Trends in Immunology
Volume 22, Issue 6, 1 June 2001, Pages 285-288
Journal home page for Trends in Immunology

Research update
Vertebrate innate immunity resembles a mosaic of invertebrate immune responses

https://doi.org/10.1016/S1471-4906(01)01895-6Get rights and content

Abstract

Research on the innate immune response of mammals has revealed similarities with the invertebrate immune system. Thus, insects have developed an acute response resembling that seen in humans, implicating similar effectors, receptors and regulation of gene expression. Mussels have developed intracellular phagocytosis resembling that seen in mammalian neutrophils, using cationic antibacterial peptides in phagolysosomes. Leeches, like amphibians, contain antibacterial peptides and immune stimulators that derive from the processing of neuropeptide precursors. This pattern of similarities suggests that the vertebrate innate immune response resembles a patchwork of those responses seen in several invertebrate models.

Section snippets

Human antimicrobial responses

In humans, some antimicrobial peptides are produced by the epithelial cells that line the respiratory, gastrointestinal and urogenital tracts and the skin [9]. Epithelial granulocytes of the small intestine contribute to the barrier function of the gastric mucosa by the apical release of granules containing a variety of antimicrobial products, including human α-defensin-5 and -6 (Ref. 5). Other similar peptides are found in the glandular secretions that moisten and lubricate such surfaces [2].

Invertebrate immune responses

Insects, such as Drosophila, respond to septic injuries by rapidly synthesizing antimicrobial peptides (Fig. 1). These peptides are predominantly produced in the fat body; they are then secreted into the hemolymph and participate in a systemic response [10]. Seven distinct antimicrobial peptides (plus isoforms) have been described for Drosophila. Interestingly, they appear to have distinct target specificities, and induction of the expression of the various peptides depends on the type of

Epithelial immune responses

Recent studies on antimicrobial peptides from Drosophila have shown that a variety of epithelial tissues in direct contact with the external environment can express the antifungal Drosophila peptide drosomycin, suggesting that a local response to infections is affecting these barrier tissues [12]. The imd gene in Drosophila plays a crucial role in the activation of this local response to infection. Drosomycin expression is regulated by the Toll pathway during the systemic response, but is

Neuropeptide-derived antibacterial peptides

The presence of antibacterial neuropeptide precursors, such as proenkephalin or prodermaseptins, in both invertebrates and vertebrates further supports the hypothesis that these molecules first evolved in ancestral animals [8], [15], [16], [17] (Fig. 2). Indeed, preprodermaseptins form a group of antimicrobial peptide precursors found in the skin of a variety of frog species [8]. Precursors of this family have similar N-terminal preprosequences, followed by markedly different C-terminal domains

Hemocyte systemic response

In the Limulus model, it has been demonstrated that hemocytes are extremely sensitive to microbial substances such as lipopolysaccharides and β-glycans. Indeed, upon stimulation, the hemocytes spontaneously degranulate and release into the extracellular fluid a series of substances involved in immune defense [19], including several antimicrobial peptides, such as tachyplesins [20], big defensin [21] and tachycitin [22]. These results resemble those found in patients with bacterial infections

Antimicrobial human neutrophil-like response

In bivalve mollusks (Fig. 3), acquired results demonstrate that antibacterial concentrations in circulating hemocytes are not increased after bacterial challenge [25]. Within hours following injection, the migration and adherence of hemocytes that contain the antibacterial peptide mytilin was observed around the injection site [26]. The cells containing mytilin can engulf bacteria, and subsequently release mytilin into phagolysosomes [26]. By 24–48 hours after bacterial challenge, increased

Conclusions

Taken together, these data demonstrate that the antimicrobial response towards pathogens has been conserved in the course of evolution. However, antimicrobial responses are not identical among plants, invertebrates and vertebrates [4]. The convergent point of many studies over the past two decades is that the vertebrate innate response resembles a mosaic of different invertebrate immune mechanisms towards pathogens. Two questions are now pertinent: how are antimicrobial peptides

Acknowledgements

I thank P. Bulet (UPR CNRS 9022, Strasbourg, France) and T. Ganz (University of California at Los Angeles School of Medicine, CA, USA) for their critical reading of the manuscript. This review is dedicated to the memory of André Verbert, Director of the UMR CNRS 111, University of Lille, France. This work was supported, in part, by the Centre National de la Recherche Scientifique, the IFREMER, the ANVAR Nord Pas de Calais, and the NIH Fogarty INT 00045.

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