Skip to main content
SpringerLink
Log in

The Sialoadhesins — A family of sialic acid-dependent cellular recognition molecules within the immunoglobulin superfamily

  • Mini-Review
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

For many years evidence has accumulated that sialic acids function in cellular interactions either by masking or as a recognition site. However, receptors or adhesion molecules mediating such functions between eukaryotic cells were unknown until about 5 years ago, when it was found that the members of the Selectin family mediate adhesion of leukocytes to specific endothelia through binding to sialylated glycans like sialyl Lewisx. More recently, the Sialoadhesin family of sialic acid-dependent adhesion molecules was defined within the superfamily of immunoglobulin-like molecules. So far, it has been shown that sialoadhesin (Sn), CD22, CD33, the myelin-associated glycoprotein (MAG) and the Schwann cell myelin protein (SMP) belong to this family. In contrast to the Selectins, these proteins are associated with diverse biological processes, i.e. hemopoiesis, neuronal development and immunity. In this review their properties, carbohydrate specificities and potential biological functions are discussed. Finally, we provide perspectives with respect to the nature of ligands, implications of sialic acid modifications and future research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

IgSF:

immunoglobulin superfamily

MAG:

myelin-associated glycoprotein

Sia:

sialic acid

SMP:

Schwann cell myelin protein

Sn:

sialoadhesin

References

  1. Schauer R (1982)Adv Carbohydr Chem Biochem 40: 131–234.

    PubMed  Google Scholar 

  2. Varki A (1992)Glycobiology 2: 25–40.

    PubMed  Google Scholar 

  3. Schauer R, Kamerling JP (1996) InGlycoproteins, 29B (Montreuil J, Schachter H, Vliegenthart JFG, eds) Amsterdam: Elsevier (Science): in press.

    Google Scholar 

  4. Paulson JC, Weinstein J, Schauer R (1989)J Biol Chem 264: 10931–34.

    PubMed  Google Scholar 

  5. Van den Eijnden DH, Joziasse DH (1993)Curr Opin Struct Biol 3: 711–21.

    Google Scholar 

  6. Varki A (1993)Glycobiology 3: 97–130.

    PubMed  Google Scholar 

  7. Lasky LA (1995)Annu Rev Biochem 64: 113–39.

    PubMed  Google Scholar 

  8. Kelm S, Pelz A, Schauer R, Filbin MT, Tang S, de Bellard M-E, Schnaar RL, Mahoney JA, Hartnell A, Bradfield P, Crocker PR (1994)Curr Biol 4: 965–72.

    PubMed  Google Scholar 

  9. Crocker PR, Mucklow S, Bouckson V, McWilliam AS, Willis AC, Gordon S, Milon G, Kelm S, Bradfield P (1994)EMBO J 13: 4490–503.

    PubMed  Google Scholar 

  10. Stamenkovic I, Seed B (1990)Nature 345: 74–77.

    PubMed  Google Scholar 

  11. Stamenkovic I, Sgroi D, Aruffo A, Sy MS, Anderson T (1991)Cell 66: 1133–44.

    PubMed  Google Scholar 

  12. Stamenkovic I, Sgroi D, Aruffo A (1992)Cell 68: 1003–4.

    Google Scholar 

  13. Simmons DL, Seed B (1988)J Immunol 141: 2797–800.

    PubMed  Google Scholar 

  14. Freeman SD, Kelm S, Barber EK, Crocker PR (1995)Blood 85: 2005–12.

    PubMed  Google Scholar 

  15. Fujita N, Sato S, Kurihara T, Kuwano R, Sakimura K, Inusuka T, Takahashi Y, Miyatake T (1989)Biochem Biophys Res Commun 165: 1162–69.

    PubMed  Google Scholar 

  16. Dulac C, Tropak MB, Cameron Curry P, Rossier J, Marshak DR, Roder J, Le Douarin NM (1992)Neuron 8: 323–34.

    PubMed  Google Scholar 

  17. Crocker PR, Kelm S, Dubois C, Martin B, McWilliam AS, Shotton DM, Paulson JC, Gordon S (1991)EMBO J 10: 1661–69.

    PubMed  Google Scholar 

  18. Crocker PR, Gordon S (1986)J Exp Med 164: 1862–75.

    PubMed  Google Scholar 

  19. Van den Berg TK, Breve JJP, Damoiseaux JGMC, Dopp EA, Kelm S, Crocker PR, Dijkstra CD, Kraal G (1992)J Exp Med 176: 647–55.

    PubMed  Google Scholar 

  20. Riedl M, Förster O, Rumpold H, Bernheimer H (1982)J Immunol 128: 1205–10.

    PubMed  Google Scholar 

  21. Boltz-Nitulescu G, Ortel B, Riedl M, Förster O (1984)Immunology 51: 177–84.

    PubMed  Google Scholar 

  22. Förster O, Boltz-Nitulescu G, Holzinger C, Wiltschke C, Riedl M, Ortel B, Fellinger A, Bernheimer H (1986)Mol Immunol 23: 1267–73.

    PubMed  Google Scholar 

  23. Crocker PR, Gordon S (1989)J Exp Med 169: 1333–46.

    PubMed  Google Scholar 

  24. Crocker PR, Morris L, Gordon S (1988)J Cell Sci Suppl 9: 185–206.

    Google Scholar 

  25. Crocker PR, Kelm S, Morris L, Bainton DF, Gordon S (1992) InMononuclear Phagocytes, (Furth Rv, ed) pp. 55–69. Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  26. Crocker PR, Werb Z, Gordon S, Bainton DF (1990)Blood 76: 1131–38.

    PubMed  Google Scholar 

  27. Crocker PR, Freeman S, Gordon S, Kelm S (1995)J Clin Invest 95: 635–43.

    PubMed  Google Scholar 

  28. Wilson GL, Fox CH, Fauci AS, Kehrl JH (1991)J Exp Med 173: 137–46.

    PubMed  Google Scholar 

  29. Engel P, Wagner N, Miller AS, Tedder TF (1995)J Exp Med 181: 1581–86.

    PubMed  Google Scholar 

  30. Bast BJEG, Zhou LJ, Freeman GJ, Colley KJ, Ernst TJ, Munro JM, Tedder TF (1992)J Cell Biol 116: 423–35.

    PubMed  Google Scholar 

  31. Munro S, Bast BJEG, Colley KJ, Tedder TF (1992)Cell 68: 1003–4.

    Google Scholar 

  32. Sgroi D, Varki A, Braesch Andersen S, Stamenkovic I (1993)J Biol Chem 268: 7011–18.

    PubMed  Google Scholar 

  33. Powell LD, Sgroi D, Sjoberg ER, Stamenkovic I, Varki A (1993)J Biol Chem 268: 7019–27.

    PubMed  Google Scholar 

  34. Powell LD, Varki A (1994)J Biol Chem 269: 10628–36.

    PubMed  Google Scholar 

  35. Powell LD, Jain RK, Matta KL, Sabesan S, Varki A (1995)J Biol Chem 270: 7523–32.

    PubMed  Google Scholar 

  36. Torres RM, Law CL, Santos Argumedo L, Kirkham PA, Grabstein K, Parkhouse RM, Clark EA (1992)J Immunol 149: 2641–49.

    PubMed  Google Scholar 

  37. Engel P, Nojima Y, Rothstein D, Zhou LJ, Wilson GL, Kehrl JH, Tedder TF (1993)J Immunol 150: 4719–32.

    PubMed  Google Scholar 

  38. Hanasaki K, Varki A, Stamenkovic I, Bevilacqua MP (1994)J Biol Chem 269: 10637–43.

    PubMed  Google Scholar 

  39. Hanasaki K, Varki A, Powell LD (1995)J Biol Chem 270: 7533–42.

    PubMed  Google Scholar 

  40. Leprince C, Draves KE, Geahlen RL, Ledbetter JA, Clark EA (1993)Proc Natl Acad Sci USA 90: 3236–40.

    PubMed  Google Scholar 

  41. Peaker CJ, Neuberger MS (1993)Eur J Immunol 23: 1358–63.

    PubMed  Google Scholar 

  42. Schulte RJ, Campbell MA, Fischer WH, Sefton BM (1992)Science 258: 1001–4.

    PubMed  Google Scholar 

  43. Doody GM, Justement LB, Delibrias CC, Mathews RJ, Lin J, Thomas ML, Fearon DT (1995)Science 269: 242–44.

    PubMed  Google Scholar 

  44. Chaouchi N, Vazquez A, Galanaud P, Leprince C (1995)J Immunol 154: 3096–104.

    PubMed  Google Scholar 

  45. Aruffo A, Kanner SB, Sgroi D, Ledbetter JA, Stamenkovic I (1992)Proc Natl Acad Sci USA 89: 10242–46.

    PubMed  Google Scholar 

  46. Bernard G, Zoccola D, Ticchioni M, Breittmayer JP, Aussel C, Bernard A (1994)J Immunol 152: 5161–70.

    PubMed  Google Scholar 

  47. Peaker CJ (1994)Curr Opin Immunol 6: 359–63.

    PubMed  Google Scholar 

  48. Sgroi D, Koretzky GA, Stamenkovic I (1995)Proc Natl Acad Sci USA 92: 4026–30.

    PubMed  Google Scholar 

  49. Wang XC, Vertino A, Eddy RL, Byers MG, Janisait SN, Shows TB, Lau JTY (1993)J Biol Chem 268: 4355–61.

    PubMed  Google Scholar 

  50. Braesch-Andersen S, Stamenkovic I (1994)J Biol Chem 269: 11783–86.

    PubMed  Google Scholar 

  51. Hanasaki K, Powell LD, Varki A (1995)J Biol Chem 270: 7543–50.

    PubMed  Google Scholar 

  52. Pierelli L, Teofili L, Menichella G, Rumi C, Paoloni A, Iovino S, Puggioni PL, Leone G, Bizzi B (1993)Br J Haematol 84: 24–30.

    PubMed  Google Scholar 

  53. Kristensen JS, Hokland P (1991)Leuk Res 15: 693–700.

    PubMed  Google Scholar 

  54. Del Poeta G, Stasi R, Venditti A, Suppo G, Aronica G, Bruno A, Masi M, Tabilio A, Papa G (1994)Leukemia 8: 388–94.

    PubMed  Google Scholar 

  55. Knapp W, Strobl H, Majdic O (1994)Cytometry 18: 187–98.

    PubMed  Google Scholar 

  56. Scheinberg DA, Lovett D, Divgi CR, Graham MC, Berman E, Pentlow K, Feirt N, Finn RD, Clarkson BD, Gee TS, et al. (1991)J Clin Oncol 9: 478–90.

    PubMed  Google Scholar 

  57. Stiff PJ, Schulz WC, Bishop M, Marks L (1991)Blood 77: 355–62.

    PubMed  Google Scholar 

  58. La Russa VF, Griffin JD, Kessler SW, Cutting MA, Knight RD, Blattler WA, Lambert JM, Wright DG (1992)Exp Hematol 20: 442–48.

    PubMed  Google Scholar 

  59. Robertson MJ, Soiffer RJ, Freedman AS, Rabinowe SL, Anderson KC, Ervin TJ, Murray C, Dear K, Griffin JD, Nadler LM, et al. (1992)Blood 79: 2229–36.

    PubMed  Google Scholar 

  60. Tchilian EZ, Beverley PC, Young BD, Watt SM (1994)Blood 83: 3188–98.

    PubMed  Google Scholar 

  61. Trapp BD (1990)Ann N Y Acad Sci 605: 29–43.

    PubMed  Google Scholar 

  62. Nakano R, Fujita N, Sato S, Inuzuka T, Sakimura K, Ishiguro H, Mishina M, Miyatake T (1991)Biochem Biophys Res Commun 178: 282–90.

    PubMed  Google Scholar 

  63. Inuzuka T, Fujita N, Sato S, Baba H, Nakano R, Ishiguro H, Miyatake T (1991)Brain Res 562: 173–75.

    PubMed  Google Scholar 

  64. Ishiguro H, Sato S, Fujita N, Inuzuka T, Nakano R, Miyatake T (1991)Brain Res 563: 288–92.

    PubMed  Google Scholar 

  65. Sadoul R, Fahrig T, Bartsch U, Schachner M (1990)J Neurosci Res 25: 1–13.

    PubMed  Google Scholar 

  66. Probstmeier R, Fahrig T, Spiess E, Schachner M (1992)J Cell Biol 116: 1063–70.

    PubMed  Google Scholar 

  67. Low K, Orberger G, Schmitz B, Martini R, Schachner M (1994)Eur J Neurosci 6: 1773–81.

    PubMed  Google Scholar 

  68. Owens GC, Bunge RP (1989)Glia 2: 119–28.

    PubMed  Google Scholar 

  69. Owens GC, Bunge RP (1991)Neuron 7: 565–75.

    PubMed  Google Scholar 

  70. Li C, Tropak MB, Gerlai R, Clapoff S, Abramow Newerly W, Trapp B, Peterson A, Roder J (1994)Nature 369: 747–50.

    PubMed  Google Scholar 

  71. Montag D, Giese KP, Bartsch U, Martini R, Lang Y, bluthmann H, Karthigasan J, Kirschner DA, Wintergerst ES, Nave KA, et al. (1994)Neuron 13: 229–46.

    PubMed  Google Scholar 

  72. Bartsch U, Montag D, Bartsch S, Schachner M (1995)Glia 14: 115–22.

    PubMed  Google Scholar 

  73. Fruttiger M, Montag D, Schachner M, Martini R (1995)Eur J Neurosci 7: 511–55.

    PubMed  Google Scholar 

  74. Johnson PW, Abramow-Newerly W, Seilheimer B, Sadoul R, Tropak MB, Arquint M, Dunn RJ, Schachner M, Roder JC (1989)Neuron 3: 377–85.

    PubMed  Google Scholar 

  75. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT (1994)Neuron 13: 757–67.

    PubMed  Google Scholar 

  76. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994)Neuron 13: 805–11.

    PubMed  Google Scholar 

  77. Afar DE, Salzer JL, Roder J, Braun PE, Bell JC (1990)J Neurochem 55: 1418–26.

    PubMed  Google Scholar 

  78. Agrawal HC, Noronha AB, Agrawal D, Quarles RH (1990)Biochem Biophys Res Commun 169: 953–98.

    PubMed  Google Scholar 

  79. Bambrick LL, Braun PE (1991)Dev Neurosci 13: 412–16.

    PubMed  Google Scholar 

  80. Kirchhoff F, Hofer HW, Schachner M (1993)J Neurosci Res 36: 368–81.

    PubMed  Google Scholar 

  81. Jaramillo ML, Afar DEH, Almazan G, Bell JC (1994)J Biol Chem 269: 27240–45.

    PubMed  Google Scholar 

  82. Umemori H, Sato S, Yagi T, Aizawa S, Yamamoto T (1994)Nature 367: 572–76.

    PubMed  Google Scholar 

  83. Williams AF, Barclay AN (1988)Annu Rev Immunol 6: 381–405.

    PubMed  Google Scholar 

  84. Reid KB, Day AJ (1989)Immunol Today 10: 177–80.

    PubMed  Google Scholar 

  85. Williams AF, Davis SJ, He Q, Barclay AN (1989)Cold Spring Harbor Symp Quant Biol 54: 637–47.

    PubMed  Google Scholar 

  86. Barclay AN, Beyers AD, Birkeland ML, Brown MH, Davis SJ, Somoza C, Williams AF (1993) InThe Leukocyte Antigen Factsbook, (Barclay AN, Beyers AD, Birkeland ML, Brown MH, Davis SJ, Somoza C, Williams AF, eds) London: Academic Press.

    Google Scholar 

  87. Jones EY, Davis SJ, Williams AF, Harlos K, Stuart DI (1992)Nature 360: 232–39.

    PubMed  Google Scholar 

  88. Jones EY, Harlos K, Bottomley MJ, Robinson RC, Driscoll PC, Edwards RM, Clements JM, Dudgeon TJ, Stuart DI (1995)Nature 373: 539–44.

    PubMed  Google Scholar 

  89. van der Merwe PA, Mcnamee PN, Davies EA, Barclay AN, Davis SJ (1995)Curr Biol 5: 74–84.

    PubMed  Google Scholar 

  90. Powell LD, Varki A (1995)J Biol Chem 270: 14243–46.

    PubMed  Google Scholar 

  91. Nath D, van der Merwe PA, Kelm S, Bradfield P, Crocker PR (1995)J Biol Chem 270: 26184–91.

    PubMed  Google Scholar 

  92. Kelm S, Schauer R, Manuguerra JC, Gross HJ, Crocker PR (1994)Glycoconjugate J 11: 576–85.

    Google Scholar 

  93. Law CL, Torres RM, Sundberg HA, Parkhouse RM, Brannan CI, Copeland NG, Jenkins NA, Clark EA (1993)J Immunol 151: 175–87.

    PubMed  Google Scholar 

  94. Wilson GL, Najfeld V, Kozlow E, Menniger J, Ward D, Kehrl JH (1993)J Immunol 150: 5013–24.

    PubMed  Google Scholar 

  95. Mucklow S, Hartnell A, Mattei M-G, Gordon S, Crocker PR (1995)Genomics 28: 344–46.

    PubMed  Google Scholar 

  96. Drickamer K (1988)J Biol Chem 263: 9557–60.

    PubMed  Google Scholar 

  97. Norgard KE, Moore KL, Diaz S, Stults NL, Ushiyama S, McEver RP, Cummings RD, Varki A (1993)J Biol Chem 268: 12764–74.

    PubMed  Google Scholar 

  98. Norgard KE, Han H, Powell L, Kriegler M, Varki A, Varki NM (1993)Proc Natl Acad Sci USA 90: 1068–72.

    PubMed  Google Scholar 

  99. Brandley BK, Kiso M, Abbas S, Nikrad P, Srivasatava O, Foxall C, Oda Y, Hasegawa A (1993)Glycobiology 3: 633–41.

    PubMed  Google Scholar 

  100. Green PJ, Tamatani T, Watanabe T, Miyasaka M, Hasegawa A, Kiso M, Yuen CT, Stoll MS, Feizi T (1992)Biochem Biophys Res Commun 188: 244–51.

    PubMed  Google Scholar 

  101. Yuen CT, Lawson AM, Chai WG, Larkin M, Stoll MS, Stuart AC, Sullivan FX, Ahern TJ, Feizi T (1992)Biochemistry 31: 9126–31.

    PubMed  Google Scholar 

  102. Yuen CT, Bezouska K, Obrien J, Stoll M, Lemoine R, Lubineau A, Kiso M, Hasegawa A, Bockovich NJ, Nicolaou KC, Feizi T (1994)J Biol Chem 269: 1595–98.

    PubMed  Google Scholar 

  103. Abdullah KM, Udoh EA, Shewen PE, Mellors A (1992)Infect Immun 60: 56–62.

    PubMed  Google Scholar 

  104. Paulson JC (1985) InThe Receptors, (Conn M, ed) pp 131–219. New York: Academic Press.

    Google Scholar 

  105. Zhou Q, Moore KL, Smith DF, Varki A, McEver RP, Cummings RD (1991)J Cell Biol 115: 557–64.

    PubMed  Google Scholar 

  106. Moore KL, Patel KD, Bruehl RE, Li FG, Johnson DA, Lichenstein HS, Cummings RD, Bainton DF, McEver RP (1995)J Cell Biol 128: 661–71.

    PubMed  Google Scholar 

  107. Sjoberg ER, Powell LD, Klein A, Varki A (1994)J Cell Biol 126: 549–62.

    PubMed  Google Scholar 

  108. Kelm S, Paulson JC, Rose U, Brossmer R, Schmid W, Bandgar BP, Schreiner E, Hartmann M, Zbiral E (1992)Eur J Biochem 205: 147–53.

    PubMed  Google Scholar 

  109. Schauer R (1987)Methods Enzymol 138: 611–26.

    PubMed  Google Scholar 

  110. Butor C, Diaz S, Varki A (1993)J Biol Chem 268: 10197–206.

    PubMed  Google Scholar 

  111. Shaw L, Schauer R (1988)Biol Chem Hoppe-Seyler 369: 477–86.

    PubMed  Google Scholar 

  112. Lepers A, Shaw L, Schneckenburger P, Cacan R, Verbert A, Schauer R (1990)Eur J Biochem 193: 715–23.

    PubMed  Google Scholar 

  113. Kawano T, Kozutsumi Y, Takematsu H, Kawasaki T, Suzuki A (1993)Glycoconjugate J 10: 109–15.

    Google Scholar 

  114. Schauer R, Kelm S, Reuter G, Roggentin P, Shaw L (1995) InBiology of the Sialic Acids, (Rosenberg A, ed.) pp. 7–67. New York: Plenum Publ. Corp.

    Google Scholar 

Note added in proof while this manuscript was in process, the following reports were published

  1. Debellard ME, Tang S, Makhopadhyay G, Shen YJ, Filbin MT (1996)Mol Cell Neurosci 7: 89–101.

    PubMed  Google Scholar 

  2. Yang LJS, Zeller CB, Shaper NL, Kiso M, Hasegawa A, Shapiro RE, Schnaar RL (1996)Proc Natl Acad Sci USA 93: 814–18.

    PubMed  Google Scholar 

  3. Vinson M, van der Merke PA, Kelm S, May A, Jones EY, Crocker PR (1996)J Biol Chem 271: 9267–72.

    PubMed  Google Scholar 

  4. van der Merwe PA, Crocker PR, Vinson M, Barclay AN, Schauer R, Kelm S (1996)J Biol Chem 271: 9273–80.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biochemisches Institut, University of Kiel, Olshausenstraße 40, 24098, Kiel, Germany

    Sørge Kelm & Roland Schauer

  2. ICRF, Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital, Headington, OX3 9DU, Oxford, UK

    Paul R. Crocker

Authors
  1. Sørge Kelm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roland Schauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul R. Crocker
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kelm, S., Schauer, R. & Crocker, P.R. The Sialoadhesins — A family of sialic acid-dependent cellular recognition molecules within the immunoglobulin superfamily. Glycoconjugate J 13, 913–926 (1996). https://doi.org/10.1007/BF01053186

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01053186

Keywords

Search

Navigation