Skip to main content
SpringerLink
Log in

Molecular diversity and evolution of the Siglec family of cell-surface lectins

  • Review
  • Published:
Molecular Diversity Aims and scope Submit manuscript

Summary

Sialic acids are a family of acidic sugars with a 9-carbon backbone, prominently expressed in animals of deuterostome lineage. Siglecs are the largest family of vertebrate endogenous receptors that recognize glycoconjugates containing sialic acids. Although a few Siglecs are well-conserved throughout vertebrate evolution and show similar binding preference regardless of the species of origin, most others, particularly the CD33-related subfamily of Siglecs, show marked inter-species differences in repertoire, sequence, and binding preference. The diversification of CD33-related Siglecs may be driven by direct competition against pathogens, and/or by necessity to catch up with the changing landscape of endogenous glycans, which may in turn be changing to escape exploitation by other pathogens.

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

Neu5Ac:

N-acetylneuraminic acid

Neu5Gc:

N-glycolylneuraminic acid

KDN:

2-keto-3-deoxy-d-glycero-d-galacto-nononic acid

Sia:

sialic acid, type not specified

CMP-Neu5Ac:

cytidine 5′-monophospho-Neu5Ac

Gal:

d-galactose

GalNAc:

N-acetyl-d-galactosamine

GlcNAc:

N-acetyl-d-glucosamine

HexNAc:

N-acetyl-d-hexosamine, i.e., GlcNAc or GalNAc

Fuc:

l-fucose

ITIM:

immunoreceptor tyrosine-based inhibitory motif

Sn:

sialoadhesin

MAG:

myelin-associated glycoprotein

SMP:

Schwann cell myelin protein

CD33rSiglec:

CD33/Siglec-3–related Siglec

EST:

expressed sequence tag

References

  1. Varki, A., Biological roles of oligosaccharides: All of the theories are correct, Glycobiology, 3 (1993) 97–130.

    CAS  Google Scholar 

  2. Gagneux, P. and Varki, A., Evolutionary considerations in relating oligosaccharide diversity to biological function, Glycobiology, 9 (1999) 747–755.

    Article  CAS  Google Scholar 

  3. Freeze, H.H., Update and perspectives on congenital disorders of glycosylation, Glycobiology, 11 (2001) 129R–143R.

    Article  CAS  Google Scholar 

  4. Jaeken, J. and Carchon, H., Congenital disorders of glycosylation: A booming chapter of pediatrics, Curr. Opin. Pediatr., 16 (2004) 434–439.

    Article  Google Scholar 

  5. Aebi, M. and Hennet, T., Congenital disorders of glycosylation: Genetic model systems lead the way, Trends Cell Biol., 11 (2001) 136–141.

    Article  CAS  Google Scholar 

  6. Angata, T. and Varki, A., Chemical diversity in the sialic acids and related alpha-keto acids: An evolutionary perspective, Chem. Rev., 102 (2002) 439–470.

    Article  CAS  Google Scholar 

  7. Kelm, S. and Schauer, R., Sialic acids in molecular and cellular interactions, Int. Rev. Cytol., 175 (1997) 137–240.

    Article  CAS  Google Scholar 

  8. Suzuki, Y., Sialobiology of influenza: Molecular mechanism of host range variation of influenza viruses, Biol. Pharm. Bull., 28 (2005) 399–408.

    Article  CAS  Google Scholar 

  9. Holmgren, J., Lonnroth, I., Mansson, J. and Svennerholm, L., Interaction of cholera toxin and membrane GM1 ganglioside of small intestine, Proc. Natl. Acad. Sci. U. S. A., 72 (1975) 2520–2524.

    Article  CAS  Google Scholar 

  10. Mahdavi, J., Sonden, B., Hurtig, M., Olfat, F.O., Forsberg, L., Roche, N., Angstrom, J., Larsson, T., Teneberg, S., Karlsson, K.A., Altraja, S., Wadstrom, T., Kersulyte, D., Berg, D.E., Dubois, A., Petersson, C., Magnusson, K.E., Norberg, T., Lindh, F., Lundskog, B.B., Arnqvist, A., Hammarstrom, L. and Boren, T., Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation, Science, 297 (2002) 573–578.

    Article  CAS  Google Scholar 

  11. Orlandi, P.A., Klotz, F.W. and Haynes, J.D., A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha 2-3)Gal- sequences of glycophorin A, J. Cell Biol., 116 (1992) 901–909.

    Article  CAS  Google Scholar 

  12. Kawano, T., Koyama, S., Takematsu, H., Kozutsumi, Y., Kawasaki, H., Kawashima, S., Kawasaki, T. and Suzuki, A., Molecular cloning of cytidine monophospho-N-acetylneuraminic acid hydroxylase. Regulation of species- and tissue-specific expression of N-glycolylneuraminic acid, J. Biol. Chem., 270 (1995) 16458–16463.

    Article  CAS  Google Scholar 

  13. Kawano, T., Kozutsumi, Y., Kawasaki, T. and Suzuki, A., Biosynthesis of N-glycolylneuraminic acid-containing glycoconjugates. Purification and characterization of the key enzyme of the cytidine monophospho-N-acetylneuraminic acid hydroxylation system, J. Biol. Chem., 269 (1994) 9024–9029.

    CAS  Google Scholar 

  14. Schwarzkopf, M., Knobeloch, K.P., Rohde, E., Hinderlich, S., Wiechens, N., Lucka, L., Horak, I., Reutter, W. and Horstkorte, R., Sialylation is essential for early development in mice, Proc. Natl. Acad. Sci. U. S. A., 99 (2002) 5267–5270.

    Article  CAS  Google Scholar 

  15. Eisenberg, I., Avidan, N., Potikha, T., Hochner, H., Chen, M., Olender, T., Barash, M., Shemesh, M., Sadeh, M., Grabov-Nardini, G., Shmilevich, I., Friedmann, A., Karpati, G., Bradley, W.G., Baumbach, L., Lancet, D., Asher, E.B., Beckmann, J.S., Argov, Z. and Mitrani-Rosenbaum, S., The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy, Nat. Genet., 29 (2001) 83–87.

    Article  CAS  Google Scholar 

  16. Martinez-Duncker, I., Dupre, T., Piller, V., Piller, F., Candelier, J.J., Trichet, C., Tchernia, G., Oriol, R. and Mollicone, R., Genetic complementation reveals a novel human congenital disorder of glycosylation of type II, due to inactivation of the Golgi CMP-sialic acid transporter, Blood, 105 (2005) 2671–2676.

    Article  CAS  Google Scholar 

  17. Crocker, P.R. and Varki, A., Siglecs, sialic acids and innate immunity, Trends Immunol., 22 (2001) 337–342.

    Article  CAS  Google Scholar 

  18. Crocker, P.R., Siglecs in innate immunity, Curr. Opin. Pharmacol., 5 (2005) 431–437.

    Article  CAS  Google Scholar 

  19. Varki, A. and Angata, T., iglecs - the major subfamily of I-type lectin, Glycobiology, 16 (2006) 1R–27R.

    Article  CAS  Google Scholar 

  20. Crocker, P.R., Clark, E.A., Filbin, M., Gordon, S., Jones, Y., Kehrl, J.H., Kelm, S., Le Douarin, N., Powell, L., Roder, J., Schnaar, R.L., Sgroi, D.C., Stamenkovic, K., Schauer, R., Schachner, M., Van den Berg, T.K., Van der Merwe, P.A., Watt, S.M. and Varki, A., Siglecs: A family of sialic-acid binding lectins [letter], Glycobiology, 8 (1998)v.

  21. Angata, T., Hingorani, R., Varki, N.M. and Varki, A., Cloning and characterization of a novel mouse Siglec, mSiglec-F: Differential evolution of the mouse and human (CD33) Siglec-3-related gene clusters, J. Biol. Chem., 276 (2001) 45128–45136.

    Article  CAS  Google Scholar 

  22. Angata, T., Margulies, E.H., Green, E.D. and Varki, A., Large-scale sequencing of the CD33-related Siglec gene cluster in five mammalian species reveals rapid evolution by multiple mechanisms, Proc. Natl. Acad. Sci. U. S. A., 101 (2004) 13251–13256.

    Article  CAS  Google Scholar 

  23. Crocker, P.R. and Varki, A., Siglecs in the immune system, Immunology, 103 (2001) 137–145.

  24. Patel, N., Brinkman-Van der Linden, E.C.M., Altmann, S.W., Gish, K., Balasubramanian, S., Timans, J.C., Peterson, D., Bell, M.P., Bazan, J.F., Varki, A. and Kastelein, R.A., OB-BP1/Siglec-6 - A leptin- and sialic acid-binding protein of the immunoglobulin superfamily, J. Biol. Chem., 274 (1999) 22729–22738.

    Article  CAS  Google Scholar 

  25. May, A.P., Robinson, R.C., Vinson, M., Crocker, P.R. and Jones, E.Y., Crystal structure of the N-terminal domain of sialoadhesin in complex with 3′ sialyllactose at 1.85 A resolution, Mol. Cell., 1 (1998) 719–728.

    Article  CAS  Google Scholar 

  26. Alphey, M.S., Attrill, H., Crocker, P.R. and Van Aalten, D.M., High resolution crystal structures of siglec-7. Insights into ligand specificity in the Siglec family, J. Biol. Chem., 278 (2003) 3372–3377.

    Article  CAS  Google Scholar 

  27. Pedraza, L., Owens, G.C., Green, L.A. and Salzer, J.L., The myelin-associated glycoproteins: Membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation, J. Cell Biol., 111 (1990) 2651–2661.

    Article  CAS  Google Scholar 

  28. Crocker, P.R., Mucklow, S., Bouckson, V., McWilliam, A., Willis, A.C., Gordon, S., Milon, G., Kelm, S. and Bradfield, P., Sialoadhesin, a macrophage sialic acid binding receptor for haemopoietic cells with 17 immunoglobulin-like domains, EMBO J., 13 (1994) 4490–4503.

    CAS  Google Scholar 

  29. Connolly, N.P., Jones, M. and Watt, S.M., Human Siglec-5: Tissue distribution, novel isoforms and domain specificities for sialic acid-dependent ligand interactions, Br. J. Haematol., 119 (2002) 221–238.

    Article  CAS  Google Scholar 

  30. Domeniconi, M., Cao, Z.U., Spencer, T., Sivasankaran, R., Wang, K.C., Nikulina, E., Kimura, N., Cai, H., Deng, K.W., Gao, Y., He, Z.G. and Filbin, M.T., Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth, Neuron, 35 (2002) 283–290.

    Article  CAS  Google Scholar 

  31. Liu, B.P., Fournier, A., GrandPré, T. and Strittmatter, S.M., Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor, Science, 297 (2002) 1190–1193.

    Article  CAS  Google Scholar 

  32. Zhang, M. and Varki, A., Cell surface sialic acids do not affect primary CD22 interactions with CD45 and sIgM, nor the rate of constitutive CD22 endocytosis, Glycobiology, 14 (2004) 939–949.

    Article  CAS  Google Scholar 

  33. Kumamoto, Y., Higashi, N., Denda-Nagai, K., Tsuiji, M., Sato, K., Crocker, P.R. and Irimura, T., Identification of sialoadhesin as a dominant lymph node counter-receptor for mouse macrophage galactose-type C-type lectin 1, J. Biol. Chem., 279 (2004) 49274–49280.

    Article  CAS  Google Scholar 

  34. Martínez-Pomares, L., Crocker, P.R., Da Silva, R., Holmes, N., Colominas, C., Rudd, P., Dwek, R. and Gordon, S., Cell-specific glycoforms of sialoadhesin and CD45 are counter-receptors for the cysteine-rich domain of the mannose receptor, J. Biol. Chem., 274 (1999) 30325–30318.

    Article  Google Scholar 

  35. Brinkman-Van der Linden, E.C.M., Sjoberg, E.R., Juneja, L.R., Crocker, P.R., Varki, N. and Varki, A., Loss of N-glycolylneuraminic acid in human evolution – Implications for sialic acid recognition by siglecs, J. Biol. Chem., 275 (2000) 8633–8640.

    Article  CAS  Google Scholar 

  36. Blixt, O., Collins, B.E., Van Den Nieuwenhof, I.M., Crocker, P.R. and Paulson, J.C., Sialoside specificity of the Siglec family assessed using novel multivalent probes: Identification of potent inhibitors of myelin associated glycoprotein, J. Biol. Chem., 278 (2003) 31007–31019.

    Article  CAS  Google Scholar 

  37. Van der Merwe, P.A., Crocker, P.R., Vinson, M., Barclay, A.N., Schauer, R. and Kelm, S., Localization of the putative sialic acid-binding site on the immunoglobulin superfamily cell-surface molecule CD22, J. Biol. Chem., 271 (1996) 9273–9280.

    Article  CAS  Google Scholar 

  38. Kelm, S., Brossmer, R., Isecke, R., Gross, H.J., Strenge, K. and Schauer, R., Functional groups of sialic acids involved in binding to siglecs (sialoadhesins) deduced from interactions with synthetic analogues, Eur. J. Biochem., 255 (1998) 663–672.

    Article  CAS  Google Scholar 

  39. Collins, B.E., Ito, H., Sawada, N., Ishida, H., Kiso, M. and Schnaar, R.L., Enhanced binding of the neural siglecs, myelin-associated glycoprotein and Schwann cell myelin protein, to Chol-1 (alpha-series) gangliosides and novel sulfated Chol-1 analogs, J. Biol. Chem., 274 (1999) 27899–27893.

    Google Scholar 

  40. Collins, B.E., Kiso, M., Hasegawa, A., Tropak, M.B., Roder, J.C., Crocker, P.R. and Schnaar, R.L., Binding specificities of the sialoadhesin family of I-type lectins – Sialic acid linkage and substructure requirements for binding of myelin-associated glycoprotein, Schwann cell myelin protein, and sialoadhesin, J. Biol. Chem., 272 (1997) 16889–16895.

    Article  CAS  Google Scholar 

  41. Collins, B.E., Yang, L.J.S., Mukhopadhyay, G., Filbin, M.T., Kiso, M., Hasegawa, A. and Schnaar, R.L., Sialic acid specificity of myelin-associated glycoprotein binding, J. Biol. Chem., 272 (1997) 1248-1255.

    Google Scholar 

  42. Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M.E., Alvarez, R., Bryan, M.C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D.J., Skehel, J.J., van Die, I., Burton, D.R., Wilson, I.A., Cummings, R., Bovin, N., Wong, C.H. and Paulson, J.C., Printed covalent glycan array for ligand profiling of diverse glycan binding proteins, Proc. Natl. Acad. Sci. U. S. A., 101 (2004) 17033–17038.

    Article  CAS  Google Scholar 

  43. Bochner, B.S., Alvarez, R.A., Mehta, P., Bovin, N.V., Blixt, O., White, J.R. and Schnaar, R.L., Glycan array screening reveals a candidate ligand for siglec-8, J. Biol. Chem., 280 (2005) 4307–4312.

    Article  CAS  Google Scholar 

  44. Tateno, H., Crocker, P.R. and Paulson, J.C., Mouse Siglec-F and human Siglec-8 are functionally convergent paralogs that are selectively expressed on eosinophils and recognize 6′-sulfo-sialyl Lewis X as a preferred glycan ligand, Glycobiology, 15 (2005) 1125–1135.

  45. Ito, A., Handa, K., Withers, D.A., Satoh, M. and Hakomori, S., Binding specificity of siglec7 to disialogangliosides of renal cell carcinoma: Possible role of disialogangliosides in tumor progression, FEBS Lett., 498 (2001) 116–120.

    Article  CAS  Google Scholar 

  46. Miyazaki, K., Ohmori, K., Izawa, M., Koike, T., Kumamoto, K., Furukawa, K., Ando, T., Kiso, M., Yamaji, T., Hashimoto, Y., Suzuki, A., Yoshida, A., Takeuchi, M. and Kannagi, R., Loss of disialyl Lewis(a), the ligand for lymphocyte inhibitory receptor sialic acid-binding immunoglobulin-like lectin-7 (Siglec-7) associated with increased sialyl Lewis(a) expression on human colon cancers, Cancer Res., 64 (2004) 4498–4505.

    Article  CAS  Google Scholar 

  47. Ravetch, J.V. and Lanier, L.L., Immune inhibitory receptors, Science, 290 (2000) 84–89.

    Article  CAS  Google Scholar 

  48. Doody, G.M., Justement, L.B., Delibrias, C.C., Matthews, R.J., Lin, J., Thomas, M.L. and Fearon, D.T., A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP, Science, 269 (1995) 242–244.

    Article  CAS  Google Scholar 

  49. Blasioli, J., Paust, S. and Thomas, M.L., Definition of the sites of interaction between the protein tyrosine phosphatase SHP-1 and CD22, J. Biol. Chem., 274 (1999) 2303–2307.

    Article  CAS  Google Scholar 

  50. Ulyanova, T., Blasioli, J., Woodford-Thomas, T.A. and Thomas, M.L., The sialoadhesin CD33 is a myeloid-specific inhibitory receptor, Eur. J. Immunol., 29 (1999) 3440–3449.

    Article  CAS  Google Scholar 

  51. Paul, S.P., Taylor, L.S., Stansbury, E.K. and McVicar, D.W., Myeloid specific human CD33 is an inhibitory receptor with differential ITIM function in recruiting the phosphatases SHP-1 and SHP-2, Blood, 96 (2000) 483–490.

    CAS  Google Scholar 

  52. Falco, M., Biassoni, R., Bottino, C., Vitale, M., Sivori, S., Augugliaro, R., Moretta, L. and Moretta, A., Identification and molecular cloning of p75/AIRM1, a novel member of the sialoadhesin family that functions as an inhibitory receptor in human natural killer cells, J. Exp. Med., 190 (1999) 793–801.

    Article  CAS  Google Scholar 

  53. Whitney, G., Wang, S.L., Chang, H., Cheng, K.Y., Lu, P., Zhou, X.D., Yang, W.P., McKinnon, M. and Longphre, M., A new siglec family member, siglec-10, is expressed in cells of the immune system and has signaling properties similar to CD33, Eur. J. Biochem., 268 (2001) 6083–6096.

    Article  CAS  Google Scholar 

  54. Ulyanova, T., Shah, D.D. and Thomas, M.L., Molecular cloning of MIS, a myeloid inhibitory siglec, that binds protein-tyrosine phosphatases SHP-1 and SHP-2, J. Biol. Chem., 276 (2001) 14451–14458.

    CAS  Google Scholar 

  55. Ikehara, Y., Ikehara, S.K. and Paulson, J.C., Negative regulation of T cell receptor signaling by Siglec-7 (p70/AIRM) and Siglec-9, J. Biol. Chem., 279 (2004) 43117–43125.

    Article  CAS  Google Scholar 

  56. Kitzig, F., Martinez-Barriocanal, A., López-Botet, M. and Sayós, J., Cloning of two new splice variants of Siglec-10 and mapping of the interaction between Siglec-10 and SHP-1, Biochem. Biophys. Res. Commun., 296 (2002) 355–362.

    Article  CAS  Google Scholar 

  57. Bonifacino, J.S. and Traub, L.M., Signals for sorting of transmembrane proteins to endosomes and lysosomes, Annu. Rev. Biochem., 72 (2003) 395–447.

    Article  CAS  Google Scholar 

  58. John, B., Herrin, B.R., Raman, C., Wang, Y.N., Bobbitt, K.R., Brody, B.A. and Justement, L.B., The B cell coreceptor CD22 associates with AP50, a clathrin-coated pit adapter protein, via tyrosine-dependent interaction, J. Immunol., 170 (2003) 3534–3543.

    CAS  Google Scholar 

  59. Lanier, L.L. and Bakker, A.B., The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function, Immunol. Today, 21 (2000) 611–614.

    Article  CAS  Google Scholar 

  60. Blasius, A.L., Cella, M., Takai, T. and Colonna, M., Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12, Blood, 107 (2006) 2474–2476.

  61. Jin, L., McLean, P.A., Neel, B.G. and Wortis, H.H., Sialic acid binding domains of CD22 are required for negative regulation of B cell receptor signaling, J. Exp. Med., 195 (2002) 1199–1205.

    Article  CAS  Google Scholar 

  62. Kelm, S., Gerlach, J., Brossmer, R., Danzer, C.P. and Nitschke, L., The ligand-binding domain of CD22 is needed for inhibition of the B cell receptor signal, as demonstrated by a novel human CD22-specific inhibitor compound, J. Exp. Med., 195 (2002) 1207–1213.

    Article  CAS  Google Scholar 

  63. Taylor, V.C., Buckley, C.D., Douglas, M., Cody, A.J., Simmons, D.L. and Freeman, S.D., The myeloid-specific sialic acid-binding receptor, CD33, associates with the protein-tyrosine phosphatases, SHP-1 and SHP-2, J. Biol. Chem., 274 (1999) 11505–11512.

    Article  CAS  Google Scholar 

  64. Avril, T., Floyd, H., Lopez, F., Vivier, E. and Crocker, P.R., The membrane-proximal immunoreceptor tyrosine-based inhibitory motif is critical for the inhibitory signaling mediated by Siglecs-7 and -9, CD33-related Siglecs expressed on human monocytes and NK cells, J. Immunol., 173 (2004) 6841–6849.

    CAS  Google Scholar 

  65. Avril, T., Freeman, S.D., Attrill, H., Clarke, R.G. and Crocker, P.R., Siglec-5 (CD170) can mediate inhibitory signalling in the absence of immunoreceptor tyrosine-based inhibitory motif phosphorylation, J. Biol. Chem., 280 (2005) 19843–19851.

    Article  CAS  Google Scholar 

  66. Grobe, K. and Powell, L.D., Role of protein kinase C in the phosphorylation of CD33 (Siglec-3) and its effect on lectin activity, Blood, 99 (2002) 3188–3196.

    Article  CAS  Google Scholar 

  67. Powell, L.D., Jain, R.K., Matta, K.L., Sabesan, S. and Varki, A., Characterization of sialyloligosaccharide binding by recombinant soluble and native cell-associated CD22. Evidence for a minimal structural recognition motif and the potential importance of multisite binding, J. Biol. Chem., 270 (1995) 7523–7532.

    Article  CAS  Google Scholar 

  68. Han, S., Collins, B.E., Bengston, P. and Paulson, J.C., Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking, Nat. Chem. Biol., 1 (2005) 93–97.

    Article  CAS  Google Scholar 

  69. Sgroi, D., Nocks, A. and Stamenkovic, I., A single N-linked glycosylation site is implicated in the regulation of ligand recognition by the I-type lectins CD22 and CD33, J. Biol. Chem., 271 (1996) 18803–18809.

    Article  CAS  Google Scholar 

  70. Tropak, M.B. and Roder, J.C., Regulation of myelin-associated glycoprotein binding by sialylated cis-ligands, J. Neurochem., 68 (1997) 1753–1763.

    Article  CAS  Google Scholar 

  71. Freeman, S., Birrell, H.C., D’Alessio, K., Erickson-Miller, C., Kikly, K. and Camilleri, P., A comparative study of the asparagine-linked oligosaccharides on siglec-5, siglec-7 and siglec-8, expressed in a CHO cell line, and their contribution to ligand recognition, Eur. J. Biochem., 268 (2001) 1228–1237.

    Article  CAS  Google Scholar 

  72. Bartsch, U., Bandtlow, C.E., Schnell, L., Bartsch, S., Spillmann, A.A., Rubin, B.P., Hillenbrand, R., Montag, D., Schwab, M.E. and Schachner, M., Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS, Neuron, 15 (1995) 1375–1381.

    Article  CAS  Google Scholar 

  73. Schachner, M. and Bartsch, U., Multiple functions of the myelin-associated glycoprotein MAG (siglec-4a) in formation and maintenance of myelin, Glia, 29 (2000) 154–165.

    Article  CAS  Google Scholar 

  74. O’Keefe, T.L., Williams, G.T., Davies, S.L. and Neuberger, M.S., Hyperresponsive B cells in CD22-deficient mice, Science, 274 (1996) 798–801.

    Article  CAS  Google Scholar 

  75. Otipoby, K.L., Andersson, K.B., Draves, K.E., Klaus, S.J., Farr, A.G., Kerner, J.D., Perlmutter, R.M., Law, C.L. and Clark, E.A., CD22 regulates thymus-independent responses and the lifespan of B cells, Nature, 384 (1996) 634–637.

    Article  CAS  Google Scholar 

  76. Sato, S., Miller, A.S., Inaoki, M., Bock, C.B., Jansen, P.J., Tang, M.L. and Tedder, T.F., CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: Altered signaling in CD22-deficient mice, Immunity, 5 (1996) 551–562.

    Article  CAS  Google Scholar 

  77. Nitschke, L., Carsetti, R., Ocker, B., Kohler, G. and Lamers, M.C., CD22 is a negative regulator of B-cell receptor signalling, Curr. Biol., 7 (1997) 133–143.

    Article  CAS  Google Scholar 

  78. Brinkman-Van der Linden, E.C., Angata, T., Reynolds, S.A., Powell, L.D., Hedrick, S.M. and Varki, A., CD33/Siglec-3 binding specificity, expression pattern, and consequences of gene deletion in mice, Mol. Cell. Biol., 23 (2003) 4199–4206.

    Article  CAS  Google Scholar 

  79. Jones, C., Virji, M. and Crocker, P.R., Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake, Mol. Microbiol., 49 (2003) 1213–1225.

    Article  CAS  Google Scholar 

  80. Vitale, C., Romagnani, C., Puccetti, A., Olive, D., Costello, R., Chiossone, L., Pitto, A., Bacigalupo, A., Moretta, L. and Mingari, M.C., Surface expression and function of p75/AIRM-1 or CD33 in acute myeloid leukemias: Engagement of CD33 induces apoptosis of leukemic cells, Proc. Natl. Acad. Sci. U. S. A., 98 (2001) 5764–5769.

    Article  CAS  Google Scholar 

  81. Nutku, E., Aizawa, H., Hudson, S.A. and Bochner, B.S., Ligation of Siglec-8: A selective mechanism for induction of human eosinophil apoptosis, Blood, 101 (2003) 5014–5020.

    Article  CAS  Google Scholar 

  82. von Gunten, S., Yousefi, S., Seitz, M., Jakob, S.M., Schaffner, T., Seger, R., Takala, J., Villiger, P.M. and Simon, H.U., Siglec-9 transduces apoptotic and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment, Blood, 106 (2005) 1423–1431.

    Article  CAS  Google Scholar 

  83. Vitale, C., Romagnani, C., Falco, M., Ponte, M., Vitale, M., Moretta, A., Bacigalupo, A., Moretta, L. and Mingari, M.C., Engagement of p75/AIRM1 or CD33 inhibits the proliferation of normal or leukemic myeloid cells, Proc. Natl. Acad. Sci. U. S. A., 96 (1999) 15091–15096.

    Article  CAS  Google Scholar 

  84. Dehal, P., Satou, Y., Campbell, R.K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., Goodstein, D.M., Harafuji, N., Hastings, K.E., Ho, I., Hotta, K., Huang, W., Kawashima, T., Lemaire, P., Martinez, D., Meinertzhagen, I.A., Necula, S., Nonaka, M., Putnam, N., Rash, S., Saiga, H., Satake, M., Terry, A., Yamada, L., Wang, H.G., Awazu, S., Azumi, K., Boore, J., Branno, M., Chin-Bow, S., DeSantis, R., Doyle, S., Francino, P., Keys, D.N., Haga, S., Hayashi, H., Hino, K., Imai, K.S., Inaba, K., Kano, S., Kobayashi, K., Kobayashi, M., Lee, B.I., Makabe, K.W., Manohar, C., Matassi, G., Medina, M., Mochizuki, Y., Mount, S., Morishita, T., Miura, S., Nakayama, A., Nishizaka, S., Nomoto, H., Ohta, F., Oishi, K., Rigoutsos, I., Sano, M., Sasaki, A., Sasakura, Y., Shoguchi, E., Shin-i, T., Spagnuolo, A., Stainier, D., Suzuki, M.M., Tassy, O., Takatori, N., Tokuoka, M., Yagi, K., Yoshizaki, F., Wada, S., Zhang, C., Hyatt, P.D., Larimer, F., Detter, C., Doggett, N., Glavina, T., Hawkins, T., Richardson, P., Lucas, S., Kohara, Y., Levine, M., Satoh, N. and Rokhsar, D.S., The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins, Science, 298 (2002) 2157–2167.

    Article  CAS  Google Scholar 

  85. Cameron, R.A., Mahairas, G., Rast, J.P., Martinez, P., Biondi, T.R., Swartzell, S., Wallace, J.C., Poustka, A.J., Livingston, B.T., Wray, G.A., Ettensohn, C.A., Lehrach, H., Britten, R.J., Davidson, E.H. and Hood, L., A sea urchin genome project: Sequence scan, virtual map, and additional resources, Proc. Natl. Acad. Sci. U. S. A., 97 (2000) 9514–9518.

    Article  Google Scholar 

  86. Poustka, A.J., Groth, D., Hennig, S., Thamm, S., Cameron, A., Beck, A., Reinhardt, R., Herwig, R., Panopoulou, G. and Lehrach, H., Generation, annotation, evolutionary analysis, and database integration of 20,000 unique sea urchin EST clusters, Genome. Res., 13 (2003) 2736–2746.

    Article  Google Scholar 

  87. Lehmann, F., Gathje, H., Kelm, S. and Dietz, F., Evolution of sialic acid-binding proteins: Molecular cloning and expression of fish siglec-4, Glycobiology, 14 (2004) 959–968.

    Article  CAS  Google Scholar 

  88. Lindblad-Toh, K., Wade, C.M., Mikkelsen, T.S., Karlsson, E.K., Jaffe, D.B., Kamal, M., Clamp, M., Chang, J.L., Kulbokas, E.J. III, Zody, M.C., Mauceli, E., Xie, X., Breen, M., Wayne, R.K., Ostrander, E.A., Ponting, C.P., Galibert, F., Smith, D.R., DeJong, P.J., Kirkness, E., Alvarez, P., Biagi, T., Brockman, W., Butler, J., Chin, C.W., Cook, A., Cuff, J., Daly, M.J., DeCaprio, D., Gnerre, S., Grabherr, M., Kellis, M., Kleber, M., Bardeleben, C., Goodstadt, L., Heger, A., Hitte, C., Kim, L., Koepfli, K.P., Parker, H.G., Pollinger, J.P., Searle, S.M., Sutter, N.B., Thomas, R., Webber, C., Broad Institute Genome Sequencing Platform and Lander, E.S., Genome sequence, comparative analysis and haplotype structure of the domestic dog, Nature, 438 (2005) 803–819.

    Article  CAS  Google Scholar 

  89. Hayakawa, T., Angata, T., Lewis, A.L., Mikkelsen, T.S., Varki, N.M. and Varki, A., A human-specific gene in microglia, Science, 309 (2005) 1693.

    CAS  Google Scholar 

  90. Irie, A., Koyama, S., Kozutsumi, Y., Kawasaki, T. and Suzuki, A., The molecular basis for the absence of N-glycolylneuraminic acid in humans, J. Biol. Chem., 273 (1998) 15866–15871.

    Article  CAS  Google Scholar 

  91. Chou, H.H., Hayakawa, T., Diaz, S., Krings, M., Indriati, E., Leakey, M., Paabo, S., Satta, Y., Takahata, N. and Varki, A., Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution, Proc. Natl. Acad. Sci. U. S. A., 99 (2002) 11736–11741.

    Article  CAS  Google Scholar 

  92. Chou, H.H., Takematsu, H., Diaz, S., Iber, J., Nickerson, E., Wright, K.L., Muchmore, E.A., Nelson, D.L., Warren, S.T. and Varki, A., A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence, Proc. Natl. Acad. Sci. U. S. A., 95 (1998) 11751–11756.

    Article  CAS  Google Scholar 

  93. Muchmore, E.A., Diaz, S. and Varki, A., A structural difference between the cell surfaces of humans and the great apes, Am. J. Phys. Anthropol., 107 (1998) 187–198.

    Article  CAS  Google Scholar 

  94. Angata, T., Varki, N.M. and Varki, A., A second uniquely human mutation affecting sialic acid biology, J. Biol. Chem., 276 (2001) 40282–40287.

    CAS  Google Scholar 

  95. Yu, Z., Lai, C.M., Maoui, M., Banville, D. and Shen, S.H., Identification and characterization of S2V, a novel putative siglec that contains two V set Ig-like domains and recruits protein-tyrosine phosphatases SHPs, J. Biol. Chem., 276 (2001) 23816–23824.

    Article  CAS  Google Scholar 

  96. Sonnenburg, J.L., Altheide, T.K. and Varki, A., A uniquely human consequence of domain-specific functional adaptation in a sialic acid-binding receptor, Glycobiology, 14 (2004) 339–346.

    Article  CAS  Google Scholar 

  97. Varki, A., Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences and implications for hominid evolution, Yearbook Phys. Anthropol., 44 (2002) 54–69.

    Google Scholar 

  98. The Chimpanzee Sequencing and Analysis Consortium, Initial sequence of the chimpanzee genome and comparison with the human genome, Nature, 437 (2005) 69–87.

  99. Vanderheijden, N., Delputte, P.L., Favoreel, H.W., Vandekerckhove, J., Van Damme, J., Van Woensel, P.A. and Nauwynck, H.J., Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages, J. Virol., 77 (2003) 8207–8215.

    Article  CAS  Google Scholar 

  100. Delputte, P.L. and Nauwynck, H.J., Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus, J. Virol., 78 (2004) 8094–8101.

    Article  CAS  Google Scholar 

  101. Galili, U., Clark, M.R., Shohet, S.B., Buehler, J. and Macher, B.A., Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha1-3Gal epitope in primates, Proc. Natl. Acad. Sci. U. S. A., 84 (1987) 1369–1373.

    Article  CAS  Google Scholar 

  102. Galili, U., Shohet, S.B., Kobrin, E., Stults, C.L. and Macher, B.A., Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells, J. Biol. Chem., 263 (1988) 17755–17762.

    CAS  Google Scholar 

  103. Galili, U. and Swanson, K., Gene sequences suggest inactivation of α-1,3-galactosyltransferase in catarrhines after the divergence of apes from monkeys, Proc. Natl. Acad. Sci. U. S. A., 88 (1991) 7401–7404.

    Article  CAS  Google Scholar 

  104. International Chicken Genome Sequencing Consortium, Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution, Nature, 432 (2004) 695–716.

  105. Aparicio, S., Chapman, J., Stupka, E., Putnam, N., Chia, J.M., Dehal, P., Christoffels, A., Rash, S., Hoon, S., Smit, A., Gelpke, M.D., Roach, J., Oh, T., Ho, I.Y., Wong, M., Detter, C., Verhoef, F., Predki, P., Tay, A., Lucas, S., Richardson, P., Smith, S.F., Clark, M.S., Edwards, Y.J., Doggett, N., Zharkikh, A., Tavtigian, S.V., Pruss, D., Barnstead, M., Evans, C., Baden, H., Powell, J., Glusman, G., Rowen, L., Hood, L., Tan, Y.H., Elgar, G., Hawkins, T., Venkatesh, B., Rokhsar, D. and Brenner, S., Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes, Science, 297 (2002) 1301–1310.

    Article  CAS  Google Scholar 

  106. Jaillon, O., Aury, J.M., Brunet, F., Petit, J.L., Stange-Thomann, N., Mauceli, E., Bouneau, L., Fischer, C., Ozouf-Costaz, C., Bernot, A., Nicaud, S., Jaffe, D., Fisher, S., Lutfalla, G., Dossat, C., Segurens, B., Dasilva, C., Salanoubat, M., Levy, M., Boudet, N., Castellano, S., Anthouard, V., Jubin, C., Castelli, V., Katinka, M., Vacherie, B., Biemont, C., Skalli, Z., Cattolico, L., Poulain, J., De Berardinis, V., Cruaud, C., Duprat, S., Brottier, P., Coutanceau, J.P., Gouzy, J., Parra, G., Lardier, G., Chapple, C., McKernan, K.J., McEwan, P., Bosak, S., Kellis, M., Volff, J.N., Guigo, R., Zody, M.C., Mesirov, J., Lindblad-Toh, K., Birren, B., Nusbaum, C., Kahn, D., Robinson-Rechavi, M., Laudet, V., Schachter, V., Quetier, F., Saurin, W., Scarpelli, C., Wincker, P., Lander, E.S., Weissenbach, J. and Roest Crollius, H., Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype, Nature, 431 (2004) 946–957.

    Article  Google Scholar 

  107. Angata, T., Kerr, S.C., Greaves, D.R., Varki, N.M., Crocker, P.R. and Varki, A., Cloning and characterization of human Siglec-11. A recently evolved signaling molecule that can interact with SHP-1 and SHP-2 and is expressed by tissue macrophages, including brain microglia, J. Biol. Chem., 277 (2002) 24466–24474.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Center for Glycoscience, National Institute of Advanced Industrial Science and Technology, 1-1-1 Umezono, Tsukuba, Ibaraki, 305-8568, JAPAN

    Takashi Angata

Authors
  1. Takashi Angata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takashi Angata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angata, T. Molecular diversity and evolution of the Siglec family of cell-surface lectins. Mol Divers 10, 555–566 (2006). https://doi.org/10.1007/s11030-006-9029-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11030-006-9029-1

Key words

Search

Navigation