A novel multiprotein complex is required to generate the prechylomicron transport vesicle from intestinal ER

Journal of Lipid Research

Volumn 51, Issue 7, 2010, Pages 1918-1928

  Siddiqi, Shahzad ^a   Saleem, Umair ^a   Abumrad, Nada A ^c   Davidson, Nicholas O ^c   Storch, Judith ^d   Siddiqi, Shadab A ^e   Mansbach II, Charles M ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

CD36; Chylomicron; L FABP; Lipid absorption; Vesicle budding complex

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOLIPOPROTEIN B48; CD36 ANTIGEN; CHYLOMICRON; COAT PROTEIN COMPLEX II; FATTY ACID BINDING PROTEIN; LIVER FATTY ACID BINDING PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN KINASE C ZETA; SYNAPTOBREVIN; SYNAPTOBREVIN 7; UNCLASSIFIED DRUG; CHAPERONE; FABP1 PROTEIN, RAT; FAT INTAKE; PRKCZ PROTEIN, RAT; SYBL1 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; IMMUNOPRECIPITATION; LIPID ABSORPTION; MALE; NONHUMAN; PRECHYLOMICRON TRANSPORT VESICLE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; TRANSPORT VESICLE; ANIMAL; C57BL MOUSE; COATED VESICLE; CYTOLOGY; FAT INTAKE; INTESTINE; INTESTINE ABSORPTION; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANTIGENS, CD36; APOLIPOPROTEIN B-48; BIOLOGICAL TRANSPORT; CHYLOMICRONS; COP-COATED VESICLES; DIETARY FATS; ENDOPLASMIC RETICULUM; FATTY ACID-BINDING PROTEINS; INTESTINAL ABSORPTION; INTESTINES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; R-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TRANSPORT VESICLES;

EID: 77953513138     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M005611     Document Type: Article

References (51)

1. Stagg, S. M., P. LaPointe, and W. E. Balch. 2007. Structural design of cage and coat scaffolds that direct membrane traffic. Curr. Opin. Struct. Biol. 17: 221-228.
2. Stagg, S. M., P. LaPointe, A. Razvi, C. Gurkan, C. S. Potter, B. Carragher, and W. E. Balch. 2008. Structural basis for cargo regulation of COPII coat assembly. Cell. 134: 474-484.
3. Fromme, J. C., M. Ravazzola, S. Hamamoto, M. Al-Balwi, W. Eyaid, S. A. Boyadjiev, P. Cosson, R. Schekman, and L. Orci. 2007. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell. 13: 623-634.
4. Fromme, J. C., L. Orci, and R. Schekman. 2008. Coordination of COPII vesicle trafficking by Sec23. Trends Cell Biol. 18: 330-336.
5. Aridor, M., K. N. Fish, S. Bannykh, J. Weisman, T. H. Roberts, J. Lippincott-Schwartz, and W. E. Balch. 2001. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152: 213-229.
6. Siddiqi, S. A., F. S. Gorelick, J. T. Mahan, and C. M. Mansbach 2nd. 2003. COPII proteins are required for Golgi fusion but not for endoplasmic reticulum budding of the pre-chylomicron transport vesicle. J. Cell Sci. 116: 415-427.
7. Ockner, R. K., F. B. Hughes, and K. J. Isselbacher. 1969. Very low density lipoproteins in intestinal lymph: origin, composition, and role in lipid transport in the fasting state. J. Clin. Invest. 48: 2079-2088.
8. Mansbach 2nd, C. M., and A. Arnold. 1986. Steady-state kinetic analysis of triacylglycerol delivery into mesenteric lymph. Am. J. Physiol. 251: G263-G269.
9. Hayashi, H., K. Fujimoto, J. A. Cardelli, D. F. Nutting, S. Bergstedt, and P. Tso. 1990. Fat feeding increases size, but not number, of chylomicrons produced by small intestine. Am. J. Physiol. 259: G709-G719.
10. Matsuoka, K., L. Orci, M. Amherdt, S. Y. Bednarek, S. Hamamoto, R. Schekman, and T. Yeung. 1998. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell. 93: 263-275.
11. Kim, J., S. Hamamoto, M. Ravazzola, L. Orci, and R. Schekman. 2005. Uncoupled packaging of amyloid precursor protein and pre-senilin 1 into coat protein complex II vesicles. J. Biol. Chem. 280: 7758-7768.
12. Siddiqi, S., S. A. Siddiqi, and C. M. Mansbach II. 2010. Sec24C is required for docking the prechylomicron transport vesicle with the Golgi. J Lipid Res. 51: 1093-1100.
13. Neeli, I., S. A. Siddiqi, S. Siddiqi, J. Mahan, W. S. Lagakos, B. Binas, T. Gheyi, J. Storch, and C. M. Mansbach II. 2007. Liver fatty acid-binding protein initiates budding of pre-chylomicron transport vesicles from intestinal endoplasmic reticulum. J. Biol. Chem. 282: 17974-17984.
14. Bannykh, S. I., T. Rowe, and W. E. Balch. 1996. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135: 19-35.
15. Kuge, O., C. Dascher, L. Orci, T. Rowe, M. Amherdt, H. Plutner, M. Ravazzola, G. Tanigawa, J. E. Rothman, and W. E. Balch. 1994. Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125: 51-65.
16. Stagg, S. M., C. Gurkan, D. M. Fowler, P. LaPointe, T. R. Foss, C. S. Potter, B. Carragher, and W. E. Balch. 2006. Structure of the Sec13/31 COPII coat cage. Nature. 439: 234-238.
17. Miller, E., B. Antonny, S. Hamamoto, and R. Schekman. 2002. Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J. 21: 6105-6113.
18. Phillips, M. L., C. Pullinger, I. Kroes, J. Kroes, D. A. Hardman, G. Chen, L. K. Curtiss, M. M. Gutierrez, J. P. Kane, and V. N. Schumaker. 1997. A single copy of apolipoprotein B-48 is present on the human chylomicron remnant. J. Lipid Res. 38: 1170-1177.
19. Siddiqi, S. A., S. Siddiqi, J. Mahan, K. Peggs, F. S. Gorelick, and C. M. Mansbach II. 2006. The identification of a novel endoplasmic reticulum to Golgi SNARE complex used by the prechylomicron transport vesicle. J. Biol. Chem. 281: 20974-20982.
20. Siddiqi, S. A., J. Mahan, S. Siddiqi, F. S. Gorelick, and C. M. Mansbach 2nd. 2006. Vesicle-associated membrane protein 7 is expressed in intestinal ER. J. Cell Sci. 119: 943-950.
21. Storch, J., and N. M. Bass. 1990. Transfer of fluorescent fatty acids from liver and heart FABP to model membranes. J. Biol. Chem. 265: 7827-7831.
22. Newberry, E. P., Y. Xie, S. Kennedy, X. Han, K. K. Buhman, J. Luo, R. W. Gross, and N. O. Davidson. 2003. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 278: 51664-51672.
23. Coburn, C. T., F. F. Knapp, M. Febbraio, A. L. Beets, R. L. Silverstein, and N. A. Abumrad. 2000. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissue of CD36 knockout mice. J. Biol. Chem. 275: 32523-32529.
24. Drover, V. A., M. Ajmal, F. Nassir, N. O. Davidson, A. M. Nauli, D. Sahoo, P. Tso, and N. A. Abumrad. 2005. CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. J. Clin. Invest. 115: 1290-1297.
25. Kumar, N. S., and C. M. Mansbach. 1997. Determinants of triacylglycerol transport from the endoplasmic reticulum to the Golgi in intestine. Am. J. Physiol. 273: G18-G30.
26. Siddiqi, S. A., and C. M. Mansbach II. 2008. PKC zeta-mediated phosphorylation controls budding of the pre-chylomicron transport vesicle. J. Cell Sci. 121: 2327-2338.
27. Kane, J. P., D. A. Hardman, and H. E. Paulus. 1980. Heterogeneity of apolipoprotein B: isolation of a new species from human chylomicrons. Proc. Natl. Acad. Sci. USA. 77: 2465-2469.
28. Miller, E. A., T. H. Beilharz, P. N. Malkus, M. C. S. Lee, S. Hamamoto, L. Orci, and R. Schekman. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell. 114: 497-509.
29. Greenwalt, D. E., K. W. Watt, O. Y. So, and N. Jiwani. 1990. PAS IV, an integral membrane protein of mammary epithelial cells, is related to platelet and endothelial cell CD36 (GP IV). Biochemistry. 29: 7054-7059.
30. Drover, V. A., D. V. Nguyen, C. C. Bastie, Y. F. Darlington, N. A. Abumrad, J. E. Pessin, E. London, D. Sahoo, and M. C. Phillips. 2008. CD36 mediates both cellular uptake of very long chain fatty acids and their intestinal absorption in mice. J. Biol. Chem. 283: 13108-13115.
31. Calvo, D., D. Gomez-Coronado, Y. Suarez, M. A. Lasuncion, and M. A. Vega. 1998. Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J. Lipid Res. 39: 777-788. (Pubitemid 28163280)
32. Joglekar, A. P., D. Xu, D. J. Rigotti, R. Fairman, and J. C. Hay. 2003. The SNARE motif contributes to rbet1 intracellular targeting and dynamics independently of SNARE interactions. J. Biol. Chem. 278: 14121-14133.
33. Rusinol, A. E., H. Jamil, and J. E. Vance. 1997. In vitro reconstitution of assembly of apolipoprotein B48-containing lipoproteins. J. Biol. Chem. 272: 8019-8025.
34. Nauli, A. M., F. Nassir, S. Zheng, Q. Yang, C. M. Lo, S. B. Vonlehmden, D. Lee, R. J. Jandacek, N. A. Abumrad, and P. Tso. 2006. CD36 is important for chylomicron formation and secretion and may mediate cholesterol uptake in the proximal intestine. Gastroenterology. 131: 1197-1207.
35. Hasdemir, B., D. J. Fitzgerald, I. A. Prior, A. V. Tepikin, and R. D. Burgoyne. 2005. Traffic of Kv4 K+ channels mediated by KChIP1 is via a novel post-ER vesicular pathway. J. Cell Biol. 171: 459-469.
36. Juschke, C., A. Wachter, B. Schwappach, and M. Seedorf. 2005. SEC18/NSF-independent, protein-sorting pathway from the yeast cortical ER to the plasma membrane. J. Cell Biol. 169: 613-622.
37. Schepetilnikov, M. V., U. Manske, A. G. Solovyev, A. A. Zamyatnin, Jr., J. Schiemann, and S. Y. Morozov. 2005. The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J. Gen. Virol. 86: 2379-2391.
38. Zuber, C., J. H. Cormier, B. Guhl, R. Santimaria, D. N. Hebert, and J. Roth. 2007. EDEM1 reveals a quality control vesicular transport pathway out of the endoplasmic reticulum not involving the COPII exit sites. Proc. Natl. Acad. Sci. USA. 104: 4407-4412.
39. Fatal, N., L. Karhinen, E. Jokitalo, and M. Makarow. 2004. Active and specific recruitment of a soluble cargo protein for endoplasmic reticulum exit in the absence of functional COPII component Sec24p. J. Cell Sci. 117: 1665-1673.
40. Fatal, N., T. Suntio, and M. Makarow. 2002. Selecive protein exit from yeast endoplasmic reticulum in absence of functional GOPII coat component Sec13p. Mol. Biol. Cell. 13: 4130-4140.
41. Advani, R., R. Prekeris, K. Lee, J. Klumperman, and R. Scheller. 1999. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146: 765-775.
42. Zeng, Q., T. T. Tran, H. X. Tan, and W. Hong. 2003. The cytoplasmic domain of Vamp4 and Vamp5 is responsible for their correct subcellular targeting: the N-terminal extension of VAMP4 contains a dominant autonomous targeting signal for the trans-Golgi network. J. Biol. Chem. 278: 23046-23054.
43. Uemura, T., M. H. Sato, and K. Takeyasu. 2005. The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana. FEBS Lett. 579: 2842-2846.
44. Galli, T. 1998. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol. Biol. Cell. 9: 1437-1438.
45. Trotter, P. J., and J. Storch. 1991. Fatty acid uptake and metabolism in a human intestinal cell line (Caco-2): comparison of apical and basolateral incubation. J. Lipid Res. 32: 293-304.
46. Traber, M. G., H. J. Kayden, and M. J. Rindler. 1987. Polarized secretion of newly synthesized lipoproteins by the Caco-2 human intestinal cell line. J. Lipid Res. 28: 1350-1363.
47. Townley, A. K., Y. Feng, K. Schmidt, D. A. Carter, R. Porter, P. Verkade, and D. J. Stephens. 2008. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121: 3025-3034.
48. Duden, R. 2003. ER-to-Golgi transport: COP I and COP II function. [Review] Mol. Membr. Biol. 20: 197-207.
49. Nassir, F., B. Wilson, X. Han, R. W. Gross, and N. A. Abumrad. 2007. CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J. Biol. Chem. 282: 19493-19501.
50. Bass, N. M., J. A. Manning, R. K. Ockner, J. I. Gordon, S. Seetharam, and D. H. Alpers. 1985. Regulation of the biosynthesis of two distinct fatty acid-binding proteins in rat liver and intestine. J. Biol. Chem. 260: 1432-1436.
51. Newberry, E. P., Y. Xie, S. M. Kennedy, and N. O. Davidson. 2006. Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology. 44: 1191-1205.