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.
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.