Targeting CD22 reprograms b-cells and reverses autoimmune diabetes

Diabetes

Volumn 57, Issue 11, 2008, Pages 3013-3024

  Fiorina, Paolo ^a,b   Vergani, Andrea ^a,b   Dada, Shirine ^a   Jurewicz, Mollie ^a   Wong, Masie ^a   Law, Kenneth ^c   Wu, Erxi ^d   Tian, Ze ^d   Abdi, Reza ^a   Guleria, Indira ^a   Rodig, Scott ^c   Dunussi Joannopoulos, Kyri ^e   Bluestone, Jeffrey ^f   Sayegh, Mohamed H ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^e PFIZER INC   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD22 ANTIGEN; GLUCOSE; INOTUZUMAB OZOGAMICIN; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ANIMAL; CYTOLOGY; DRUG EFFECT; IMMUNOLOGY; IMPAIRED GLUCOSE TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; NONOBESE DIABETIC MOUSE; PANCREAS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD22; ANTIGENS, CD4; B-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPH NODES; MICE; MICE, INBRED NOD; PANCREAS; PREDIABETIC STATE;

EID: 58149359257     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db08-0420     Document Type: Article

References (48)

1. Noorchashm H, Reed AJ, Rostami SY, Mozaffari R, Zekavat G, Koeberlein B, Caton AJ, Naji A: B cell-mediated antigen presentation is required for the pathogenesis of acute cardiac allograft rejection. J Immunol 177:7715-7722, 2006
2. Wong FS, Wen L, Tang M, Ramanathan M, Visintin I, Daugherty J, Hannum LG, Janeway CA Jr, Shlomchik MJ: Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes 53:2581-2587, 2004
3. Serreze DV, Chapman HD, Varnum DS, Hanson MS, Reifsnyder PC, Richard SD, Fleming SA, Leiter EH, Shultz LD: B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J Exp Med 184:2049-2053, 1996
4. Serreze DV, Fleming SA, Chapman HD, Richard SD, Leiter EH, Tisch RM: B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol 161:3912-3918, 1998
5. Atkinson MA, Eisenbarth GS: Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 358:221-229, 2001
6. Todd JA, Wicker LS: Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity 15:387-395, 2001
7. Larsson K, Elding-Larsson H, Cederwall E, Kockum K, Neiderud J, Sjoblad S, Lindberg B, Lernmark B, Cilio C, Ivarsson SA, Lernmark A: Genetic and perinatal factors as risk for childhood type 1 diabetes. Diabete Metab Res Rev 20:429-437, 2004
8. Hu CY, Rodriguez-Pinto D, Du W, Ahuja A, Henegariu O, Wong FS, Shlomchik MJ, Wen L: Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest 117:3857-3867, 2007
9. O'Neill SK, Shlomchik MJ, Glant TT, Cao Y, Doodes PD, Finnegan A: Antigen-specific B cells are required as APCs and autoantibody-producing cells for induction of severe autoimmune arthritis. J Immunol 174:3781-3788, 2005
10. Pearson T, Markees TG, Serreze DV, Pierce MA, Wicker LS, Peterson LB, Shultz LD, Mordes JP, Rossini AA, Greiner DL: Islet cell autoimmunity and transplantation tolerance: two distinct mechanisms? Ann N Y Acad Sci 1005:148-156, 2003
11. Serreze DV, Silveira PA: The role of B lymphocytes as key antigen- presenting cells in the development of T cell-mediated autoimmune type 1 diabetes. Curr Dir Autoimmun 6:212-227, 2003
12. Wasserfall CH, Atkinson MA: Autoantibody markers for the diagnosis and prediction of type 1 diabetes. Autoimmun Rev 5:424 -428, 2006
13. Dunussi-Joannopoulos K, Hancock GE, Kunz A, Hegen M, Zhou XX, Sheppard BJ, Lamothe J, Li E, Ma HL, Hamann PR, Damle NK, Collins M: B-cell depletion inhibits arthritis in a collagen-induced arthritis (CIA) model, but does not adversely affect humoral responses in a respiratory syncytial virus (RSV) vaccination model. Blood 106:2235-2243, 2005
14. Robak T: Monoclonal antibodies in the treatment of autoimmune cytope- nias. Eur J Haematol 72:79-88, 2004
15. Rastetter W, Molina A, White CA: Rituximab: expanding role in therapy for lymphomas and autoimmune diseases. Annu Rev Med 55:477-503, 2004
16. Au WY, Ma ES, Choy C, Chung LP, Fung TK, Liang R, Kwong YL: Therapy-related lymphomas in patients with autoimmune diseases after treatment with disease-modifying anti-rheumatic drugs. Am J Hematol 81:5-11, 2006
17. Schollkopf C, Kjeldsen L, Bjerrum OW, Mourits-Andersen HT, Nielsen JL, Christensen BE, Jensen BA, Pedersen BB, Taaning EB, Klausen TW, Birgens H: Rituximab in chronic cold agglutinin disease: a prospective study of 20 patients. Leuk Lymphoma 47:253-260, 2006
18. Regazzi MB, Iacona I, Avanzini MA, Arcaini L, Merlini G, Perfetti V, Zaja F, Montagna M, Morra E, Lazzarino M: Pharmacokinetic behavior of ritux- imab: a study of different schedules of administration for heterogeneous clinical settings. Ther Drug Monit 27:785-792, 2005
19. Trelinski J, Chojnowski K, Kurenko-Deptuch M, Kasznicki M, Bernatowska E, Robak T: Successful treatment of refractory autoimmune thrombocy- topenia with rituximab and cyclosporin A in a patient with chronic granulomatous disease. Ann Hematol 84:835-836, 2005
20. Sfikakis PP, Boletis JN, Tsokos GC: Rituximab anti-B-cell therapy in systemic lupus erythematosus: pointing to the future. Curr Opin Rheumatol 17:550-557, 2005
21. TrialNet Study: Further research to prevent and treat type 1. Diabetes Forecast 57:77-79, 2004
22. Skyler JS: Prediction and prevention of type 1 diabetes: progress, problems, and prospects. Clin Pharmacol Ther 81:768-771, 2007
23. Arif S, Tree TI, Astill TP, Tremble JM, Bishop AJ, Dayan CM, Roep BO, Peakman M: Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J Clin Invest 113:451-463, 2004
24. Katz JD, Wang B, Haskins K, Benoist C, Mathis D: Following a diabetogenic T cell from genesis through pathogenesis. Cell 74:1089-1100, 1993
25. Masteller EL, Warner MR, Tang Q, Tarbell KV, McDevitt H, Bluestone JA: Expansion of functional endogenous antigen-specific CD4+CD25+ regulatory T cells from nonobese diabetic mice. J Immunol 175:3053-3059, 2005
26. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P, Santamaria P, Locksley RM, Krummel MF, Bluestone JA: Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 7:83-92, 2006
27. Gao JL, Guillabert A, Hu J, Le Y, Urizar E, Seligman E, Fang KJ, Yuan X, Imbault V, Communi D, Wang JM, Parmentier M, Murphy PM, Migeotte I: F2L, a peptide derived from heme-binding protein, chemoattracts mouse neutrophils by specifically activating Fpr2, the low-affinity N-formylpeptide receptor. J Immunol 178:1450-1456, 2007
28. Shiratori I, Ogasawara K, Saito T, Lanier LL, Arase H: Activation of natural killer cells and dendritic cells upon recognition of a novel CD99-like ligand by paired immunoglobulin-like type 2 receptor. J Exp Med 199:525-533, 2004
29. Szatmari I, Rajnavolgyi E, Nagy L: PPARgamma, a lipid-activated transcription factor as a regulator of dendritic cell function. Ann N Y Acad Sci 1088:207-218, 2006
30. Merrell KT, Benschop RJ, Gauld SB, Aviszus K, Decote-Ricardo D, Wysocki LJ, Cambier JC: Identification of anergic B cells within a wild-type repertoire. Immunity 25:953-962, 2006
31. Xiu Y, Wong CP, Bouaziz JD, Hamaguchi Y, Wang Y, Pop SM, Tisch RM, Tedder TF: B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in Fc{gamma}R effector functions. J Immunol 180:2863-2875, 2008
32. Edwards JC, Cambridge G: B-cell targeting in rheumatoid arthritis and other autoimmune diseases. Nat Rev Immunol 6:394-403, 2006
33. Atzeni F, Doria A, Maurizio T, Sarzi-Puttini P: What is the role of rituximab in the treatment of rheumatoid arthritis? Autoimmun Rev 6:553-558, 2007
34. Schroder C, Azimzadeh AM, Wu G, Price JO, Atkinson JB, Pierson RN: Anti-CD20 treatment depletes B-cells in blood and lymphatic tissue of cynomolgus monkeys. Transpl Immunol 12:19-28, 2003
35. Genberg H, Hansson A, Wernerson A, Wennberg L, Tyden G: Pharmaco- dynamics of rituximab in kidney transplantation. Transplantation 84:S33-S36, 2007
36. Sabahi R, Anolik JH: B-cell-targeted therapy for systemic lupus erythem-atosus. Drugs 66:1933-1948, 2006
37. Nitschke L, Tsubata T: Molecular interactions regulate BCR signal inhibition by CD22 and CD72. Trends Immunol 25:543-550, 2004
38. Steinfeld SD, Youinou P: Epratuzumab (humanised anti-CD22 antibody) in autoimmune diseases. Expert Opin Biol Ther 6:943-949, 2006
39. Coleman M, Goldenberg DM, Siegel AB, Ketas JC, Ashe M, Fiore JM, Leonard JP: Epratuzumab: targeting B-cell malignancies through CD22. Clin Cancer Res 9:3991S-3994S, 2003
40. Anderson MS, Bluestone JA: The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 23:447-485, 2005
41. Atkinson MA, Leiter EH: The NOD mouse model of type 1 diabetes: as good as it gets? Nat Med 5:601-604, 1999
42. Ogasawara K, Hamerman JA, Ehrlich LR, Bour-Jordan H, Santamaria P, Bluestone JA, Lanier LL: NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 20:757-767, 2004
43. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L: TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 9:1202-1208, 2003
44. Kodama S, Kuhtreiber W, Fujimura S, Dale EA, Faustman DL: Islet regeneration during the reversal of autoimmune diabetes in NOD mice. Science 302:1223-1227, 2003
45. Chong AS, Shen J, Tao J, Yin D, Kuznetsov A, Hara M, Philipson LH: Reversal of diabetes in non-obese diabetic mice without spleen cell- derived beta cell regeneration. Science 311:1774-1775, 2006
46. Tarbell KV, Petit L, Zuo X, Toy P, Luo X, Mqadmi A, Yang H, Suthanthiran M, Mojsov S, Steinman RM: Dendritic cell-expanded, islet-specific CD4 + CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 204:191-201, 2007
47. Herold KC, Hagopian W, Auger JA, Poumian-Ruiz E, Taylor L, Donaldson D, Gitelman SE, Harlan DM, Xu D, Zivin RA, Bluestone JA: Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. NEngl J Med 346:1692-1698, 2002
48. Chatenoud L, Thervet E, Primo J, Bach JF: Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc Natl Acad SciUSA91:123-127, 1994