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Article ; Online: Functions of IgM fc receptor (FcµR) related to autoimmunity.

Kubagawa, Hiromi / Mahmoudi Aliabadi, Pedram / Al-Qaisi, Khlowd / Jani, Peter K / Honjo, Kazuhito / Izui, Shozo / Radbruch, Andreas / Melchers, Fritz

Autoimmunity

2024 Volume 57, Issue 1, Page(s) 2323563

Abstract: Unlike Fc receptors for switched immunoglobulin (Ig) isotypes, Fc receptor for IgM (FcµR) is selectively expressed by lymphocytes. The ablation of the FcµR gene in mice impairs B cell tolerance as evidenced by concomitant production of autoantibodies of ... ...

Abstract	Unlike Fc receptors for switched immunoglobulin (Ig) isotypes, Fc receptor for IgM (FcµR) is selectively expressed by lymphocytes. The ablation of the FcµR gene in mice impairs B cell tolerance as evidenced by concomitant production of autoantibodies of IgM and IgG isotypes. In this essay, we reiterate the autoimmune phenotypes observed in mutant mice, ie IgM homeostasis, dysregulated humoral immune responses including autoantibodies, and Mott cell formation. We also propose the potential phenotypes in individuals with
MeSH term(s)	Mice ; Animals ; Autoimmunity ; Receptors, Fc/genetics ; Autoantibodies ; Immunoglobulin M
Chemical Substances	immunoglobulin M receptor ; Receptors, Fc ; Autoantibodies ; Immunoglobulin M
Language	English
Publishing date	2024-03-11
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1025450-x
ISSN	1607-842X ; 0891-6934
ISSN (online)	1607-842X
ISSN	0891-6934
DOI	10.1080/08916934.2024.2323563
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Article ; Online: FCRL1 immunoregulation in B cell development and malignancy.

Mamidi, Murali K / Huang, Jifeng / Honjo, Kazuhito / Li, Ran / Tabengwa, Edlue M / Neeli, Indira / Randall, Nar'asha L / Ponnuchetty, Manasa V / Radic, Marko / Leu, Chuen-Miin / Davis, Randall S

Frontiers in immunology

2023 Volume 14, Page(s) 1251127

Abstract: Immunotherapeutic targeting of surface regulatory proteins and pharmacologic inhibition of critical signaling pathways has dramatically shifted our approach to the care of individuals with B cell malignancies. This evolution in therapy reflects the ... ...

Abstract	Immunotherapeutic targeting of surface regulatory proteins and pharmacologic inhibition of critical signaling pathways has dramatically shifted our approach to the care of individuals with B cell malignancies. This evolution in therapy reflects the central role of the B cell receptor (BCR) signaling complex and its co-receptors in the pathogenesis of B lineage leukemias and lymphomas. Members of the Fc receptor-like gene family (
MeSH term(s)	Animals ; Mice ; Humans ; Neoplasms/metabolism ; B-Lymphocytes/metabolism ; Receptors, Fc/genetics ; Receptors, Fc/metabolism ; Receptors, Cell Surface/metabolism ; Lymphoma/metabolism ; Membrane Proteins/metabolism
Chemical Substances	Receptors, Fc ; Receptors, Cell Surface ; FCRL1 protein, human ; Membrane Proteins
Language	English
Publishing date	2023-09-25
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1251127
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Article ; Online: Enhanced Mott cell formation linked with IgM Fc receptor (FcμR) deficiency.

Mahmoudi Aliabadi, Pedram / Al-Qaisi, Khlowd / Jani, Peter K / Honjo, Kazuhito / Klemm, Uwe / Lee, Kyeong-Hee / Baumgarth, Nicole / Radbruch, Andreas / Melchers, Fritz / Kubagawa, Hiromi

European journal of immunology

2023 Volume 53, Issue 7, Page(s) e2250315

Abstract: In previous studies, Mott cells, an unusual form of plasma cells containing Ig-inclusion bodies, were frequently observed in peripheral lymphoid tissues in our IgM Fc receptor (FcμR)-deficient (KO) mouse strain. Because of discrepancies in the reported ... ...

Abstract	In previous studies, Mott cells, an unusual form of plasma cells containing Ig-inclusion bodies, were frequently observed in peripheral lymphoid tissues in our IgM Fc receptor (FcμR)-deficient (KO) mouse strain. Because of discrepancies in the reported phenotypes of different Fcmr KO mouse strains, we here examined two additional available mutant strains and confirmed that such enhanced Mott-cell formation was a general phenomenon associated with FcμR deficiency. Splenic B cells from Fcmr KO mice clearly generated more Mott cells than those from WT mice when stimulated in vitro with LPS alone or a B-1, but not B-2, activation cocktail. Nucleotide sequence analysis of the Ig variable regions of a single IgMλ
MeSH term(s)	Animals ; Mice ; Receptors, Fc/genetics ; B-Lymphocytes/metabolism ; Plasma Cells/metabolism ; Immunoglobulin M/genetics ; Immunoglobulin M/metabolism
Chemical Substances	immunoglobulin M receptor ; Receptors, Fc ; Immunoglobulin M
Language	English
Publishing date	2023-05-11
Publishing country	Germany
Document type	Journal Article
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.202250315
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Article ; Online: Comprehensive mapping of SARS-CoV-2 peptide epitopes for development of a highly sensitive serological test for total and neutralizing antibodies.

Kumar, Garima / Sterrett, Sarah / Hall, Lucinda / Tabengwa, Edlue / Honjo, Kazuhito / Larimer, Michael / Davis, Randall S / Goepfert, Paul A / Larimer, Benjamin M

Protein engineering, design & selection : PEDS

2022 Volume 35

Abstract: Quantification of the anti-SARS-CoV-2 antibody response has proven to be a prominent diagnostic tool during the COVID-19 pandemic. Antibody measurements have aided in the determination of humoral protection following infection or vaccination and will ... ...

Abstract	Quantification of the anti-SARS-CoV-2 antibody response has proven to be a prominent diagnostic tool during the COVID-19 pandemic. Antibody measurements have aided in the determination of humoral protection following infection or vaccination and will likely be essential for predicting the prevalence of population level immunity over the next several years. Despite widespread use, current tests remain limited in part, because antibody capture is accomplished through the use of complete spike and nucleocapsid proteins that contain significant regions of overlap with common circulating coronaviruses. To address this limitation, a unique epitope display platform utilizing monovalent display and protease-driven capture of peptide epitopes was used to select high affinity peptides. A single round of selection using this strategy with COVID-19 positive patient plasma samples revealed surprising differences and specific patterns in the antigenicity of SARS-CoV-2 proteins, especially the spike protein. Putative epitopes were assayed for specificity with convalescent and control samples, and the individual binding kinetics of peptides were also determined. A subset of prioritized peptides was used to develop an antibody diagnostic assay that showed low cross reactivity while detecting 37% more positive antibody cases than a gold standard FDA EUA test. Finally, a subset of peptides were compared with serum neutralization activity to establish a 2 peptide assay that strongly correlates with neutralization. Together, these data demonstrate a novel phage display method that is capable of comprehensively and rapidly mapping patient viral antibody responses and selecting high affinity public epitopes for the diagnosis of humoral immunity.
MeSH term(s)	Antibodies, Neutralizing ; Antibodies, Viral ; COVID-19 ; Epitopes ; Humans ; Pandemics ; Peptides ; SARS-CoV-2 ; Serologic Tests ; Spike Glycoprotein, Coronavirus
Chemical Substances	Antibodies, Neutralizing ; Antibodies, Viral ; Epitopes ; Peptides ; Spike Glycoprotein, Coronavirus
Language	English
Publishing date	2022-03-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1466729-0
ISSN	1741-0134 ; 1741-0126
ISSN (online)	1741-0134
ISSN	1741-0126
DOI	10.1093/protein/gzab033
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Article ; Online: Questioning whether IgM Fc receptor (FcµR) is expressed by innate immune cells.

Skopnik, Christopher M / Riedel, René / Addo, Richard K / Heinz, Gitta Anne / Heinrich, Frederik / Honjo, Kazuhito / Durek, Pawel / Enghard, Philipp / Mashreghi, Mir-Farzin / Radbruch, Andreas / Kubagawa, Hiromi

Nature communications

2022 Volume 13, Issue 1, Page(s) 3951

MeSH term(s)	Immunity, Innate ; Immunoglobulin M ; Receptors, Fc
Chemical Substances	Immunoglobulin M ; Receptors, Fc ; immunoglobulin M receptor
Language	English
Publishing date	2022-07-11
Publishing country	England
Document type	Letter ; Research Support, Non-U.S. Gov't ; Comment
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-29407-0
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Article ; Online: Fc receptor-like 2 (FCRL2) is a novel marker of low-risk CLL and refines prognostication based on IGHV mutation status.

Shea, Lauren K / Honjo, Kazuhito / Redden, David T / Tabengwa, Edlue / Li, Ran / Li, Fu-Jun / Shakhmatov, Mikhail / Chiorazzi, Nicholas / Davis, Randall S

Blood cancer journal

2019 Volume 9, Issue 6, Page(s) 47

MeSH term(s)	Adult ; Aged ; Aged, 80 and over ; Biomarkers, Tumor ; Female ; Gene Expression Regulation, Leukemic ; Humans ; Immunoglobulin Heavy Chains/genetics ; Immunophenotyping ; Leukemia, Lymphocytic, Chronic, B-Cell/diagnosis ; Leukemia, Lymphocytic, Chronic, B-Cell/genetics ; Leukemia, Lymphocytic, Chronic, B-Cell/mortality ; Male ; Middle Aged ; Mutation ; Prognosis ; Receptors, Cell Surface/genetics
Chemical Substances	Biomarkers, Tumor ; FCRL2 protein, human ; Immunoglobulin Heavy Chains ; Receptors, Cell Surface
Language	English
Publishing date	2019-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2600560-8
ISSN	2044-5385 ; 2044-5385
ISSN (online)	2044-5385
ISSN	2044-5385
DOI	10.1038/s41408-019-0207-7
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Article ; Online: Is Toso/IgM Fc receptor (FcμR) expressed by innate immune cells?

Honjo, Kazuhito / Kubagawa, Yoshiki / Kubagawa, Hiromi

Proceedings of the National Academy of Sciences of the United States of America

2013 Volume 110, Issue 28, Page(s) E2540–1

MeSH term(s)	Animals ; Carrier Proteins/immunology ; Granulocytes/immunology ; Immunity, Innate/immunology ; Listeriosis/immunology ; Macrophage Activation/immunology ; Membrane Proteins/immunology ; Monocytes/immunology
Chemical Substances	Carrier Proteins ; Membrane Proteins
Language	English
Publishing date	2013-05-13
Publishing country	United States
Document type	Letter ; Comment
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1304904110
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Article ; Online: Differences between Human and Mouse IgM Fc Receptor (FcµR).

Kubagawa, Hiromi / Skopnik, Christopher M / Al-Qaisi, Khlowd / Calvert, Rosaleen A / Honjo, Kazuhito / Kubagawa, Yoshiki / Teuber, Ruth / Aliabadi, Pedram Mahmoudi / Enghard, Philipp / Radbruch, Andreas / Sutton, Brian J

International journal of molecular sciences

2021 Volume 22, Issue 13

Abstract: Both non-immune "natural" and antigen-induced "immune" IgM are important for protection against pathogens and for regulation of immune responses to self-antigens. Since the bona fide IgM Fc receptor (FcµR) was identified in humans by a functional cloning ...

Abstract	Both non-immune "natural" and antigen-induced "immune" IgM are important for protection against pathogens and for regulation of immune responses to self-antigens. Since the bona fide IgM Fc receptor (FcµR) was identified in humans by a functional cloning strategy in 2009, the roles of FcµR in these IgM effector functions have begun to be explored. In this short essay, we describe the differences between human and mouse FcµRs in terms of their identification processes, cellular distributions and ligand binding activities with emphasis on our recent findings from the mutational analysis of human FcµR. We have identified at least three sites of human FcµR, i.e., Asn66 in the CDR2, Lys79 to Arg83 in the DE loop and Asn109 in the CDR3, responsible for its constitutive IgM-ligand binding. Results of computational structural modeling analysis are consistent with these mutational data and a model of the ligand binding, Ig-like domain of human FcµR is proposed. Serendipitously, substitution of Glu41 and Met42 in the CDR1 of human FcµR with mouse equivalents Gln and Leu, either single or more prominently in combination, enhances both the receptor expression and IgM binding. These findings would help in the future development of preventive and therapeutic interventions targeting FcµR.
Language	English
Publishing date	2021-06-29
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms22137024
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Article ; Online: Exposure of progressive immune dysfunction by SARS-CoV-2 mRNA vaccination in patients with chronic lymphocytic leukemia: A prospective cohort study.

PLoS medicine

2023 Volume 20, Issue 6, Page(s) e1004157

Abstract: Background: Patients with chronic lymphocytic leukemia (CLL) have reduced seroconversion rates and lower binding antibody (Ab) and neutralizing antibody (NAb) titers than healthy individuals following Severe Acute Respiratory Syndrome Coronavirus 2 ( ... ...

Abstract	Background: Patients with chronic lymphocytic leukemia (CLL) have reduced seroconversion rates and lower binding antibody (Ab) and neutralizing antibody (NAb) titers than healthy individuals following Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) mRNA vaccination. Here, we dissected vaccine-mediated humoral and cellular responses to understand the mechanisms underlying CLL-induced immune dysfunction. Methods and findings: We performed a prospective observational study in SARS-CoV-2 infection-naïve CLL patients (n = 95) and healthy controls (n = 30) who were vaccinated between December 2020 and June 2021. Sixty-one CLL patients and 27 healthy controls received 2 doses of the Pfizer-BioNTech BNT162b2 vaccine, while 34 CLL patients and 3 healthy controls received 2 doses of the Moderna mRNA-1273 vaccine. The median time to analysis was 38 days (IQR, 27 to 83) for CLL patients and 36 days (IQR, 28 to 57) for healthy controls. Testing plasma samples for SARS-CoV-2 anti-spike and receptor-binding domain Abs by enzyme-linked immunosorbent assay (ELISA), we found that all healthy controls seroconverted to both antigens, while CLL patients had lower response rates (68% and 54%) as well as lower median titers (23-fold and 30-fold; both p < 0.001). Similarly, NAb responses against the then prevalent D614G and Delta SARS-CoV-2 variants were detected in 97% and 93% of controls, respectively, but in only 42% and 38% of CLL patients, who also exhibited >23-fold and >17-fold lower median NAb titers (both p < 0.001). Interestingly, 26% of CLL patients failed to develop NAbs but had high-titer binding Abs that preferentially reacted with the S2 subunit of the SARS-CoV-2 spike. Since these patients were also seropositive for endemic human coronaviruses (HCoVs), these responses likely reflect cross-reactive HCoV Abs rather than vaccine-induced de novo responses. CLL disease status, advanced Rai stage (III-IV), elevated serum beta-2 microglobulin levels (β2m >2.4 mg/L), prior therapy, anti-CD20 immunotherapy (<12 months), and intravenous immunoglobulin (IVIg) prophylaxis were all predictive of an inability to mount SARS-CoV-2 NAbs (all p ≤ 0.03). T cell response rates determined for a subset of participants were 2.8-fold lower for CLL patients compared to healthy controls (0.05, 95% CI 0.01 to 0.27, p < 0.001), with reduced intracellular IFNγ staining (p = 0.03) and effector polyfunctionality (p < 0.001) observed in CD4+ but not in CD8+ T cells. Surprisingly, in treatment-naïve CLL patients, BNT162b2 vaccination was identified as an independent negative risk factor for NAb generation (5.8, 95% CI 1.6 to 27, p = 0.006). CLL patients who received mRNA-1273 had 12-fold higher (p < 0.001) NAb titers and 1.7-fold higher (6.5, 95% CI 1.3 to 32, p = 0.02) response rates than BNT162b2 vaccinees despite similar disease characteristics. The absence of detectable NAbs in CLL patients was associated with reduced naïve CD4+ T cells (p = 0.03) and increased CD8+ effector memory T cells (p = 0.006). Limitations of the study were that not all participants were subjected to the same immune analyses and that pre-vaccination samples were not available. Conclusions: CLL pathogenesis is characterized by a progressive loss of adaptive immune functions, including in most treatment-naïve patients, with preexisting memory being preserved longer than the capacity to mount responses to new antigens. In addition, higher NAb titers and response rates identify mRNA-1273 as a superior vaccine for CLL patients.
MeSH term(s)	Humans ; Leukemia, Lymphocytic, Chronic, B-Cell ; 2019-nCoV Vaccine mRNA-1273 ; BNT162 Vaccine ; Prospective Studies ; SARS-CoV-2 ; COVID-19/prevention & control ; Vaccination
Chemical Substances	2019-nCoV Vaccine mRNA-1273 (EPK39PL4R4) ; BNT162 Vaccine
Language	English
Publishing date	2023-06-29
Publishing country	United States
Document type	Observational Study ; Journal Article
ZDB-ID	2185925-5
ISSN	1549-1676 ; 1549-1277
ISSN (online)	1549-1676
ISSN	1549-1277
DOI	10.1371/journal.pmed.1004157
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Article ; Online: Functional Roles of the IgM Fc Receptor in the Immune System.

Kubagawa, Hiromi / Honjo, Kazuhito / Ohkura, Naganari / Sakaguchi, Shimon / Radbruch, Andreas / Melchers, Fritz / Jani, Peter K

Frontiers in immunology

2019 Volume 10, Page(s) 945

Abstract: It is now evident from studies of mice unable to secrete IgM that both non-immune "natural" and antigen-induced "immune" IgM are important for protection against pathogens and for regulation of immune responses to self-antigens. Since identification of ... ...

Abstract	It is now evident from studies of mice unable to secrete IgM that both non-immune "natural" and antigen-induced "immune" IgM are important for protection against pathogens and for regulation of immune responses to self-antigens. Since identification of its Fc receptor (FcμR) by a functional cloning strategy in 2009, the roles of FcμR in these IgM effector functions have begun to be explored. Unlike Fc receptors for switched Ig isotypes (e.g., FcγRs, FcεRs, FcαR, Fcα/μR, pIgR, FcRn), FcμR is selectively expressed by lymphocytes: B, T, and NK cells in humans and only B cells in mice. FcμR may have dual signaling ability: one through a potential as yet unidentified adaptor protein non-covalently associating with the FcμR ligand-binding chain via a His in transmembrane segment and the other through its own Tyr and Ser residues in the cytoplasmic tail. FcμR binds pentameric and hexameric IgM with a high avidity of ~10 nM in solution, but more efficiently binds IgM when it is attached to a membrane component via its Fab region on the same cell surface (
MeSH term(s)	Animals ; Autoimmunity ; B-Lymphocytes/immunology ; Epigenesis, Genetic ; Humans ; Receptors, Fc/immunology ; T-Lymphocytes, Regulatory/immunology
Chemical Substances	Receptors, Fc ; immunoglobulin M receptor
Language	English
Publishing date	2019-05-03
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2019.00945
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