Maturation of Marginal Zone and Follicular B Cells Requires B Cell Activating Factor of the Tumor Necrosis Factor Family and is Independent of B Cell Maturation Antigen

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2001 Dec 26

PMID 11733583

Citations 69

Authors

P Schneider

H Takatsuka

A Wilson

F Mackay

A Tardivel

S Lens

T G Cachero

D Finke

F Beermann

J Tschopp

Affiliations

Soon will be listed here.

Abstract

B cells undergo a complex series of maturation and selection steps in the bone marrow and spleen during differentiation into mature immune effector cells. The tumor necrosis factor (TNF) family member B cell activating factor of the TNF family (BAFF) (BLyS/TALL-1) plays an important role in B cell homeostasis. BAFF and its close homologue a proliferation-inducing ligand (APRIL) have both been shown to interact with at least two receptors, B cell maturation antigen (BCMA) and transmembrane activator and cyclophilin ligand interactor (TACI), however their relative contribution in transducing BAFF signals in vivo remains unclear. To functionally inactivate both BAFF and APRIL, mice transgenic for a soluble form of TACI were generated. They display a developmental block of B cell maturation in the periphery, leading to a severe depletion of marginal zone and follicular B2 B cells, but not of peritoneal B1 B cells. In contrast, mice transgenic for a soluble form of BCMA, which binds APRIL, have no detectable B cell phenotype. This demonstrates a crucial role for BAFF in B cell maturation and strongly suggests that it signals via a BCMA-independent pathway and in an APRIL-dispensable way.

Citing Articles

Cellular indexing of transcriptomes and epitopes (CITE-Seq) in hidradenitis suppurativa identifies dysregulated cell types in peripheral blood and facilitates diagnosis via machine learning.

Kumar S, Orcales F, Shih B, Fang X, Yin C, Yates A Res Sq. 2024; .

PMID: 39315268 PMC: 11419166. DOI: 10.21203/rs.3.rs-4791069/v1.

An unappreciated cell survival-independent role for BAFF initiating chronic lymphocytic leukemia.

Ullah M, Garcillan B, Whitlock E, Figgett W, Infantino S, Eslami M Front Immunol. 2024; 15:1345515.

PMID: 38469292 PMC: 10927009. DOI: 10.3389/fimmu.2024.1345515.

The bidirectional immune crosstalk in metabolic dysfunction-associated steatotic liver disease.

Sawada K, Chung H, Softic S, Moreno-Fernandez M, Divanovic S Cell Metab. 2023; 35(11):1852-1871.

PMID: 37939656 PMC: 10680147. DOI: 10.1016/j.cmet.2023.10.009.

The BAFF-APRIL System in Cancer.

Ullah M, Mackay F Cancers (Basel). 2023; 15(6).

PMID: 36980677 PMC: 10046288. DOI: 10.3390/cancers15061791.

Pattern recognition receptor ligand-induced differentiation of human transitional B cells.

McMillan J, ODonnell P, Chang S PLoS One. 2022; 17(8):e0273810.

PMID: 36040923 PMC: 9426890. DOI: 10.1371/journal.pone.0273810.

References

von Bulow G, Van Deursen J, Bram R . Regulation of the T-independent humoral response by TACI. Immunity. 2001; 14(5):573-82. DOI: 10.1016/s1074-7613(01)00130-3. View

Yan M, Wang H, Chan B, Roose-Girma M, Erickson S, Baker T . Activation and accumulation of B cells in TACI-deficient mice. Nat Immunol. 2001; 2(7):638-43. DOI: 10.1038/89790. View

Gross J, Dillon S, Mudri S, Johnston J, Littau A, Roque R . TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. impaired B cell maturation in mice lacking BLyS. Immunity. 2001; 15(2):289-302. DOI: 10.1016/s1074-7613(01)00183-2. View

Schiemann B, Gommerman J, Vora K, Cachero T, Dobles M, Frew E . An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 2001; 293(5537):2111-4. DOI: 10.1126/science.1061964. View

Thompson J, Bixler S, Qian F, Vora K, Scott M, Cachero T . BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science. 2001; 293(5537):2108-11. DOI: 10.1126/science.1061965. View

Strasser A, Whittingham S, Vaux D, Bath M, Adams J, Cory S . Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A. 1991; 88(19):8661-5. PMC: 52569. DOI: 10.1073/pnas.88.19.8661. View

Brakebusch C, Varfolomeev E, Batkin M, Wallach D . Structural requirements for inducible shedding of the p55 tumor necrosis factor receptor. J Biol Chem. 1994; 269(51):32488-96. View

Garcia I, Miyazaki Y, Araki K, Araki M, Lucas R, Grau G . Transgenic mice expressing high levels of soluble TNF-R1 fusion protein are protected from lethal septic shock and cerebral malaria, and are highly sensitive to Listeria monocytogenes and Leishmania major infections. Eur J Immunol. 1995; 25(8):2401-7. DOI: 10.1002/eji.1830250841. View

Lentz V, Hayes C, Cancro M . Bcmd decreases the life span of B-2 but not B-1 cells in A/WySnJ mice. J Immunol. 1998; 160(8):3743-7. View

10.

Lam K, Rajewsky K . Rapid elimination of mature autoreactive B cells demonstrated by Cre-induced change in B cell antigen receptor specificity in vivo. Proc Natl Acad Sci U S A. 1998; 95(22):13171-5. PMC: 23748. DOI: 10.1073/pnas.95.22.13171. View

11.

Loder F, Mutschler B, Ray R, Paige C, Sideras P, Torres R . B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J Exp Med. 1999; 190(1):75-89. PMC: 2195560. DOI: 10.1084/jem.190.1.75. View

12.

Bouillet P, Metcalf D, Huang D, Tarlinton D, Kay T, Kontgen F . Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 1999; 286(5445):1735-8. DOI: 10.1126/science.286.5445.1735. View

13.

Mackay F, Woodcock S, Lawton P, Ambrose C, Baetscher M, Schneider P . Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med. 1999; 190(11):1697-710. PMC: 2195729. DOI: 10.1084/jem.190.11.1697. View

14.

Khare S, Sarosi I, Xia X, McCabe S, Miner K, Solovyev I . Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci U S A. 2000; 97(7):3370-5. PMC: 16246. DOI: 10.1073/pnas.97.7.3370. View

15.

Gross J, Johnston J, Mudri S, Enselman R, Dillon S, Madden K . TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature. 2000; 404(6781):995-9. DOI: 10.1038/35010115. View

16.

Macpherson A, Gatto D, Sainsbury E, Harriman G, Hengartner H, Zinkernagel R . A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 2000; 288(5474):2222-6. DOI: 10.1126/science.288.5474.2222. View

17.

Thompson J, Schneider P, Kalled S, Wang L, Lefevre E, Cachero T . BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J Exp Med. 2000; 192(1):129-35. PMC: 1887706. DOI: 10.1084/jem.192.1.129. View

18.

Marsters S, Yan M, Pitti R, Haas P, Dixit V, Ashkenazi A . Interaction of the TNF homologues BLyS and APRIL with the TNF receptor homologues BCMA and TACI. Curr Biol. 2000; 10(13):785-8. DOI: 10.1016/s0960-9822(00)00566-2. View

19.

Hardy R, Li Y, Allman D, Asano M, Gui M, Hayakawa K . B-cell commitment, development and selection. Immunol Rev. 2000; 175:23-32. View

20.

Martin F, Kearney J . B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a "natural immune memory". Immunol Rev. 2000; 175:70-9. View