu, M. M. Hussain, D. Atkinson, and C. J. McKnight. 2008. Reconstituting initial events during the assembly of apolipoprotein B-containing lipoproteins in a cell-free system. J. Mol. Biol. 383: 1181-1194.
39. Rava, P., G. K. Ojakian, G. S. Shelness, and M. M. Hussain. 2006. Phospholipid transfer activity of microsomal triacylglycerol transfer protein is sufficient for the assembly and secretion of apolipoprotein B lipoproteins. J. Biol. Chem. 281: 11019-11027.
40. Dashti, N., M. Gandhi, X. Liu, X. Lin, and J. P. Segrest. 2002. The N-terminal 1000 residues of apolipoprotein B associate with microsomal triglyceride transfer protein to create a lipid transfer pocket required for lipoprotein assembly. Biochemistry. 41: 6978-6987.
41. Dashti, N., W. J. McConathy, and J. A. Ontko. 1980. Production of apolipoproteins E and A-I by rat hepatocytes in primary culture. Biochim. Biophys. Acta. 618: 347-358.
42. Yao, Z. M., B. D. Blackhart, D. F. Johnson, S. M. Taylor, K. W. Haubold, and B. J. McCarthy. 1992. Elimination of apolipoprotein B48 formation in rat hepatoma cell lines transfected with mutant human apolipoprotein B cDNA constructs. J. Biol. Chem. 267: 1175-1182.
43. Miller, A. D., D. G. Miller, J. V. Garcia, and C. M. Lynch. 1993. Use of retroviral vectors for gene transfer and expression. Methods Enzymol. 217: 581-599.
44. Manchekar, M., P. E. Richardson, Z. Sun, Y. Liu, J. P. Segrest, and N. Dashti. 2008. Charged amino acid residues 997-1000 of human apolipoprotein B100 are critical for the initiation of lipoprotein assembly and the formation of a stable lipidated primordial particle in McA-RH7777 cells. J. Biol. Chem. 283: 29251-29265.
45. Lin, M. C., D. Gordon, and J. R. Wetterau. 1995. Microsomal triglyceride transfer protein (MTP) regulation in HepG2 cells: insulin negatively regulates MTP gene expression. J. Lipid Res. 36: 1073-1081.
46. Burnette, W. N. 1981. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112: 195-203.
47. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with Folin phenol reagent. J. Biol. Chem. 193: 265-275.
48. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
49. Athar, H., J. Iqbal, X. C. Jiang, and M. M. Hussain. 2004. A simple, rapid, and sensitive fluorescence assay for microsomal triglyceride transfer protein. J. Lipid Res. 45: 764-772.
50. Dykxhoorn, D. M., C. D. Novina, and P. A. Sharp. 2003. Killing the messenger: short RNAs that silence gene expression. Nat. Rev. Mol. Cell Biol. 4: 457-467.
51. Yao, Z., and R. S. McLeod. 1994. Synthesis and secretion of hepatic apolipoprotein B-containing lipoproteins. Biochim. Biophys. Acta. 1212: 152-166.
52. Sparks, J. D., H. L. Collins, I. Sabio, M. P. Sowden, H. C. Smith, J. Cianci, and C. E. Sparks. 1997. Effects of fatty acids on apolipoprotein B secretion by McArdle RH-7777 rat hepatoma cells. Biochim. Biophys. Acta. 1347: 51-61.
53. Cardozo, C., X. Wu, M. Pan, H. Wang, and E. A. Fisher. 2002. The inhibition of microsomal triglyceride transfer protein activity in rat hepatoma cells promotes proteasomal and nonproteasomal degradation of apoprotein b100. Biochemistry. 41: 10105-10114.
54. Chang, B. H., W. Liao, L. Li, M. Nakamuta, D. Mack, and L. Chan. 1999. Liver-specific inactivation of the abetalipoproteinemia gene completely abrogates very low density lipoprotein/low density lipoprotein production in a viable conditional knockout mouse. J. Biol. Chem. 274: 6051-6055.
55. Lieu, H. D., S. K. Withycombe, Q. Walker, J. X. Rong, R. L. Walzem, J. S. Wong, R. L. Hamilton, E. A. Fisher, and S. G. Young. 2003. Eliminating atherogenesis in mice by switching off hepatic lipoprotein secretion. Circulation. 107: 1315-1321.
56. Leiper, J. M., J. D. Bayliss, R. J. Pease, D. J. Brett, J. Scott, and C. C. Shoulders. 1994. Microsomal triglyceride transfer protein, the abetalipoproteinemia gene product, mediates the secretion of apolipoprotein B-containing lipoproteins from heterologous cells. J. Biol. Chem. 269: 21951-21954.
57. Gordon, D. A., H. Jamil, D. Sharp, D. Mullaney, Z. Yao, R. E. Gregg, and J. Wetterau. 1994. Secretion of apolipoprotein B-containing lipoproteins from HeLa cells is dependent on expression of the microsomal triglyceride transfer protein and is regulated by lipid availability. Proc. Natl. Acad. Sci. USA. 91: 7628-7632.
58. Jamil, H., J. K. Dickson, Jr., C. H. Chu, M. W. Lago, J. K. Rinehart, S. A. Biller, R. E. Gregg, and J. R. Wetterau. 1995. Microsomal triglyceride transfer protein. Specificity of lipid binding and transport. J. Biol. Chem. 270: 6549-6554.
59. Nicodeme, E., F. Benoist, R. McLeod, Z. Yao, J. Scott, C. C. Shoulders, and T. Grand-Perret. 1999. Identification of domains in apolipoprotein B100 that confer a high requirement for the microsomal triglyceride transfer protein. J. Biol. Chem. 274: 1986-1993.
60. Herscovitz, H., A. Kritis, I. Talianidis, E. Zanni, V. Zannis, and D. M. Small. 1995. Murine mammary-derived cells secrete the N-terminal 41% of human apolipoprotein B on high density lipoprotein-sized lipoproteins containing a triacylglycerol-rich core. Proc. Natl. Acad. Sci. USA. 92: 659-663.
61. Carraway, M., H. Herscovitz, V. Zannis, and D. M. Small. 2000. Specificity of lipid incorporation is determined by sequences in the N-terminal 37 of apoB. Biochemistry. 39: 9737-9745.
62. Gretch, D. G., S. L. Sturley, L. Wang, B. A. Lipton, A. Dunning, K. A. Grunwald, J. R. Wetterau, Z. Yao, P. Talmud, and A. D. Attie. 1996. The amino terminus of apolipoprotein B is necessary but not sufficient for microsomal triglyceride transfer protein responsiveness. J. Biol. Chem. 271: 8682-8691.