Evolution and development of immunological structures in the lamprey

Abstract

Comparative immunology has been revitalized by the integration of genomics approaches, which allow a foothold into addressing problems that previously had been difficult to study. One such problem had been the enigmatic finding of overt immune anatomical structures in the lamprey, yet its apparent lack of bona fide immunoglobulin or T cell receptor molecules. The genomic characterization of a novel extended locus that undergoes rearrangements to generate receptor diversity and the subsequent implementation of this diversity in the immune system of lampreys have generated considerable interest as well as new avenues for investigation. Here, we review the anatomical structures of the lamprey that exhibit lympho-hematopoietic characteristics, with the ultimate goal of reconciling these data with contemporary molecular findings. By integrating these datasets we seek to better understand how an alternative adaptive immune system could have evolved.

Figure 1

Immune structures in the sea lamprey, Petromyzon marinus. (a) Lympho-hematopoietic tissue in the typhlosole of an ammocoete. Note the masses of developing blood cells around the central blood vessel, CBV that constitutes the axis of typhlosole. (b) Hemato-lymphoid aggregations between the renal tubules of the larval opisthonephros (semi-thin section). Three renal tubules, RT, are denoted; a few hemato-lymphoid aggregations are indicated by arrows. (c) Groups of hematopoietic cells (arrows) in the adipose tissue of the supraneural body of a post-metamorphic sea lamprey. SB, supraneural body; SC, spinal column; NC, notochord. (d) A thin section of larval opisthonephros observed via transmission electron microscopy (TEM). Different developing and mature blood cells, including macrophages (M) and lymphocyte-like (L) cells, occur between renal tubules, RT.

Figure 2

Immune structures in the sea lamprey, Petromyzon marinus. (a) Typhlosole in regression of a metamorphosing lamprey. A few, small groups of lympho-hematopoietic cells occur in lamina propria (arrows) that accumulate an increasing amount of dense connective tissue. CBV, central blood vessel. (b) Thin section of a typhlosole of metamorphosing lamprey (TEM). Fibrocytes and large masses of collagenous fibers have supplanted the loose connective tissue of the larval typhlosole resulting in the disappearance of lympho-hematopoietic tissue. (c) Larval pharyngeal epithelium (gill region). A labyrinth of dense connective tissue walls (CTW) and sinusoidal blood vessels containing numerous circulating blood cells occur closely associated with the pharyngeal epithelium of ammocoetes. L, lymphocyte-like cells; E, erythrocytes. (d) TEM of a mature plasma cell in the sea lamprey. Note the abundant, enlarged cisternae of rough endoplasmic reticulum and the lateral disposition of the nucleus in this cell type.

Figure 3

Expression of VLR in a sea lamprey larva. An antisense VLR riboprobe was used for whole mount in situ hybridization to a 45-day ammocoete. (a) Intact specimen (anterior half) is shown. The blue staining represents hybridization of the VLR probe (which was designed to the highly conserved and non-repetitive portion of the VLR-B sequence). Staining is seen particularly in the pharyngeal region. The eye spot is denoted by ES. (b) Same specimen as in (a) but after partially sectioning the specimen sagitally using a cryostat in order to remove the overlying skin and muscle. The cutaway view allows better visualization of the gill filaments, GF, and oral tentacles, OT, both structures being specifically hybridized with the VLR probe. (c) A 10 µM sagittal cryosection of the same specimen as in (a and b) showing individual gill filaments that were hybridized by the VLR probe. The identity of the stained structures is under investigation.