Plasmablasts and plasma cells: Reconsidering teleost immune system organization

Ye, Jianmin; Kaattari, Ilsa; Kaattari, Stephen L.

doi:10.1016/j.dci.2011.03.005

Cited by 60 publications

(33 citation statements)

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“…First, the kinetics, magnitude, and affinity of the TI and TD responses were quite similar. Both responses exhibited a relatively short primary phase versus a prolonged secondary and both maintained the high affinity achieved late in the primary (by week 16), even as the titers began to wane (week [25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43][44]. This heightened affinity continued into the secondary, with even a slight increase (∼from −log aK 5.9 to 6.2), late in the secondary.…”

Section: Discussionmentioning

confidence: 99%

“…However, precise quantitative comparisons between antibody titers and ASCs cannot be made as (i) the secretion rate of the ASCs (composed of PCs and plasmablasts) increases over time postimmunization [41], and (ii) high-affinity antibodies, which dominate the late immune response [20], possess more prolonged half-lives [42,43] thus making such comparisons problematic. Indeed, based on these previous studies [41][42][43], one should expect that fewer ASCs would give rise to higher antibody titers as the response matures.Two features of these antibody responses; however, were particularly notable. First, the kinetics, magnitude, and affinity of the TI and TD responses were quite similar.…”

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confidence: 99%

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Differential compartmentalization of memory B cells versus plasma cells in salmonid fish

Kaattari

2013

Eur J Immunol

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The disposition of teleost memory and plasma cells (PCs) has essentially been unexplored. As the organization of the teleost immune system differs significantly from that of mammals (i.e. no bone marrow or lymph nodes, hematopoietic anterior kidney), this disposition could be essential in understanding how comparable functions are achieved. To address this question, the primary and secondary antibody-secreting cell, B memory cell, and antibody responses to T-independent and T-dependent antigens were analyzed in trout. Although the TI and TD antibody responses did not differ substantively from one another, the secondary responses to both were significantly prolonged compared with the primary responses. Logarithmic increases in titer and affinity were achieved for both antigens during the primary, with only modest increases during the secondary response. Antibody-secreting cells, both PCs and plasmablasts, quantitatively paralleled antibody production, with antibody-secreting cells skewing to the hematopoietic anterior kidney for both antigens. However, the enhanced antigen-inducible response of immune fish (indicative of the memory pool) skewed to the peripheral blood and spleen. This pattern of memory versus PC disposition parallels that observed in mammals even though the organization of the respective immune systems differs considerably. Keywords: Anterior kidney r Memory cells r Plasma cells r Trout IntroductionTeleost memory has been defined by the development of a differentially heightened responsive state to antigen, albeit lacking in a number of mammalian features. Primary immunization can, thus, lead to increased immunogen sensitivity [1], enhanced in vivo [2][3][4][5][6] and in vitro [6][7][8] antibody responsiveness, expansion of antigen-sensitive precursor pools [9] and, most importantly, anamestic responses to pathogens [4,5,10,11] and immunoprophylaxis [4,[12][13][14]. Anamestic features absent from teleost responses include isotype switching [15] (although they possess multiple isotypes [16]), relatively modest somatic mutaCorrespondence: Dr. Stephen L. Kaattari e-mail: kaattari@vims.edu tion [17][18][19] and affinity maturation [20][21][22] as compared with the IgG responses of mammals. Intriguingly, characteristics of teleost memory B cells (MBCs) [9] parallel those associated with a class of mammalian MBCs. Recent evidence reveals that human MBCs can include unswitched, mutated IgM + cells [23]; nonmutated, CD27 + IgM + cells [24], those induced by T-independent (TI) antigens [25,26], preimmune diversified repertoires [27] (as has recently been posed for the catfish [19]), or arise independently of GCs [27,28]. Together, these previous studies prompt a renewed focus on the critical elements of μ specific memory, both in teleosts and mammals. For example, perhaps the requisites for exceptionally high-titered, extensively mutated, high-affinity responses in * These authors contributed equally to this work. [32][33][34], which home to their respective hematopoietic tissues, even though the organs ...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Differential compartmentalization of memory B cells versus plasma cells in salmonid fish

Kaattari

2013

Eur J Immunol

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“…All teleost B cells that express surface IgM also express surface IgD. Teleost IgM is secreted mainly by plasmablasts and plasma-like cells that are located mostly in the head kidney and are key to eliciting memory IgM responses 65 . After booster immunization, teleost fish undergo a substantial increase in IgM titers 59,60 , a process that is temperature dependent.…”

Section: Figurementioning

confidence: 99%

Fishing for mammalian paradigms in the teleost immune system

2013

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Recent years have witnessed a renaissance in the study of fish immune systems. Such studies have greatly expanded the knowledge of the evolution and diversification of vertebrate immune systems. Several findings in those studies have overturned old paradigms about the immune system and led to the discovery of novel aspects of mammalian immunity. Here I focus on how findings pertaining to immunity in teleost (bony) fish have led to major new insights about mammalian B cell function in innate and adaptive immunity. Additionally, I illustrate how the discovery of the most ancient mucosal immunoglobulin described thus far will help resolve unsettled paradigms of mammalian mucosal immunity.

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“…In rainbow trout (Oncorhynchus mykiss), different types of Ab secreting cells have been distinguished, as in mouse and human [13]: plasmablasts, which produce low amount of Ab, replicate, and express low level of B cell receptor (BCR), and plasma cells (long-or short-lived), which produce high level of Ab, do not replicate nor express BCR [5,6,14]. Importantly, while B cells encounter their specific target in spleen or kidney, and differentiate into Ab secreting cells in these tissues, mature plasma cells migrate and persist in the anterior kidney [15], as observed in mouse or in human for the bone marrow [16]. However, fish B cells lack efficient affinity maturation, as observed also in amphibians [9,10].…”

Section: Introductionmentioning

confidence: 99%

Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection

Castro

Jouneau

Pham

et al. 2013

Fish & Shellfish Immunology

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Upon infection, B-lymphocytes expressing antibodies specific for the intruding pathogen develop clonal responses triggered by pathogen recognition via the B-cell receptor. The constant region of antibodies produced by such responding clones dictates their functional properties. In teleost fish, the clonal structure of B-cell responses and the respective contribution of the three isotypes IgM, IgD and IgT remain unknown. The expression of IgM and IgT are mutually exclusive, leading to the existence of two B-cell subsets expressing either both IgM and IgD or only IgT. Here, we undertook a comprehensive analysis of the variable heavy chain (VH) domain repertoires of the IgM, IgD and IgT in spleen of homozygous isogenic rainbow trout (Onchorhynchus mykiss) before, and after challenge with a rhabdovirus, the Viral Hemorrhagic Septicemia Virus (VHSV), using CDR3-length spectratyping and pyrosequencing of immunoglobulin (Ig) transcripts. In healthy fish, we observed distinct repertoires for IgM, IgD and IgT, respectively, with a few amplified m and t junctions, suggesting the presence of IgM-and IgT-secreting cells in the spleen. In infected animals, we detected complex and highly diverse IgM responses involving all VH subgroups, and dominated by a few large public and private clones. A lower number of robust clonal responses involving only a few VH were detected for the mucosal IgT, indicating that both IgM + and IgT + spleen B cells responded to systemic infection but at different degrees. In contrast, the IgD response to the infection was faint. Although fish IgD and IgT present different structural features and evolutionary origin compared to mammalian IgD and IgA, respectively, their implication in the B-cell response evokes these mouse and human counterparts. Thus, it appears that the general properties of antibody responses were already in place in common ancestors of fish and mammals, and were globally conserved during evolution with possible functional convergences.

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Plasmablasts and plasma cells: Reconsidering teleost immune system organization

Cited by 60 publications

References 78 publications

Differential compartmentalization of memory B cells versus plasma cells in salmonid fish

Differential compartmentalization of memory B cells versus plasma cells in salmonid fish

Fishing for mammalian paradigms in the teleost immune system

Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection

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