Intracellular trafficking of ceramide by ceramide transfer protein

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 86, Issue 4, 2010, Pages 426-437

  Hanada, Kentaro ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Ceramide; Endoplasmic reticulum; Golgi; Lipid transport; Sphingomyelin

Indexed keywords

CERAMIDE; PROTEIN SERINE THREONINE KINASE;

ANIMAL; CHEMISTRY; GENETICS; HUMAN; INTRACELLULAR SPACE; METABOLISM; MUTATION; NEOPLASM; PATHOLOGY; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CERAMIDES; HUMANS; INTRACELLULAR SPACE; MUTATION; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES;

MAMMALIA;

EID: 77955112195     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.86.426     Document Type: Review

References (66)

1. van Meer, G., Voelker, D. R. and Feigenson, G. W. (2008) Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124.
2. Lee, M. C, Miller, E. A., Goldberg, J., Orci, L. and Schekman, R. (2004) Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87-123.
3. Watson, P. and Stephens, D. J. (2005) ER-to-Golgi transport: form and formation of vesicular and tubular carriers. Biochim. Biophys. Acta 1744, 304-315.
4. Pagano, R. E., Puri, V., Dominguez, M. and Marks, D. L. (2000) Membrane traffic in sphingolipid storage diseases. Traffic 1, 807-815.
5. Mayor, S. and Pagano, R. E. (2007) Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612.
6. Ikonen, E. (2008) Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138.
7. Holthuis, J. C. and Levine, T. P. (2005) Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6, 209-220.
8. Vance, J. E. (1991) Newly made phosphatidylserine and phosphatidylethanolamine are preferentially translocated between rat liver mitochondria and endoplasmic reticulum. J. Biol. Chem. 266, 89-97.
9. Voelker, D. R. (2003) New perspectives on the regulation of intermembrane glycerophospholipid traffic. J. Lipid Res. 44, 441-449.
10. Hakomori, S. I. (2008) Structure and function of glycosphingolipids and sphingolipids: recollections and future trends. Biochim. Biophys. Acta 1780, 325-346.
11. Merrill, A. H., Jr. (2002) De novo sphingolipid biosynthesis: A necessary, but dangerous, pathway. J. Biol. Chem. 277, 25843-25846.
12. Hanada, K. (2003) Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta 1632, 16-30.
13. Yamaji, A., Sekizawa, Y., Emoto, K., Sakuraba, H., Inoue, K., Kobayashi, H. et al. (1998) Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 273, 5300-5306.
14. Hanada, K., Hara, T., Fukasawa, M., Yamaji, A., Umeda, M. and Nishijima, M. (1998) Mammalian cell mutants resistant to a sphingomyelin-directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase. J. Biol. Chem. 273, 33787-33794.
15. Fukasawa, M., Nishijima, M. and Hanada, K. (1999) Genetic evidence for ATP-dependent endoplasmic reticulum-to-Golgi apparatus trafficking of ceramide for sphingomyelin synthesis in Chinese hamster ovary cells. J. Cell Biol. 144, 673-685.
16. Funakoshi, T., Yasuda, S., Fukasawa, M., Nishijima, M. and Hanada, K. (2000) Reconstitution of ATP-and cytosol-dependent transport of de novo synthesized ceramide to the site of sphingomyelin synthesis in semi-intact cells. J. Biol. Chem. 275, 29938-29945.
17. Ohvo-Rekila, H., Ramstedt, B., Leppimaki, P. and Slotte, J. P. (2002) Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41, 66-97.
18. Fukasawa, M., Nishijima, M., Itabe, H., Takano, T. and Hanada, K. (2000) Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-β-cyclodextrin. J. Biol. Chem. 275, 34028-34034.
19. Hanada, K., Kumagai, K., Yasuda, S., Miura, Y., Kawano, M., Fukasawa, M. et al. (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803-809.
20. Raya, A., Revert, F., Navarro, S. and Saus, J. (1999) Characterization of a novel type of serine/threonine kinase that specifically phosphorylates the human goodpasture antigen. J. Biol. Chem. 274, 12642-12649.
21. Raya, A., Revert-Ros, F., Martinez-Martinez, P., Navarro, S., Rosello, E., Vieites, B. et al. (2000) Goodpasture antigen-binding protein, the kinase that phosphorylates the goodpasture antigen, is an alternatively spliced variant implicated in autoimmune pathogenesis. J. Biol. Chem. 275, 40392-40399.
22. Ponting, C. P. and Aravind, L. (1999) START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24, 130-132.
23. Lemmon, M. A. (2008) Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
24. Levine, T. P. and Munro, S. (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr. Biol. 12, 695-704.
25. Wang, Y. J., Wang, J., Sun, H. Q., Martinez, M., Sun, Y. X., Macia, E. et al. (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310.
26. Godi, A., Di Campli, A., Konstantakopoulos, A., Di Tullio, G., Alessi, D. R., Kular, G. S. et al. (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6, 393-404.
27. Christenson, L. K. and Strauss, J. F., 3rd (2000) Steroidogenic acute regulatory protein (StAR) and the intramitochondrial translocation of cholesterol. Biochim. Biophys. Acta 1529, 175-187.
28. Miller, W. L. (2007) Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim. Biophys. Acta 1771, 663-676.
29. Rone, M. B., Fan, J. and Papadopoulos, V. (2009) Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim. Biophys. Acta 1791, 646-658.
30. Soccio, R. E. and Breslow, J. L. (2003) StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J. Biol. Chem. 278, 22183-22186.
31. Alpy, F. and Tomasetto, C. (2005) Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. J. Cell Sci. 118, 2791-2801.
32. Schrick, K., Nguyen, D., Karlowski, W. M. and Mayer, K. F. (2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 5, R41.
33. Kallen, C. B., Billheimer, J. T., Summers, S. A., Stayrook, S. E., Lewis, M. and Strauss, J. F., 3rd (1998) Steroidogenic acute regulatory protein (StAR) is a sterol transfer protein. J. Biol. Chem. 273, 26285-26288.
34. Tsujishita, Y. and Hurley, J. H. (2000) Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Biol. 7, 408-414.
35. Wirtz, K. W. A. (1991) Phospholipid transfer proteins. Ann. Rev. Biochem. 60, 73-99.
36. Kanno, K., Wu, M. K., Scapa, E. F., Roderick, S. L. and Cohen, D. E. (2007) Structure and function of phosphatidylcholine transfer protein (PC-TP)/StarD2. Biochim. Biophys. Acta 1771, 654-662.
37. Olayioye, M. A., Vehring, S., Muller, P., Herrmann, A., Schiller, J., Thiele, C. et al. (2005) StarD10, a START domain protein overexpressed in breast cancer, functions as a phospholipid transfer protein. J. Biol. Chem. 280, 27436-27442.
38. Tabunoki, H., Sugiyama, H., Tanaka, Y., Fujii, H., Banno, Y., Jouni, Z. E. et al. (2002) Isolation, characterization, and cDNA sequence of a carotenoid binding protein from the silk gland of Bombyx mori larvae. J. Biol. Chem. 277, 32133-32140.
39. Kumagai, K., Yasuda, S., Okemoto, K., Nishijima, M., Kobayashi, S. and Hanada, K. (2005) CERT mediates intermembrane transfer of various molecular species of ceramides. J. Biol. Chem. 280, 6488-6495.
40. Lev, S., Ben Halevy, D., Peretti, D. and Dahan, N. (2008) The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol. 18, 282-290.
41. Loewen, C. J., Roy, A. and Levine, T. P. (2003) A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22, 2025-2035.
42. Kawano, M., Kumagai, K., Nishijima, M. and Hanada, K. (2006) Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein-interacting FFAT motif of CERT. J. Biol. Chem. 281, 30279-30288.
43. Kudo, N., Kumagai, K., Tomishige, N., Yamaji, T., Wakatsuki, S., Nishijima, M. et al. (2008) Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide. Proc. Natl. Acad. Sci. USA 105, 488-493.
44. Munro, S. (2003) Cell biology: earthworms and lipid couriers. Nature 426, 775-776.
45. Ladinsky, M. S., Mastronarde, D. N., McIntosh, J. R., Howell, K. E. and Staehelin, L. A. (1999) Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.
46. Marsh, B. J., Mastronarde, D. N., Buttle, K. F., Howell, K. E. and McIntosh, J. R. (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl. Acad. Sci. USA 98, 2399-2406.
47. Halter, D., Neumann, S., van Dijk, S. M., Wolthoorn, J., de Maziere, A. M., Vieira, O. V. et al. (2007) Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 179, 101-115.
48. D'Angelo, G., Vicinanza, M., Di Campli, A. and De Matteis, M. A. (2008) The multiple roles of PtdIns(4)P not just the precursor of PtdIns(4,5)P2. J. Cell Sci. 121, 1955-1963.
49. Toth, B., Balla, A., Ma, H., Knight, Z. A., Shokat, K. M. and Balla, T. (2006) Phosphatidylinositol 4-kinase IIIβ regulates the transport of ceramide between the endoplasmic reticulum and Golgi. J. Biol. Chem. 281, 36369-36377.
50. Lopez-Montero, I., Rodriguez, N., Cribier, S., Pohl, A., Velez, M. and Devaux, P. F. (2005) Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes. J. Biol. Chem. 280, 25811-25819.
51. Kumagai, K., Kawano, M., Shinkai-Ouchi, F., Nishijima, M. and Hanada, K. (2007) Interorganelle trafficking of ceramide is regulated by phosphorylation-dependent cooperativity between the PH and START domains of CERT. J. Biol. Chem. 282, 17758-17766.
52. Fugmann, T., Hausser, A., Schoffler, P., Schmid, S., Pfizenmaier, K. and Olayioye, M. A. (2007) Regulation of secretory transport by protein kinase D-mediated phosphorylation of the ceramide transfer protein. J. Cell Biol. 178, 15-22.
53. Tomishige, N., Kumagai, K., Kusuda, J., Nishijima, M. and Hanada, K. (2009) Casein kinase Iγ2 down-regulates trafficking of ceramide in the synthesis of sphingomyelin. Mol. Biol. Cell 20, 348-357.
54. Saito, S., Matsui, H., Kawano, M., Kumagai, K., Tomishige, N., Hanada, K. et al. (2007) Protein phosphatase 2Cε is an endoplasmic reticulum integral membrane protein that dephosphorylates the ceramide transport protein CERT to enhance its association with organelle membranes. J. Biol. Chem. 283, 6584-6593.
55. Revert, F., Ventura, I., Martinez-Martinez, P., Granero-Molto, F., Revert-Ros, F., Macias, J. et al. (2008) Goodpasture antigen-binding protein is a soluble exportable protein which interacts with type IV collagen: Identification of novel membrane-bound isoforms. J. Biol. Chem. 283, 30246-30255.
56. Rao, R. P., Yuan, C, Allegood, J. C, Rawat, S. S., Edwards, M. B., Wang, X. et al. (2007) Ceramide transfer protein function is essential for normal oxidative stress response and lifespan. Proc. Natl. Acad. Sci. USA 104, 11364-11369.
57. Wang, X., Rao, R. P., Kosakowska-Cholody, T., Masood, M. A., Southon, E., Zhang, H. et al. (2009) Mitochondrial degeneration and not apoptosis is the primary cause of embryonic lethality in ceramide transfer protein mutant mice. J. Cell Biol. 184, 143-158.
58. Granero-Molto, F., Sarmah, S., O'Rear, L., Spagnoli, A., Abrahamson, D., Saus, J. et al. (2008) Goodpasture antigen-binding protein and its spliced variant, ceramide transfer protein, have different functions in the modulation of apoptosis during zebrafish development. J. Biol. Chem. 283, 20495-20504.
59. Yasuda, S., Kitagawa, H., Ueno, M., Ishitani, H., Fukasawa, M., Nishijima, M. et al. (2001) A novel inhibitor of ceramide trafficking from the endoplasmic reticulum to the site of sphingomyelin synthesis. J. Biol. Chem. 276, 43994-44002.
60. Nakamura, Y., Matsubara, R., Kitagawa, H., Kobayashi, S., Kumagai, K., Yasuda, S. et al. (2003) Stereoselective synthesis and structure-activity relationship of novel ceramide trafficking inhibitors, (1R,3R)-N-(3-hydroxy-1-hydroxymethyl-3-phenylpropyl)dodecanamide (HPA-12) and its analogues. J. Med. Chem. 46, 3688-3695.
61. Swanton, C, Marani, M., Pardo, O., Warne, P. H., Kelly, G., Sahai, E. et al. (2007) Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 11, 498-512.
62. Stiban, J., Caputo, L. and Colombini, M. (2008) Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins. J. Lipid Res. 49, 625-634.
63. Revert, F., Merino, R., Monteagudo, C, Macias, J., Peydro, A., Alcacer, J. et al. (2007) Increased Goodpasture antigen-binding protein expression induces type IV collagen disorganization and deposit of immunoglobulin A in glomerular basement membrane. Am. J. Pathol. 171, 1419-1430.
64. Levine, T. (2004) Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol. 14, 483-490.
65. de Brito, O. M. and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610.
66. Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., Weissman, J. S. et al. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481.