Emergence and Evolution of Secondary Lymphoid Organs

Abstract

For effective adaptive immunity to foreign antigens (Ag), secondary lymphoid organs (SLO) provide the confined environment in which Ag-restricted lymphocytes, with very low precursor frequencies, interact with Ag on Ag-presenting cells (APC). The spleen is the primordial SLO, arising in conjunction with adaptive immunity in early jawed vertebrates. The spleen, especially the spleen’s lymphoid compartment, the white pulp (WP), has undergone numerous modifications over evolutionary time. We describe the progressive advancement of splenic WP complexity, which evolved in parallel with the increasing functionality of adaptive immunity. The Ag-presenting function of follicular dendritic cells (FDC) also likely emerged at the inception of adaptive immunity, and we propose that a single type of hematopoietically derived APC displayed Ag to both T and B cells. A dedicated FDC, derived from a vascular precursor, is a recent evolutionary innovation that likely permitted the robust affinity maturation found in mammals.

Themacrophage-expressed gene(mpeg)1identifies a subpopulation of B cells in the adult zebrafish

“…However, histologic examination of secondary lymphoid tissues did not allow identifying any specific anatomic areas where these two populations would segregate. As teleosts lack well‐organized lymphoid structures and do not form germinal centers (a feature that arose in birds across the vertebrate phylum), whether mpeg1.1 can discriminate different zebrafish B cell subsets based on their locations thus remains an open question. In addition, Mpeg1 expression in mammals was also reported in a large array of innate immune cells, including dendritic cells, neutrophils, and NK cells .…”

A cold-blooded view of adaptive immunity

“…Only warm-blooded vertebrates have lymph nodes, Peyer’s patches and germinal centres, all of which are dependent on the cytokine lymphotoxin for their development 28,159 . Almost all gnathostomes, however, do have a spleen in which adaptive immune responses are generated, concentrating the antigens for interactions between antigen-specific T cells, B cells and antigen-presenting cells (APCs) (FIG.…”

“…2). The last major advance in vertebrate evolution was the advent of lymph nodes and the formation of germinal centres in mammals 27–29 ; the ectothermic vertebrates allow for the study of immunity that preceded the emergence of follicular dendritic cells (FDCs), the major cellular player in mammalian affinity maturation 28,30 . This Review will delve into all of these characteristics of adaptive immunity, focusing on basic questions that intrigue all immunologists, and explore what we can and should tackle over the next decade.…”

Anatomical Uniqueness of the Mucosal Immune System (GALT, NALT, iBALT) for the Induction and Regulation of Mucosal Immunity and Tolerance

“…For example, bony fish lack an obvious segregation of B and T cells in the lymphocyte clusters associated with the gut, gills, and nasopharynx [14À16], whereas amphibians and reptiles separate B and T cell areas in the spleen but not in the GALT [17]. In contrast, mucosal lymphoid tissues in birds and mammals are highly organized [13,14], with separated B and T cell areas, specialized fibroblastic stromal cells, strategically placed phagocytic and antigen-presenting cells, and well-demarcated germinal centers.…”