Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets

Adamo, Shelley A.; Roberts, Janet L.; Easy, Russell H.; Ross, Neil W.

doi:10.1242/jeb.013136

Cited by 136 publications

(102 citation statements)

References 51 publications

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“…Increased immune responses during infection or experimental manipulation may shunt energetic resources or critical macromolecules away from traits such as performance (Schall et al, 1982;Martin et al, 2003Martin et al, , 2012Adamo et al, 2008;Adelman and Martin, 2009), resulting in reduced performance capacity. For example, in Psammodromus algirus lizards, experimental induction of an immune response by injection of lipopolysaccharide significantly reduced sprint speed (Zamora-Camacho et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Exercise training reveals trade-offs among endurance performance and immune function, but not growth, in juvenile lizards

Husak

Roy

Lovern

2017

Journal of Experimental Biology

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Acquired energetic resources allocated to a particular trait cannot then be re-allocated to a different trait. This often results in a trade-off between survival and reproduction for the adults of many species, but such a trade-off may be manifested differently in juveniles not yet capable of reproduction. Whereas adults may allocate resources to current and/or future reproduction, juveniles can only allocate to future reproduction. Thus, juveniles should allocate resources toward traits that increase survival and their chances of future reproductive success. We manipulated allocation of resources to performance, via endurance exercise training, to examine trade-offs among endurance capacity, immune function and growth in juvenile green anole lizards. We trained male and female captive anoles on a treadmill for 8 weeks, with increasing intensity, and compared traits with those of untrained individuals. Our results show that training enhanced endurance capacity equally in both sexes, but immune function was suppressed only in females. Training had no effect on growth, but males had higher growth rates than females. Previous work showed that trained adults have enhanced growth, so juvenile growth is either insensitive to stimulation with exercise, or they are already growing at maximal rates. Our results add to a growing body of literature indicating that locomotor performance is an important part of life-history trade-offs that are sex and age specific.

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Section: Introductionmentioning

confidence: 99%

Exercise training reveals trade-offs among endurance performance and immune function, but not growth, in juvenile lizards

Husak

Roy

Lovern

2017

Journal of Experimental Biology

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“…For example, during short-term fight-or-flight behaviours, molecular resources are shifted away from the immune system (i.e. a resource trade-off; Adamo et al, 2008), but at the same time, stress hormones upregulate other immune functions; these changes appear to compensate for the loss of molecular resources (Adamo, 2014). Similarly, during starvation, insect immune systems appear to be able to adaptively reconfigure in order to maintain immune function even though resource availability is reduced (Adamo et al, 2016a,b).…”

Section: Introductionmentioning

confidence: 99%

Predator stress-induced immunosuppression: trade-off, immune redistribution or immune reconfiguration?

Adamo

Easy

Kovalko

et al. 2016

Journal of Experimental Biology

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Although predator exposure increases the risk of wound infections, it typically induces immunosuppression. A number of non-mutually exclusive hypotheses have been put forward to explain this immunosuppression, including: trade-offs between the immune system and other systems required for anti-predator behaviour, redistribution of immune resources towards mechanisms needed to defend against wound infections, and reconfiguration of the immune system to optimize defence under the physiological state of fight-orflight readiness. We tested the ability of each hypothesis to explain the effects of chronic predator stress on the immune system of the caterpillar Manduca sexta. Predator exposure induced defensive behaviours, reduced mass gain, increased development time and increased the concentration of the stress neurohormone octopamine. It had no significant effect on haemocyte number, melanization rate, phenoloxidase activity, lysozyme-like activity or nodule production. Predator stress reduced haemolymph glutathione concentrations. It also increased constitutive expression of the antimicrobial peptide attacin-1 but reduced attacin-1 expression in response to an immune challenge. These results best fit the immune reconfiguration hypothesis, although the other hypotheses are also consistent with some results. Interpreting stress-related changes in immune function may require an examination at the level of the whole organism.

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“…Apolipophorin III, for instance, is not only a lipid transport protein, but also plays a role in the recognition of parasites [19]. In crickets, energetically expensive activities such as flight reduces the amount of available apolipophorins in the haemolymph [20], and experimentally reducing apolipophorin reduces immune function. Similarly, if crickets were given a high fat diet they had higher lipid concentrations in their haemolymph but were more susceptible to parasites, then a result of intensive lipid transport that binds apolipophorin and makes it unavailable for defence [21].…”

Section: Introductionmentioning

confidence: 99%

Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris

2014

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Parasites infect hosts non-randomly as genotypes of hosts vary in susceptibility to the same genotypes of parasites, but this specificity may be modulated by environmental factors such as nutrition. Nutrition plays an important role for any physiological investment. As immune responses are costly, resource limitation should negatively affect immunity through trade-offs with other physiological requirements. Consequently, nutritional limitation should diminish immune capacity in general, but does it also dampen differences among hosts? We investigated the effect of short-term pollen deprivation on the immune responses of our model host Bombus terrestris when infected with the highly prevalent natural parasite Crithidia bombi. Bumblebees deprived of pollen, their protein source, show reduced immune responses to infection. They failed to upregulate a number of genes, including antimicrobial peptides, in response to infection. In particular, they also showed less specific immune expression patterns across individuals and colonies. These findings provide evidence for how immune responses on the individual-level vary with important elements of the environment and illustrate how nutrition can functionally alter not only general resistance, but also alter the pattern of specific host-parasite interactions.

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Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets

Abstract: SUMMARY

Cited by 136 publications

References 51 publications

Exercise training reveals trade-offs among endurance performance and immune function, but not growth, in juvenile lizards

Exercise training reveals trade-offs among endurance performance and immune function, but not growth, in juvenile lizards

Predator stress-induced immunosuppression: trade-off, immune redistribution or immune reconfiguration?

Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris

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