Functional compartmentalization of the plasma membrane of neurons by a unique acyl chain composition of phospholipids

Journal of Biological Chemistry

Volumn 289, Issue 39, 2014, Pages 26783-26793

  Kuge, Hideaki ^a   Akahori, Kana ^a   Yagyu, Ken Ichi ^a   Honke, Koichi ^a  

^a KOCHI MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CELL MEMBRANES; MOLECULAR STRUCTURE; PHOSPHOLIPIDS;

CULTURE CELLS; DOPAMINE TRANSPORTERS; FUNCTIONAL SEGMENTS; LATERAL DISTRIBUTIONS; MOLECULAR SPECIES; NEURONAL DIFFERENTIATION; NEURONAL SYNAPSIS; PHOSPHOLIPASES;

NEURONS;

1 OLEOYL 2 PALMITOYL PHOSPHATIDYLCHOLINE; DOPAMINE TRANSPORTER; NERVE GROWTH FACTOR; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A1; UNCLASSIFIED DRUG; 1-OLEOYL-2-PALMITOYLPHOSPHATIDYLCHOLINE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; LIPID COMPOSITION; MALE; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE; NONHUMAN; PC12 CELL LINE; PRESYNAPTIC NERVE; PROTEIN DOMAIN; PROTEIN LOCALIZATION; ANIMAL; CELL DIFFERENTIATION; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; METABOLISM; NERVE CELL; PHYSIOLOGY; RAT; SYNAPSE;

ANIMALS; CELL DIFFERENTIATION; CELL MEMBRANE; GTP-BINDING PROTEIN ALPHA SUBUNITS; MICE; NERVE GROWTH FACTOR; NEURONS; PC12 CELLS; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASES A1; RATS; SYNAPSES;

EID: 84907587729     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.571075     Document Type: Article

References (40)

1. Winckler, B., and Poo, M. (1996) No diffusion barrier at axon hillock. Nature 379, 213
2. Winckler, B., Forscher, P., and Mellman, I. (1999) A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397, 698-701
3. Katsuki, T., Ailani, D., Hiramoto, M., and Hiromi, Y. (2009) Intra-axonal patterning: intrinsic compartmentalization of the axonal membrane in Drosophila neurons. Neuron 64, 188-199
4. Hermansson, M., Hokynar, K., and Somerharju, P. (2011) Mechanisms of glycerophospholipid homeostasis in mammalian cells. Prog. Lipid Res. 50, 240-257
5. Taguchi, R., and Ishikawa, M. (2010) Precise and global identification of phospholipid molecular species by an Orbitrap mass spectrometer and automated search engine Lipid Search. J. Chromatogr. A 1217, 4229-4239
6. Chaurand, P., Cornett, D. S., Angel, P. M., and Caprioli, R. M. (2011) From whole-body sections down to cellular level, multiscale imaging of phospholipids by MALDI mass spectrometry. Mol. Cell Proteomics 10.1074/mcp.O110.004259
7. Goto-Inoue, N., Hayasaka, T., Zaima, N., and Setou, M. (2011) Imaging mass spectrometry for lipidomics. Biochim. Biophys. Acta 1811, 961-969
8. Lands, W. E. (1958) Metabolism of glycerolipides: a comparison of lecithin and triglyceride synthesis. J. Biol. Chem. 231, 883-888
9. Yamashita, A., Sugiura, T., and Waku, K. (1997) Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells. J. Biochem. 122, 1-16
10. Shindou, H., Hishikawa, D., Harayama, T., Yuki, K., and Shimizu, T. (2009) Recent progress on acyl CoA: lysophospholipid acyltransferase research. J. Lipid Res. 50, S46-S51
11. Mizuguchi, H., and Kay, M. A. (1999) A simple method for constructing E1 and E1/E4 deleted recombinant adenovirus vector. Hum. Gene Ther. 10, 2013-2017
12. Brown, D. A., and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
13. Shepherd, P., and Dean, C. (2000) Monoclonal Antibodies, pp. 1-23 Oxford University Press, Oxford, UK
14. Pfenninger, K. H., Ellis, L., Johnson, M. P., Friedman, L. B., and Somlo, S. (1983) Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35, 573-584
15. Strittmatter, S. M., Valenzuela, D., Kennedy, T. E., Neer, E. J., and Fishman, M. C. (1990) G0 is a major growth cone protein subject to regulation by GAP-43. Nature 344, 836-841
16. Cvacka, J., and Svatos, A. (2003) Matrix-assisted laser desorption/ionization analysis of lipids and high molecular weight hydrocarbons with lithium 2,5-dihydroxybenzoate matrix. Rapid Commun. Mass Spectrom. 17, 2203-2207
17. Al-Saad, K. A., Siems, W. F., Hill, H. H., Zabrouskov, V., and Knowles, N. R. (2003) Structural analysis of phosphatidylcholines by post-source decay matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Am. Soc. Mass Spectrom. 14, 373-382
18. Tamaki, H., and Yamashina, S. (1994) Improved method for post-embedding cytochemistry using reduced osmium and LR white resin. J. Histochem. Cytochem. 42, 1285-1293
19. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
20. Zhao, Z., and Xu, Y. (2010) An extremely simple method for extraction of lysophospholipids and phospholipids from blood samples. J. Lipid Res. 51, 652-659
21. Hsu, F. F., Bohrer, A., and Turk, J. (1998) Formation of lithiated adducts of glycerophosphocholine lipids facilitates their identification by electrospray ionization tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 9, 516-526
22. Santiago-Tirado, F. H., and Bretscher, A. (2011) Membrane-trafficking sorting hubs: cooperation between PI4P and small GTPases at the trans-Golgi network. Trends Cell Biol. 21, 515-525
23. Darrow, A. L., Olson, M. W., Xin, H., Burke, S. L., Smith, C., Schalk-Hihi, C., Williams, R., Bayoumy, S. S., Deckman, I. C., Todd, M. J., Damiano, B. P., and Connelly, M. A. (2011) A novel fluorogenic substrate for the measurement of endothelial lipase activity. J. Lipid Res. 52, 374-382
24. Rahman, M. S., Ammerman, N. C., Sears, K. T., Ceraul, S. M., and Azad, A. F. (2010) Functional characterization of a phospholipase A2 homolog from Rickettsia typhi. J. Bacteriol. 192, 3294-3303
25. Sutherland, C. A., and Amin, D. (1982) Relative activities of rat and dog platelet phospholipase A2 and diglyceride lipase. J. Biol. Chem. 257, 14006-14010
26. Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E.-J., Gangadharan, U., Hobbs, C., Di Marzo, V., and Doherty, P. (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163, 463-468
27. Nirenberg, M. J., Chan, J., Pohorille, A., Vaughan, R. A., Uhl, G. R., Kuhar, M. J., and Pickel, V. M. (1997) The dopamine transporter: comparative ultrastructure of dopaminergic axons in limbic and motor compartments of the nucleus accumbens. J. Neurosci. 17, 6899-6907
28. Kadota, T., Yamaai, T., Saito, Y., Akita, Y., Kawashima, S., Moroi, K., Inagaki, N., and Kadota, K. (1996) Expression of dopamine transporter at the tips of growing neurites of PC12 cells. J. Histochem. Cytochem. 44, 989-996
29. Mumby, S. M., Heukeroth, R. O., Gordon, J. I., and Gilman, A. G. (1990) G-protein α-subunit expression, myristoylation, and membrane association in COS cells. Proc. Natl. Acad. Sci. U.S.A. 87, 728-732
30. Parenti, M., Vigano, M. A., Newman, C. M. H., Milligant, G., and Magee, A. (1993) A novel N-terminal motif for palmitoylation of G-protein α subunits. Biochem. J. 353, 349-353
31. Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Hirabayashi, T., and Yamamoto, K. (2011) Recent progress in phospholipase A2 research: from cells to animals to humans. Prog. Lipid Res. 50, 152-192
32. Richmond, G. S., and Smith, T. K. (2011) Phospholipases A1. Int. J. Mol. Sci. 12, 588-612
33. Kanamori, T., Inoue, T., Sakamoto, T., Gengyo-Ando, K., Tsujimoto, M., Mitani, S., Sawa, H., Aoki, J., and Arai, H. (2008) β-Catenin asymmetry is regulated by PLA1 and retrograde traffic in C. elegans stem cell divisions. EMBO J. 27, 1647-1657
34. Imae, R., Inoue, T., Kimura, M., Kanamori, T., Tomioka, N. H., Kage-Nakadai, E., Mitani, S., and Arai, H. (2010) Intracellular phospholipase A 1 and acyltransferase, which are involved in Caenorhabditis elegans stem cell divisions, determine the sn-1 fatty acyl chain of phosphatidylinositol. Mol. Biol. Cell 21, 3114-3124
35. Contreras, F.-X., Ernst, A. M., Haberkant, P., Björkholm, P., Lindahl, E., Gönen, B., Tischer, C., Elofsson, A., von Heijne, G., Thiele, C., Pepperkok, R., Wieland, F., and Brügger, B. (2012) Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 481, 525-529
36. Fujita, M., Watanabe, R., Jaensch, N., Romanova-Michaelides, M., Satoh, T., Kato, M., Riezman, H., Yamaguchi, Y., Maeda, Y., and Kinoshita, T. (2011) Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. J. Cell Biol. 194, 61-75
37. Spira F., Mueller N. S., Beck G., von Olshausen P., Beig J., and Wedlich-Söldner R. (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14, 640-648
38. Baas, A. F., Kuipers, J., van der Wel, N. N., Batlle, E., Koerten, H. K., Peters, P. J., and Clevers, H. C. (2004) Complete polarization of single intestinal epithelial cells upon activation of LKB1 by STRAD. Cell 116, 457-466
39. Ikenouchi, J., Suzuki, M., Umeda, K., Ikeda, K., Taguchi, R., Kobayashi, T., Sato, S. B., Kobayashi, T., Stolz, D. B., and Umeda, M. (2012) Lipid polarity is maintained in the absence of tight junctions. J. Biol. Chem. 287, 9525-9533
40. Ha, K. D., Clarke, B. A., and Brown, W. J. (2012) Regulation of the Golgi complex by phospholipid remodeling enzymes. Biochim. Biophys. Acta 1821, 1078-1088