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

Abstract

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 ...

Differential Transcriptomic Response in the Spleen and Head Kidney Following Vaccination and Infection of Asian Seabass with Streptococcus iniae

“…The relative similarity of the head kidney transcriptomes among vaccinated seabass compared to control seabass could hence be a consequence of the presence of a large mono-population of long-live plasma cells. This pattern of B cell differentiation, proliferation and migration was similarly observed in a study based on ELISPOT assays and carried out on rainbow trout ( Oncorhynchus mykiss ) subjected to an exposure of bacterial-based antigens [37]. Our result also implied that vaccinated seabass could still possibly be vulnerable to a bacterial infection shortly after vaccination (at least within one week) since long-lived plasma cells need some time to establish themselves in the head kidneys.…”

Isolation of the Fathead Minnow Nidovirus from Muskellunge Experiencing Lingering Mortality

“…injection, it is currently unknown how the virus is transmitted under natural conditions (e.g., cohabitation with or ingestion of infected fish). Regardless of the route of infection (natural or by injection), it is clear that FHMNV can cause significant necrotic changes in hematopoietic tissues in multiple organs such as liver, kidneys, and spleen, a matter that may affect the ability of resident white blood cells to mount potent immune responses (Bromage et al 2004;Ma et al 2013). The studies of Iwanowicz and Goodwin (2002) described similar lesions in the liver, kidneys, and spleen of experimentally infected Fathead Minnows.…”

Successive Oral Immunizations Against Piscirickettsia Salmonis and Infectious Salmon Anemia Virus are Required to Maintain a Long-Term Protection in Farmed Salmonids

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