The mechanistic impact of CD22 engagement with epratuzumab on B cell function: Implications for the treatment of systemic lupus erythematosus

Autoimmunity Reviews

Volumn 14, Issue 12, 2015, Pages 1079-1086

  Dörner, Thomas ^a   Shock, Anthony ^b   Goldenberg, David M ^c   Lipsky, Peter E ^d  

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^b UCB PHARMA   (Belgium)

^c IMMUNOMEDICS INC   (United States)

^d NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

B cells; Biologic therapies; CD22; Epratuzumab; Systemic lupus erythematosus

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD22 ANTIGEN; CELL ADHESION MOLECULE; EPRATUZUMAB; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; CD22 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY;

B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL MIGRATION; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG MECHANISM; HUMAN; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; B-LYMPHOCYTES; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTORS, ANTIGEN, B-CELL; SIALIC ACID BINDING IG-LIKE LECTIN 2; SIGNAL TRANSDUCTION;

EID: 84945485927     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2015.07.013     Document Type: Review

References (136)

1. Crispín J.C., Liossis S.-N.C., Kis-Toth K., Lieberman L.A., Kyttaris V.C., Juang Y.-T., et al. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 2010, 16:47-57.
2. Tsokos G.C. Systemic lupus erythematosus. N Engl J Med 2011, 365:2110-2121.
3. Gatto M., Zen M., Ghirardello A., Bettio S., Bassi N., Iaccarino L., et al. Emerging and critical issues in the pathogenesis of lupus. Autoimmun Rev 2013, 12:523-536.
4. Furie R., Petri M., Zamani O., Cervera R., Wallace D.J., Tegzová D., et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum 2011, 63:3918-3930.
5. Navarra S.V., Guzmán R.M., Gallacher A.E., Hall S., Levy R.A., Jimenez R.E., et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011, 377:721-731.
6. Isenberg D., Gordon C., Licu D., Copt S., Rossi C.P., Wofsy D. Efficacy and safety of atacicept for prevention of flares in patients with moderate-to-severe systemic lupus erythematosus (SLE): 52-week data (APRIL-SLE randomised trial). Ann Rheum Dis 2014, [annrheumdis-2013-205067] [Epub ahead of print].
7. Ginzler E.M., Wax S., Rajeswaran A., Copt S., Hillson J., Ramos E., et al. Atacicept in combination with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trial. Arthritis Res Ther 2012, 14:R33.
8. Leone A., Sciascia S., Kamal A., Khamashta M. Biologicals for the treatment of systemic lupus erythematosus: current status and emerging therapies. Expert Rev Clin Immunol 2015, 11:109-116.
9. Merrill J.T., Neuwelt C.M., Wallace D.J., Shanahan J.C., Latinis K.M., Oates J.C., et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum 2010, 62:222-233.
10. Mysler E., Spindler A., Guzman R., Bijl M., Jayne D., Furie R., et al. Efficacy and safety of ocrelizumab, a humanized antiCD20 antibody, in patients with active proliferative lupus nephritis (LN): results from the randomized, double-blind phase III BELONG study. Arthritis Rheum 2010, 62:1455.
11. Rovin B.H., Furie R., Latinis K., Looney R.J., Fervenza F.C., Sanchez-Guerrero J., et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum 2012, 64:1215-1226.
12. Leonard J., Goldenberg D.M. Preclinical and clinical evaluation of epratuzumab (anti-CD22 IgG) in B-cell malignancies. Oncogene 2007, 26:3704-3713.
13. Leonard J., Coleman M., Ketas J.C., Chadburn A., Ely S., Furman R.R., et al. Phase I/II trial of epratuzumab (humanized anti-CD22 antibody) in indolent non-Hodgkin's lymphoma. J Clin Oncol 2003, 21:3051-3059.
14. Goldenberg D.M. Epratuzumab in the therapy of oncological and immunological diseases. Expert Rev Anticancer Ther 2006, 6:1341.
15. Wallace D.J., Kalunian K., Petri M.A., Strand V., Houssiau F.A., Pike M., et al. Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a phase IIb, randomised, double-blind, placebo-controlled, multicentre study. Ann Rheum Dis 2014, 73:183-190.
16. Clowse M.E., Houssiau F., Petri M.A., Kilgallen B., Kalunian K., Strand V., et al. Epratuzumab maintains improvements in disease activity for over 2years in patients with moderate-to-severe systemic lupus erythematosus: results from an open-label long-term extension study. Arthritis Rheum 2013, 65:S737-S738.
17. Kalunian K., Clowse M.E., Houssiau F., Petri M.A., Kilgallen B., Gordon C., et al. Sustained British Isles Lupus Assessment Group-measured improvement in moderately-and-severely affected body systems in patients with systemic lupus erythematosus by epratuzumab: results from an open-label extension study. Arthritis Rheum 2013, S738.
18. Mauri C., Bosma A. Immune regulatory function of B cells. Annu Rev Immunol 2012, 30:221-241.
19. Lipsky P.E. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001, 2:764-766.
20. Engel P., Gómez-Puerta J.A., Ramos-Casals M., Lozano F., Bosch X. Therapeutic targeting of B cells for rheumatic autoimmune diseases. Pharmacol Rev 2011, 63:127-156.
21. Fillatreau S. Cytokine-producing B cells as regulators of pathogenic and protective immune responses. Ann Rheum Dis 2013, 72:ii80-ii84.
22. Macauley M.S., Pfrengle F., Rademacher C., Nycholat C.M., Gale A.J., von Drygalski A., et al. Antigenic liposomes displaying CD22 ligands induce antigen-specific B cell apoptosis. J Clin Invest 2013, 123:3074-3083.
23. Grimaldi C.M., Hicks R., Diamond B. B cell selection and susceptibility to autoimmunity. J Immunol 2005, 174:1775-1781.
24. Keren Z., Melamed D. Antigen receptor signaling competence and the determination of B cell fate in B-lymphopoiesis. Histol Histopathol 2005, 20:187-196.
25. Anolik J. B cell biology: implications for treatment of systemic lupus erythematosus. Lupus 2013, 22:342-349.
26. Dörner T., Giesecke C., Lipsky P.E. Mechanisms of B cell autoimmunity in SLE. Arthritis Res Ther 2011, 13:243.
27. Dörner T., Jacobi A.M., Lee J., Lipsky P.E. Abnormalities of B cell subsets in patients with systemic lupus erythematosus. J Immunol Methods 2011, 363:187-197.
28. Odendahl M., Jacobi A., Hansen A., Feist E., Hiepe F., Burmester G.R., et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 2000, 165:5970-5979.
29. Wei C., Anolik J., Cappione A., Zheng B., Pugh-Bernard A., Brooks J., et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol 2007, 178:6624-6633.
30. Jacobi A.M., Reiter K., Mackay M., Aranow C., Hiepe F., Radbruch A., et al. Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum 2008, 58:1762-1773.
31. Culton D.A., Nicholas M.W., Bunch D.O., Zhen Q.L., Kepler T.B., Dooley M.A., et al. Similar CD19 dysregulation in two autoantibody-associated autoimmune diseases suggests a shared mechanism of B-cell tolerance loss. J Clin Immunol 2007, 27:53-68.
32. Nicholas M.W., Dooley M.A., Hogan S.L., Anolik J., Looney J., Sanz I., et al. A novel subset of memory B cells is enriched in autoreactivity and correlates with adverse outcomes in SLE. Clin Immunol 2008, 126:189-201.
33. Warnatz K., Wehr C., Dräger R., Schmidt S., Eibel H., Schlesier M., et al. Expansion of CD19 hi CD21 lo/neg B cells in common variable immunodeficiency (CVID) patients with autoimmune cytopenia. Immunobiology 2002, 206:502-513.
34. Wehr C., Eibel H., Masilamani M., Illges H., Schlesier M., Peter H.-H., et al. A new CD21 low B cell population in the peripheral blood of patients with SLE. Clin Immunol 2004, 113:161-171.
35. Fleischer S.J., Giesecke C., Mei H.E., Lipsky P.E., Daridon C., Dörner T. Increased frequency of a unique spleen tyrosine kinase bright memory B cell population in systemic lupus erythematosus. Arthritis Rheum 2014, 66:3424-3435.
36. Jacobi A.M., Mei H., Hoyer B.F., Mumtaz I.M., Thiele K., Radbruch A., et al. HLA-DRhigh/CD27high plasmablasts indicate active disease in patients with systemic lupus erythematosus. Ann Rheum Dis 2010, 69:305-308.
37. Tipton C.M., Fucile C.F., Darce J., Chida A., Ichikawa T., Gregoretti I., et al. Diversity, cellular origin and autoreactivity of antibody-secreting cell population expansions in acute systemic lupus erythematosus. Nat Immunol 2015, 16:755-765.
38. Blair P.A., Noreña L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., et al. CD19+ CD24 hi CD38 hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010, 32:129-140.
39. Wahren-Herlenius M., Dörner T. Immunopathogenic mechanisms of systemic autoimmune disease. Lancet 2013, 382:819-831.
40. Pugh-Bernard A.E., Cambier J.C. B cell receptor signaling in human systemic lupus erythematosus. Curr Opin Rheumatol 2006, 18:451-455.
41. Grammer A.C., Dorner T., Lipsky P.E. Abnormalities in B cell activity and the human immunoglobulin repertoire in human systemic lupus erythematosus. Mol Pathol Autoimmun Dis 2001, 2:282-318.
42. Grammer A.C., Fischer R., Lee O., Zhang X., Lipsky P.E. Flow cytometric assessment of the signaling status of human B lymphocytes from normal and autoimmune individuals. Arthritis Res Ther 2004, 6:28-38.
43. Liossis S., Kovacs B., Dennis G., Kammer G.M., Tsokos G.C. B cells from patients with systemic lupus erythematosus display abnormal antigen receptor-mediated early signal transduction events. J Clin Invest 1996, 98:2549-2557.
44. Mackay M., Stanevsky A., Wang T., Aranow C., Li M., Koenig S., et al. Selective dysregulation of the FcγIIB receptor on memory B cells in SLE. J Exp Med 2006, 203:2157-2164.
45. Wu X.-N., Ye Y.-X., Niu J.-W., Li Y., Li X., You X., et al. Defective PTEN regulation contributes to B cell hyperresponsiveness in systemic lupus erythematosus. Sci Transl Med 2014, 6. [246ra99-ra99].
46. Chang N.-H., Li T.T., Kim J.J., Landolt-Marticorena C., Fortin P.R., Gladman D.D., et al. Interferon-α induces altered transitional B cell signaling and function in systemic lupus erythematosus. J Autoimmun 2015, 58:100-110.
47. Taher T.E., Parikh K., Flores-Borja F., Mletzko S., Isenberg D.A., Peppelenbosch M.P., et al. Protein phosphorylation and kinome profiling reveal altered regulation of multiple signaling pathways in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum 2010, 62:2412-2423.
48. Desai-Mehta A., Lu L., Ramsey-Goldman R., Datta S.K. Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production. J Clin Invest 1996, 97:2063-2073.
49. Enyedy E.J., Mitchell J.P., Nambiar M.P., Tsokos G.C. Defective FcγRIIb1 signaling contributes to enhanced calcium response in B cells from patients with systemic lupus erythematosus. Clin Immunol 2001, 101:130-135.
50. Liu S., Cerutti A., Casali P., Crow M.K. Ongoing immunoglobulin class switch DNA recombination in lupus B cells: analysis of switch regulatory regions. Autoimmunity 2004, 37:431-443.
51. Dörner T., Foster S.J., Farner N.L., Lipsky P.E. Immunoglobulin kappa chain receptor editing in systemic lupus erythematosus. J Clin Invest 1998, 102:688-694.
52. Sieber J., Daridon C., Fleischer S.J., Fleischer V., Hiepe F., Alexander T., et al. Active systemic lupus erythematosus is associated with a reduced cytokine production by B cells in response to TLR9 stimulation. Arthritis Res Ther 2014, 16:477.
53. Jacobi A.M., Goldenberg D.M., Hiepe F., Radbruch A., Burmester G.R., Dörner T. Differential effects of epratuzumab on peripheral blood B cells of patients with systemic lupus erythematosus versus normal controls. Ann Rheum Dis 2008, 67:450-457.
54. Flores-Borja F., Kabouridis P.S., Jury E.C., Isenberg D.A., Mageed R.A. Altered lipid raft-associated proximal signaling and translocation of CD45 tyrosine phosphatase in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum 2007, 56:291-302.
55. Huck S., Corre R.L., Youinou P., Zouali M. Expression of B cell receptor-associated signaling molecules in human lupus. Autoimmunity 2001, 33:213-224.
56. Hom G., Graham R.R., Modrek B., Taylor K.E., Ortmann W., Garnier S., et al. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N Engl J Med 2008, 358:900-909.
57. Kozyrev S.V., Abelson A.-K., Wojcik J., Zaghlool A., Reddy M.P.L., Sanchez E., et al. Functional variants in the B-cell gene BANK1 are associated with systemic lupus erythematosus. Nat Genet 2008, 40:211-216.
58. Pradhan V., Borse V., Ghosh K. PTPN22 gene polymorphisms in autoimmune diseases with special reference to systemic lupus erythematosus disease susceptibility. J Postgrad Med 2010, 56:239-242.
59. Vaughn S.E., Foley C., Lu X., Patel Z.H., Zoller E.E., Magnusen A.F., et al. Lupus risk variants in the PXK locus alter B-cell receptor internalization. Front Genet 2015, 5. [Article 450].
60. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol 2007, 7:255-266.
61. Pillai S., Netravali I.A., Cariappa A., Mattoo H. Siglecs and immune regulation. Annu Rev Immunol 2012, 30:357-392.
62. Daridon C., Blassfeld D., Reiter K., Mei H.E., Giesecke C., Goldenberg D.M., et al. Epratuzumab targeting of CD22 affects adhesion molecule expression and migration of B-cells in systemic lupus erythematosus. Arthritis Res Ther 2010, 12:R204.
63. Giltiay N.V., Shu G.L., Shock A., Clark E.A. Regulation of the responses of human B cell subsets to innate immune signals by epratuzumab, a humanized monoclonal antibody targeting CD22. Arthritis Rheum 2014, S855.
64. Dörner T., Shock A., Smith K.G. CD22 and autoimmune disease. Int Rev Immunol 2012, 31:363-378.
65. Doody G.M., Justement L.B., Delibrias C.C., Matthews R.J., Lin J., Thomas M.L., et al. A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 1995, 269:242-244.
66. Tamir I., Dal Porto J.M., Cambier J.C. Cytoplasmic protein tyrosine phosphatases SHP-1 and SHP-2: regulators of B cell signal transduction. Curr Opin Immunol 2000, 12:307-315.
67. Monroe J.G. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat Rev Immunol 2006, 6:283-294.
68. Kulathu Y., Grothe G., Reth M. Autoinhibition and adapter function of Syk. Immunol Rev 2009, 232:286-299.
69. Srinivasan L., Sasaki Y., Calado D.P., Zhang B., Paik J.H., DePinho R.A., et al. PI3 kinase signals BCR-dependent mature B cell survival. Cell 2009, 139:573-586.
70. Ruprecht C.R., Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 2006, 36:810-816.
71. Chaturvedi A., Dorward D., Pierce S.K. The B cell receptor governs the subcellular location of Toll-like receptor 9 leading to hyperresponses to DNA-containing antigens. Immunity 2008, 28:799-809.
72. Pone E.J., Zhang J., Mai T., White C.A., Li G., Sakakura J.K., et al. BCR-signalling synergizes with TLR-signalling for induction of AID and immunoglobulin class-switching through the non-canonical NF-κB pathway. Nat Commun 2012, 3:767.
73. Eckl-Dorna J., Batista F.D. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 2009, 113:3969-3977.
74. Mizuno T., Rothstein T.L. B cell receptor (BCR) cross-talk: CD40 engagement creates an alternate pathway for BCR signaling that activates IκB kinase/IκBα/NF-κB without the need for PI3K and phospholipase Cγ. J Immunol 2005, 174:6062-6070.
75. Mizuno T., Rothstein T.L. B cell receptor (BCR) cross-talk: CD40 engagement enhances BCR-induced ERK activation. J Immunol 2005, 174:3369-3376.
76. Fujimoto M., Kuwano Y., Watanabe R., Asashima N., Nakashima H., Yoshitake S., et al. B cell antigen receptor and CD40 differentially regulate CD22 tyrosine phosphorylation. J Immunol 2006, 176:873-879.
77. Kawasaki N., Rademacher C., Paulson J.C. CD22 regulates adaptive and innate immune responses of B cells. J Innate Immun 2011, 3:411-419.
78. Jellusova J., Wellmann U., Amann K., Winkler T.H., Nitschke L. CD22× Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J Immunol 2010, 184:3618-3627.
79. Poe J.C., Haas K.M., Uchida J., Lee Y., Fujimoto M., Tedder T.F. Severely impaired B lymphocyte proliferation, survival, and induction of the c-Myc: Cullin 1 ubiquitin ligase pathway resulting from CD22 deficiency on the C57BL/6 genetic background. J Immunol 2004, 172:2100-2110.
80. Smith S.H., Haas K.M., Poe J.C., Yanaba K., Ward C.D., Migone T.-S., et al. B-cell homeostasis requires complementary CD22 and BLyS/BR3 survival signals. Int Immunol 2010, 22:681-691.
81. Pierce S.K. Lipid rafts and B-cell activation. Nat Rev Immunol 2002, 2:96-105.
82. Stoddart A., Jackson A.P., Brodsky F.M. Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol Biol Cell 2005, 16:2339-2348.
83. Tateno H., Li H., Schur M.J., Bovin N., Crocker P.R., Wakarchuk W.W., et al. Distinct endocytic mechanisms of CD22 (Siglec-2) and Siglec-F reflect roles in cell signaling and innate immunity. Mol Cell Biol 2007, 27:5699-5710.
84. Yu J., Sawada T., Adachi T., Gao X., Takematsu H., Kozutsumi Y., et al. Synthetic glycan ligand excludes CD22 from antigen receptor-containing lipid rafts. Biochem Biophys Res Commun 2007, 360:759-764.
85. Weintraub B.C., Jun J.E., Bishop A.C., Shokat K.M., Thomas M.L., Goodnow C.C. Entry of B cell receptor into signaling domains is inhibited in tolerant B cells. J Exp Med 2000, 191:1443-1448.
86. Qu Z., Goldenberg D.M., Cardillo T.M., Shi V., Hansen H.J., Chang C.-H. Bispecific anti-CD20/22 antibodies inhibit B-cell lymphoma proliferation by a unique mechanism of action. Blood 2008, 111:2211-2219.
87. Leprince C., Draves K.E., Geahlen R.L., Ledbetter J.A., Clark E.A. CD22 associates with the human surface IgM-B-cell antigen receptor complex. Proc Natl Acad Sci 1993, 90:3236-3240.
88. Peaker C.J., Neuberger M.S. Association of CD22 with the B cell antigen receptor. Eur J Immunol 1993, 23:1358-1363.
89. Lanoue A., Batista F.D., Stewart M., Neuberger M.S. Interaction of CD22 with α2,6-linked sialoglycoconjugates: innate recognition of self to dampen B cell autoreactivity?. Eur J Immunol 2002, 32:348-355.
90. Collins B.E., Smith B.A., Bengtson P., Paulson J.C. Ablation of CD22 in ligand-deficient mice restores B cell receptor signaling. Nat Immunol 2006, 7:199-206.
91. Zhang M., Varki A. Cell surface sialic acids do not affect primary CD22 interactions with CD45 and surface IgM nor the rate of constitutive CD22 endocytosis. Glycobiology 2004, 14:939-949.
92. Tedder T.F. Introduction: response-regulators of B lymphocyte signaling thresholds provide a context for antigen receptor signal transduction. Semin Immunol 1998, 10:259-265.
93. Tsubata T. Co-receptors on B lymphocytes. Curr Opin Immunol 1999, 11:249-255.
94. Fujimoto M., Sato S. B cell signaling and autoimmune diseases: CD19/CD22 loop as a B cell signaling device to regulate the balance of autoimmunity. J Dermatol Sci 2007, 46:1-9.
95. Carnahan J., Wang P., Kendall R., Chen C., Hu S., Boone T., et al. Epratuzumab, a humanized monoclonal antibody targeting CD22: characterization of in vitro properties. Clin Cancer Res 2003, 9:3982s-3990s.
96. Sieger N., Fleischer S., Mei H., Reiter K., Shock A., Burmester G., et al. CD22 ligation inhibits downstream B cell receptor signaling and Ca2+ flux upon activation. Arthritis Rheum 2013, 65:770-779.
97. Brandl C., Oezgoer L., Woehner M., Shock A., Nitschke L. In vivo effects of epratuzumab, a monoclonal antibody targeting human CD22, on B cell function in human CD22 knock-in (Huki) mice. Arthritis Rheum 2014, S855-S856.
98. Maloney A., Hotson D., Rapecki S., Fossati G., Lumb S., Rosen D., et al. Epratuzumab induces broad inhibition of B cell receptor proximal signaling but has opposing effects on distal signaling in B cell subsets: a profile of effects on functional immune signaling by single cell network profiling. Arthritis Rheum 2014, S1255-S1256.
99. Séïté J.-F., Cornec D., Renaudineau Y., Youinou P., Mageed R.A., Hillion S. IVIg modulates BCR signaling through CD22 and promotes apoptosis in mature human B lymphocytes. Blood 2010, 116:1698-1704.
100. Rossi E.A., Goldenberg D.M., Michel R., Rossi D.L., Wallace D.J., Chang C.-H. Trogocytosis of multiple B-cell surface markers by CD22 targeting with epratuzumab. Blood 2013, 122:3020-3029.
101. Shan D., Press O.W. Constitutive endocytosis and degradation of CD22 by human B cells. J Immunol 1995, 154:4466-4475.
102. O'Reilly M.K., Tian H., Paulson J.C. CD22 is a recycling receptor that can shuttle cargo between the cell surface and endosomal compartments of B cells. J Immunol 2011, 186:1554-1563.
103. Ingle G.S., Scales S.J. DropArray™, a wall-less 96-well plate for uptake and immunofluorescence microscopy, confirms CD22 recycles. Traffic 2014, 15:255-272.
104. Kuroki K., Tsuchiya N., Tsao B., Grossman J., Fukazawa T., Hagiwara K., et al. Polymorphisms of human CD19 gene: possible association with susceptibility to systemic lupus erythematosus in Japanese. Genes Immun 2002, 3:S21-S30.
105. Tedder T.F., Inaoki M., Sato S. The CD19-CD21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity 1997, 6:107-118.
106. Duong B.H., Tian H., Ota T., Completo G., Han S., Vela J.L., et al. Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo. J Exp Med 2010, 207:173-187.
107. Courtney A.H., Puffer E.B., Pontrello J.K., Yang Z.-Q., Kiessling L.L. Sialylated multivalent antigens engage CD22 in trans and inhibit B cell activation. Proc Natl Acad Sci 2009, 106:2500-2505.
108. Smith K.G., Tarlinton D.M., Doody G.M., Hibbs M.L., Fearon D.T. Inhibition of the B cell by CD22: a requirement for Lyn. J Exp Med 1998, 187:807-811.
109. Macauley M.S., Paulson J.C. Siglecs induce tolerance to cell surface antigens by BIM-dependent deletion of the antigen-reactive B cells. J Immunol 2014, 193:4312-4321.
110. Chappell C.P., Clark E.A. STALing B cell responses with CD22. J Clin Invest 2013, 123:2778-2780.
111. Courtney A.H., Bennett N.R., Zwick D.B., Hudon J., Kiessling L.L. Synthetic antigens reveal dynamics of BCR endocytosis during inhibitory signaling. ACS Chem Biol 2014, 9:202-210.
112. Han S., Collins B.E., Bengtson P., Paulson J.C. Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking. Nat Chem Biol 2005, 1:93-97.
113. Pezzutto A., Rabinovitch P., Dörken B., Moldenhauer G., Clark E. Role of the CD22 human B cell antigen in B cell triggering by anti-immunoglobulin. J Immunol 1988, 140:1791-1795.
114. Carnahan J., Stein R., Qu Z., Hess K., Cesano A., Hansen H.J., et al. Epratuzumab, a CD22-targeting recombinant humanized antibody with a different mode of action from rituximab. Mol Immunol 2007, 44:1331-1341.
115. Tuscano J., Engel P., Tedder T., Kehrl J. Engagement of the adhesion receptor CD22 triggers a potent stimulatory signal for B cells and blocking CD22/CD22L interactions impairs T-cell proliferation. Blood 1996, 87:4723-4730.
116. Chaouchi N., Vazquez A., Galanaud P., Leprince C. B cell antigen receptor-mediated apoptosis. Importance of accessory molecules CD19 and CD22, and of surface IgM cross-linking. J Immunol 1995, 154:3096-3104.
117. Chang C.-H., Wang Y., Gupta P., Goldenberg D.M. Extensive crosslinking of CD22 by epratuzumab triggers BCR signaling and caspase-dependent apoptosis in human lymphoma cells. MAbs 2015, 7:199-211.
118. Santos L., Draves K.E., Boton M., Grewal P.K., Marth J.D., Clark E.A. Dendritic cell-dependent inhibition of B cell proliferation requires CD22. J Immunol 2008, 180:4561-4569.
119. Fleischer V., Sieber J., Fleischer S.J., Shock A., Heine G., Daridon C., et al. Epratuzumab inhibits the production of the proinflammatory cytokines IL-6 and TNF-α, but not the regulatory cytokine IL-10, by B cells from healthy donors and SLE patients. Arthritis Res Ther 2015, 17:185.
120. Shock A., Kilgallen B., Koetse W., Stach C., Bongardt S., Galateanu C. Pharmacodynamic effects of the CD22-targeted monoclonal antibody epratuzumab on B cells in patients with systemic lupus erythematosus. Arthritis Rheum 2014, S856.
121. Steinfeld S.D., Tant L., Burmester G.R., Teoh N.K., Wegener W.A., Goldenberg D.M., et al. Epratuzumab (humanized anti-CD22 antibody) in primary Sjogren's syndrome: an open-label phase I/II study. Arthritis Res Ther 2006, 8:R129.
122. Mei H.E., Frölich D., Giesecke C., Loddenkemper C., Reiter K., Schmidt S., et al. Steady-state generation of mucosal IgA+ plasmablasts is not abrogated by B-cell depletion therapy with rituximab. Blood 2010, 116:5181-5190.
123. McCluskey G., McKnight A., Brown D. The ability of epratuzumab to induce cell death in primary human B cells. Ann Rheum Dis 2008, 67:469.
124. Taylor R.P. Gnawing at Metchnikoff's paradigm. Blood 2013, 122:2922-2924.
125. Reddy V., Cambridge G., Isenberg D., Glennie M., Cragg M., Leandro M. Internalization of rituximab and the efficiency of B cell depletion in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Rheum 2015, 10.1002/art.39167.
126. Reichlin A., Hu Y., Meffre E., Nagaoka H., Gong S., Kraus M., et al. B cell development is arrested at the immature B cell stage in mice carrying a mutation in the cytoplasmic domain of immunoglobulin β. J Exp Med 2001, 193:13-24.
127. Kraus M., Saijo K., Torres R.M., Rajewsky K. Ig-α cytoplasmic truncation renders immature B cells more sensitive to antigen contact. Immunity 1999, 11:537-545.
128. Kraus M., Alimzhanov M.B., Rajewsky N., Rajewsky K. Survival of resting mature B lymphocytes depends on BCR signaling via the Igα/β heterodimer. Cell 2004, 117:787-800.
129. Tze L.E., Schram B.R., Lam K.-P., Hogquist K.A., Hippen K.L., Liu J., et al. Basal immunoglobulin signaling actively maintains developmental stage in immature B cells. PLoS Biol 2005, 3:e82.
130. 2+ signaling. Proc Natl Acad Sci 2013, 110:12402-12407.
131. Onodera T., Poe J.C., Tedder T.F., Tsubata T. CD22 regulates time course of both B cell division and antibody response. J Immunol 2008, 180:907-913.
132. Papayannopoulou T. Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood 2004, 103:1580-1585.
133. Hidalgo A., Sanz-Rodríguez F., Rodríguez-Fernández J.L., Albella B., Blaya C., Wright N., et al. Chemokine stromal cell-derived factor-1α modulates VLA-4 integrin-dependent adhesion to fibronectin and VCAM-1 on bone marrow hematopoietic progenitor cells. Exp Hematol 2001, 29:345-355.
134. Allen C.D., Ansel K.M., Low C., Lesley R., Tamamura H., Fujii N., et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol 2004, 5:943-952.
135. Stein J.V., Nombela-Arrieta C. Chemokine control of lymphocyte trafficking: a general overview. Immunology 2005, 116:1-12.
136. Edwards J.C., Cambridge G. B-cell targeting in rheumatoid arthritis and other autoimmune diseases. Nat Rev Immunol 2006, 6(5):394-403.