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Membrane Lipid Rafts and Their Role in Axon Guidance

  • Carmine Guirland
  • James Q. Zheng
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 621)

Abstract

The plasma membrane of cells contains a variety of lipid and protein molecules that are often segregated and heterogeneously distributed in microdomains. Lipid rafts represent a generalized concept of membrane microdomains that are enriched in cholesterol and sphingolipids and, characteristically, resistant to cold detergent extraction. Lipid rafts have recently received considerable attention because they are thought to be involved in many cellular functions, in particular, signal transduction for extracellular stimuli. Many of these functions are also intimately related to the processes involved in neural development, including neurotrophic factor signaling and synaptic plasticity. Recent studies from our lab and others have indicated an important role for lipid rafts in axonal growth and guidance. Specifically, our data show that lipid rafts on the plasma membrane provide platforms for spatial and temporal control of guidance signaling by extracellular cues. In addition, lipid rafts may also function in other aspects of axonal growth and guidance, including spatial and temporal regulation of adhesion, cytoskeletal dynamics, and growth cone motility. Further elucidating how membrane rafts are involved in guided axonal growth would provide important insights into the intricate signaling mechanisms underlying neuronal wiring, which is fundamental for normal brain development and functional recovery after injury and diseases.

Keywords

Lipid Raft Growth Cone Fluorescence Resonance Energy Transfer Axon Growth Axon Guidance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Singer SJ, Nicolson GL. The fluid mosaic model of the structure of cell membranes. Science 1972; 175(23):720–31.PubMedCrossRefGoogle Scholar
  2. 2.
    Edidin M. Lipids on the frontier: A century of cell-membrane bilayers. Nat Rev Mol Cell Biol 2003; 4(5):414–8.PubMedCrossRefGoogle Scholar
  3. 3.
    Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998; 67:199–225.PubMedCrossRefGoogle Scholar
  4. 4.
    Sargiacomo M, Sudol M, Tang Z et al. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 1993; 122(4):789–807.PubMedCrossRefGoogle Scholar
  5. 5.
    Harder T, Simons K. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr Opin Cell Biol 1997; 9(4):534–42.PubMedCrossRefGoogle Scholar
  6. 6.
    Munro S. Lipid rafts: Elusive or illusive? Cell 2003; 115(4):377–88.PubMedCrossRefGoogle Scholar
  7. 7.
    Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998; 14:111–36.PubMedCrossRefGoogle Scholar
  8. 8.
    Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1(1):31–9.PubMedCrossRefGoogle Scholar
  9. 9.
    Edidin M. The state of lipid rafts: From model membranes to cells. Annu Rev Biophys Biomol Struct 2003; 32:257–83, (Epub 2003 Jan 16).PubMedCrossRefGoogle Scholar
  10. 10.
    Lai EC. Lipid rafts make for slippery platforms. J Cell Biol 2003; 162(3):365–70.PubMedCrossRefGoogle Scholar
  11. 11.
    Kenworthy AK, Petranova N, Edidin M. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol Biol Cell 2000; 11(5): 1645–55.PubMedGoogle Scholar
  12. 12.
    Varma R, Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 1998; 394(6695):798–801.PubMedCrossRefGoogle Scholar
  13. 13.
    Glebov OO, Nichols BJ. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat Cell Biol 2004; 6(3):238–43, (Epub 2004 Feb 8).PubMedCrossRefGoogle Scholar
  14. 14.
    Pitto M, Palestini P, Ferraretto A et al. Dynamics of glycolipid domains in the plasma membrane of living cultured neurons, following protein kinase C activation: A study performed by excimer-formation imaging. Biochem J 1999; 34(Pt 1):177–84.CrossRefGoogle Scholar
  15. 15.
    Sekar RB, Periasamy A. Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations J Cell Biol 2003; 160(5):629–33.PubMedCrossRefGoogle Scholar
  16. 16.
    Hering H, Lin CC, Sheng M. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci 2003; 23(8):3262–71.PubMedGoogle Scholar
  17. 17.
    He Q, Meiri KF. Isolation and characterization of detergent-resistant microdomains responsive to NCAM-mediated signaling from growth cones. Mol Cell Neurosci 2002; 19(1):18–31.PubMedCrossRefGoogle Scholar
  18. 18.
    Winckler B, Mellman I. Neuronal polarity: Controlling the sorting and diffusion of membrane components. Neuron 1999; 23(4):637–40.PubMedCrossRefGoogle Scholar
  19. 19.
    Foletti DL, Prekeris R, Scheller RH. Generation and maintenance of neuronal polarity: Mechanisms of transport and targeting. Neuron 1999; 23(4):641–4.PubMedCrossRefGoogle Scholar
  20. 20.
    Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387(6633):569–72.PubMedCrossRefGoogle Scholar
  21. 21.
    Tsui-Pierchala BA, Encinas M, Milbrandt J et al. Lipid rafts in neuronal signaling and function. Trends Neurosci 2002; 25(8):412–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Paratcha G, Ibanez CF. Lipid rafts and the control of neurotrophic factor signaling in the nervous system: Variations on a theme. Curr Opin Neurobiol 2002; 12(5):542–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Huang CS, Zhou J, Feng AK et al. Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J Biol Chem 1999; 274(51):36707–14.PubMedCrossRefGoogle Scholar
  24. 24.
    Paratcha G, Ledda F, Baars L et al. Released GFRalpha1 potentiates downstream signaling, neuronal survival, and differentiation via a novel mechanism of recruitment of c-Ret to lipid rafts. Neuron 2001; 29(1):171–84.PubMedCrossRefGoogle Scholar
  25. 25.
    Suzuki S, Numakawa T, Shimazu K et al. BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: Roles in synaptic modulation. J Cell Biol 2004; 167(6):1205–15. (Epub 2004 Dec 13).PubMedCrossRefGoogle Scholar
  26. 26.
    Golub T, Wacha S, Caroni P. Spatial and temporal control of signaling through lipid rafts. Curr Opin Neurobiol 2004; 14(5):542–50.PubMedCrossRefGoogle Scholar
  27. 27.
    del Pozo MA, Alderson NB, Kiosses WB et al. Integrins regulate Rac targeting by internalization of membrane domains. Science 2004; 303(5659):839–42.PubMedCrossRefGoogle Scholar
  28. 28.
    Palazzo AF, Eng CH, Schlaepfer DD et al. Localized stabilization of microtubules by integrin-and FAK-facilitated Rho signaling. Science 2004; 303(5659):836–9.PubMedCrossRefGoogle Scholar
  29. 29.
    Nakai Y, Kamiguchi H. Migration of nerve growth cones requires detergent-resistant membranes in a spatially defined and substrate-dependent manner. J Cell Biol 2002; 159(6):1097–108.PubMedCrossRefGoogle Scholar
  30. 30.
    Tessier-Lavigne M, Goodman CS. The Molecular Biology of Axon Guidance. Science 1996; 274:1123–33.PubMedCrossRefGoogle Scholar
  31. 31.
    Dickson BJ. Molecular mechanisms of axon guidance. Science 2002; 298(5600):1959–64.PubMedCrossRefGoogle Scholar
  32. 32.
    Pasterkamp RJ, Kolodkin AL. Semaphorin junction: Making tracks toward neural connectivity. Curr Opin Neurobiol 2003; 13(1):79–89.PubMedCrossRefGoogle Scholar
  33. 33.
    Huber AB, Kolodkin AL, Ginty DD et al. Signaling at the Growth Cone: Ligand-Receptor Complexes and the Control of Axon Growth and Guidance. Annu Rev Neurosci 2003; 28:28.Google Scholar
  34. 34.
    Stein E, Tessier-Lavigne M. Hierarchical organization of guidance receptors: Silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001; 291(5510):1928–38.PubMedCrossRefGoogle Scholar
  35. 35.
    Dekker LV, Segal AW. Perspectives: Signal transduction. Signals to move cells. Science 2000; 287(5455):982–3, 85.PubMedCrossRefGoogle Scholar
  36. 36.
    Parent CA, Devreotes PN. A cell’s sense of direction. Science 1999; 284(5415):765–70.PubMedCrossRefGoogle Scholar
  37. 37.
    Laux T, Fukami K, Thelen M et al. GAP43, MARCKS, and CAP23 modulate, PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 2000; 149(7):1455–72.PubMedCrossRefGoogle Scholar
  38. 38.
    Bruckner K, Pablo Labrador J, Scheiffele P et al. EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 1999; 22(3):511–24.PubMedCrossRefGoogle Scholar
  39. 39.
    McKerracher L. Ganglioside rafts as MAG receptors that mediate blockade of axon growth. Proc Natl Acad Sci USA 2002; 99(12):7811–3.PubMedCrossRefGoogle Scholar
  40. 40.
    Yu W, Guo W, Feng L. Segregation of Nogo66 receptors into lipid rafts in rat brain and inhibition of Nogo66 signaling by cholesterol depletion. FEBS Lett 2004; 577(1–2):87–92.PubMedCrossRefGoogle Scholar
  41. 41.
    Higuchi H, Yamashita T, Yoshikawa H et al. PKA phosphorylates the p75 receptor and regulates its localization to lipid rafts. EMBO J 2003; 22(8):1790–800.PubMedCrossRefGoogle Scholar
  42. 42.
    Guirland C, Suzuki S, Kojima M et al. Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 2004; 42(1):51–62.PubMedCrossRefGoogle Scholar
  43. 43.
    Ming G, Song H, Berninger B et al. Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 1999; 23(1):139–48.PubMedCrossRefGoogle Scholar
  44. 44.
    Inoue H, Miyaji M, Kosugi A et al. Lipid rafts as the signaling scaffold for NK cell activation: Tyrosine phosphorylation and association of LAT with phosphatidylinositol 3-kinase and phospholipase C-gamma following CD2 stimulation. Eur J Immunol 2002; 32(8):2188–98.PubMedCrossRefGoogle Scholar
  45. 45.
    Castellani V, Rougon G. Control of semaphorin signaling. Curr Opin Neurobiol 2002; 12(5):532–41.PubMedCrossRefGoogle Scholar
  46. 46.
    Michaely PA, Mineo C, Ying YS et al. Polarized distribution of endogenous Rac1 and RhoA at the cell surface. J Biol Chem 1999; 274(30):21430–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Gomez-Mouton C, Abad JL, Mira E et al. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 2001; 98(17):9642–7. Epub 2001 Aug 7.PubMedCrossRefGoogle Scholar
  48. 48.
    Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003; 100(10):5813–8. Epub 2003 Apr 30.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  • Carmine Guirland
    • 1
  • James Q. Zheng
    • 1
  1. 1.Department of Neuroscience and Cell BiologyUMDNJ-R.W. Johnson Medical SchoolPiscatawayUSA

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