PKCζ-mediated phosphorylation controls budding of the pre-chylomicron transport vesicle

Journal of Cell Science

Volumn 121, Issue 14, 2008, Pages 2327-2338

  Siddiqi, Shadab A ^a   Mansbach II, Charles M ^a,b  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Chylomicron; PKC ; Pre chylomicron transport vesicle; Protein phosphorylation

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; ADENOSINE TRIPHOSPHATE; CHYLOMICRON; ISOPROTEIN; PROTEIN KINASE C ZETA; RECOMBINANT PROTEIN; RECOMBINANT PROTEIN KINASE C ZETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTORADIOGRAPHY; CELL BUDDING; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME REGULATION; GROWTH INHIBITION; INTESTINE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; TRANSPORT VESICLE;

ANIMALS; APOLIPOPROTEIN B-48; CHYLOMICRONS; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVATORS; EXOCYTOSIS; FATTY ACID-BINDING PROTEINS; INTESTINES; MOLECULAR WEIGHT; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; R-SNARE PROTEINS; RATS; SUBCELLULAR FRACTIONS; TRANSPORT VESICLES;

EID: 49649118045     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.022780     Document Type: Article

References (58)

1. Aridor, M. and Balch, W. E. (2000). Kinase signaling initiates coat complex II (COP II) recruitment and export from the mammalian endoplasmic reticulum. J. Biol. Chem. 275, 35673-35676.
2. Balendran, A., Biondi, R. M., Cheung, P. C., Casamayor, A., Deak, M. and Alesi, D. R. (2000). A 3-phosphoinositide-dependent protein kinase-1 (PDK1) docking site is required for the phosphorylation of protein kinase Czera (PKCzeta) and PKC-related kinase 2 by PDK1. J. Biol. Chem. 275, 20806-20813.
3. Banan, A., Fields, J. Z., Talmage, D. A., Zhang, L. and Keshavarzian, A. (2002). PKC-zeta is required in EGF protection of microtubules and intestinal barrier integrity against oxidant injury. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G794-G808.
4. Barlowe, C., d'Enfert, C. and Schekman, R. (1993). Purification and characterization of SAR1p, a small GTP-binding protein required for transport vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 268, 873-879.
5. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M. F., Ravazzola, M., Amherdt, M. and Schekman, R. (1994). COPII: a membrane coat formed by See proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
6. Bass, N. A., Manning, J. A., Ockner, R. K., Gordon, J. I., Seetharam, S. and Alpers, D. H. (1985). Regulation ofthe biosynthesis of two distinct fatty acid-binding proteins in rat liver and intestine. J. Biol. Chem. 260, 1432-1436.
7. Bourbon, N. A., Yun, J. and Kester, M. (2000). Ceramide directly activates protein kinase C ζ to regulate a stress-activated protein kinase signaling complex. EMBO J. 14, 1961-1969.
8. Brady, S. C., Allan, L. A. and Clarke, P. R. (2005). Regulation of caspase 9 through phosphorylation by protein kinase C zeta in response to hyperosmotic stress. Mol. Biol. Cell 25, 10543-10555.
9. Bruns, R. F., Miller, F. D., Merriman, R. L., Howbert, J. J., Heath, W. F., Kobayashi, E., Takahashi, I., Tamaoki, T. and Nakano, H. (1991). Inhibition of protein kinase C by calphostin C is light-dependent. Biochem. Biophys. Res. Commun. 176, 288-293.
10. Buccione, R., DiTullio, G., Caretta, M., Marinetti, M. R., Bizzarri, C., Francavilla, S., Luini, A. and De Matteis, M. A. (1994). Analysis of protein kinase C requirement for exocytosis in permeabilized rat basophilic, leukaemic RBL-2H3 cells: a GTP-binding protein(s) as a potential target for protein kinase C. Biochem. J. 298, 149-156.
11. Corbit, K. C., Trakul, N., Eves, E. M., Diaz, B., Marshall, M. and Rosner, M. R. (2003). Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J. Biol. Chem. 278, 13061-13068.
12. DeFeo-Jones, D., Barnett, S. F., Fu, S., Hancock, P. J., Haskell, K. M., Leander, K. R., McAvoy, E., Robinson, R. G., Duggan, M. E., Lindsley, C. W. et al. (2005). Tumor cell sensitization to apoptotic stimuli by selective inhibition of specific Akt/PKB family members. Mol. Cancer Ther 4, 271-279.
13. Du, X., Kristiana, I., Wong, J. and Brown, A. J. (2006). Involvement of Akt in ER-to-Golgi transport of SCAP/SREBP: a link between a key cell proliferative pathway and membrane synthesis. Mol. Biol. Cell 17, 2735-2745.
14. Fabbri, M., Bannykh, S. and Balch, W. E. (1994). Export of protein from the endoplasmic reticulum is regulated by a diacylglycerol/phorbol ester binding protein. J. Biol. Chem. 269, 26848-26857.
15. Goodnight, J. A., Mischak, H., Kolch, W. and Mushinski, J. F. (1995). Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts. Isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J. Biol. Chem. 270, 9991-10001.
16. Gschwendt, M., Dieterich, S., Rennecke, J., Kittstein, W., Mueller, H. J. and Johannes, F. J. (1996). Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett. 392, 77-80.
17. Hirai, T. and Chida, K. (2003). Protein Kinase Czeta (PKCzeta): activation mechanisms and cellular functions. J. Biochem. 133, 1-7.
18. Hui, D. Y. and Howles, P. N. (2002). Carboxyl ester lipase: structure-function relationship and physiological role in lipoprotein metabolism and atherosclerosis. J. Lipid Res. 43, 2017-2030.
19. Husain, M. and Moss, B. (2003). Evidence against an essential role of the COPII-mediated cargo transport to the endoplasmic reticulum-Golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J. Virol. 77, 11754-11766.
20. Kano, F., Tanaka, A. R., Yamauchi, S., Kondo, H. and Murata, M. (2004). Cdc2 kinase-dependent disassembly of endoplasmic reticulum (ER) exit sites inhibits ER-to-Golgi vesicular transport during mitosis. Mol. Biol. Cell 15, 4289-4298.
21. Kirby, R. J., Zheng, S., Tso, P., Howles, A N. and Hui, D. Y. (2002). Bile salt-stimulated carboxyl ester lipase influences lipoprotein assembly and secretion in intestine: a process mediated via ceramide hydrolysis. J. Biol. Chem. 277, 4104-4109.
22. Kobayashi, E., Ando, K., Nakano, H., Iida, T., Ohno, H., Morimoto, M. and Tamaoki, T. (1989a). Calphostin (UCN-1028), novel and specific inhibitors of protein kinase C. I. Fermentation, isolation, physico-chemical properties and biological activities. J. Antibiol. 42, 1470-1474.
23. Kobayashi, E., Nakano, H., Morimoto, M. and Tamaoki T. (1989b). Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 159, 548-553.
24. Krotova, K., Hu, H., Xia, S. L., Belayev, L., Patel, J. M., Block, E. R. and Zharikov, S. (2006). Peptides modified by myristoylation activate eNOS in endothelial cells through Akt phosphorylation. Br. J. Pharmacol. 148, 732-740.
25. Kuge, O., Dascher, C., Orci, L., Rowe, T., Amherdt, M., Plutney, H., Ravazzola, M., Tanigawa, G., Rothman, J. E. and Balch, W. E. (1994). Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125, 51-65.
26. Kumar, N. S. and Mansbach, C. M. (1997). Determinants of triacylglycerol transport from the endoplasmic reticulum to the Golgi in intestine. Am. J. Physiol. 273, G378-G386.
27. Kumar, N. S. and Mansbach, C. M., 2nd (1999). Prechylomicron transport vesicle: isolation and partial characterization. Am. J. Physiol. 276, G378-G386.
28. Lee, T. H. and Lindstedt, A. D. (2000). Potential role for protein kinases in regulation of bidirectional endoplasmic reticulum-to-Golgi transport revealed by protein kinase inhibitor H89. Mol. Biol. Cell 11, 2577-2590.
29. Leitges, M., Sanz, L., Martin, P., Duran, A., Braun, U., Garcia, J. F., Camacho, F., Diaz-Meco, M. T., Rennert, P. D. and Moscal, J. (2001). Targeted disruption of the zetaPKC gene results in the impairment of the NF-kappaB pathway. Mol. Cell 8, 771-780.
30. Limatola, C., Schaap, D., Moolenaar, W. H. and van Blitterswijk, W. J. (1994). Phosphatidic acid activation of protein kinase C-zeta overexpressed in COS cells: comparison with other protein kinase C isotypes and other acidic lipids. Biochem. J. 304, 1001-1008.
31. Lin, C. R., Chen, W., Lazar, C., Carpenter, C., Gill, G. and Evans, R. (1986). Protein kinase C phosphorylation at Thr 654 of the unoccupied EGF receptor and EGF binding regulate functional receptor loss by independent mechanisms. Cell 44, 839-848.
32. Mansbach, C. M., 2nd and Arnold, A. (1986). Steady-state kinetic analysis of triacylglycerol delivery into mesenteric lymph. Am. J. Physiol. 251, G263-G269.
33. Mansbach, C. M. and Dowell, R. (2000). Effect of increasing lipid loads an the ability of the endoplasmic reticulum to transport lipid to the Golgi. J. Lipid Res. 41, 605-612.
34. Matsuoka, K., Orci, L., Amherdt, M., Bednarek, S. Y., Hamamoto, S., Schekman, R. and Yeung, T. (1998). COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263-275.
35. Mochly-Rosen, D., Khaner, H. and Lopez, J. (1991). Identification of intracellular receptor proteins for activated protein kinase C. Proc. Natl. Acad. Sci. USA 88, 3997-4000.
36. Muller, G., Ayoub, M., Storz, P., Rennecke, J., Fabbro, D. and Pfizenmair, K. (1995). PKCζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J. 14, 1961-1969.
37. Muniz, M., Martin, M. E., Hidalgo, J. and Velasco, A. (1997). Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi network. Proc. Natl. Acad. Sci. USA 94, 14461-14466.
38. Neeli, I., Siddiqi, S. A., Siddiqi, S., Mahan, J., Lagakos, W. S., Binas, B., Gheyi, T., Storch, J. and Mansbach, C. M., 2nd (2007). Liver fatty acid-binding protein initiates budding of pre-chylumicron transport vesicles from intestinal endoplasmic reticulum. J. Biol. Chem. 282, 17974-17984.
39. Nilsson, A. and Duan, R.-D. (2006). Absorption and lipoprotein transport of sphingomyelin. J. Lipid Res. 47, 154-171.
40. Nishizuka, Y. (1992). Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258, 607-614.
41. Ozawa, K., Szallasi, Z., Kazanietz, M., Blumberg, P., Mischak, H., Mushinski, J. and Beaven, M. (1993). Ca(2+)-dependent and Ca(2+)-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. Reconstitution of secretory responses with Ca(2+) and purified isozymes in washed permeabilized cells. J. Biol. Chem. 268, 1749-1756.
42. Palmer, K. J., Kunkel, J. E. and Stephens, D. J. (2005). PCTAIRE protein kinases interact directly with the COPII complex and modulate secretory cargo transport. J. Cell Sci. 118, 3839-3847.
43. Pinton, P., Leo, S., Wieckowski, M. R., DiBenedetto, G. and Rizzuto, R. (2004). Long-term modulation of mitochondrial Ca2+ signals by protein kinase C isozymes. J. Cell Biol. 165, 223-232.
44. Poirier, H., Niot, I., Degrace, P., Monnot, M. C., Bernard, A. and Besnard, P. (1997). Fatty acid regulation of fatty acid-binding protein expression in the small intestine. Am. J. Physiol. 273, G289-G295.
45. Puls, A., Schmidt, S., Grawe, F. and Stabel, S. (1997). Interaction of protein kinase C zeta with ZIP, a novel protein kinase C-binding protein. Proc. Natl. Acad. Sci. USA 94, 6191-6196.
46. Rexach, M. F. and Schekman, R. W. (1991). Distinct biochemical requirements for the budding, targeting, and fusion of ER-derived transport vesicles. J. Cell Biol. 114, 219-229.
47. Salama, N. R., Chuang, J. S. and Schekman, R. W. (1997). Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol. Biol. Cell 8, 205-217.
48. Sharma, D. K., Brown, J. C., Choudbury, A., Peterson, T. E., Holicky, E., Marks, D. L., Simari, R., Parton, R. G. and Pagano, R. E. (2004). Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell 15, 3114-3122.
49. Siddiqi, S. A., Gorelick, F. S., Mahan, J. T. and Mansbach, C. M., 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.
50. Siddiqi, S. A., Mahan, J., Siddiqi, S., Gorelick, F. S. and Mansbach, C. M., 2nd (2006a). Vesicle-associated membrane protein 7 is expressed in intestinal ER. J. Cell Sci. 119, 943-950.
51. Siddiqi, S. A., Siddiqi, S., Mahan, J., Peggs, K., Gorelick, F. S. and Mansbach, C. M., 2nd (2006b). The identification of a novel endoplasmic reticulum to Golgi SNARE complex used by the prechylomicron transport vesicle. J. Biol. Chem. 281, 20974-20982.
52. Simon, J. P., Ivanov, I. E., Adesnik, M. and Sabatini, D. D. (1996). The production of post-Golgi vesicles requires a protein kinase C-like molecule, but not its phosphorylating activity. J. Cell Biol. 135, 355-370.
53. Standaert, M. L., Galloway, L., Karnam, P., Bandyopadhyay, G., Moscat, J. and Farese, R. V. (1997). Protein kinase C-zeta as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. J. Biol. Chem. 272, 30075-30082.
54. Tisdale, E. J. (2000). Rab2 requires PKC iota/lambda to recruit beta-COP for vesicle formation. Traffic 1, 702-712.
55. Tisdale, E. J. and Artalejo, C. R. (2006). Src-dependent aprotein kinase C iota/lambda (aPKCiota/lambda) tyrosine phosphorylation is required for aPKCiota/lambda association with Rab2 and glyceraldehyde-3-phosphate dehydrogenase on pre-golgi intermediates. J. Biol. Chem. 281, 8436-8442.
56. Tso, P., Kendrick, M., Balint, J. A. and Simmonds, W. J. (1981). Role of biliary phosphatidylcholine in the absorption and transport of dietary triolein in the rat. Gastroenterology 80, 60-65.
57. Westermann, P., Knoblich, M., Maier, O., Lindschau, C. and Haller, H. (1996). Protein kinase C bound to the Golgi apparatus supports the formation of constitutive transport vesicles. Biochem. J. 320, 651-658.
58. Zilversmit, D. B. (1967). Formation and transport of chylomicrons. Fed. Proc. 26, 1599-1605.