PUBLICATION

B cells in teleost fish act as pivotal initiating APCs in priming adaptive immunity: an evolutionary perspective on the origin of the B-1 cell subset and B7 molecules

Authors
Zhu, L.Y., Lin, A.F., Shao, T., Nie, L., Dong, W.R., Xiang, L.X., and Shao, J.Z.
ID
ZDB-PUB-140509-8
Date
2014
Source
Journal of immunology (Baltimore, Md. : 1950)   192(6): 2699-2714 (Journal)
Registered Authors
Keywords
none
MeSH Terms
  • Adaptive Immunity/genetics
  • Adaptive Immunity/immunology*
  • Amino Acid Sequence
  • Animals
  • Antigen-Presenting Cells/immunology*
  • Antigen-Presenting Cells/metabolism
  • Antigens, CD/genetics
  • Antigens, CD/immunology
  • Antigens, CD/metabolism
  • B-Lymphocyte Subsets/immunology*
  • B-Lymphocyte Subsets/metabolism
  • B-Lymphocytes/immunology*
  • B-Lymphocytes/metabolism
  • B7 Antigens/genetics
  • B7 Antigens/immunology*
  • B7 Antigens/metabolism
  • B7-1 Antigen/genetics
  • B7-1 Antigen/immunology
  • B7-1 Antigen/metabolism
  • B7-2 Antigen/genetics
  • B7-2 Antigen/immunology
  • B7-2 Antigen/metabolism
  • Base Sequence
  • Blotting, Western
  • CD4-Positive T-Lymphocytes/immunology
  • CD4-Positive T-Lymphocytes/metabolism
  • Evolution, Molecular
  • Female
  • Gene Expression Profiling
  • Immunoglobulins/genetics
  • Immunoglobulins/immunology
  • Immunoglobulins/metabolism
  • Lymphocyte Activation/immunology
  • Male
  • Membrane Glycoproteins/genetics
  • Membrane Glycoproteins/immunology
  • Membrane Glycoproteins/metabolism
  • Molecular Sequence Data
  • Phylogeny
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Amino Acid
  • Vibrio alginolyticus/immunology
  • Zebrafish/genetics
  • Zebrafish/immunology*
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/immunology
  • Zebrafish Proteins/metabolism
PubMed
24532580 Full text @ J. Immunol.
Abstract

The long-held paradigm that B cells cannot uptake nonspecific particulate Ags for the initiation of primary adaptive immunity has been challenged by the recent discovery that teleost B cells have potent phagocytic and microbicidal abilities. This discovery provides preliminary clues that primitive B cells might act as initiating APCs in priming adaptive immunity. In this study, zebrafish B cells clearly showed a potent Ag-presenting ability to both soluble Ags and bacterial particles to prime naive CD4+ T cell activation. This finding demonstrates the innate-like nature of teleost B cells in the interface of innate and adaptive immunity, indicating that they might consist of a major population of initiating APCs whose performance is similar to that of dendritic cells. Given the functional similarities between teleost B cells and the mammalian B-1 subset, we hypothesize that B-1 lineage and teleost B cells might originate from a common ancestor with potent phagocytic and initiating APC capacities. In addition, CD80/86 and CD83 costimulatory signals were identified as being essential for B cell–initiated adaptive immunity. This result suggests that the costimulatory mechanism originated as early as the origin of adaptive immunity and is conserved throughout vertebrate evolution. In fish, only a single CD80/86 copy exists, which is similar to mammalian CD86 rather than to CD80. Thus, CD86 might be a more primordial B7 family member that originated from fish. This study provides valuable insights into the evolutionary history of professional APCs, B cell lineages, and the costimulatory mechanism underlying adaptive immunity as a whole.

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