Individual immune priming immune memory

In vertebrates, the development of B and T cells into memory cells provides a molecular mechanism for the formation of an immune memory. No such cells exist in invertebrates such as insects, and therefore it has long been controversial whether something functionally akin to immune memory can exist in this taxon. However, it has been known for some time that in moths 'immunity' is transferable. Injecting the haemolymph of challenged individuals into a test individual led to an improved resistance of the test individual when it was challenged (Wagner, 1961). Similarly, in a series of studies with cockroaches results hinted that immunization of these animals was at least plausible (Rheins and Karp, 1985; Faulhaber and Karp, 1992). The shortcomings of these experiments, and the failure to find appropriate molecular mechanisms have lead to the dogma that invertebrates cannot possess an immune phenomenon that is functionally analogous to immune memory (Klein, 1997). While it is unlikely that this dogma will go away overnight, evidence has started to accumulate that invertebrates do possess a functional equivalent of immune memory. That is, a lasting improved response after an initial exposure is here referred to as immune priming.

In crickets lifetime upregulation of immune components following a nymphal immune challenge has been demonstrated (Jacot et al., 2005). Furthermore, it has been demonstrated in insects that immune priming increases the probability of survival against subsequent exposures of fungi (Rosengaus et al., 1999b; Moret and Siva-Jothy, 2003) and bacteria (Rosengaus et al., 1999b). In shrimps, the effects of a commonly occurring viral infection are reduced following an earlier priming with a controlled dose of the virus (Wu et al., 2002), and this effect can be replicated when only using a particular viral envelope protein (Witteveldt et al., 2004). These studies do not show specificity, nor aim to investigate it; however; functional studies showing protective immune priming and specificity in tandem are beginning to emerge. Strain-specific immune priming has been shown for crustaceans infected by cestodes (Kurtz and Franz, 2003), but some of the best evidence for lasting specific immune priming in invertebrates comes from a well-controlled study of antibacterial immunity and resistance in the bumblebee. Workers of B. terrestris were challenged with sublethal doses of different bacteria before being exposed to a lethal dose 8 or 22 days later. In these tests, worker bees exposed to the same bacterium had a greater probability of survival and a higher proportion of them cleared the bacteria from their haemocoel compared to those exposed to a different bacterium (Sadd and Schmid-Hempel, 2006) (Figure 14.2). This study strongly suggests that insects do have a functional equivalent of immune memory even though the mechanisms are not yet known (Arala-Chaves and Sequeira, 2000; Kurtz, 2004).

Clearly, the level of specificity associated with immune priming will depend on the exact immune mechanisms that are involved. Initial studies suggest that a wide spectrum, through cross-reactive, coarsely specific, and highly specific immune priming, is present in invertebrates. This level or even the existence of immune priming may also depend on the pathogens involved. Specific immune priming in Drosophila was found for the bacteria Streptococcus pneumoniae, but not for

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Figure 14.2 Demonstration of specific immune priming in insects. (a) Bumblebee workers exposed to a clearable dose of bacteria had an increased probability of survival when challenged with a lethal dose of the same bacteria (homologous ▲) 22 days later, over and above that of animals challenged with a different bacteria (heterologous □ and related heterologous 0) and those that had only previously received a control Ringer injection (•). (b) This specificity is also reflected in the proportion of individuals that have cleared their haemocoel of bacteria 24 h after a second challenge. Redrawn after Sadd and Schmid-Hempel (2006).

Salmonella typhimurium, Listeria monocytogenes, and Mycobacterium marinum (Pham et al., 2007). In the beetle Tribolium castaneum, results suggestive of strain-specific immune priming against Bacillus thuringiensis were found, but no such results could be found for defence against Escherichia coli (Roth et al, 2009).

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