A 22-mer segment in the structurally pliable regulatory domain of metazoan CTP: Phosphocholine cytidylyltransferase facilitates both silencing and activating functions

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38980-38991

  Ding, Ziwei ^a   Taneva, Svetla G ^a   Huang, Harris K H ^a,b   Campbell, Stephanie A ^a,c   Semenec, Lucie ^a,d   Chen, Nansheng ^a   Cornell, Rosemary B ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BC CHILDREN S HOSPITAL   (Canada)

^d IData Research   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING FUNCTION; AMPHIPATHIC; CAENORHABDITIS ELEGANS; CATALYTIC DOMAINS; CATALYTIC EFFICIENCIES; CHIMERIC ENZYMES; CONFORMATIONAL PLASTICITY; CYTIDYLYLTRANSFERASE; DUAL FUNCTION; ENZYME ACTIVATION; LIPID VESICLES; MEMBRANE BINDING; PHOSPHATIDYLCHOLINE SYNTHESIS; PHOSPHOCHOLINE; REGULATORY DOMAIN; SEQUENCE MOTIFS; SYNUCLEIN;

BINDING ENERGY; ENZYMES; RATS; YEAST;

CHEMICAL ACTIVATION;

ALPHA SYNUCLEIN; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME LOCALIZATION; ENZYME REGULATION; LIPID VESICLE; MEMBRANE BINDING; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESIDUE ANALYSIS; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

ALPHA-SYNUCLEIN; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; CATALYTIC DOMAIN; CHOLINE-PHOSPHATE CYTIDYLYLTRANSFERASE; COMPUTATIONAL BIOLOGY; CYTIDINE TRIPHOSPHATE; ENZYME ACTIVATION; GENE SILENCING; KINETICS; LIPIDS; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLCHOLINES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; CAENORHABDITIS ELEGANS; INVERTEBRATA; METAZOA; RATTUS; SACCHAROMYCES CEREVISIAE; VERTEBRATA;

EID: 84869038203     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.402081     Document Type: Article

References (61)

1. Behnia, R., and Munro, S. (2005) Organelle identity and the signposts for membrane traffic. Nature 438, 597-604 (Pubitemid 41740563)
2. Frost, A. (2011) Membrane trafficking. Decoding vesicle identity with contrasting chemistries. Curr. Biol. 21, R811-813
3. Shih, Y. L., Huang, K. F., Lai, H. M., Liao, J. H., Lee, C. S., Chang, C. M., Mak, H. M., Hsieh, C. W., and Lin, C. C. (2011) The N-terminal amphipathic helix of the topological specificity factor MinE is associated with shaping membrane curvature. PLoS ONE 6, e21425
4. Cornell, R. B., and Taneva, S. G. (2006) Amphipathic helices as mediators of the membrane interaction of amphitropic proteins and as modulators of bilayer physical properties. Curr. Protein Pept. Sci. 7, 539-552 (Pubitemid 44883931)
5. Campelo, F., McMahon, H. T., and Kozlov, M. M. (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys J. 95, 2325-2339
6. Drin, G., and Antonny, B. (2010) Amphipathic helices and membrane curvature. FEBS Lett. 584, 1840-1847
7. Neumann, P., Weidner, A., Pech, A., Stubbs, M. T., and Tittmann, K. (2008) Structural basis for membrane binding and catalytic activation of the peripheral membrane enzyme pyruvate oxidase from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 105, 17390-17395
8. Weidner, A., Neumann, P., Pech, A., Stubbs, M. T., and Tittmann, K. (2009) New insights into the membrane-binding and activation mechanism of pyruvate oxidase from Escherichia coli. J. Mol. Catal. B Enzym. 61, 88-92
9. Cornell, R. B. (1998)Howcytidylyltransferase uses an amphipathic helix to sense membrane phospholipid composition. Biochem. Soc. Trans. 26, 539-544
10. Cornell, R. B., and Northwood, I. C. (2000) Regulation of CTP:phosphocholine cytidylyltransferase by amphitropism and relocalization. Trends Biochem. Sci. 25, 441-447 (Pubitemid 30662412)
11. 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 (Pubitemid 37243638)
12. Lee, J., Johnson, J., Ding, Z., Paetzel, M., and Cornell, R. B. (2009) Crystal structure of a mammalian CTP:phosphocholine cytidylyltransferase catalytic domain reveals novel active site residues within a highly conserved nucleotidyltransferase fold. J. Biol. Chem. 284, 33535-33548
13. 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
14. Taneva, S., Dennis, M. K., Ding, Z., Smith, J. L., and Cornell, R. B. (2008) Contribution of each membrane binding domain of the CTP:phosphocholine cytidylyltransferase-α dimer to its activation, membrane binding, and membrane cross-bridging. J. Biol. Chem. 283, 28137-28148
15. Yang, W., Boggs, K. P., and Jackowski, S. (1995) The association of lipid activators with the amphipathic helical domain of CTP:phosphocholine cytidylyltransferase accelerates catalysis by increasing the affinity of the enzyme for CTP. J. Biol. Chem. 270, 23951-23957
16. Taneva, S. G., Lee, J. M., and Cornell, R. B. (2012) The amphipathic helix of an enzyme that regulates phosphatidylcholine synthesis remodels membranes into highly curved nanotubules. Biochim. Biophys. Acta 1818, 1173-1186
17. Bogan, M. J., Agnes, G. R., Pio, F., and Cornell, R. B. (2005) Interdomain and membrane interactions of CTP:phosphocholine cytidylyltransferase revealed via limited proteolysis and mass spectrometry. J. Biol. Chem. 280, 19613-19624 (Pubitemid 41379484)
18. Cornell, R. B., Kalmar, G. B., Kay, R. J., Johnson, M. A., Sanghera, J. S., and Pelech, S. L. (1995) Functions of the C-terminal domain of CTP:phosphocholine cytidylyltransferase. Effects of C-terminal deletions on enzyme activity, intracellular localization, and phosphorylation potential. Biochem. J. 310, 699-708
19. MacDonald, J. I., and Kent, C. (1994) Identification of phosphorylation sites in rat liver CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 269, 10529-10537 (Pubitemid 24198253)
20. Johnson, J. E., and Cornell, R. B. (1994) Membrane-binding amphipathic α-helical peptide derived from CTP:phosphocholine cytidylyltransferase. Biochemistry 33, 4327-4335
21. 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 mem-brane- binding domain of CTP:phosphocholine cytidylyltransferase. Biochemistry 37, 9509-9519 (Pubitemid 28307707)
22. Johnson, J. E., Xie, M., Singh, 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 (Pubitemid 36043604)
23. Larvor, M. P., Cerdan, R., Gumila, C., Maurin, L., Seta, P., Roustan, C., and Vial, H. (2003) Characterization of the lipid-binding domain of the Plasmodium falciparum CTP:phosphocholine cytidylyltransferase through synthetic peptide studies. Biochem. J. 375, 653-661 (Pubitemid 37433513)
24. Wang, Y., and Kent, C. (1995) Identification of an inhibitory domain of CTP: phosphocholine cytidylyltransferase. J. Biol. Chem. 270, 18948-18952
25. Friesen, J. A., Liu, M. F., and Kent, C. (2001) Cloning and characterization of a lipid-activated CTP:phosphocholine cytidylyltransferase from Caenorhabditis elegans. Identification of a 21-residue segment critical for lipid activation. Biochim. Biophys. Acta 1533, 86-98 (Pubitemid 32879385)
26. Ridsdale, R., Tseu, I., Wang, J., and Post, M. (2010) Functions of membrane binding domain of CTP:phosphocholine cytidylyltransferase in alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 43, 74-87
27. Yang, J., Wang, J., Tseu, I., Kuliszewski, M., Lee, W., and Post, M. (1997) Identification of an 11-residue portion of CTP-phosphocholine cytidylyltransferase that is required for enzyme-membrane interactions. Biochem. J. 325, 29-38 (Pubitemid 27322682)
28. Braker, J. D., Hodel, K. J., Mullins, D. R., and Friesen, J. A. (2009) Identification of hydrophobic amino acids required for lipid activation of C. elegans CTP:phosphocholine cytidylyltransferase. Arch. Biochem. Biophys. 492, 10-16
29. Bussell, R., Jr., and Eliezer, D. (2003) A structural and functional role for 11-mer repeats in α-synuclein and other exchangeable lipid-binding proteins. J. Mol. Biol. 329, 763-778
30. Gautier, R., Douguet, D., Antonny, B., and Drin, G. (2008) HELIQUEST.A web server to screen sequences with specific α-helical properties. Bioinformatics 24, 2101-2102
31. Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Finn, R. D., and Sonnhammer, E. L. (1999) Pfam 3.1. 1313 multiple alignments and profile HMMs match the majority of proteins. Nucleic Acids Res. 27, 260-262 (Pubitemid 29209455)
32. Higgins, D. G., Thompson, J. D., and Gibson, T. J. (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383-402 (Pubitemid 26165878)
33. Felsenstein, J. (1988) Phylogenies from molecular sequences. Inference and reliability. Annu. Rev. Genet. 22, 521-565
34. Page, R. D. (1996) TreeView. An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358
35. 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 (Pubitemid 38900167)
36. Beck, R., and Burtscher, H. (1994) Introduction of arbitrary sequences into genes by use of class IIs restriction enzymes. Nucleic Acids Res. 22, 886-887 (Pubitemid 24160920)
37. Helmink, B. A., and Friesen, J. A. (2004) Characterization of a lipid-activated CTP:phosphocholine cytidylyltransferase from Drosophila melanogaster. Biochim. Biophys. Acta 1683, 78-88 (Pubitemid 38844662)
38. Cornell, R. B. (1991) Regulation of CTP:phosphocholine cytidylyltransferase by lipids. 2. Surface curvature, acyl chain length, and lipid-phase dependence for activation. Biochemistry 30, 5881-5888
39. Drobnies, A. E., Davies, S. M., Kraayenhof, R., Epand, R. F., Epand, R. M., and Cornell, R. B. (2002) CTP:phosphocholine cytidylyltransferase and protein kinase C recognize different physical features of membranes. Differential responses to an oxidized phosphatidylcholine. Biochim. Biophys. Acta 1564, 82-90 (Pubitemid 34717872)
40. Dennis, M. K., Taneva, S. G., and Cornell, R. B. (2011) The intrinsically disordered nuclear localization signal and phosphorylation segments distinguish the membrane affinity of two cytidylyltransferase isoforms. J. Biol. Chem. 286, 12349-12360
41. Ng, M. N., Kitos, T. E., and Cornell, R. B. (2004) Contribution of lipid second messengers to the regulation of phosphatidylcholine synthesis during cell cycle re-entry. Biochim. Biophys. Acta 1686, 85-99 (Pubitemid 39446881)
42. 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 (Pubitemid 30626668)
43. Davies, S. M., 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 (Pubitemid 32816663)
44. Craig, L., Johnson, J. E., and Cornell, R. B. (1994) Identification of the membrane-binding domain of rat liver CTP:phosphocholine cytidylyltransferase using chymotrypsin proteolysis. J. Biol. Chem. 269, 3311-3317 (Pubitemid 24237645)
45. Johnson, J. E., Aebersold, R., and Cornell, R. B. (1997) An amphipathic α-helix is the principal membrane-embedded region of CTP:phosphocholine cytidylyltransferase. Identification of the 3-(trifluoromethyl)-3-(m-[125I] iodophenyl)diazirine photolabeled domain. Biochim. Biophys. Acta 1324, 273-284 (Pubitemid 27117834)
46. McGuffin, L. J. (2008) Intrinsic disorder prediction from the analysis of multiple protein fold recognition models. Bioinformatics 24, 1798-1804
47. Dunne, S. J., 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 (Pubitemid 26313668)
48. Georgieva, E. R., Ramlall, T. F., Borbat, P. P., Freed, J. H., and Eliezer, D. (2010) The lipid-binding domain of wild-type and mutant α-synuclein. Compactness and interconversion between the broken and extended helix forms. J. Biol. Chem. 285, 28261-28274
49. Lokappa, S. B., and Ulmer, T. S. (2011) α-Synuclein populates both elongated and broken helix states on small unilamellar vesicles. J. Biol. Chem. 286, 21450-21457
50. Walkey, C. J., Kalmar, G. B., and Cornell, R. B. (1994) Overexpression of rat liver CTP:phosphocholine cytidylyltransferase accelerates phosphatidylcholine synthesis and degradation. J. Biol. Chem. 269, 5742-5749 (Pubitemid 24242946)
51. Gehrig, K., Morton, C. C., and Ridgway, N. D. (2009) Nuclear export of the rate-limiting enzyme in phosphatidylcholine synthesis is mediated by its membrane binding domain. J. Lipid Res. 50, 966-976
52. Wright, P. E., and Dyson, H. J. (2009) Linking folding and binding. Curr. Opin. Struct. Biol. 19, 31-38
53. 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 (Pubitemid 26303007)
54. Jamil, H., Hatch, G. M., 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 nonbilayer-forming lipids. Biochem. J. 291, 419-427 (Pubitemid 23127023)
55. Friesen, J. A., Park, Y. S., and Kent, C. (2001) Purification and kinetic characterization of CTP:phosphocholine cytidylyltransferase from Saccharomyces cerevisiae. Protein Expr. Purif. 21, 141-148 (Pubitemid 32614507)
56. Johnson, J. E., Kalmar, G. B., Sohal, P. S., Walkey, C. J., Yamashita, S., and Cornell, R. B. (1992) Comparison of the lipid regulation of yeast and rat CTP:phosphocholine cytidylyltransferase expressed in COS cells. Biochem. J. 285, 815-820
57. Wang, X., and Moore, T. S. (1990) Phosphatidylcholine biosynthesis in castor bean endosperm. Purification and properties of cytidine 5′-triphosphate: choline-phosphate cytidylyltransferase. Plant Physiol. 93, 250-255 (Pubitemid 120029865)
58. Yeo, H. J., Larvor, M. P., Ancelin, M. L., and Vial, H. J. (1997) Plasmodium falciparum CTP:phosphocholine cytidylyltransferase expressed in Escherichia coli. Purification, characterization, and lipid regulation. Biochem. J. 324, 903-910
59. Kalmar, G. B., Kay, R. J., Lachance, A., Aebersold, R., and Cornell, R. B. (1990) Cloning and expression of rat liver CTP:phosphocholine cytidylyltransferase. An amphipathic protein that controls phosphatidylcholine synthesis. Proc. Natl. Acad. Sci. U.S.A. 87, 6029-6033
60. Eisenberg, D., Weiss, R. M., and Terwilliger, T. C. (1982 The helical hydrophobic moment. A measure of the amphiphilicity of a helix. Nature 299, 271-374
61. Fauchere, J., and Pliska, V. (1983) Hydrophobic parameters of amino acid side chains from the partitioning of N-acetylamino acid amides. Eur. J. Med. Chem. 8, 369-375