Advertisement

Glycoconjugate Journal

, Volume 17, Issue 3–4, pp 191–197 | Cite as

Signaling through sphingolipid microdomains of the plasma membrane: The concept of signaling platform

  • Daniel C. Hoessli
  • Subburaj Ilangumaran
  • Alex Soltermann
  • Peter J. Robinson
  • Bettina Borisch
  • Nasir- Ud-Din
Article

Abstract

Transmembrane signaling requires modular interactions between signaling proteins, phosphorylation or dephosphorylation of the interacting protein partners [1] and temporary elaboration of supramolecular structures [2], to convey the molecular information from the cell surface to the nucleus. Such signaling complexes at the plasma membrane are instrumental in translating the extracellular cues into intracellular signals for gene activation. In the most straightforward case, ligand binding promotes homodimerization of the transmembrane receptor which facilitates modular interactions between the receptor's cytoplasmic domains and intracellular signaling and adaptor proteins [3]. For example, most growth factor receptors contain a cytoplasmic protein tyrosine kinase (PTK) domain and ligand-mediated receptor dimerization leads to cross phosphorylation of tyrosines in the receptor's cytoplasmic domains, an event that initiates the signaling cascade [4]. In other signaling pathways where the receptors have no intrinsic kinase activity, intracellular non-receptor PTKs (i.e. Src family PTKs, JAKs) are recruited to the cytoplasmic domain of the engaged receptor. Execution of these initial phosphorylations and their translation into efficient cellular stimulation requires concomitant activation of diverse signaling pathways. Availability of stable, preassembled matrices at the plasma membrane would facilitate scaffolding of a large array of receptors, coreceptors, tyrosine kinases and other signaling and adapter proteins, as it is the case in signaling via the T cell antigen receptor [5]. The concept of the signaling platform [6] has gained usage to characterize the membrane structure where many different membrane-bound components need to be assembled in a coordinated manner to carry out signaling.

The structural basis of the signaling platform lies in preferential assembly of certain classes of lipids into distinct physical and functional compartments within the plasma membrane [7,8]. These membrane microdomains or rafts (Figure 1) serve as privileged sites where receptors and proximal signaling molecules optimally interact [9]. In this review, we shall discuss first how signaling platforms are assembled and how receptors and their signaling machinery could be functionally linked in such structures. The second part of our review will deal with selected examples of raft-based signaling pathways in T lymphocytes and NK cells to illustrate the ways in which rafts may facilitate signaling.

rafts transmembrane signaling sphingolipids protein tyrosine kinase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Pawson T, Nature 373, 573–80 (1995).Google Scholar
  2. 2.
    Bray D, Annu Rev Biophys Biomol Struct 27, 59–75 (1998).Google Scholar
  3. 3.
    Pawson T, Scott JD, Science 278, 2075–80 (1998).Google Scholar
  4. 4.
    Weiss A, Schlessinger J, Cell 94, 277–80 (1998).Google Scholar
  5. 5.
    Ilangumaran S, He H-T, Hoessli DC, Immunol Today 21, 2–7 (2000).Google Scholar
  6. 6.
    Arni S, Ilangumaran S, van Echten-Deckert G, Sandhoff K, Poincelet M, Briol A, Rungger-Brandle E, Hoessli DC, Biochem Biophys Res Commun 225, 801–7 (1996).Google Scholar
  7. 7.
    Brown DA, London E, J Membrane Biol 164, 103–14 (1998).Google Scholar
  8. 8.
    Brown RE, J Cell Science 111, 1–9 (1998).Google Scholar
  9. 9.
    Simons K, Ikonen E, Nature 387, 569–72 (1997).Google Scholar
  10. 10.
    Singer SJ, Nicolson GL, Science 175, 720–31 (1972).Google Scholar
  11. 11.
    Jacobson KE, Sheets D, Simson R, Science 268, 1441–2 (1995).Google Scholar
  12. 12.
    Simson R, Yang B, Moore SE, Doherty P, Walsh FS, Jacobson KA, Biophys J 74, 297–308 (1998).Google Scholar
  13. 13.
    Jacobson K, Dietrich C, Trends Cell Biol 9, 87–91 (1999).Google Scholar
  14. 14.
    Hoessli DC, Rungger-Brandle E, Exp Cell Res 156, 239–50 (1985).Google Scholar
  15. 15.
    Cinek T, Horejsi V, J Immunol 149, 2262–70 (1992).Google Scholar
  16. 16.
    Brown DA, Trends Cell Biol 2, 338–43 (1992).Google Scholar
  17. 17.
    Varma R, Mayor S, Nature 394, 798–801 (1998).Google Scholar
  18. 18.
    Friedrichson T, Kurzchalia TV, Nature 394, 802–5 (1998).Google Scholar
  19. 19.
    Schroeder R, London E, Brown DA, Proc Natl Acad Sci USA 91, 12130–4 (1994).Google Scholar
  20. 20.
    Sheets ED, Lee GM, Simson R, Jacobson K, Biochemistry 36, 12449–58 (1997).Google Scholar
  21. 21.
    Schütz GJ, Kada G, Pastushenko VP, Schindler H, EMBO J 19, 892–901 (2000).Google Scholar
  22. 22.
    Korlach J, Schwille P, Webb WW, Feigenson GW, Proc Natl Acad Sci 96, 8461–6 (1999).Google Scholar
  23. 23.
    Schroeder RJ, Ahmed SN, Zhu Y, London E, Brown DA, J Biol Chem 273, 1150–7 (1998).Google Scholar
  24. 24.
    Ilangumaran S, Briol A, Hoessli D, Biochim Biophys Acta 1328, 227–236 (1997).Google Scholar
  25. 25.
    Ostermeyer AG, Beckrich BT, Ivarson KA, Grove KE, Brown DA, J Biol Chem 274, 34459–66 (1999).Google Scholar
  26. 26.
    Brown DA, London E, Annu Rev Cell Dev Biol 14, 111–36 (1998).Google Scholar
  27. 27.
    Hakomori S-I, Handa K, Iwabuchi K, Yamamura S, Prinetti A, Glycobiology 8, xi–xix (1998).Google Scholar
  28. 28.
    Ilangumaran S, Hoessli DC, Biochem J 335, 433–40 (1998).Google Scholar
  29. 29.
    Keller P, Simons K, J Cell Biol 140, 1357–67 (1998).Google Scholar
  30. 30.
    Okamoto T, Schlegel A, Scherer PE, Lisanti MP, J Biol Chem 273, 5419–22 (1998).Google Scholar
  31. 31.
    Anderson RGW, Ann Rev Biochem 67, 199–225 (1998).Google Scholar
  32. 32.
    Robinson PJ, Immunol Today 12, 35–41 (1991).Google Scholar
  33. 33.
    Horejsi V, Draber P, Stockinger H, In GPI-anchored membrane proteins and carbohydrates, edited by Hoessli DC and Ilangumaran S, (R.G Landes Company Austin, TX, 1999), p. 71–91.Google Scholar
  34. 34.
    Ip NY, Nye SH, Boulton TG, Davis S, Taga T, Li Y, Birren SJ, Yasukawa K, Kishimoto T, Anderson DJ, Cell 69, 1121–32 (1992).Google Scholar
  35. 35.
    Klein RD, Sherman D, Ho W-H, Stone D, Bennett GL, Moffat B, Vandlen R, Simmons L, Gu Q, Hongo J-A, Devaux B, Poulsen K, Armandini M, Nozak C, Asai N, Goddard A, Phillips H, Henderson CE, Takahashi M, Rosenthal A, Nature 387, 717–21 (1997).Google Scholar
  36. 36.
    Treanor JJS, Goodman L, Desauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, Phillips HS, Goddard A, Moore MW, Buj-Bello A, Davies AM, Asai N, Takahashi M, Vandlen R, Henderson CE, Rosenthal A, Nature 382, 80–3 (1996).Google Scholar
  37. 37.
    Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, Stockinger H, Science 254, 1016–8 (1991).Google Scholar
  38. 38.
    Brown DA, Curr Opin Immunol 5, 349–54 (1993).Google Scholar
  39. 39.
    Casey PJ, Science 268, 221–5 (1995).Google Scholar
  40. 40.
    Shenoy-Scaria AM, Gauen LKT, Kwong J, Shaw AS, Lublin DM, Mol Cell Biol 13, 6385–92 (1993).Google Scholar
  41. 41.
    Rodgers W, Crise B, Rose JK, Mol Cell Biol 14, 5384–91 (1994).Google Scholar
  42. 42.
    Harder T, Scheiffele P, Verkade P, Simons K, J Cell Biology 141, 929–42 (1998).Google Scholar
  43. 43.
    Harder T, Simons K, Eur J Immunol 29, 556–62 (1999).Google Scholar
  44. 44.
    Harder T, Simons K, Current Op Cell Biol 9, 534–42 (1997).Google Scholar
  45. 45.
    Stulnig TM, Berger M, Sigmund T, Raederstorff D, Stockinger H, Waldhausl W, J Cell Biol 143, 637–44 (1998).Google Scholar
  46. 46.
    Webb Y, Hermida-Matsumoto L, Resh MD, J Biol Chem 275, 261–70 (2000).Google Scholar
  47. 47.
    Weiss A, Cell 73, 209–12 (1993).Google Scholar
  48. 48.
    Gunter KC, Germain RN, Kroczek RA, Saito T, Yokoyama WM, Chan C, Weiss A, Shevach EM, Nature 326, 505–7 (1987).Google Scholar
  49. 49.
    Sussman JJ, Saito T, Shevach EM, Germain RN, Ashwell JD, J Immunol 140, 2520–6 (1988).Google Scholar
  50. 50.
    Tosello A-C, Mary F, Amiot M, Bernard A, Mary D, J Inflammation 48, 13–27 (1998).Google Scholar
  51. 51.
    Yeh ETH, Reiser H, Bamezai A, Rock KL, Cell 52, 665–74 (1988).Google Scholar
  52. 52.
    Romagnoli P, Bron C, J Immunol 158, 5757–64 (1997).Google Scholar
  53. 53.
    Marmor MD, Bachmann MF, Ohashi PS, Malek TR, Julius M, Int Immunol 11, 1381–93 (1999).Google Scholar
  54. 54.
    Moran M, Miceli MC, Immunity 9, 787–96 (1998).Google Scholar
  55. 55.
    Kabouridis PS, Magee AI, Ley SC, EMBO J 16, 4983–98 (1997).Google Scholar
  56. 56.
    Montixi C, Langlet C, Bernard AM, Thimonier J, Dubois C, Wurbel M-A, Chauvin J-P, Pierres M, He H-T, EMBO J 17, 5334–48 (1998).Google Scholar
  57. 57.
    van't Hof W, Resh MD, J Cell Biol 145, 377–89 (1999).Google Scholar
  58. 58.
    Xavier R, Brennan T, Li Q, McCormack C, Seed B, Immunity 8, 723–32 (1998).Google Scholar
  59. 59.
    Zhang W, Trible RP, Samelson LE, Immunity 8, 239–46 (1998).Google Scholar
  60. 60.
    Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A, Nature 395, 82–6 (1998).Google Scholar
  61. 61.
    Shaw AS, Dustin ML, Immunity 6, 361–9 (1997).Google Scholar
  62. 62.
    Sperling AI, Sedy JR, Manjunath N, Kupfer A, Ardman B, Burkhardt JK, J Immunol 161, 6459–62 (1998).Google Scholar
  63. 63.
    Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A, Science 283, 680–2 (1999).Google Scholar
  64. 64.
    Holdorf AD, Green JM, Levin SD, Denny MF, Strous DB, Link V, Changelian PS, Allen PM, Shaw AS, J Exp Med 190, 375–84 (1999).Google Scholar
  65. 65.
    Lou Z, Jevremovic D, Billadeau DD, Leibson PJ, J Exp Med 191, 347–54 (2000).Google Scholar
  66. 66.
    Ilangumaran S, Arni S, van Echten-Deckert G, Borisch B, Hoessli DC, Mol Biol Cell 10, 891–905 (1999).Google Scholar
  67. 67.
    Newton A, Ann Rev Biophys Biomol Struct 22, 1–25 (1993).Google Scholar
  68. 68.
    Cooper JA, Howell BW, Cell 73, 1051–54 (1993).Google Scholar
  69. 69.
    Moarefi I, Lafevre-Bernt M, Sicheri F, Huse M, Lee CH, Kuriyan J, Miller WT, Nature 385, 650–3 (1997).Google Scholar
  70. 70.
    Holowka D, Baird B, Ann Rev Biophys Biomol Struct 25, 79–112 (1996).Google Scholar
  71. 71.
    Ardouin L, Boyer C, Gillet A, Trucy J, Bernard AM, Nunes J, Delon J, Trautmann A, He HT, Malissen B, Malissen M, Immunity 10, 409–20 (1999).Google Scholar
  72. 72.
    Ilangumaran S, Briol A, Hoessli DC, Blood 91, 3901–8 (1998).Google Scholar
  73. 73.
    Oliferenko S, Paiha KTH, Gerke V, Schwärzler C, Schwarz H, Beug H, Günthert U, Huber LA, J Cell Biol 146, 843–54 (1999).Google Scholar
  74. 74.
    Cheong KH, Zachetti D, Schneeberger EE, Simons K, PNAS 96, 6241–8 (1999).Google Scholar
  75. 75.
    Puertollano R, Alonso MA, Mol Biol Cell 10, 3435–47 (1999).Google Scholar
  76. 76.
    Millan J, Alonso MA, Eur J Immunol 28, 3675–84 (1998).Google Scholar
  77. 77.
    Deans JP, Robbins SM, Polyak MJ, Savage JA, J Biol Chem 273, 344–8 (1998).Google Scholar
  78. 78.
    Clausse B, Fizazi K, Walczak V, Tetaud C, Wiels J, Tursz T, Busson P, Virology 228, 285–93 (1997).Google Scholar
  79. 79.
    Puertollano R, Menendez M, Alonso MA, Biochem Biophys Res Commun 266, 330–3 (1999).Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Daniel C. Hoessli
    • 1
  • Subburaj Ilangumaran
    • 2
  • Alex Soltermann
    • 1
  • Peter J. Robinson
    • 3
  • Bettina Borisch
    • 1
  • Nasir- Ud-Din
    • 4
  1. 1.Department of PathologyUniversity of GenevaGeneva 4Switzerland
  2. 2.Department of Experimental TherapeuticsOntario Cancer InstituteTorontoCanada
  3. 3.Department of BiosciencesUniversity of KentCanterbury, KentUnited Kingdom
  4. 4.Institute of Biomedical SciencesLahorePakistan

Personalised recommendations