Lympho-Hematopoietic Microenvironments and Fish Immune System

Abstract

In the last 50 years information on the fish immune system has increased importantly, particularly that on species of marked commercial interest (i.e., salmonids, cods, catfish, sea breams), that occupy a key position in the vertebrate phylogenetical tree (i.e., Agnatha, Chondrichtyes, lungfish) or represent consolidated experimental models, such as zebrafish or medaka. However, most obtained information was based on genetic sequence analysis with little or no information on the cellular basis of the immune responses. Although jawed fish contain a thymus and lympho-hematopoietic organs equivalents to mammalian bone marrow, few studies have accounted for the presumptive relationships between the organization of these cell microenvironments and the known immune capabilities of the fish immune system. In the current review, we analyze this topic providing information on: (1) The origins of T and B lymphopoiesis in Agnatha and jawed fish; (2) the remarkable organization of the thymus of teleost fish; (3) the occurrence of numerous, apparently unrelated organs housing lympho-hematopoietic progenitors and, presumably, B lymphopoiesis; (4) the existence of fish immunological memory in the absence of germinal centers.

Keywords: MALT; T and B lymphocytes; germinal centers and immune memory; immunity; peripheral lymphoid organs; teleost fish; thymus.

Figure 1

Lympho-hematopoietic sites in the developing zebrafish. First haemopoietic loci include ICM (Intercellular mass), PBI (posterior blood islands) and VDA (ventral wall of the dorsal aorta). From this last region, definitive HSC (hematopoietic stem cells) colonize the caudal hematopoietic tissue (CHT), and both HSC-independent and HSC-dependent T cell progenitors seed into the thymic primordium. From CHT, progenitor cells colonize the nephros that is the main hematopoietic organ of adult teleosts.

Figure 2

Serial sections of 3-month-old zebrafish thymus. Note that it is only possible to distinguish a central medulla (m) surrounded by a cortex densely occupied by thymocytes when the section shape changes.

Figure 3

Light microscopy of the carbon uptake (arrowheads) by macrophages surrounding the splenic ellipsoids of Carassius auratus (a). By electron microscopy, ellipsoid macrophages (arrows) appear full off engulfed bacteria after intraperitoneal injection of Yersinia ruckeri (b).

Figure 4

A melano-macrophage center close to the renal glomerulus of Carassius auratus. Note the presence of isolated melano-macrophages (arrowheads) and other phagocytic cells (asterisks) full of cell debris.