CD22 is a recycling receptor that can shuttle cargo between the cell surface and endosomal compartments of B cells

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1554-1563

  O'Reilly, Mary K ^a   Tian, Hua ^a   Paulson, James C ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD22 ANTIGEN; GLYCAN;

ANIMAL CELL; ANTIGEN BINDING CELL; ARTICLE; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL METABOLISM; CELL SURFACE; CELL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION;

ANIMALS; ANTIGENS, CD22; B-LYMPHOCYTE SUBSETS; BURKITT LYMPHOMA; CELL LINE, TUMOR; CELL MEMBRANE; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENDOSOMES; HUMANS; INTRACELLULAR FLUID; LIGANDS; LYMPHOCYTE DEPLETION; LYMPHOMA, B-CELL; MICE; MICE, INBRED C57BL; PROTEIN TRANSPORT;

EID: 79251555969     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003005     Document Type: Article

References (63)

1. Crocker, P. R., J. C. Paulson, and A. Varki. 2007. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7: 255-266.
2. Crocker, P. R., and P. Redelinghuys. 2008. Siglecs as positive and negative regulators of the immune system. Biochem. Soc. Trans. 36: 1467-1471.
3. Doody, G. M., L. B. Justement, C. C. Delibrias, R. J. Matthews, J. Lin, M. L. Thomas, and D. T. Fearon. 1995. A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 269: 242-244.
4. Walker, J. A., and K. G. Smith. 2008. CD22: an inhibitory enigma. Immunology 123: 314-325.
5. Otipoby, K. L., K. E. Draves, and E. A. Clark. 2001. CD22 regulates B cell receptor-mediated signals via two domains that independently recruit Grb2 and SHP-1. J. Biol. Chem. 276: 44315-44322.
6. Zhu, C., M. Sato, T. Yanagisawa, M. Fujimoto, T. Adachi, and T. Tsubata. 2008. Novel binding site for Src homology 2-containing protein-tyrosine phosphatase-1 in CD22 activated by B lymphocyte stimulation with antigen. J. Biol. Chem. 283: 1653-1659.
7. Collins, B. E., O. Blixt, A. R. DeSieno, N. Bovin, J. D. Marth, and J. C. Paulson. 2004. Masking of CD22 by cis ligands does not prevent redistribution of CD22 to sites of cell contact. Proc. Natl. Acad. Sci. USA 101: 6104-6109.
8. Han, S., B. E. Collins, P. Bengtson, and J. C. Paulson. 2005. Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking. Nat. Chem. Biol. 1: 93-97.
9. Ramya, T. N., E. Weerapana, L. Liao, Y. Zeng, H. Tateno, L. Liao, J. R. Yates, 3rd, B. F. Cravatt, and J. C. Paulson. 2010. In situ trans ligands of CD22 identified by glycan-protein photocross-linking-enabled proteomics. Mol. Cell Proteomics 9: 1339-1351.
10. Razi, N., and A. Varki. 1998. Masking and unmasking of the sialic acid-binding lectin activity of CD22 (Siglec-2) on B lymphocytes. Proc. Natl. Acad. Sci. USA 95: 7469-7474.
11. John, B., B. R. Herrin, C. Raman, Y. N. Wang, K. R. Bobbitt, B. A. Brody, and L. B. Justement. 2003. The B cell coreceptor CD22 associates with AP50, a clathrin-coated pit adapter protein, via tyrosine-dependent interaction. J. Immunol. 170: 3534-3543.
12. Tateno, H., H. Li, M. J. Schur, N. Bovin, P. R. Crocker, W. W. Wakarchuk, and J. C. Paulson. 2007. Distinct endocytic mechanisms of CD22 (Siglec-2) and Siglec-F reflect roles in cell signaling and innate immunity. Mol. Cell. Biol. 27: 5699-5710.
13. Stoddart, A., M. L. Dykstra, B. K. Brown, W. Song, S. K. Pierce, and F. M. Brodsky. 2002. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 17: 451-462.
14. Stoddart, A., A. P. Jackson, and F. M. Brodsky. 2005. Plasticity of B cell receptor internalization upon conditional depletion of clathrin.Mol. Biol. Cell 16: 2339-2348.
15. Leprince, C., K. E. Draves, R. L. Geahlen, J. A. Ledbetter, and E. A. Clark. 1993. CD22 associates with the human surface IgM-B-cell antigen receptor complex. Proc. Natl. Acad. Sci. USA 90: 3236-3240.
16. Collins, B. E., B. A. Smith, P. Bengtson, and J. C. Paulson. 2006. Ablation of CD22 in ligand-deficient mice restores B cell receptor signaling. Nat. Immunol. 7: 199-206.
17. Grewal, P. K., M. Boton, K. Ramirez, B. E. Collins, A. Saito, R. S. Green, K. Ohtsubo, D. Chui, and J. D. Marth. 2006. ST6Gal-I restrains CD22-dependent antigen receptor endocytosis and Shp-1 recruitment in normal and pathogenic immune signaling. Mol. Cell. Biol. 26: 4970-4981.
18. Chan, C. H., J. Wang, R. R. French, and M. J. Glennie. 1998. Internalization of the lymphocytic surface protein CD22 is controlled by a novel membrane proximal cytoplasmic motif. J. Biol. Chem. 273: 27809-27815.
19. Shan, D., and O. W. Press. 1995. Constitutive endocytosis and degradation of CD22 by human B cells. J. Immunol. 154: 4466-4475.
20. Du, X., R. Beers, D. J. Fitzgerald, and I. Pastan. 2008. Differential cellular internalization of anti-CD19 and -CD22 immunotoxins results in different cytotoxic activity. Cancer Res. 68: 6300-6305.
21. Chen, W. C., G. C. Completo, D. S. Sigal, P. R. Crocker, A. Saven, and J. C. Paulson. 2010. In vivo targeting of B-cell lymphoma with glycan ligands of CD22. Blood 115: 4778-4786.
22. Collins, B. E., O. Blixt, S. Han, B. Duong, H. Li, J. K. Nathan, N. Bovin, and J. C. Paulson. 2006. High-affinity ligand probes of CD22 overcome the threshold set by cis ligands to allow for binding, endocytosis, and killing of B cells. J. Immunol. 177: 2994-3003.
23. Kaltgrad, E., M. K. O'Reilly, L. Liao, S. Han, J. C. Paulson, and M. G. Finn. 2008. On-virus construction of polyvalent glycan ligands for cell-surface receptors. J. Am. Chem. Soc. 130: 4578-4579.
24. O'Reilly, M. K., B. E. Collins, S. Han, L. Liao, C. Rillahan, P. I. Kitov, D. R. Bundle, and J. C. Paulson. 2008. Bifunctional CD22 ligands use multimeric immunoglobulins as protein scaffolds in assembly of immune complexes on B cells. J. Am. Chem. Soc. 130: 7736-7745.
25. Press, O. W., A. G. Farr, K. I. Borroz, S. K. Anderson, and P. J. Martin. 1989. Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res. 49: 4906-4912.
26. Castillo, J., E. Winer, and P. Quesenberry. 2008. Newer monoclonal antibodies for hematological malignancies. Exp. Hematol. 36: 755-768.
27. O'Reilly, M. K., and J. C. Paulson. 2009. Siglecs as targets for therapy in immune-cell-mediated disease. Trends Pharmacol. Sci. 30: 240-248.
28. Dijoseph, J. F., M. M. Dougher, D. C. Armellino, D. Y. Evans, and N. K. Damle. 2007. Therapeutic potential of CD22-specific antibody-targeted chemotherapy using inotuzumab ozogamicin (CMC-544) for the treatment of acute lymphoblastic leukemia. Leukemia 21: 2240-2245.
29. DiJoseph, J. F., M. M. Dougher, L. B. Kalyandrug, D. C. Armellino, E. R. Boghaert, P. R. Hamann, J. K. Moran, and N. K. Damle. 2006. Antitumor efficacy of a combination of CMC-544 (inotuzumab ozogamicin), a CD22-targeted cytotoxic immunoconjugate of calicheamicin, and rituximab against non-Hodgkin's B-cell lymphoma. Clin. Cancer Res. 12: 242-249.
30. DiJoseph, J. F., A. Popplewell, S. Tickle, H. Ladyman, A. Lawson, A. Kunz, K. Khandke, D. C. Armellino, E. R. Boghaert, P. Hamann, et al. 2005. Antibody-targeted chemotherapy of B-cell lymphoma using calicheamicin conjugated to murine or humanized antibody against CD22. Cancer Immunol. Immunother. 54: 11-24.
31. Sieber, T., D. Schoeler, F. Ringel, M. Pascu, and F. Schriever. 2003. Selective internalization of monoclonal antibodies by B-cell chronic lymphocytic leukaemia cells. Br. J. Haematol. 121: 458-461.
32. Keppler, O. T., S. Hinderlich, J. Langner, R. Schwartz-Albiez, W. Reutter, and M. Pawlita. 1999. UDP-GlcNAc 2-epimerase: a regulator of cell surface sialylation. Science 284: 1372-1376.
33. Jin, L., P. A. McLean, B. G. Neel, and H. H. Wortis. 2002. Sialic acid binding domains of CD22 are required for negative regulation of B cell receptor signaling. J. Exp. Med. 195: 1199-1205.
34. Le, T. L., A. S. Yap, and J. L. Stow. 1999. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146: 219-232.
35. Morimoto, S., N. Nishimura, T. Terai, S. Manabe, Y. Yamamoto, W. Shinahara, H. Miyake, S. Tashiro,M. Shimada, and T. Sasaki. 2005. Rab13 mediates the continuous endocytic recycling of occludin to the cell surface. J. Biol. Chem. 280: 2220-2228.
36. Baratti-Elbaz, C., N. Ghinea, O. Lahuna, H. Loosfelt, C. Pichon, and E. Milgrom. 1999. Internalization and recycling pathways of the thyrotropin receptor. Mol. Endocrinol. 13: 1751-1765.
37. Heuser, J. E., and R. G. Anderson. 1989. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108: 389-400.
38. Johnson, L. S., K. W. Dunn, B. Pytowski, and T. E. McGraw. 1993. Endosome acidification and receptor trafficking: bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif. Mol. Biol. Cell 4: 1251-1266.
39. Presley, J. F., S. Mayor, T. E. McGraw, K. W. Dunn, and F. R. Maxfield. 1997. Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J. Biol. Chem. 272: 13929-13936.
40. Koníková, E., J. Kusenda, O. Babusíková, and M. Glasová. 1995. Human hematopoietic cell lines: a model system for study of minimal residual disease detection technique in acute leukemia. Neoplasma 42: 227-234.
41. Tuscano, J., P. Engel, T. F. Tedder, and J. H. Kehrl. 1996. Engagement of the adhesion receptor CD22 triggers a potent stimulatory signal for B cells and blocking CD22/CD22L interactions impairs T-cell proliferation. Blood 87: 4723-4730.
42. Tuscano, J. M., P. Engel, T. F. Tedder, A. Agarwal, and J. H. Kehrl. 1996. Involvement of p72syk kinase, p53/56lyn kinase and phosphatidyl inositol-3 kinase in signal transduction via the human B lymphocyte antigen CD22. Eur. J. Immunol. 26: 1246-1252.
43. Tuscano, J. M., A. Riva, S. N. Toscano, T. F. Tedder, and J. H. Kehrl. 1999. CD22 cross-linking generates B-cell antigen receptor-independent signals that activate the JNK/SAPK signaling cascade. Blood 94: 1382-1392.
44. Haas, K. M., S. Sen, I. G. Sanford, A. S. Miller, J. C. Poe, and T. F. Tedder. 2006. CD22 ligand binding regulates normal and malignant B lymphocyte survival in vivo. J. Immunol. 177: 3063-3073.
45. Tuscano, J. M., R. T. O'Donnell, L. A. Miers, L. A. Kroger, D. L. Kukis, K. R. Lamborn, T. F. Tedder, and G. L. DeNardo. 2003. Anti-CD22 ligand-blocking antibody HB22.7 has independent lymphomacidal properties and augments the efficacy of 90Y-DOTA-peptide-Lym-1 in lymphoma xenografts. Blood 101: 3641-3647.
46. Ciechanover, A., A. L. Schwartz, A. Dautry-Varsat, and H. F. Lodish. 1983. Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J. Biol. Chem. 258: 9681-9689.
47. Ciechanover, A., A. L. Schwartz, and H. F. Lodish. 1983. The asialoglycoprotein receptor internalizes and recycles independently of the transferrin and insulin receptors. Cell 32: 267-275.
48. Avril, T., E. R. Wagner, H. J. Willison, and P. R. Crocker. 2006. Sialic acid-binding immunoglobulin-like lectin 7 mediates selective recognition of sialylated glycans expressed on Campylobacter jejuni lipooligosaccharides. Infect. Immun. 74: 4133-4141.
49. Carlin, A. F., S. Uchiyama, Y. C. Chang, A. L. Lewis, V. Nizet, and A. Varki. 2009. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 113: 3333-3336.
50. Rempel, H., C. Calosing, B. Sun, and L. Pulliam. 2008. Sialoadhesin expressed on IFN-induced monocytes binds HIV-1 and enhances infectivity. PLoS One 3: e1967.
51. Kreitman, R. J., and I. Pastan. 2006. BL22 and lymphoid malignancies. Best Pract. Res. Clin. Haematol. 19: 685-699.
52. Bogner, C., T. Dechow, I. Ringshausen, M. Wagner, M. Oelsner, G. Lutzny, T. Licht, C. Peschel, I. Pastan, R. J. Kreitman, and T. Decker. 2010. Immunotoxin BL22 induces apoptosis in mantle cell lymphoma (MCL) cells dependent on Bcl-2 expression. Br. J. Haematol. 148: 99-109.
53. Wayne, A. S., R. J. Kreitman, H. W. Findley, G. Lew, C. Delbrook, S. M. Steinberg, M. Stetler-Stevenson, D. J. Fitzgerald, and I. Pastan. 2010. Anti-CD22 immunotoxin RFB4(dsFv)-PE38 (BL22) for CD22-positive hematologic malignancies of childhood: preclinical studies and phase I clinical trial. Clin. Cancer Res. 16: 1894-1903.
54. Keppler-Hafkemeyer, A., R. J. Kreitman, and I. Pastan. 2000. Apoptosis induced by immunotoxins used in the treatment of hematologic malignancies. Int. J. Cancer 87: 86-94. (Pubitemid 30368420)
55. Kreitman, R. J., I. Margulies, M. Stetler-Stevenson, Q. C. Wang, D. J. FitzGerald, and I. Pastan. 2000. Cytotoxic activity of disulfide-stabilized recombinant immunotoxin RFB4(dsFv)-PE38 (BL22) toward fresh malignant cells from patients with B-cell leukemias. Clin. Cancer Res. 6: 1476-1487.
56. Kreitman, R. J., W. H. Wilson, K. Bergeron, M. Raggio, M. Stetler-Stevenson, D. J. FitzGerald, and I. Pastan. 2001. Efficacy of the anti-CD22 recombinant immunotoxin BL22 in chemotherapy-resistant hairy-cell leukemia. N. Engl. J. Med. 345: 241-247.
57. Decker, T., M. Oelsner, R. J. Kreitman, G. Salvatore, Q. C. Wang, I. Pastan, C. Peschel, and T. Licht. 2004. Induction of caspase-dependent programmed cell death in B-cell chronic lymphocytic leukemia by anti-CD22 immunotoxins. Blood 103: 2718-2726.
58. Bang, S., S. Nagata, M. Onda, R. J. Kreitman, and I. Pastan. 2005. HA22 (R490A) is a recombinant immunotoxin with increased antitumor activity without an increase in animal toxicity. Clin. Cancer Res. 11: 1545-1550.
59. Ho, M., R. J. Kreitman, M. Onda, and I. Pastan. 2005. In vitro antibody evolution targeting germline hot spots to increase activity of an anti-CD22 immunotoxin. J. Biol. Chem. 280: 607-617.
60. Kreitman, R. J., D. R. Squires, M. Stetler-Stevenson, P. Noel, D. J. FitzGerald, W. H. Wilson, and I. Pastan. 2005. Phase I trial of recombinant immunotoxin RFB4(dsFv)-PE38 (BL22) in patients with B-cell malignancies. J. Clin. Oncol. 23: 6719-6729.
61. Onda, M., R. Beers, L. Xiang, S. Nagata, Q. C. Wang, and I. Pastan. 2008. An immunotoxin with greatly reduced immunogenicity by identification and removal of B cell epitopes. Proc. Natl. Acad. Sci. USA 105: 11311-11316.
62. Kreitman, R. J., M. Stetler-Stevenson, I. Margulies, P. Noel, D. J. Fitzgerald, W. H. Wilson, and I. Pastan. 2009. Phase II trial of recombinant immunotoxin RFB4(dsFv)-PE38 (BL22) in patients with hairy cell leukemia. J. Clin. Oncol. 27: 2983-2990.
63. Polson, A. G., J. Calemine-Fenaux, P. Chan, W. Chang, E. Christensen, S. Clark, F. J. de Sauvage, D. Eaton, K. Elkins, J. M. Elliott, et al. 2009. Antibody-drug conjugates for the treatment of non-Hodgkin's lymphoma: target and linker-drug selection. Cancer Res. 69: 2358-2364.