Role of Glycosphingolipids in Formation and Function of Membrane Microdomains

Recent years have been characterized by a huge interest in the structure and function of mammalian cell membrane lipid domains. The interest in this subject grew further, when their participation in important membrane-associated events such as signal transmission, cell adhesion and lipid/protein sor...

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Published inTrends in Glycoscience and Glycotechnology Vol. 13; no. 71; pp. 239 - 250
Main Authors Masserini, Massimo, Ravasi, Daniela, Sonnino, Sandro
Format Journal Article
LanguageEnglish
Published FCCA(Forum: Carbohydrates Coming of Age) 2001
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Online AccessGet full text
ISSN0915-7352
1883-2113
1883-2113
DOI10.4052/tigg.13.239

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Abstract Recent years have been characterized by a huge interest in the structure and function of mammalian cell membrane lipid domains. The interest in this subject grew further, when their participation in important membrane-associated events such as signal transmission, cell adhesion and lipid/protein sorting was postulated. A common feature of cell membrane domains is their peculiar lipid composition, being enriched in glycosphingolipids, sphingomyelin and cholesterol. A series of theoretical considerations and several experimental data suggest that glycosphingolipids play an important role in the formation and function of membrane domains. Within this review, the involvement of glycosphingolipids in the biogenesis, structure and function of domains is discussed in light of their strong amphiphilic nature and of their peculiar chemical features. These features differentiate glycosphingolipids from other lipids in the membrane, allowing either self-interaction or interaction with other membrane components and external ligands. Due to these interactions, glycosphingolipids undergo lateral phase, separation, segregation, and therefore form core domains within the membrane; glycosphingolipid domains constitute the nucleation point that allows co-segregation of other lipids and proteins in a complex domain; finally, glycosphingolipids confer dynamic properties on domains, that are essential to the modulation of cell functions.
AbstractList Recent years have been characterized by a huge interest in the structure and function of mammalian cell membrane lipid domains. The interest in this subject grew further, when their participation in important membrane-associated events such as signal transmission, cell adhesion and lipid/protein sorting was postulated. A common feature of cell membrane domains is their peculiar lipid composition, being enriched in glycosphingolipids, sphingomyelin and cholesterol. A series of theoretical considerations and several experimental data suggest that glycosphingolipids play an important role in the formation and function of membrane domains. Within this review, the involvement of glycosphingolipids in the biogenesis, structure and function of domains is discussed in light of their strong amphiphilic nature and of their peculiar chemical features. These features differentiate glycosphingolipids from other lipids in the membrane, allowing either self-interaction or interaction with other membrane components and external ligands. Due to these interactions, glycosphingolipids undergo lateral phase, separation, segregation, and therefore form core domains within the membrane; glycosphingolipid domains constitute the nucleation point that allows co-segregation of other lipids and proteins in a complex domain; finally, glycosphingolipids confer dynamic properties on domains, that are essential to the modulation of cell functions.
Author Sonnino, Sandro
Masserini, Massimo
Ravasi, Daniela
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27. Pitto, M., Mutoh, T., Kuriyama, M., Ferraretto, A., Palestini, P., and Masserini, M. (1998) FEBS Lett. 439, 93-96
59. Cantù, L., Corti, M., Casellato, R., Acquotti, D., and Sonnino, S. (1991) Chem. Phys. Lipids 60, 111-118
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35. Acquotti, D., Poppe, L., Dabrowski, J., von der Lieth, G.W., Sonnino, S., and Tettamanti, G. (1990) J. Am. Chem. Soc. 112, 7772-7778
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30. Riboni, L., Viani, P., Bassi, R., Prinetti, A., Tettamanti, G. (1997) Progress in Lipid Research 36, 153-195
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41. Terzaghi, A., Tettamanti, G., and Masserini, M. (1993) Biochemistry 32, 9722-9725
15. Moss, D.J., and White, C.A. (1992) Eur. J. Cell Biol. 57, 59-65
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12. Cinek, T., and Horejsi, V. (1992) J. Immunol. 149, 2262-2270
18. Chigorno, V., Palestini, P., Sciannamblo, M. T., Dolo, V., Pavan, A., Tettamanti, G., and Sonnino, S. (2000) Eur. J. Biochem. 267, 4187-4197
61. Sonnino, S., Acquotti, D., Cantù, L., Chigorno, V., Valsecchi, M., Casellato, R., Masserini, M., Corti, M., Allevi, P., and Tettamanti, G. (1994) Chem. Phys. Lipids 69, 95-104
21. Fra, A.M., Masserini, M., Palestini, P., Sonnino, S., and Simons, K. (1995) FEBS Lett. 375, 11-14
16. Ledesma, M.D., Simons, K., and Dotti, C.G. (1998) Proc. Natl. Acad. Sci. USA 95, 3966-3971
22. Olive, S., Dubois, C., Schachner, M., and Rougon, G. (1995) J. Neurochem. 65, 2307-2317
14. Sargiacomo, M., Sudol, M., Tang, Z., and Lisanti, M.P. (1993) J. Cell Biol. 122, 789-807
42. Schroeder, E, Nemecz, G., Wood, W.G., Joiner, C., Morrot, G., Ayraut-Jarrier, M., and Devaux, PF. (1991) Biochim. Biophys. Acta 1066, 183-192
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17. Wu, C., Butz, S., Ying, Y., and Anderson, R.G. (1997) J. Biol. Chem. 272, 3554-3559
3. Anderson, R.G.W. (1993) Proc. Natl. Acad. Sci. USA 90, 10909-10913
29. Masserini, M., Giuliani, A., Palestini, P., Acquotti, D., Pitto, M., Chigorno, V., and Tettamanti, G. (1990) Biochemistry 29, 697-701
28. Goins, B., and Freire, E. (1985) Biochemistry 24, 1791-1797
58. Sonnino, S., Acquotti, D., Fronza, G., Cantù, L., Chigorno, V., Pitto, M., Kirschner, G., and Tettamanti, G. (1988) Chem. Phys. Lipids 46, 181-191
50. Palestini, P., Pitto, M., Tedeschi, G., Ferraretto, A., Parenti, M., Brunner, J., and Masserini, M. (2000) J. of Biol. Chem. 275, 9978-9986
39. Nyholm, P.G., and Pascher, I. (1993) Biochemistry 32, 1225-1234
19. Prinetti, A., Chigorno, V., Tettamanti, G., and Sonnino, S. (2000) J. Biol. Chem. 275, 11658-11665
43. Pitto, M., Brunner, J. Ferraretto, A., Ravasi, D., Palestini, P., and Masserini M. (2000) Glycoconjugate J. 17, 215-222.
1. Thompson, T.E., and Tillack, T.W. (1985) Ann. Rev. Biophys. Chem. 14, 361-386
57. Cantù, L., Corti, M., Sonnino, S., and Tettamanti, G. (1986) Chem. Phys. Lipids 41, 315-328
55. Sonnino, S., Cantiù, L., Acquotti, D., Corti, M., and Tettamanti, G. (1990) Chem. Phys. Lipids 52, 231-241
48. Palestini, P., Masserini, M., Bottiroli, G., Brunner, J., Mutoh, T., Ferraretto, A., Ravasi, D., and Pitto, M. (1999) Biosci. Reports 19, 385-395
34. Bach, D., Sela, B., and Miller, I.R. (1982) Chem. Phys. Lipids 31, 381-394
56. Cantù, L., Corti, M., Sonnino, S., and Tettamanti, G. (1990) Chem. Phys. Lipids 55, 223-229
7. Okamoto, T., Schelgel, A., Scherer, P.E., and Lisanti, M.P. (1998) J. Biol. Chem. 273, 5419-5422
31. Wiegandt, H. (1985) in “New Comprehesive Biochemistry” (Wiegandt, H., ed.) Glycosphingolipids 10, 199-260
36. Acquotti, D., Cantù, L., Ragg, E., and Sonnino, S. (1994) Eur. J. Biochem. 225, 271-288
2. Simons, K., and Van Meer, G. (1988) Biochemistry 27, 6197-6202
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9. Smart, E.J., Mineo, C., and Anderson, R.G.W. (1996) J. Cell Biol. 134, 1169-1177
40. Masserini, M., Palestini, P., and Freire, E. (1989) Biochemistry 28, 5029-5039
10. Kurzchalia, T.V., and Parton, R.G. (1996) FEBS Lett. 389, 52-54
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References_xml – reference: 46. Pitto, M., Palestini, P., Ferraretto, A., Flati, S., Pavan, A., Ravasi, D., Masserini, M., and Bottiroli, G. (1999) Biochem. J. 343, 177-184
– reference: 3. Anderson, R.G.W. (1993) Proc. Natl. Acad. Sci. USA 90, 10909-10913
– reference: 30. Riboni, L., Viani, P., Bassi, R., Prinetti, A., Tettamanti, G. (1997) Progress in Lipid Research 36, 153-195
– reference: 54. Benowitz, L.I., and Routtenberg, A. (1997) Trends Neurosci. 20, 84-91
– reference: 61. Sonnino, S., Acquotti, D., Cantù, L., Chigorno, V., Valsecchi, M., Casellato, R., Masserini, M., Corti, M., Allevi, P., and Tettamanti, G. (1994) Chem. Phys. Lipids 69, 95-104
– reference: 41. Terzaghi, A., Tettamanti, G., and Masserini, M. (1993) Biochemistry 32, 9722-9725
– reference: 53. Kasahara, K., Watanabe, K., Takeuchi, K., Kaneko, H., Oohira, A., Yamamoto, T., and Sanai, Y. (2000) J. Biol. Chem. 275, 34701-34709
– reference: 12. Cinek, T., and Horejsi, V. (1992) J. Immunol. 149, 2262-2270
– reference: 19. Prinetti, A., Chigorno, V., Tettamanti, G., and Sonnino, S. (2000) J. Biol. Chem. 275, 11658-11665
– reference: 59. Cantù, L., Corti, M., Casellato, R., Acquotti, D., and Sonnino, S. (1991) Chem. Phys. Lipids 60, 111-118
– reference: 6. Lisanti, M.P., Scherer, P.E., Tang, Z., and Sargiacomo, M. (1994) Trends Cell Biol. 4, 231-235
– reference: 56. Cantù, L., Corti, M., Sonnino, S., and Tettamanti, G. (1990) Chem. Phys. Lipids 55, 223-229
– reference: 26. Palestini, P., Pitto, M., Ferraretto, A., Tettamanti, G., and Masserini, M. (1998) Biochemistry 37, 3143-3148
– reference: 15. Moss, D.J., and White, C.A. (1992) Eur. J. Cell Biol. 57, 59-65
– reference: 52. Kasahara, K., Watanabe, Y., Yamamoto, T., and Sanai, Y. (1997) J. Biol. Chem. 272, 29947-29953
– reference: 39. Nyholm, P.G., and Pascher, I. (1993) Biochemistry 32, 1225-1234
– reference: 49. Yang, L., and Glaser, M., (1996) Biochemistry 35, 13966-13974
– reference: 29. Masserini, M., Giuliani, A., Palestini, P., Acquotti, D., Pitto, M., Chigorno, V., and Tettamanti, G. (1990) Biochemistry 29, 697-701
– reference: 42. Schroeder, E, Nemecz, G., Wood, W.G., Joiner, C., Morrot, G., Ayraut-Jarrier, M., and Devaux, PF. (1991) Biochim. Biophys. Acta 1066, 183-192
– reference: 18. Chigorno, V., Palestini, P., Sciannamblo, M. T., Dolo, V., Pavan, A., Tettamanti, G., and Sonnino, S. (2000) Eur. J. Biochem. 267, 4187-4197
– reference: 16. Ledesma, M.D., Simons, K., and Dotti, C.G. (1998) Proc. Natl. Acad. Sci. USA 95, 3966-3971
– reference: 22. Olive, S., Dubois, C., Schachner, M., and Rougon, G. (1995) J. Neurochem. 65, 2307-2317
– reference: 31. Wiegandt, H. (1985) in “New Comprehesive Biochemistry” (Wiegandt, H., ed.) Glycosphingolipids 10, 199-260
– reference: 37. Acquotti, D., Fronza, G., Ragg, E., and Sonnino, S. (1991) Chem. Phys. Lipids 59, 107-125
– reference: 27. Pitto, M., Mutoh, T., Kuriyama, M., Ferraretto, A., Palestini, P., and Masserini, M. (1998) FEBS Lett. 439, 93-96
– reference: 24. Sharom, F.J., and Grant, C.W., (1978) Biochem. Biophys. Acta 507, 280-293
– reference: 45. Mutoh, T., Tokuda, A., Miyadai, T., Hamaguchi, M., and Fujiki, N. (1995) Proc. Natl. Acad. Sci. U.S.A. 92, 5087-5091
– reference: 28. Goins, B., and Freire, E. (1985) Biochemistry 24, 1791-1797
– reference: 36. Acquotti, D., Cantù, L., Ragg, E., and Sonnino, S. (1994) Eur. J. Biochem. 225, 271-288
– reference: 25. Ferraretto, A., Pitto, M., Palestini, P., and Masserini, M. (1997) Biochemistry 36, 9232-9236
– reference: 32. Pascher, I. (1976) Biochim. Biophys. Acta 455, 433-451
– reference: 57. Cantù, L., Corti, M., Sonnino, S., and Tettamanti, G. (1986) Chem. Phys. Lipids 41, 315-328
– reference: 58. Sonnino, S., Acquotti, D., Fronza, G., Cantù, L., Chigorno, V., Pitto, M., Kirschner, G., and Tettamanti, G. (1988) Chem. Phys. Lipids 46, 181-191
– reference: 8. Schnitzer, J.E., Liu, J., and Oh, P. (1995) J. Biol. Chem. 270, 14399-14404
– reference: 23. Vey, M., Pilkuhn, S., Wille, H., Nixon, R., DeArmond, S.J., Smart, E.J., Anderson, R.G., Taraboulos, A., and Prusiner, S.B. (1996) Proc. Natl. Acad. Sci. USA 93, 14945-14949
– reference: 1. Thompson, T.E., and Tillack, T.W. (1985) Ann. Rev. Biophys. Chem. 14, 361-386
– reference: 47. Calappi, E., Masserini, M., Schiavo, G., Montecucco, C., and Tettamanti, G. (1992) FEBS Lett. 309, 107-110
– reference: 10. Kurzchalia, T.V., and Parton, R.G. (1996) FEBS Lett. 389, 52-54
– reference: 5. Oka, N., Yamamoto, M., Schwencke, C., Kawabe, J., Ebina, T., Ohno, S., Couet, J., Lisanti, M.P., and Ishikawa, Y. (1997) J. Biol. Chem. 272, 33416-33421
– reference: 40. Masserini, M., Palestini, P., and Freire, E. (1989) Biochemistry 28, 5029-5039
– reference: 7. Okamoto, T., Schelgel, A., Scherer, P.E., and Lisanti, M.P. (1998) J. Biol. Chem. 273, 5419-5422
– reference: 2. Simons, K., and Van Meer, G. (1988) Biochemistry 27, 6197-6202
– reference: 4. Masserini, M., Palestini, P., and Pitto, M. (1999) J. Neurochem. 73, 1-11
– reference: 17. Wu, C., Butz, S., Ying, Y., and Anderson, R.G. (1997) J. Biol. Chem. 272, 3554-3559
– reference: 9. Smart, E.J., Mineo, C., and Anderson, R.G.W. (1996) J. Cell Biol. 134, 1169-1177
– reference: 33. Brocca, P., Berthault, P., and Sonnino, S. (1998) Biophysical J. 74, 309-318
– reference: 48. Palestini, P., Masserini, M., Bottiroli, G., Brunner, J., Mutoh, T., Ferraretto, A., Ravasi, D., and Pitto, M. (1999) Biosci. Reports 19, 385-395
– reference: 11. Brown, D., and Rose, J.K. (1992) Cell 68, 533-544
– reference: 13. Rothberg, K.G., Heuser, J.E., Donzell, W.C., Ying, Y., Glenney, J.R., and Anderson, R.G.W. (1992) Cell 68, 673-682
– reference: 20. Parton, R.G. (1994) J. Histochem. Cytochem. 42, 155-166
– reference: 44. Cameron, P.L., Ruffin, J.W., Bollag, R., Rasmussen, H., and Cameron, R.S. (1997) J. Neurosci. 17, 9520-9535
– reference: 38. Pascher, I., and Sundel, S. (1977) Chem. Phys. Lipids 20, 175-191
– reference: 50. Palestini, P., Pitto, M., Tedeschi, G., Ferraretto, A., Parenti, M., Brunner, J., and Masserini, M. (2000) J. of Biol. Chem. 275, 9978-9986
– reference: 14. Sargiacomo, M., Sudol, M., Tang, Z., and Lisanti, M.P. (1993) J. Cell Biol. 122, 789-807
– reference: 34. Bach, D., Sela, B., and Miller, I.R. (1982) Chem. Phys. Lipids 31, 381-394
– reference: 51. Aderem, A. (1995) Biochemical Society Transactions 23, 587-591
– reference: 43. Pitto, M., Brunner, J. Ferraretto, A., Ravasi, D., Palestini, P., and Masserini M. (2000) Glycoconjugate J. 17, 215-222.
– reference: 60. Sonnino, S., Cantù, L., Corti, M., Acquotti, D., Kirschner, G., and Tettamanti, G. (1990) Chem. Phys. Lipids 56, 49-57
– reference: 21. Fra, A.M., Masserini, M., Palestini, P., Sonnino, S., and Simons, K. (1995) FEBS Lett. 375, 11-14
– reference: 35. Acquotti, D., Poppe, L., Dabrowski, J., von der Lieth, G.W., Sonnino, S., and Tettamanti, G. (1990) J. Am. Chem. Soc. 112, 7772-7778
– reference: 55. Sonnino, S., Cantiù, L., Acquotti, D., Corti, M., and Tettamanti, G. (1990) Chem. Phys. Lipids 52, 231-241
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Snippet Recent years have been characterized by a huge interest in the structure and function of mammalian cell membrane lipid domains. The interest in this subject...
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jstage
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StartPage 239
SubjectTerms caveolae
domains
glycosphingolipids
lipid rafts
Title Role of Glycosphingolipids in Formation and Function of Membrane Microdomains
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https://www.jstage.jst.go.jp/article/tigg1989/13/71/13_71_239/_pdf
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ispartofPNX Trends in Glycoscience and Glycotechnology, 2001/05/02, Vol.13(71), pp.239-250
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