ApoA-IV modulates the secretory trafficking of apoB and the size of triglyceride-rich lipoproteins

Journal of Lipid Research

Volumn 53, Issue 4, 2012, Pages 736-743

  Weinberg, Richard B ^a   Gallagher, James W ^a,b   Fabritius, Melissa A ^a   Shelness, Gregory S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b LINCOLN UNIVERSITY   (United States)

Author keywords

Apolipoprotein A IV; Apolipoprotein B; Lipid trafficking; Lipoprotein assembly; Triglyceride; Very low density lipoprotein

Indexed keywords

APOLIPOPROTEIN A4; APOLIPOPROTEIN B; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CELL LEVEL; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENDOPLASMIC RETICULUM; ENZYME KINETICS; GENE; HUMAN; IMMUNOPRECIPITATION; MOLECULAR DYNAMICS; MTP GENE; NONHUMAN; PARTICLE SIZE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOLIPOPROTEINS A; APOLIPOPROTEINS B; CARRIER PROTEINS; CELL LINE, TUMOR; CULTURE MEDIA; DOXYCYCLINE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPRECIPITATION; LIPID METABOLISM; LIPOPROTEINS, VLDL; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; RATS; TETRACYCLINE; TRANSFECTION; TRIGLYCERIDES;

EID: 84859414772     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M019992     Document Type: Article

References (57)

1. Black, D. D. 2007. Development and physiological regulation of intestinal lipid absorption. I. Development of intestinal lipid absorption: cellular events in chylomicron assembly and secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 293: G519-G524. (Pubitemid 47435377)
2. Shelness, G. S., and A. S. Ledford. 2005. Evolution and mechanism of apolipoprotein B-containing lipoprotein assembly. Curr. Opin. Lipidol. 16: 325-332. (Pubitemid 40839762)
3. 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. (Pubitemid 36114766)
4. Iqbal, J., and M. M. Hussain. 2009. Intestinal lipid absorption. Am. J. Physiol. Endocrinol. Metab. 296: E1183-E1194.
5. Hussain, M. M., P. Rava, X. Pan, K. Dai, S. K. Dougan, J. Iqbal, F. Lazare, and I. Khatun. 2008. Microsomal triglyceride transfer protein in plasma and cellular lipid metabolism. Curr. Opin. Lipidol. 19: 277-284. (Pubitemid 351653566)
6. Shoulders, C. C., and G. S. Shelness. 2005. Current biology of MTP: implications for selective inhibition. Curr. Top. Med. Chem. 5: 283-300. (Pubitemid 40614129)
7. Olofsson, S. O., L. Asp, and J. Borén. 1999. The assembly and secretion of apolipoprotein B-containing lipoproteins. Curr. Opin. Lipidol. 10: 341-346. (Pubitemid 29419691)
8. 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.
9. Shelness, G. S., and J. A. Sellers. 2001. Very-low-density lipoprotein assembly and secretion. Curr. Opin. Lipidol. 12: 151-157. (Pubitemid 32242922)
10. Valyi-Nagy, K., C. Harris, and L. L. Swift. 2002. The assembly of hepatic very low density lipoproteins: evidence of a role for the Golgi apparatus. Lipids. 37: 879-884. (Pubitemid 35332926)
11. Kulinski, A., S. Rustaeus, and J. E. Vance. 2002. Microsomal triglyceride transfer protein is required for lumenal accretion of triacylglycerol not associated with apo B, as well as for apoB lipidation. J. Biol. Chem. 277: 31516-31525. (Pubitemid 34968953)
12. Wang, Y., K. Tran, and Z. Yao. 1999. The activity of microsomal triglyceride transfer protein is essential for accumulation of triglyceride within the microsomes in McA-RH7777 cells. J. Biol. Chem. 274: 27793-27800.
13. Tran, K., G. Thorne-Tjomsland, C. J. DeLong, S. Cui, J. Shan, L. Burton, J. C. Jamieson, and Z. Yao. 2002. Intracellular assembly of very low density lipoproteins containing apoB100 in rat hepatoma McA-RH7777 cells. J. Biol. Chem. 277: 31187-31200. (Pubitemid 34970825)
14. Yamaguchi, J., M. V. Gamble, D. Conlon, J. S. Liang, and H. N. Ginsberg. 2003. The conversion of apoB100 low density lipoprotein/high density lipoprotein particles to apoB100 very low density lipoproteins in response to oleic acid occurs in the endoplasmic reticulum and not in the Golgi in McA RH7777 cells. J. Biol. Chem. 278: 42643-42651. (Pubitemid 37310538)
15. 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. (Pubitemid 28377918)
16. Rusiñol, A., H. Verkade, and J. E. Vance. 1993. Assembly of rat hepatic very low density lipoproteins in the endoplasmic reticulum. J. Biol. Chem. 268: 3555-3562. (Pubitemid 23070997)
17. Tso, P., and J. A. Balint. 1986. Formation and transport of chylomicrons by enterocytes to the lymphatics. Am. J. Physiol. 250: G715-G726.
18. Farese, R. V., Jr., M. M. Véniant, C. M. Cham, L. M. Flynn, V. Pierotti, J. F. Loring, M. Traber, S. Ruland, R. S. Stokowski, D. Huszar, et al. 1996. Phenotypic analysis of mice expressing exclusively apolipoprotein B48 or apolipoprotein B100. Proc. Natl. Acad. Sci. USA. 93: 6393-6398. (Pubitemid 26230316)
19. Luo, C. C., W. H. Li, M. N. Moore, and L. Chan. 1986. Structure and evolution of the apolipoprotein multigene family. J. Mol. Biol. 187: 325-340. (Pubitemid 16083775)
20. Green, P. H., 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. (Pubitemid 9216539)
21. Hayashi, H., D. F. Nutting, K. Fujimoto, J. A. Cardelli, D. Black, and P. Tso. 1990. Transport of lipid and apolipoproteins A-I and A-IV in intestinal lymph of the rat. J. Lipid Res. 31: 1613-1625.
22. Stan, S., E. Delvin, M. Lambert, E. Seidman, and E. Levy. 2003. Apo A-IV: an update on regulation and physiologic functions. Biochim. Biophys. Acta. 1631: 177-187. (Pubitemid 36292149)
23. Kalogeris, T. J., K. Fukagawa, and P. Tso. 1994. Synthesis and lymphatic transport of intestinal apolipoprotein A-IV in response to graded doses of triglyceride. J. Lipid Res. 35: 1141-1151. (Pubitemid 24209389)
24. Kalogeris, T. J., M-D. Rodriguez, and P. Tso. 1997. Control of synthesis and secretion of intestinal apolipoprotein A-IV by lipid. J. Nutr. 127: 537S-543S. (Pubitemid 27120012)
25. Kalogeris, T. J., F. Monroe, S. J. Demichele, and P. Tso. 1996. Intestinal synthesis and lymphatic secretion of apolipoprotein A-IV vary with chain length of intestinally infused fatty acids in rats. J. Nutr. 126: 2720-2729. (Pubitemid 26376607)
26. Tso, P., J. A. Balint, M. B. Bishop, and J. B. Rodgers. 1981. Acute inhibition of intestinal lipid transport by Pluronic L-81 in the rat. Am. J. Physiol. 241: G487-G497.
27. Kumar, N. S., and C. M. Mansbach 2nd. 1999. Prechylomicron transport vesicle: isolation and partial characterization. Am. J. Physiol. 276: G378-G386. (Pubitemid 29104151)
28. Weinberg, R. B., R. A. Anderson, V. R. Cook, F. Emmanuel, P. Denefle, M. Hermann, and A. Steinmetz. 2000. Structure and interfacial properties of chicken apolipoprotein A-IV. J. Lipid Res. 41: 1410-1418.
29. Weinberg, R. B., V. R. Cook, J. A. DeLozier, and G. S. Shelness. 2000. Dynamic interfacial properties of human apolipoprotein A-IV and B17 at the air/water and oil/water interface. J. Lipid Res. 41: 1419-1427.
30. Green, P. H., R. M. Glickman, J. W. Riley, and E. Quinet. 1980. Human apolipoprotein A-IV. Intestinal origin and distribution in plasma. J. Clin. Invest. 65: 911-919. (Pubitemid 10144067)
31. Koga, S., Y. Miyata, A. Funakoshi, and H. Ibayashi. 1985. Plasma apolipoprotein A-IV levels decrease in patients with chronic pancreatitis and malabsorption syndrome. Digestion. 32: 19-24. (Pubitemid 15099253)
32. Lu, S., Y. Yao, S. Meng, D. Cheng, and D. D. Black. 2002. Overexpression of apolipoprotein A-IV enhances lipid transport in newborn swine epithelia cells. J. Biol. Chem. 277: 31929-31937. (Pubitemid 34969001)
33. Lu, S., Y. Yao, X. Y. Cheng, S. Mitchell, S. Y. Leng, S. M. Meng, J. W. Gallagher, G. S. Shelness, G. S. Morris, J. Mahan, et al. 2006. Overexpression of apolipoprotein A-IV enhances lipid secretion in IPEC-1 cells by increasing chylomicron size. J. Biol. Chem. 281: 3473-3483. (Pubitemid 43845963)
34. Gallagher, J. W., R. B. Weinberg, and G. S. Shelness. 2004. ApoA-IV tagged with the ER retention signal KDEL perturbs the intracellular trafficking and secretion of apoB. J. Lipid Res. 45: 1826-1834. (Pubitemid 40990874)
35. Yao, Z., S. J. Lauer, D. A. Sanan, and S. Fazio. 1993. ApoA-IV is secreted on discrete HDL particles by the rat hepatoma cell line McA-RH7777 transfected with ApoA-IV cDNA. Arterioscler. Thromb. 13: 1476-1486. (Pubitemid 23303401)
36. Blade, A. M., M. A. Fabritius, L. Hou, R. B. Weinberg, and G. S. Shelness. 2011. Biogenesis of apolipoprotein A-V and impact its on VLDL triglyceride secretion. J. Lipid Res. 52: 237-244.
37. Sellers, J. A., and G. S. Shelness. 2001. Lipoprotein assembly capacity of the mammary tumor-derived cell line C127 is due to the expression of functional microsomal triglyceride transfer protein. J. Lipid Res. 42: 1897-1904. (Pubitemid 33116721)
38. Sellers, J. A., L. Hou, H. Athar, M. M. Hussain, and G. S. Shelness. 2003. A Drosophila microsomal triglyceride transfer protein homolog promotes the assembly and secretion of human apolipoprotein B-implications for human and insect lipid transport and metabolism. J. Biol. Chem. 278: 20367-20373. (Pubitemid 36799237)
39. Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, and D. C. Klenk. 1985. Protein assay using bicinchoninic acid. Anal. Biochem. 150: 76-85. (Pubitemid 16258399)
40. Cheng, D., P. S. MacArthur, S. Rong, J. S. Parks, and G. S. Shelness. 2010. Alternative splicing attenuates transgenic expression directed by the ApoE promoter-enhancer based expression vector, pLIV11. J. Lipid Res. 51: 849-855.
41. Yao, Y., S. Lu, Y. Huang, C. C. Beeman-Black, R. Lu, X. Pan, M. M. Hussain, and D. D. Black. 2011. Regulation of microsomal triglyceride transfer protein by apolipoprotein A-IV in newborn swine intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 300: G357-G363.
42. Borén, 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. (Pubitemid 24336289)
43. Langner, C. A., E. H. Birkenmeier, O. Ben-Zeev, M. C. Schotz, H. O. Sweet, M. T. Davisson, and J. I. Gordon. 1989. The fatty liver dystrophy (fld) mutation. A new mutant mouse with a developmental abnormality in triglyceride metabolism and associated tissuespecific defects in lipoprotein lipase and hepatic lipase activities. J. Biol. Chem. 264: 7994-8003. (Pubitemid 19137280)
44. 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)
45. Inui, Y., Y. Keno, K. Fukuda, T. Igura, T. Makamura, K. Tokunaga, S. Kawata, and Y. Matsuzawa. 1997. Modulation of apolipoprotein gene expression in fatty liver of obese rats: enhanced APOA-IV, but no APOB expression by a high sucrose diet. Int. J. Obes. Relat. Metab. Disord. 21: 231-238. (Pubitemid 27117037)
46. Gusarova, V., J. Seo, M. L. Sullivan, S. C. Watkins, J. L. Brodsky, and E. A. Fisher. 2007. Golgi-associated maturation of very low density lipoproteins involves conformational changes in apolipoprotein B, but is not dependent on apolipoprotein E. J. Biol. Chem. 282: 19453-19462. (Pubitemid 47100087)
47. Weinberg, R. B. 1994. Identification of functional domains in the plasma apolipoproteins by analysis of inter-species sequence variability. J. Lipid Res. 35: 2212-2222.
48. Zhang, J., and H. Herscovitz. 2003. Nascent lipidated apolipoprotein B is transported to the Golgi as an incompletely folded intermediate as probed by its association with network of endoplasmic reticulum molecular chaperones, GRP94, ERp72, BiP, calreticulin, and cyclophilin B. J. Biol. Chem. 278: 7459-7468. (Pubitemid 36800752)
49. Linnik, K. M., and H. Herscovitz. 1998. Multiple molecular chaperones interact with apolipoprotein B during its maturation. J. Biol. Chem. 273: 21368-21373.
50. Weinstock, P. H., C. L. Bisgaier, T. Hayek, K. Aalto-Setala, E. Sehayek, L. Wu, P. Sheiffele, M. Merkel, A. D. Essenburg, and J. L. Breslow. 1997. Decreased HDL cholesterol levels but normal lipid absorption, growth, and feeding behavior in apolipoprotein A-IV knockout mice. J. Lipid Res. 38: 1782-1794. (Pubitemid 27411270)
51. Aalto-Setälä, K., C. L. Bisgaier, A. Ho, K. A. Kieft, M. G. Traber, H. J. Kayden, R. Ramakrishnan, A. Walsh, A. D. Essenburg, and J. L. Breslow. 1994. Intestinal expression of human apolipoprotein A-IV in transgenic mice fails to influence dietary lipid absorption or feeding behavior. J. Clin. Invest. 93: 1776-1786. (Pubitemid 24116421)
52. Carey, M. C., D. M. Small, and C. M. Bliss. 1983. Lipid digestion and absorption. Annu. Rev. Physiol. 45: 651-677.
53. Field, F. J., and S. N. Mathur. 1995. Intestinal lipoprotein synthesis and secretion. Prog. Lipid Res. 34: 185-198.
54. Simon, T., V. R. Cook, A. Rao, and R. B. Weinberg. 2011. Impact of murine intestinal apolipoprotein A-IV expression on regional lipid absorption, gene expression, and growth. J. Lipid Res. 52: 1984-1994.
55. Levy, E., and D. Ménard. 2000. Developmental aspects of lipid and lipoprotein synthesis and secretion in human gut. Microsc. Res. Tech. 49: 363-373. (Pubitemid 30407772)
56. Carrier, J. C., G. V. Deblois, C. Champigny, E. Levy, and V. Giguère. 2004. Estrogen-related receptor alpha (ERRalpha) is a transcriptional regulator of apolipoprotein A-IV and controls lipid handling in the intestine. J. Biol. Chem. 279: 52052-52058. (Pubitemid 39656576)
57. 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)