CTP:phosphocholine cytidylyltransferase binds anionic phospholipid vesicles in a cross-bridging mode

Biochemistry

Volumn 44, Issue 26, 2005, Pages 9382-9393

  Taneva, Svetla G ^a   Patty, Philipus J ^a   Frisken, Barbara J ^a   Cornell, Rosemary B ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CARBOXYLIC ACIDS; COLLOIDS; DIMERS; HYDRODYNAMICS; LIGHT SCATTERING; NEGATIVE IONS; PHOSPHOLIPIDS; REACTION KINETICS; SURFACE PROPERTIES; TRANSMISSION ELECTRON MICROSCOPY;

CELLULAR EVENTS; ELECTRON MICROGRAPHS; HELICAL DOMAINS; VESICLE AGGREGATION;

ENZYME KINETICS;

CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; COLLOIDAL GOLD; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL;

ARTICLE; BINDING AFFINITY; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME PURIFICATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGHT SCATTERING; MATHEMATICAL COMPUTING; PEPTIDE SYNTHESIS; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY;

ANIONS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLD; MICROSCOPY, ELECTRON, TRANSMISSION; NUCLEOTIDYLTRANSFERASES; PHOSPHOLIPIDS; PROTEIN BINDING;

EID: 21644441531     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050679p     Document Type: Article

References (68)

1. Cornell R. B., and Northwood, I. C. (2000) Regulation of CTP: phosphocholine cytidylyltransferase by amphitropism and relocalization, Trends Btochem. Sci. 25, 441-447.
2. Arnold, R. S., and Cornell, R. B. (1996) Lipid regulation of CTP: phosphocholine cytidylyltransferase: Electrostatic, hydrophobic, and synergistic interactions of anionic phospholipids and diacylglycerol, Biochemistry 35, 9917-9924.
3. Arnold, R. S., De Paoli-Roach, A., and Cornell, R. B. (1997) Binding of CTP:phosphocholine cytidylyltransferase to lipid vesicles: Diacylglycerol and enzyme dephosphorylation increase the affinity for negatively charged membranes, Biochemistry 36, 6149-6156.
4. Johnson, J. E., Rao, N. M., Hui, S.-W., and Cornell, R. B. (1998) Conformation and lipid binding properties of four peptides derived from the membrane-binding domain of CTP:phosphocholine cytidylyltransferase, Biochemistry 37, 9509-9519.
5. Johnson, J. E., Xie, M., Sing, L. M., Edge, R., and Cornell, R. B. (2003) Both acidic and basic amino acids in an amphitropic enzyme, CTP:phosphocholine cytidylyltransferase, dictate its selectivity for anionic membranes, J. Biol. Chem. 278, 514-522.
6. Cornell R. B., and Vance, D. E. (1987) Translocation of CTP: phosphocholine cytidylyltransferase from cytosol to membranes in HeLa cells: Stimulation by fatty acid, fatty alcohol, mono- and diacylglycerol, Biochim. Biophys. Acta 919, 26-36.
7. Wang, Y., MacDonald, J. I. S., and Kent, C. (1993) Regulation of CTP:phosphocholine cytidylyltransferase in HeLa cells. Effect of oleate on phosphorylation and intracellular localization, J. Biol. Chem. 268, 5512-5518.
8. Jamil, H., Hatch, G., and Vance, D. E. (1993) Evidence that binding of CTP:phosphocholine cytidylyltransferase to membranes in rat hepatocytes is modulated by the ratio of bilayer- to non-bilayer-forming lipids, Biochem. J. 291, 419-427.
9. Utal, A., Jamil, H., and Vance, D. E. (1991) Diacylglycerol signals the translocation of CTP:choline-phosphate cytidylyltransferase in HeLa cells treated with 12-O-tetradecanoylphorbol-13-acetate. J. Biol. Chem. 266, 24084-24091.
10. Attard, G. S., Templer, R. H., Smith, W. S., Hunt, A. N., and Jackowski, S. (2000) Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress, Proc. Natl. Acad. Sci. U.S.A. 97, 9032-9036.
11. Davies, S. M. A., Epand, R. M., Kraayenhof, R., and Cornell, R. B. (2001) Regulation of CTP:phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: An important role for stored curvature strain energy, Biochemistry 40, 10522-10531.
12. Watkins, J. D., and Kent, C. (1992) Immunolocalization of membrane-associated CTP:phosphocholine cytidylyltransferase in phosphatidylcholine-deficient Chinese hamster ovary cells, J. Biol. Chem. 267, 5686-5692.
13. Lagace, T. A., Story, M. K., and Ridgeway, N. D. (2000) Regulation of phosphatidylcholine metabolism in Chinese hamster ovary cells by the sterol regulatory element-binding protein (SREBP)/SREBP cleavage-activating protein pathway, J. Biol. Chem. 275, 14367-14374.
14. Lagace, T. A., and Ridgway, N. D. (2005) The rate-limiting enzyme in phosphatidylcholine synthesis regulates proliferation of the nucleoplasmic reticulum, Mol. Biol. Cell 16, 1120-1130.
15. 1 transition, J. Biol. Chem. 274, 26240-26248.
16. Lykidis, A., Baburina, I., and Jackowski, S. (1999) Distribution of CTP:phosphocholine cytidylyltransferase (CCT) isoforms. Identification of a new CCTβ splice variant, J. Biol. Chem. 274, 26992-70001.
17. D'Antuono, C., del Carmen Fernández-Tomé, M., Sterin-Speziale, N., and Bernik, D. L. (2000) Lipid-protein interactions in rat renal subcellular membranes: A biophysical and biochemical study, Arch. Biochem. Biophys. 382, 39-47.
18. Neitcheva, T., and Peeva, D. (1995) Phospholipid composition, phospholipase A2 and sphingomyelinase activities in rat liver nuclear membrane and matrix. Int. J. Biochem. Cell Biol. 27, 995-1001.
19. Cornell, R. B. (1989) Chemical cross-linking reveals a dimeric structure for CTP:phosphocholine cytidylyltransferase, J. Biol. Chem. 264, 9077-9081.
20. Weber, C. H., Park, Y. S., Sanker, S., Kent, K., and Ludwig, M. (1999) A prototypical cytidylyltransferase: CTP:glycerol-3-phosphate cytidylyltransferase from Bacillus subtilis, Structure 7, 1113-1124.
21. Xie, M., Smith, J. L., Ding, Z., Zhang, D., and Cornell, R. B. (2004) Membrane binding modulates the quaternary structure of CTP:phosphocholine cytidylyltransferase, J. Biol. Chem. 279, 28817-28825.
22. Dunne, J. S., Cornell, R. B., Johnson, J. E., Glover, N. R., and Tracey, A. S. (1996) Structure of the membrane binding domain of CTP:phosphocholine cytidylyltransferase, Biochemistry 35, 11975-11984.
23. Taneva, S., Johnson, J. E., and Cornell, R. B. (2003) Lipid-induced conformational switch in the membrane binding domain of CTP: phosphocholine cytidylyltransferase: A circular dichroism study, Biochemistry 42, 11768-11776.
24. MacDonald, J. I., and Kent, C. (1994) Identification of phosphorylation sites in rat liver CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 269, 10529-10537.
25. Wang, Y., and Kent, C. (1995) Effects of altered phosphorylation sites on the properties of CTP:phosphocholine cytidylyltransferase, J. Biol. Chem. 270, 17843-17849.
26. Yang, W., and Jackowski, S. (1995) Lipid activation of CTP: phosphocholine cytidylyltransferase is regulated by the phosphorylated carboxyl-terminal domain, J. Biol. Chem. 270, 16503-16506.
27. Wang, Y., and Kent, C. (1995) Identification of an inhibitory domain of CTP:phosphocholine cytidylyltransferase, J. Biol. Chem. 270, 18948-18952.
28. Friesen, J. A., Campbell, H. A., and Kent, C. (1999) Enzymatic and cellular characterization of a catalytic fragment of CTP: phosphocholine cytidylyltransferase α, J. Biol. Chem. 274, 13384-13389.
29. Bartlett, G. R. (1959) Phosphorus assay in column chromatography, J. Biol. Chem. 234, 466-468.
30. Houslay, M. D., and Stanley, K. K. (1982) Dynamics of biological membranes: Influence of synthesis, structure and function, Willey, New York.
31. Evans, R. W., Williams, M. A., and Tinoco, J. (1987) Surface areas of 1-palmitoyl phosphatidylcholines and their interactions with cholesterol, Biochem. J. 245, 455-462.
32. Ha, T. H., Kim, D. K., Choi, M.-U., and Kim, K. (2000) Influence of poly(ethylenimine) on the monolayer of oleic acid at the air/water Interface, J. Colloid Interface Sci. 226, 98-104.
33. Tamm, L. K. (1994) Physical Studies of Peptide-Bilayer Interactions, in Membrane Protein Structure (White, S. H., Ed.) pp 283-313, Oxford University Press, New York.
34. Berne, B. J., and Pecora, R. (1990) Dynamic Light Scattering, Robert E. Krieger Publishing Co.: Melbourne, Florida.
35. Hallet, F. R., Nickel, B., Samuels, C., and Krygsman, P. H. (1991) Determination of vesicle size distribution by freeze fracture electron microscopy, J. Electron Microsc. Tech. 17, 459-466.
36. Slot, J. W., and Geuze, H. J. (1985) A new method of preparing gold probes for multiple-labeling cytochemistry, Eur. J. Cell Biol. 38, 87-93.
37. Baschong, W., and Wrigley, N. G. (1990) Small colloidal gold conjugated to Fab fragments or to immunoglobulin G as high-resolution labels for electron microscopy: A technical overview, J. Electron Microsc. Tech. 14, 313-323.
38. De Arcuri, B. F., Vechetti, G. F., Chehin, R. N., Goni, F. M., and Morero, R. D. (1999) Protein-induced fusion of phospholipid vesicles of heterogeneous sizes, Biochem. Biophys. Res. Commun. 262, 586-590.
39. Struck, D. K., Hoekstra, D., and Pagano, R. E. (1981) Use of resonance energy transfer to monitor membrane fusion, Biochemistry 20, 4093-4099.
40. Mui, B. L.-S., Cullis, P. R., Evans, E. A., and Madden, T. D. (1993) Osmotic properties of large unilamellar vesicles prepared by extrusion, Biophys. J. 64, 443-453.
41. Suarez, T., Gallaher, W. R., Agirre, A., and Goni, F. M. (2000) The pre-transmembrane region of the human immunodeficiency virus type-1 glycoprotein: A novel fusogenic sequence, J. Virol. 74, 8038-8047.
42. Langosch, D., Crane, J. M., Brosig, B., Hellwig, A., Tamm, L. K., and Reed, J. (2001) Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity, J. Mol. Biol. 311, 709-721.
43. Kaetzel, M. A., Mo, Y. D., Mealy, T. R., Campos, B., Bergsma-Schutter, W., Brisson, A., Dedman, J. R., and Seaton, B. A. (2001) Phosphorylation mutants elucidate the mechanism of annexin IV-mediated membrane aggregation, Biochemistry 40, 4192-4199.
44. Bizzozero, O. A., and Howard, T. A. (2002) Myelin proteolipid protein-induced aggregation of lipid vesicles: Efficacy of the various molecular species, Neurochem. Res. 27, 1269-1277.
45. Bernad, S., Oellerich, S., Soulimane, T., Noinville, S., Baron, M.-H., Paternostre, M., and Lecomte, S. (2004) Interaction of horse heart and thermus thermophilus type cytochromes with phospholipid vesicles and hydrophobic surfaces, Biophys. J. 86, 3863-3872.
46. Ter Beest, M. B. A., and Hoekstra, D. (1993) Interaction of myelin basic protein with artificial membranes. Parameters governing binding, aggregation and dissociation, Eur. J. Biochem. 211, 689-696.
47. Stachowiak, O., Dolder, M., and Wallimann, T. (1996) Membrane-binding and lipid vesicle cross-linking kinetics of the mitochondrial creatine kinase octamer, Biochemistry 35, 15522-15528.
48. Kramer, S. D., Jakits-Deiser, C., and Wunderli-Allenspach, H. (1997) Free fatty acids cause pH-dependent changes in drug-lipid membrane interactions around physiological pH, Pharm. Res. 14, 827-832.
49. Seddon, J. M., Templer, R. H., Wartender, N. A., Huang, Z., Cevc, G., and Marsh, D. (1997) Phosphatidylcholine-fatty acid membranes: Effects of headgroup hydration on the phase behaviour and structural parameters of the gel and inverse hexagonal (H(II)) phases, Biochim. Biophys. Acta 1327, 131-147.
50. Templer, R. H., Seddon, J. M., and Duesing, P. M. (1998) Modeling the phase behaviour of the inverse hexagonal and inverse bicontinuous cubic phases in 2:1 fatty acid/phosphatidylcholine mixtures, J. Phys. Chem. B 102, 7262-7271.
51. Snapp, E. L., Hedge, R. S., Francolini, M., Lombarde, F., Colombo, S., Pedrazzini, E., Borgese, N., and Lippincott-Schwartz, J. (2003) Formation of stacked ER cisternae by low affinity protein interactions, J. Cell Biol. 163, 257-269.
52. Glabe, C. G. (1985) Interaction of the sperm adhesive protein, bindin, with phospholipid vesicles. I. Specific association of bindin with gel-phase phospholipid vesicles, J. Cell Biol. 100, 794-799.
53. Ulrich, A. S., Otter, M., Glabe, C. G., and Hoekstra, D. (1998) Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin, J. Biol. Chem. 273, 16748-16755.
54. Lambert, O., Cavusoglu, N., Gallay, J., Vincent, M., Rigaud, J. L., Henry, J.-P., and Ayala-Sanmartin, J. (2004) Novel organization and properties of annexin 2-membrane complexes, J. Biol. Chem. 279, 10872-10882.
55. Chattopadhyay, S., Sun, P., Wang, P., Abonyo, B., Cross, N. L., and Liu, L. (2003) Fusion of lamellar body with plasma membrane is driven by the dual action of annexin II tetramer and arachidonic acid, J. Biol. Chem. 278, 39675-39683.
56. Boggs, J. M., Yip, P. M., Rangaraj, G., and Jo, E. (1997) Effect of posttranslational modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles, Biochemistry 36, 5065-5071.
57. MacMillan, S. V., Ishiyama, N., White, G. F., Palaniyar, N., Hallett, F. R., and Harauz, G. (2000) Myelin basic protein component C1 in increasing concentrations can elicit fusion, aggregation, and fragmentation of myelin-like membranes, Eur. J. Cell Biol. 79, 327-335.
58. Ruano, M. L. F., Miguel, E., Perez-Gil, J., and Casals, C. (1996) Comparison of lipid aggregation and self-aggregation activities of pulmonary surfactant-associated protein A, Biochem. J. 313, 683-689.
59. Williams, M. C., Hawgood, S., and Hamilton, R. L. (1991) Changes in lipid structure produced by surfactant proteins SP-A, SP-B, and SP-C, Am. J. Respir. Cell Mol. Biol. 5, 41-50.
60. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., and Rothman, J. E. (1998) SNAREpins: Minimal Machinery for Membrane Fusion, Cell 92, 759-772.
61. Kent, C., and Carman, G. M. (1999) Interactions among pathways for phosphatidylcholine metabolism, CTP synthesis and secretion through the Golgi apparatus, Trends Biochem. Sci. 24, 146-150.
62. Huijbregts, R. T., Topalof, L., and Bankaitis, V. A. (2000) Lipid metabolism and regulation of membrane trafficking, Traffic 1, 195-202.
63. Howe, A. G., and McMaster, C. R. (2001) Regulation of vesicle trafficking, transcription, and meiosis: Lessons learned from yeast regarding the disparate biologies of phosphatidylcholine, Biochim. Biophys. Acta 1534, 65-77.
64. Cleves, A. E., McGee, T. P., Whitters, E. A., Champion, K., Aitken, J. R., Dowhan, W., Goebl, M., and Bankaitis, V. A. (1991) Mutations in the CDP-choline pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein, Cell 64, 789-800.
65. Litvak, V.. Dahan, N., Ramachandran, S., Sabanay, H., and Lev, S. (2005) Maintenance of the diacylglycerol level in the Golgi apparatus by the Nir2 protein is critical for Golgi secretory function, Nat. Cell Biol. 7, 225-234.
66. Amarilio, R., Ramachandran, S., Sabanay, H., and Lev, S. (2005) Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction, J. Biol. Chem. 280, 5934-5944.
67. Feldman, D. A., and Weinhold, P, A. (1998) Cytidylyltransferase-binding protein is identical to transcytosis-associated protein (TAP/p115) and enhances the lipid activation of cytidylyltransferase, J. Biol. Chem. 273, 102-109.
68. Shorter, J., Beard, M. B., Seemann, J., Dirac-Svejstrup, A. B., and Warren, G. (2002) Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115, J. Cell Biol. 157, 45-62.