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PMID: 23074274 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Humans with chronic granulomatous disease maintain humoral immunologic memory despite low frequencies of circulating memory B cells.

Blood ·Vol. 120 ·No. 24 ·2012-12-06 ·Pages 4850-8

Moir S, De Ravin SS, Santich BH, Kim JY, Posada JG, Ho J, Buckner CM, Wang W, Kardava L, Garofalo M, Marciano BE, Manischewitz J, King LR, Khurana S, Chun TW, Golding H, Fauci AS, Malech HL

Abstract

CD27(+) memory B cells are reduced in the blood of patients with chronic granulomatous disease (CGD) for reasons and consequences that remain unclear. Here we confirm not only decreased CD27(+) but also IgG(+) B cells in the blood of CGD patients compared with healthy donors (HDs). However, among IgG(+) B cells, the ratio of CD27(-) to CD27(+) was significantly higher in CGD patients compared with HDs. Similar to conventional memory B cells, CD27(-)IgG(+) B cells of CGD patients expressed activation markers and had undergone somatic hypermutation, albeit at levels lower than their CD27(+) counterparts. Functional analyses revealed slight reductions in frequencies of total IgG but not influenza-specific memory B-cell responses, as measured by Elispot in CGD patients compared with HDs. Serum IgG levels and influenza-specific antibodies were also normal in these CGD patients. Finally, we provide evidence that influenza-specific memory B cells can be present within the CD27(-)IgG(+) B-cell compartment. Together, these findings show that, despite reduced circulating CD27(+) memory B cells, CGD patients maintain an intact humoral immunologic memory, with potential contribution from CD27(-) B cells.

MeSH Terms
Adult B-Lymphocytes/immunology,metabolism Enzyme-Linked Immunospot Assay Female Flow Cytometry Granulomatous Disease, Chronic/blood,genetics,immunology Humans Immunoglobulin G/blood,immunology Immunoglobulin Heavy Chains/genetics,immunology Immunoglobulin Variable Region/genetics,immunology Immunoglobulin kappa-Chains/genetics,immunology Immunoglobulin lambda-Chains/genetics,immunology Immunologic Memory/genetics,immunology Influenza A Virus, H1N1 Subtype/immunology Male Membrane Glycoproteins/genetics,immunology Mutation NADPH Oxidase 2 NADPH Oxidases/genetics,immunology Somatic Hypermutation, Immunoglobulin Tumor Necrosis Factor Receptor Superfamily, Member 7/blood,immunology Young Adult
Chemicals
Immunoglobulin G Immunoglobulin Heavy Chains Immunoglobulin Variable Region Immunoglobulin kappa-Chains Immunoglobulin lambda-Chains Membrane Glycoproteins Tumor Necrosis Factor Receptor Superfamily, Member 7 CYBB protein, human NADPH Oxidase 2 NADPH Oxidases neutrophil cytosolic factor 1
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Moir Susan
Laboratories of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes ofHealth, Bethesda, MD 20892, USA, smoir@niaid.nih.gov
De Ravin Suk See
Santich Brian H
Kim Jin Young
Posada Jacqueline G
Ho Jason
Buckner Clarisa M
Wang Wei
Kardava Lela
Garofalo Mary
Marciano Beatriz E
Manischewitz Jody
King Lisa R
Khurana Surender
Chun Tae-Wook
Golding Hana
Fauci Anthony S
Malech Harry L
References (29)
29 references, click to expand
  1. Regulated expression of BAFF-binding receptors during human B cell differentiation.
    J Immunol. 2007 Dec 1;179(11):7276-86 PMID: 18025170
  2. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy.
    Blood. 2010 Dec 16;116(25):5571-9 PMID: 20837780
  3. Multiple routes to B-cell memory.
    Int Immunol. 2012 Jul;24(7):403-8 PMID: 22451529
  4. Memory B cells: effectors of long-lived immune responses.
    Eur J Immunol. 2009 Aug;39(8):2065-75 PMID: 19637202
  5. Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells.
    J Immunol. 2009 Jan 15;182(2):890-901 PMID: 19124732
  6. Immunoglobulin heavy chain expression shapes the B cell receptor repertoire in human B cell development.
    J Clin Invest. 2001 Sep;108(6):879-86 PMID: 11560957
  7. 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
  8. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system.
    J Immunol Methods. 2004 Mar;286(1-2):111-22 PMID: 15087226
  9. Chronic granulomatous disease: overview and hematopoietic stem cell transplantation.
    J Allergy Clin Immunol. 2011 Jun;127(6):1319-26; quiz 1327-8 PMID: 21497887
  10. The establishment of early B cell tolerance in humans: lessons from primary immunodeficiency diseases.
    Ann N Y Acad Sci. 2011 Dec;1246:1-10 PMID: 22236425
  11. Clinical and laboratory aspects of chronic granulomatous disease in description of eighteen patients.
    Pediatr Allergy Immunol. 2005 Feb;16(1):5-9 PMID: 15693905
  12. Characterization of the human Ig heavy chain antigen binding complementarity determining region 3 using a newly developed software algorithm, JOINSOLVER.
    J Immunol. 2004 Jun 1;172(11):6790-802 PMID: 15153497
  13. Human B cell subsets.
    Adv Immunol. 2008;98:151-224 PMID: 18772006
  14. Chronic granulomatous disease presenting with hypogammaglobulinemia.
    J Investig Allergol Clin Immunol. 2011;21(4):310-2 PMID: 21721378
  15. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus.
    N Engl J Med. 2009 Nov 12;361(20):1945-52 PMID: 19745214
  16. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection.
    J Exp Med. 2011 Jan 17;208(1):181-93 PMID: 21220454
  17. Modern management of chronic granulomatous disease.
    Br J Haematol. 2008 Feb;140(3):255-66 PMID: 18217895
  18. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing.
    Science. 2011 Sep 16;333(6049):1593-602 PMID: 21835983
  19. B cells in HIV infection and disease.
    Nat Rev Immunol. 2009 Apr;9(4):235-45 PMID: 19319142
  20. Reference values for B cell subpopulations from infancy to adulthood.
    Clin Exp Immunol. 2010 Nov;162(2):271-9 PMID: 20854328
  21. The immortality of humoral immunity.
    Immunol Rev. 2010 Jul;236:139-50 PMID: 20636814
  22. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells.
    Proc Natl Acad Sci U S A. 2012 Jun 5;109(23):9047-52 PMID: 22615367
  23. Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways.
    Blood. 2011 Aug 25;118(8):2150-8 PMID: 21690558
  24. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding.
    Science. 2011 Sep 16;333(6049):1633-7 PMID: 21764753
  25. Influenza vaccine immunology.
    Immunol Rev. 2011 Jan;239(1):167-77 PMID: 21198671
  26. Patients with chronic granulomatous disease have a reduced peripheral blood memory B cell compartment.
    J Immunol. 2006 Jun 1;176(11):7096-103 PMID: 16709872
  27. Normal human IgD+IgM- germinal center B cells can express up to 80 mutations in the variable region of their IgD transcripts.
    Immunity. 1996 Jun;4(6):603-13 PMID: 8673707
  28. Circulating human B cells that express surrogate light chains and edited receptors.
    Nat Immunol. 2000 Sep;1(3):207-13 PMID: 10973277
  29. A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation.
    J Immunol. 2006 Sep 15;177(6):3728-36 PMID: 16951333
Article Info
Journal
Blood
Abbr.
Blood
ISSN
1528-0020
Published
2012-12-06
Epub
2012-00-16
Pages
4850-8
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC3520621
Subset
IM
Grants
Intramural NIH HHS · United States
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