LBP/BPI proteins and their relatives: conservation over evolution and roles in mutualism

Abstract

LBP [LPS (lipopolysaccharide)-binding protein] and BPI (bactericidal/permeability-increasing protein) are components of the immune system that have been principally studied in mammals for their involvement in defence against bacterial pathogens. These proteins share a basic architecture and residues involved in LPS binding. Putative orthologues, i.e. proteins encoded by similar genes that diverged from a common ancestor, have been found in a number of non-mammalian vertebrate species and several non-vertebrates. Similar to other aspects of immunity, such as the activity of Toll-like receptors and NOD (nucleotide-binding oligomerization domain) proteins, analysis of the conservation of LBPs and BPIs in the invertebrates promises to provide insight into features essential to the form and function of these molecules. This review considers state-of-the-art knowledge in the diversity of the LBP/BPI proteins across the eukaryotes and also considers their role in mutualistic symbioses. Recent studies of the LBPs and BPIs in an invertebrate model of beneficial associations, the Hawaiian bobtail squid Euprymna scolopes' alliance with the marine luminous bacterium Vibrio fischeri, are discussed as an example of the use of non-vertebrate models for the study of LBPs and BPIs.

Fig. 1

Characteristics of the predicted E. scolopes LBP proteins. The derived amino acid sequence of each of the EsLBP cDNAs was analyzed for biochemical parameters and protein family domains using ExPASy ProtParam [36] and the SMART algorithm [50]. AAs, amino acids. NCBI accession numbers for sequences: JF514880, JF514881, JF514882.

Fig. 2

Immunocytochemical localization of EsLBP1 in the light organ of juvenile E. scolopes. A. The position of the organ in the whole, live juvenile squid. The organ can be seen through the translucent dorsal surface of the animal as a dark region in the center of the body (white dashed circle). B. Confocal microscopy image of the ventral surface of the juvenile light organ. Each lateral lobe of the organ bears a complex ciliated field (cf), which promotes harvesting of V. fischeri from the environment, and ducts (d), passageways through which the symbiont cells enter host tissues. Anti-EsLBP1 antibodies (green) label regions along the apical surfaces of the epithelia of the cells of the ciliated fields and the pores. The dashed oval region is where deeper images were taken in (C). C. Confocal image of the deep crypt (cr) region of the light organ. Anti-EsLBP1 antibodies (green) label the deep crypt spaces where the symbiont cells reside following colonization of the organ. In (B, C), nuclei, blue (TOTO-3); actin, red (rhodamine phalloidin). e, eye; t, tentacles. For confocal microscopy methods, see [46].