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PMID: 22426210 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Rituximab induces sustained reduction of pathogenic B cells in patients with peripheral nervous system autoimmunity.

The Journal of clinical investigation ·Vol. 122 ·No. 4 ·2012-04-00 ·Pages 1393-402

Maurer MA, Rakocevic G, Leung CS, Quast I, Lukačišin M, Goebels N, Münz C, Wardemann H, Dalakas M, Lünemann JD

Abstract

The B cell-depleting IgG1 monoclonal antibody rituximab can persistently suppress disease progression in some patients with autoimmune diseases. However, the mechanism underlying these long-term beneficial effects has remained unclear. Here, we evaluated Ig gene usage in patients with anti-myelin-associated glycoprotein (anti-MAG) neuropathy, an autoimmune disease of the peripheral nervous system that is mediated by IgM autoantibodies binding to MAG antigen. Patients with anti-MAG neuropathy showed substantial clonal expansions of blood IgM memory B cells that recognized MAG antigen. The group of patients showing no clinical improvement after rituximab therapy were distinguished from clinical responders by a higher load of clonal IgM memory B cell expansions before and after therapy, by persistence of clonal expansions despite efficient peripheral B cell depletion, and by a lack of substantial changes in somatic hypermutation frequencies of IgM memory B cells. We infer from these data that the effectiveness of rituximab therapy depends on efficient depletion of noncirculating B cells and is associated with qualitative immunological changes that indicate reconfiguration of B cell memory through sustained reduction of autoreactive clonal expansions. These findings support the continued development of B cell-depleting therapies for autoimmune diseases.

MeSH Terms
Aged Antibodies, Monoclonal, Murine-Derived/pharmacology Autoantibodies/immunology Autoantigens/immunology Autoimmune Diseases of the Nervous System/drug therapy,immunology B-Lymphocyte Subsets/drug effects Clinical Trials as Topic/statistics & numerical data Clone Cells/immunology Double-Blind Method Female Humans Immunoglobulin M/immunology Immunologic Memory Lymphocyte Depletion/methods Male Middle Aged Myelin-Associated Glycoprotein/immunology Rituximab Severity of Illness Index Somatic Hypermutation, Immunoglobulin Treatment Outcome
Chemicals
Antibodies, Monoclonal, Murine-Derived Autoantibodies Autoantigens Immunoglobulin M Myelin-Associated Glycoprotein Rituximab
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Maurer Michael A
Institute of Experimental Immunology, Department of Neuroinflammation, University of Zürich, Zürich, Switzerland.
Rakocevic Goran
Leung Carol S
Quast Isaak
Lukačišin Martin
Goebels Norbert
Münz Christian
Wardemann Hedda
Dalakas Marinos
Lünemann Jan D
References (38)
38 references, click to expand
  1. Multiple sclerosis: brain-infiltrating CD8+ T cells persist as clonal expansions in the cerebrospinal fluid and blood.
    Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2428-33 PMID: 14983026
  2. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets.
    Nat Med. 2000 Apr;6(4):443-6 PMID: 10742152
  3. Induction of experimental ataxic sensory neuronopathy in cats by immunization with purified SGPG.
    J Neuroimmunol. 2008 Jan;193(1-2):87-93 PMID: 18037501
  4. High-dose rituximab and anti-MAG-associated polyneuropathy.
    Neurology. 2006 Mar 14;66(5):742-4 PMID: 16534115
  5. Polyneuropathy and IgM monoclonal gammopathy: studies on the pathogenetic role of anti-myelin-associated glycoprotein antibody.
    Ann Neurol. 1985 Mar;17(3):243-54 PMID: 2581496
  6. Anti-myelin-associated glycoprotein neuropathy.
    Curr Opin Neurol. 2006 Oct;19(5):458-63 PMID: 16969155
  7. Mechanisms of killing by anti-CD20 monoclonal antibodies.
    Mol Immunol. 2007 Sep;44(16):3823-37 PMID: 17768100
  8. Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response.
    Ann Rheum Dis. 2008 Jul;67(7):917-25 PMID: 17965121
  9. Clonal dissection of the human memory B-cell repertoire following infection and vaccination.
    Eur J Immunol. 2009 May;39(5):1260-70 PMID: 19404981
  10. Predictors of response to rituximab in patients with neuropathy and anti-myelin associated glycoprotein immunoglobulin M.
    J Peripher Nerv Syst. 2007 Jun;12(2):102-7 PMID: 17565535
  11. Pathogenesis and Treatment of Anti-MAG Neuropathy.
    Curr Treat Options Neurol. 2010 Mar;12(2):71-83 PMID: 20842571
  12. Bone marrow B-lineage cells in patients with rheumatoid arthritis following rituximab therapy.
    Rheumatology (Oxford). 2007 Jan;46(1):29-36 PMID: 16735454
  13. Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand.
    Nat Med. 2000 Oct;6(10):1167-75 PMID: 11017150
  14. IgM in a human neuropathy related to paraproteinemia binds to a carbohydrate determinant in the myelin-associated glycoprotein and to a ganglioside.
    Proc Natl Acad Sci U S A. 1984 Feb;81(4):1225-9 PMID: 6199795
  15. Defective B cell tolerance checkpoints in systemic lupus erythematosus.
    J Exp Med. 2005 Mar 7;201(5):703-11 PMID: 15738055
  16. Randomized controlled trial of intravenous immunoglobulin versus oral prednisolone in chronic inflammatory demyelinating polyradiculoneuropathy.
    Ann Neurol. 2001 Aug;50(2):195-201 PMID: 11506402
  17. Placebo-controlled trial of rituximab in IgM anti-myelin-associated glycoprotein antibody demyelinating neuropathy.
    Ann Neurol. 2009 Mar;65(3):286-93 PMID: 19334068
  18. Demyelination induced by intraneural injection of human antimyelin-associated glycoprotein antibodies.
    Muscle Nerve. 1988 Nov;11(11):1169-76 PMID: 2465494
  19. Predominant autoantibody production by early human B cell precursors.
    Science. 2003 Sep 5;301(5638):1374-7 PMID: 12920303
  20. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis.
    Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W503-8 PMID: 18503082
  21. Intravenous immune globulin (10% caprylate-chromatography purified) for the treatment of chronic inflammatory demyelinating polyradiculoneuropathy (ICE study): a randomised placebo-controlled trial.
    Lancet Neurol. 2008 Feb;7(2):136-44 PMID: 18178525
  22. B-cell targeting in rheumatoid arthritis and other autoimmune diseases.
    Nat Rev Immunol. 2006 May;6(5):394-403 PMID: 16622478
  23. Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20.
    Blood. 1994 Jan 15;83(2):435-45 PMID: 7506951
  24. ExPASy: The proteomics server for in-depth protein knowledge and analysis.
    Nucleic Acids Res. 2003 Jul 1;31(13):3784-8 PMID: 12824418
  25. Gene-expression profiling of Waldenstrom macroglobulinemia reveals a phenotype more similar to chronic lymphocytic leukemia than multiple myeloma.
    Blood. 2006 Oct 15;108(8):2755-63 PMID: 16804116
  26. Clonotypic IgM V/D/J sequence analysis in Waldenstrom macroglobulinemia suggests an unusual B-cell origin and an expansion of polyclonal B cells in peripheral blood.
    Blood. 2004 Oct 1;104(7):2134-42 PMID: 14764523
  27. B-cell-directed therapies for autoimmune disease.
    Nat Rev Rheumatol. 2009 Aug;5(8):433-41 PMID: 19581902
  28. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning.
    J Immunol Methods. 2008 Jan 1;329(1-2):112-24 PMID: 17996249
  29. Switched memory B cells maintain specific memory independently of serum antibodies: the hepatitis B example.
    Eur J Immunol. 2011 Jun;41(6):1800-8 PMID: 21469123
  30. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences.
    Cold Spring Harb Protoc. 2011 Jun 01;2011(6):695-715 PMID: 21632778
  31. Experimental paraprotein neuropathy, demyelination by passive transfer of human IgM anti-myelin-associated glycoprotein.
    Ann Neurol. 1993 May;33(5):502-6 PMID: 7684583
  32. Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment.
    Arthritis Rheum. 2007 Dec;56(12):3909-18 PMID: 18050222
  33. Expanded T cells from pancreatic lymph nodes of type 1 diabetic subjects recognize an insulin epitope.
    Nature. 2005 May 12;435(7039):224-8 PMID: 15889096
  34. The human spleen is a major reservoir for long-lived vaccinia virus-specific memory B cells.
    Blood. 2008 May 1;111(9):4653-9 PMID: 18316630
  35. IgM antibody-related polyneuropathies: B-cell depletion chemotherapy using Rituximab.
    Neurology. 1999 May 12;52(8):1701-4 PMID: 10331706
  36. Pathogenesis and therapy of neuropathies associated with monoclonal gammopathies.
    Ann Neurol. 1995 May;37 Suppl 1:S32-42 PMID: 8968215
  37. Long-term effect of rituximab in anti-mag polyneuropathy.
    Neurology. 2008 Nov 18;71(21):1742-4 PMID: 19015493
  38. 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 May 15;178(10):6624-33 PMID: 17475894
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
1558-8238
Published
2012-04-00
Epub
2012-00-19
Pages
1393-402
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC3314454
Subset
IM
Grants
NCI NIH HHS · R01 CA108609 · United States
NCI NIH HHS · R01CA108609 · United States
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