Nuclear export of the rate-limiting enzyme in phosphatidylcholine synthesis is mediated by its membrane binding domain

Journal of Lipid Research

Volumn 50, Issue 5, 2009, Pages 966-976

  Gehrig, Karsten ^a   Morton, Craig C ^a   Ridgway, Neale D ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Amphipathic helix; CTP:phosphocholine cytidylyltransferase ; Farnesol; Fatty acid

Indexed keywords

CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE ALPHA; FARNESOL; OLEIC ACID; PHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG; HYBRID PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; MEMBRANE BINDING; MEMBRANE TRANSPORT; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ACTIVE TRANSPORT; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CHO CELL; CRICETULUS; GENETICS; HAMSTER; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CHO CELLS; CHOLINE-PHOSPHATE CYTIDYLYLTRANSFERASE; CRICETINAE; CRICETULUS; ENZYME ACTIVATION; NUCLEAR ENVELOPE; OLEIC ACID; PHOSPHATIDYLCHOLINES; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 67649684294     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800632-JLR200     Document Type: Article

References (46)

1. Vance, J. E., and D. E. Vance. 2005. Metabolic insights into phospholipid function using gene-targeted mice. J. Biol. Chem. 280: 10877-10880.
2. Cui, Z., and M. Houweling. 2002. Phosphatidylcholine and cell death. Biochim. Biophys. Acta. 1585: 87-96.
3. Vance, D. E., Z. Li, and R. L. Jacobs. 2007. Hepatic phosphatidyl-ethanolamine N-methyltransferase, unexpected roles in animal biochemistry and physiology. J. Biol. Chem. 282: 33237-33241.
4. Lykidis, A., and S. Jackowski. 2001. Regulation of mammalian cell membrane biosynthesis. Prog. Nucleic Acid Res. Mol. Biol. 65: 361-393.
5. Karim, M., P. Jackson, and S. Jackowski. 2003. Gene structure, expression and identification of a new CTP:phosphocholine cytidylyl-transferase beta isoform. Biochim. Biophys. Acta. 1633: 1-12.
6. Lykidis, A., I. Baburina, and S. Jackowski. 1999. Distribution of CTP: phosphocholine cytidylyltransferase (CCT) isoforms. Identification of a new CCTbeta splice variant. J. Biol. Chem. 274: 26992-27001.
7. Cornell, R. B. 1998. How cytidylyltransferase uses an amphipathic helix to sense membrane phospholipid composition. Biochem. Soc. Trans. 26: 539-544.
8. Davies, S. M., R. M. Epand, R. Kraayenhof, and R. B. Cornell. 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.
9. Attard, G. S., R. H. Templer, W. S. Smith, A. N. Hunt, and S. Jackowski. 2000. Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress. Proc. Natl. Acad. Sci. USA. 97: 9032-9036.
10. Yang, W., K. P. Boggs, and S. Jackowski. 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.
11. Yang, W., and S. Jackowski. 1995. Lipid activation of CTP:phosphocholine cytidylyltransferase is regulated by the phosphorylated carboxyl-terminal domain. J. Biol. Chem. 270: 16503-16506.
12. Wang, Y., and C. Kent. 1995. Effects of altered phosphorylation sites on the properties of CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 270: 17843-17849.
13. Lagace, T. A., J. R. Miller, and N. D. Ridgway. 2002. Caspase processing and nuclear export of CTP:phosphocholine cytidylyltransferase alpha during farnesol-induced apoptosis. Mol. Cell. Biol. 22: 4851-4862.
14. Watkins, J. D., and C. Kent. 1992. Immunolocalization of membrane-associated CTP:phosphocholine cytidylyltransferase in phosphatidylcholine-deficient Chinese hamster ovary cells. J. Biol. Chem. 267: 5686-5692.
15. Wang, Y., T. D. Sweitzer, P. A. Weinhold, and C. Kent. 1993. Nuclear localization of soluble CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 268: 5899-5904.
16. Wang, Y., J. I. MacDonald, and C. Kent. 1995. Identification of the nuclear localization signal of rat liver CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 270: 354-360.
17. Aoyama, C., H. Liao, and K. Ishidate. 2004. Structure and function of choline kinase isoforms in mammalian cells. Prog. Lipid Res. 43: 266-281.
18. Henneberry, A. L., M. M. Wright, and C. R. McMaster. 2002. The major sites of cellular phospholipid synthesis and molecular determinants of fatty acid and lipid head group specificity. Mol. Biol. Cell. 13: 3148-3161.
19. Lagace, T. A., and N. D. Ridgway. 2005. The rate-limiting enzyme in phosphatidylcholine synthesis regulates proliferation of the nucleoplasmic reticulum. Mol. Biol. Cell. 16: 1120-1130.
20. Gehrig, K., R. B. Cornell, and N. D. Ridgway. 2008. Expansion of the nucleoplasmic reticulum requires the coordinated activity of lamins and CTP:phosphocholine cytidylyltransferase α. Mol. Biol. Cell. 19: 237-247.
21. McClintock, D., L. B. Gordon, and K. Djabali. 2006. Hutchinson-Gilford progeria mutant lamin A primarily targets human vascular cells as detected by an anti-lamin A G608G antibody. Proc. Natl. Acad. Sci. USA. 103: 2154-2159.
22. Brandt, A., F. Papagiannouli, N. Wagner, M. Wilsch-Brauninger, M. Braun, E. E. Furlong, S. Loserth, C. Wenzl, F. Pilot, N. Vogt, et al. 2006. Developmental control of nuclear size and shape by Kugelkern and Kurzkern. Curr. Biol. 16: 543-552.
23. Jackowski, S. 1994. Coordination of membrane phospholipid synthesis with the cell cycle. J. Biol. Chem. 269: 3858-3867.
24. Houweling, M., Z. Cui, C. D. Anfuso, M. Bussiere, M. H. Chen, and D. E. Vance. 1996. CTP:phosphocholine cytidylyltransferase is both a nuclear and cytoplasmic protein in primary hepatocytes. Eur. J. Cell Biol. 69: 55-63.
25. Ridsdale, R., I. Tseu, J. Wang, and M. Post. 2001. CTP:phosphocholine cytidylyltransferase alpha is a cytosolic protein in pulmonary epithelial cells and tissues. J. Biol. Chem. 276: 49148-49155.
26. Fagone, P., R. Sriburi, C. Ward-Chapman, M. Frank, J. Wang, C. Gunter, J.W. Brewer, and S. Jackowski. 2007. Phospholipid biosynthesis program underlying membrane expansion during B-lymphocyte differentiation. J. Biol. Chem. 282: 7591-7605.
27. Northwood, I. C., A. H. Tong, B. Crawford, A. E. Drobnies, and R. B. Cornell. 1999. Shuttling of CTP:phosphocholine cytidylyltransferase between the nucleus and endoplasmic reticulum accompanies the wave of phosphatidylcholine synthesis during the G(0) → G(1) transition. J. Biol. Chem. 274: 26240-26248.
28. Lagace, T. A., and N. D. Ridgway. 2005. Induction of apoptosis by lipophilic activators of CTP:phosphocholine cytidylyltransferase alpha (CCTα). Biochem. J. 392: 449-456.
29. Zacharias, D. A., J. D. Violin, A. C. Newton, and R. Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296: 913-916.
30. Esko, J. D., M. M. Wermuth, and C. R. Raetz. 1981. Thermolabile CDP-choline synthetase in an animal cell mutant defective in lecithin formation. J. Biol. Chem. 256: 7388-7393.
31. Cornell, R., and D. E. Vance. 1987. Binding of CTP:phosphocholine cytidylyltransferase to large unilamellar vesicles. Biochim. Biophys. Acta. 919: 37-48.
32. Craig, L., J. E. Johnson, and R. B. Cornell. 1994. Identification of the membrane-binding domain of rat liver CTP:phosphocholine cytidylyltransferase using chymotrypsin proteolysis. J. Biol. Chem. 269: 3311-3317.
33. Johnson, J. E., M. Xie, L. M. Singh, R. Edge, and R. B. Cornell. 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.
34. Miquel, K., A. Pradines, F. Terce, S. Selmi, and G. Favre. 1998. Competitive inhibition of choline phosphotransferase by geranylgeraniol and farnesol inhibits phosphatidylcholine synthesis and induces apoptosis in human lung adenocarcinoma A549 cells. J. Biol. Chem. 273: 26179-26186.
35. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90: 1051-1060.
36. la Cour, T., L. Kiemer, A. Molgaard, R. Gupta, K. Skriver, and S. Brunak. 2004. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17: 527-536.
37. Cornell, R. B., and I. C. Northwood. 2000. Regulation of CTP:phosphocholine cytidylyltransferase by amphitropism and relocalization. Trends Biochem. Sci. 25: 441-447.
38. Ohba, T., E. C. Schirmer, T. Nishimoto, and L. Gerace. 2004. Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J. Cell Biol. 167: 1051-1062.
39. Wu, W., F. Lin, and H. J. Worman. 2002. Intracellular trafficking of MAN1, an integral protein of the nuclear envelope inner membrane. J. Cell Sci. 115: 1361-1371.
40. King, M. C., C. P. Lusk, and G. Blobel. 2006. Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature. 442: 1003-1007.
41. Hinshaw, J. E., B. O. Carragher, and R. A. Milligan. 1992. Architecture and design of the nuclear pore complex. Cell. 69: 1133-1141.
42. Tseu, I., R. Ridsdale, J. Liu, J. Wang, and M. Post. 2002. Cell cycle regulation of pulmonary phosphatidylcholine synthesis. Am. J. Respir. Cell Mol. Biol. 26: 506-515.
43. Wang, Y., and C. Kent. 1995. Identification of an inhibitory domain of CTP:phosphocholine cytidylyltransferase. J. Biol. Chem. 270: 18948-18952.
44. Taneva, S., M. K. Dennis, Z. Ding, J. L. Smith, and R. B. Cornell. 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.
45. Kitos, T. E., A. Drobnies, M. N. Ng, Y. Wen, and R. B. Cornell. 2006. Contribution of lipid mediators to the regulation of phosphatidyl-choline synthesis by angiotensin. Biochim. Biophys. Acta. 1761: 261-271.
46. Peterfy, M., J. Phan, and K. Reue. 2005. Alternatively spliced lipin isoforms exhibit distinct expression pattern, subcellular localization, and role in adipogenesis. J. Biol. Chem. 280: 32883-32889.