Innate immunological memory: from plants to animals

Abstract

Immunological memory is defined by the ability of the host to recognise and mount a robust secondary response against a previously encountered pathogen. Classic immune memory is an evolutionary adaptation of the vertebrate immune system that has been attributed to adaptive lymphocytes, including T and B cells. In contrast, the innate immune system was known for its conserved, non-specific roles in rapid host defence, but historically was considered to be unable to generate memory. Recent studies have challenged our understanding of innate immunity and now provides a growing body of evidence for innate immune memory. However, in many species and in various cell types the underlying mechanisms of immune 'memory' formation remain poorly understood. The purpose of this review is to explore and summarise the emerging evidence for immunological 'memory' in plants, invertebrates, and vertebrates.

Figure 1.. Antigen specificity and memory from plants to higher vertebrates.

Evidence suggests plants are able to form immune memory via broad PRR recognition but antigen specific diversity may not be present. Invertebrates, including insects, worms, crustaceans, much like plants rely solely on innate immune responses and antigen specificity may be limited but evidence suggests many species are able to develop some form of immune memory. Lower vertebrates, such as jawless fish (lamprey and hagfish), VLRs and leucine-rich repeats may represent a primitive form of adaptive immunity. In higher vertebrates (from jawed fish to mammals) antigen specificity and immune memory is mediated by immune cells with an ability to rearrange antigen receptors. PRR, pattern recognition receptor; DSCAM, Down syndrome cell adhesion molecule; RNAi, RNA interference; piRNA, Piwi-interacting RNA; VLR, variable lymphocyte region; V(D)J recombination, random combination of variable, diverse and joining gene segments in lymphocytes; TCR; T-cell receptor, BCR; B-cell receptor.

Figure 2.. Natural Killer (NK) cell memory generation during viral infection.

During MCMV infection, NK cells recognize MCMV infected cells through Ly49H (on NK cells) and m157 (on infected cells) interactions and Ly49H⁺ NK cells are able to undergo clonal-like expansion, which can be partially driven by pro-inflammatory cytokines such as IL-12 and IL-18. Following expansion, the Ly49H⁺ NK cells enter a contraction phase and produce a small pool of self-renewing, long-lived NK cells that are able to mount recall responses against subsequent viral infections. MCMV, murine cytomegalovirus; DC, dendritic cell; IFN, interferon.