Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny

Caitlin D Castro, Yuko Ohta, Helen Dooley, Martin F Flajnik

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Blimp-1 is the master regulator of plasma cell development, controlling genes such as those encoding J-chain and secretory Ig heavy chain. However, some mammalian plasma cells do not express J-chain, and mammalian B1 cells secrete "natural" IgM antibodies without upregulating Blimp-1. While these results have been controversial in mammalian systems, here we describe subsets of normally occurring Blimp-1(-) antibody-secreting cells in nurse sharks, found in lymphoid tissues at all ontogenic stages. Sharks naturally produce large amounts of both pentameric (classically '19S') and monomeric (classically '7S') IgM, the latter an indicator of adaptive immunity. Consistent with the mammalian paradigm, shark Blimp-1 is expressed in splenic 7S IgM-secreting cells, though rarely detected in the J-chain(+) cells producing 19S IgM. Although IgM transcript levels are lower in J-chain(+) cells, these cells nevertheless secrete 19S IgM in the absence of Blimp-1, as demonstrated by ELISPOT and metabolic labeling. Additionally, cells in the shark bone marrow equivalent (epigonal) are Blimp-1(-) . Our data suggest that, in sharks, 19S-secreting cells and other secreting memory B cells in the epigonal are maintained for long periods without Blimp-1, but like in mammals, Blimp-1 is required for terminating the B-cell program following an adaptive immune response in the spleen. This article is protected by copyright. All rights reserved.
Original languageEnglish
Pages (from-to)3061-3075
Number of pages15
JournalEuropean Journal of Immunology
Volume43
Issue number11
Early online date27 Aug 2013
DOIs
Publication statusPublished - Nov 2013

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Sharks
Plasma Cells
Immunoglobulin M
Nurses
Population
Adaptive Immunity
B-Lymphocytes
Enzyme-Linked Immunospot Assay
Antibody-Producing Cells
Immunoglobulin Heavy Chains
Lymphoid Tissue
Mammals
Spleen
Bone Marrow
Antibodies
Genes

Keywords

  • B cells
  • evolution
  • immunoglobins
  • lymphoid organs
  • transcription factors

Cite this

Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny. / Castro, Caitlin D; Ohta, Yuko; Dooley, Helen; Flajnik, Martin F.

In: European Journal of Immunology, Vol. 43, No. 11, 11.2013, p. 3061-3075.

Research output: Contribution to journalArticle

Castro, Caitlin D ; Ohta, Yuko ; Dooley, Helen ; Flajnik, Martin F. / Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny. In: European Journal of Immunology. 2013 ; Vol. 43, No. 11. pp. 3061-3075.
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AB - Blimp-1 is the master regulator of plasma cell development, controlling genes such as those encoding J-chain and secretory Ig heavy chain. However, some mammalian plasma cells do not express J-chain, and mammalian B1 cells secrete "natural" IgM antibodies without upregulating Blimp-1. While these results have been controversial in mammalian systems, here we describe subsets of normally occurring Blimp-1(-) antibody-secreting cells in nurse sharks, found in lymphoid tissues at all ontogenic stages. Sharks naturally produce large amounts of both pentameric (classically '19S') and monomeric (classically '7S') IgM, the latter an indicator of adaptive immunity. Consistent with the mammalian paradigm, shark Blimp-1 is expressed in splenic 7S IgM-secreting cells, though rarely detected in the J-chain(+) cells producing 19S IgM. Although IgM transcript levels are lower in J-chain(+) cells, these cells nevertheless secrete 19S IgM in the absence of Blimp-1, as demonstrated by ELISPOT and metabolic labeling. Additionally, cells in the shark bone marrow equivalent (epigonal) are Blimp-1(-) . Our data suggest that, in sharks, 19S-secreting cells and other secreting memory B cells in the epigonal are maintained for long periods without Blimp-1, but like in mammals, Blimp-1 is required for terminating the B-cell program following an adaptive immune response in the spleen. This article is protected by copyright. All rights reserved.

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