Molecular cloning, expression, and hormonal regulation of the chicken microsomal triglyceride transfer protein

Gene

Volumn 523, Issue 1, 2013, Pages 1-9

  Ivessa, N Erwin ^a   Rehberg, Edward ^b   Kienzle, Bernadette ^b   Seif, Fridolin ^a   Hermann, Robert ^a   Hermann, Marcela ^a   Schneider, Wolfgang J ^a   Gordon, David A ^b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b BRISTOL MYERS SQUIBB   (United States)

Author keywords

Chicken; Estrogen; Hormone; Microsomal triglyceride transfer protein; Very low density lipoprotein; VLDL

Indexed keywords

APOLIPOPROTEIN B; ASPARAGINE LINKED OLIGOSACCHARIDE; ESTRADIOL; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; SIGNAL PEPTIDE; VERY LOW DENSITY LIPOPROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL ACTIVITY; CHICK EMBRYO; CHICKEN; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EGG PRODUCTION; ENDOPLASMIC RETICULUM; ESTROGEN ACTIVITY; FIBROBLAST; GENE EXPRESSION; HEPATOMA CELL; HORMONAL REGULATION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OVIPARITY; PRIORITY JOURNAL; PROTEIN ELECTROPHORESIS; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; APOLIPOPROTEINS B; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE, TUMOR; CHICK EMBRYO; CHICKENS; CHOLESTEROL, VLDL; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; ESTROGENS; ETHINYL ESTRADIOL; FEMALE; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; GENE LIBRARY; LIVER; MALE; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN SORTING SIGNALS; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; AVES; DROSOPHILA MELANOGASTER; MAMMALIA; VERTEBRATA;

EID: 84877840437     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2013.03.102     Document Type: Article

References (67)

1. Ameen C., Oscarsson J. Sex difference in hepatic microsomal triglyceride transfer protein expression is determined by the growth hormone secretory pattern in the rat. Endocrinology 2003, 144:3914-3921.
2. Avarre J.C., Lubzens E., Babin P.J. Apolipocrustacein, formerly vitellogenin, is the major egg yolk precursor protein in decapod crustaceans and is homologous to insect apolipophorin II/I and vertebrate apolipoprotein B. BMC Evol. Biol. 2007, 7:3.
3. Barsalani R., Chapados N.A., Lavoie J.M. Hepatic VLDL-TG production and MTP gene expression are decreased in ovariectomized rats: effects of exercise training. Horm. Metab. Res. 2010, 42:860-867.
4. Berriot-Varoqueaux N., Aggerbeck L.P., Samson-Bouma M., Wetterau J.R. The role of the microsomal triglygeride transfer protein in abetalipoproteinemia. Annu. Rev. Nutr. 2000, 20:663-697.
5. Binder R., MacDonald C.C., Burch J.B., Lazier C.B., Williams D.L. Expression of endogenous and transfected apolipoprotein II and vitellogenin II genes in an estrogen responsive chicken liver cell line. Mol. Endocrinol. 1990, 4:201-208.
6. Bostrom K., et al. Studies on the assembly of apo B-100-containing lipoproteins in HepG2 cells. J. Biol. Chem. 1988, 263:4434-4442.
7. Capony F., Williams D.L. Apolipoprotein B of avian very low density lipoprotein: characteristics of its regulation in nonstimulated and estrogen-stimulated rooster. Biochemistry 1980, 19:2219-2226.
8. Chan L., Jackson R.L., O'Malley B.W., Means A.R. Synthesis of very low density lipoproteins in the cockerel. Effects of estrogen. J. Clin. Invest. 1976, 58:368-379.
9. Dashti N., Gandhi M., Liu X., Lin X., Segrest J.P. 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 2002, 41:6978-6987.
10. Davis R.A. Evolution of processes and regulators of lipoprotein synthesis: from birds to mammals. J. Nutr. 1997, 127:795S-800S.
11. Dixon J.L., Furukawa S., Ginsberg H.N. Oleate stimulates secretion of apolipoprotein B-containing lipoproteins from Hep G2 cells by inhibiting early intracellular degradation of apolipoprotein B. J. Biol. Chem. 1991, 266:5080-5086.
12. Evans M.I., Silva R., Burch J.B. Isolation of chicken vitellogenin I and III cDNAs and the developmental regulation of five estrogen-responsive genes in the embryonic liver. Genes Dev. 1988, 2:116-124.
13. Gavel Y., von Heijne G. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 1990, 3:433-442.
14. Gordon D.A., Jamil H. Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochim. Biophys. Acta 2000, 1486:72-83.
15. Gordon D.A., et al. 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. U. S. A. 1994, 91:7628-7632.
16. Gordon D.A., Jamil H., Gregg R.E., Olofsson S.O., Boren J. 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. 1996, 271:33047-33053.
17. Gretch D.G., et al. The amino terminus of apolipoprotein B is necessary but not sufficient for microsomal triglyceride transfer protein responsiveness. J. Biol. Chem. 1996, 271:8682-8691.
18. Hebert D.N., Simons J.F., Peterson J.R., Helenius A. Calnexin, calreticulin, and Bip/Kar2p in protein folding. Cold Spring Harb. Symp. Quant. Biol. 1995, 60:405-415.
19. Hermann M., Seif F., Schneider W.J., Ivessa N.E. Estrogen dependence of synthesis and secretion of apolipoprotein B-containing lipoproteins in the chicken hepatoma cell line, LMH-2A. J.Lipid Res. 1997, 38:1308-1317.
20. Hooper A.J., van Bockxmeer F.M., Burnett J.R. Monogenic hypocholesterolaemic lipid disorders and apolipoprotein B metabolism. Crit. Rev. Clin. Lab. Sci. 2005, 42:515-545.
21. Hussain M.M., Bakillah A. New approaches to target microsomal triglyceride transfer protein. Curr. Opin. Lipidol. 2008, 19:572-578.
22. Hussain M.M., Bakillah A., Nayak N., Shelness G.S. Amino acids 430-570 in apolipoprotein B are critical for its binding to microsomal triglyceride transfer protein. J. Biol. Chem. 1998, 273:25612-25615.
23. Hussain M.M., Shi J., Dreizen P. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res. 2003, 44:22-32.
24. Hussain M.M., Rava P., Walsh M., Rana M., Iqbal J. Multiple functions of microsomal triglyceride transfer protein. Nutr. Metab. (Lond.) 2012, 9:14.
25. Jamil H., et al. Microsomal triglyceride transfer protein. Specificity of lipid binding and transport. J. Biol. Chem. 1995, 270:6549-6554.
26. Jamil H., et al. An inhibitor of the microsomal triglyceride transfer protein inhibits apoB secretion from HepG2 cells. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11991-11995.
27. Jamil H., et al. Evidence that microsomal triglyceride transfer protein is limiting in the production of apolipoprotein B-containing lipoproteins in hepatic cells. J. Lipid Res. 1998, 39:1448-1454.
28. Johansson J.O., Wiren L., Oscarsson J., Bengtsson B.A., Johannsson G. Growth hormone (GH) replacement in GH-deficient adults: a crossover trial comparing the effect on metabolic control, well-being and compliance of three injections per week versus daily injections. Growth Hormon. IGF Res. 2003, 13:306-315.
29. Kirchgessner T.G., et al. Regulation of chicken apolipoprotein B: cloning, tissue distribution, and estrogen induction of mRNA. Gene 1987, 59:241-251.
30. Kulinski A., Rustaeus S., Vance J.E. Microsomal triacylglycerol transfer protein is required for lumenal accretion of triacylglycerol not associated with ApoB, as well as for ApoB lipidation. J. Biol. Chem. 2002, 277:31516-31525.
31. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
32. Leiper J.M., Bayliss J.D., Pease R.J., Brett D.J., Scott J., Shoulders C.C. Microsomal triglyceride transfer protein, the abetalipoproteinemia gene product, mediates the secretion of apolipoprotein B-containing lipoproteins from heterologous cells. J. Biol. Chem. 1994, 269:21951-21954.
33. Lin M.C., Arbeeny C., Bergquist K., Kienzle B., Gordon D.A., Wetterau J.R. Cloning and regulation of hamster microsomal triglyceride transfer protein. The regulation is independent from that of other hepatic and intestinal proteins which participate in the transport of fatty acids and triglycerides. J. Biol. Chem. 1994, 269:29138-29145.
34. Lin M.C., Gordon D., Wetterau J.R. Microsomal triglyceride transfer protein (MTP) regulation in HepG2 cells: insulin negatively regulates MTP gene expression. J. Lipid Res. 1995, 36:1073-1081.
35. Louvard D., Reggio H., Warren G. Antibodies to the Golgi complex and the rough endoplasmic reticulum. J. Cell Biol. 1982, 92:92-107.
36. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
37. Nakamuta M., Chang B.H., Hoogeveen R., Li W.H., Chan L. Mouse microsomal triglyceride transfer protein large subunit: cDNA cloning, tissue-specific expression and chromosomal localization. Genomics 1996, 33:313-316.
38. Narcisi T.M., et al. Mutations of the microsomal triglyceride-transfer-protein gene in abetalipoproteinemia. Am. J. Hum. Genet. 1995, 57:1298-1310.
39. Patel S.B., Grundy S.M. Interactions between microsomal triglyceride transfer protein and apolipoprotein B within the endoplasmic reticulum in a heterologous expression system. J. Biol. Chem. 1996, 271:18686-18694.
40. Pease R.J., Leiper J.M. Regulation of hepatic apolipoprotein-B-containing lipoprotein secretion. Curr. Opin. Lipidol. 1996, 7:132-138.
41. Pelham H.R. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem. Sci. 1990, 15:483-486.
42. Rava P., Hussain M.M. Acquisition of triacylglycerol transfer activity by microsomal triglyceride transfer protein during evolution. Biochemistry 2007, 46:12263-12274.
43. Rava P., Ojakian G.K., Shelness G.S., Hussain M.M. Phospholipid transfer activity of microsomal triacylglycerol transfer protein is sufficient for the assembly and secretion of apolipoprotein B lipoproteins. J. Biol. Chem. 2006, 281:11019-11027.
44. Rehberg E.F., et al. A novel abetalipoproteinemia genotype. Identification of a missense mutation in the 97-kDa subunit of the microsomal triglyceride transfer protein that prevents complex formation with protein disulfide isomerase. J. Biol. Chem. 1996, 271:29945-29952.
45. Ricci B., et al. A 30-amino acid truncation of the microsomal triglyceride transfer protein large subunit disrupts its interaction with protein disulfide-isomerase and causes abetalipoproteinemia. J. Biol. Chem. 1995, 270:14281-14285.
46. Schneider W.J. Lipoprotein receptors in oocyte growth. Clin. Investig. 1992, 70:385-390.
47. Schneider W.J., Goldstein J.L., Brown M.S. Partial purification and characterization of the low density lipoprotein receptor from bovine adrenal cortex. J. Biol. Chem. 1980, 255:11442-11447.
48. Sellers J.A., Hou L., Athar H., Hussain M.M., Shelness G.S. A Drosophila microsomal triglyceride transfer protein homolog promotes the assembly and secretion of human apolipoprotein B. Implications for human and insect transport and metabolism. J. Biol. Chem. 2003, 278:20367-20373.
49. Sensel M.G., Binder R., Lazier C.B., Williams D.L. Reactivation of apolipoprotein II gene transcription by cycloheximide reveals two steps in the deactivation of estrogen receptor-mediated transcription. Mol. Cell. Biol. 1994, 14:1733-1742.
50. Sharp D., et al. Cloning and gene defects in microsomal triglyceride transfer protein associated with abetalipoproteinaemia. Nature 1993, 365:65-69.
51. Shelness G.S., Ledford A.S. Evolution and mechanism of apolipoprotein B-containing lipoprotein assembly. Curr. Opin. Lipidol. 2005, 16:325-332.
52. Shelness G.S., Sellers J.A. Very-low-density lipoprotein assembly and secretion. Curr. Opin. Lipidol. 2001, 12:151-157.
53. Shibata Y., Branicky R., Landaverde I.O., Hekimi S. Redox regulation of germline and vulval development in Caenorhabditis elegans. Science 2003, 302:1779-1782.
54. Shoulders C.C., Shelness G.S. Current biology of MTP: implications for selective inhibition. Curr. Top. Med. Chem. 2005, 5:283-300.
55. Shoulders C.C., et al. Abetalipoproteinemia is caused by defects of the gene encoding the 97kDa subunit of a microsomal triglyceride transfer protein. Hum. Mol. Genet. 1993, 2:2109-2116.
56. Shoulders C.C., et al. The abetalipoproteinemia gene is a member of the vitellogenin family and encodes an alpha-helical domain. Nat. Struct. Biol. 1994, 1:285-286.
57. Tall A.R. Plasma cholesteryl ester transfer protein. J. Lipid Res. 1993, 34:1255-1274.
58. Tarugi P., Ballarini G., Pinotti B., Franchini A., Ottaviani E., Calandra S. Secretion of apoB- and apoA-I-containing lipoproteins by chick kidney. J. Lipid Res. 1998, 39:731-743.
59. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur. J. Biochem. 1983, 133:17-21.
60. von Heijne G. Towards a comparative anatomy of N-terminal topogenic protein sequences. J. Mol. Biol. 1986, 189:239-242.
61. Wang S., McLeod R.S., Gordon D.A., Yao Z. The microsomal triglyceride transfer protein facilitates assembly and secretion of apolipoprotein B-containing lipoproteins and decreases cotranslational degradation of apolipoprotein B in transfected COS-7 cells. J. Biol. Chem. 1996, 271:14124-14133.
62. Wetterau J.R., Aggerbeck L.P., Laplaud P.M., McLean L.R. Structural properties of the microsomal triglyceride-transfer protein complex. Biochemistry 1991, 30:4406-4412.
63. Wetterau J.R., Combs K.A., McLean L.R., Spinner S.N., Aggerbeck L.P. Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein. Biochemistry 1991, 30:9728-9735.
64. Wetterau J.R., Lin M.C., Jamil H. Microsomal triglyceride transfer protein. Biochim. Biophys. Acta 1997, 1345:136-150.
65. Wirtz K.W. Phospholipid transfer proteins. Annu. Rev. Biochem. 1991, 60:73-99.
66. Wu X., Zhou M., Huang L.S., Wetterau J., Ginsberg H.N. Demonstration of a physical interaction between microsomal triglyceride transfer protein and apolipoprotein B during the assembly of ApoB-containing lipoproteins. J. Biol. Chem. 1996, 271:10277-10281.
67. Yao Z., Tran K., McLeod R.S. Intracellular degradation of newly synthesized apolipoprotein B. J. Lipid Res. 1997, 38:1937-1953.