Epigenetics of Host–Pathogen Interactions: The Road Ahead and the Road Behind

Abstract

A growing body of evidence points towards epigenetic mechanisms being responsible for a wide range of biological phenomena, from the plasticity of plant growth and development to the nutritional control of caste determination in honeybees and the etiology of human disease (e.g., cancer). With the (partial) elucidation of the molecular basis of epigenetic variation and the heritability of certain of these changes, the field of evolutionary epigenetics is flourishing. Despite this, the role of epigenetics in shaping host–pathogen interactions has received comparatively little attention. Yet there is plenty of evidence supporting the implication of epigenetic mechanisms in the modulation of the biological interaction between hosts and pathogens. The phenotypic plasticity of many key parasite life-history traits appears to be under epigenetic control. Moreover, pathogen-induced effects in host phenotype may have transgenerational consequences, and the bases of these changes and their heritability probably have an epigenetic component. The significance of epigenetic modifications may, however, go beyond providing a mechanistic basis for host and pathogen plasticity. Epigenetic epidemiology has recently emerged as a promising area for future research on infectious diseases. In addition, the incorporation of epigenetic inheritance and epigenetic plasticity mechanisms to evolutionary models and empirical studies of host–pathogen interactions will provide new insights into the evolution and coevolution of these associations. Here, we review the evidence available for the role epigenetics on host–pathogen interactions, and the utility and versatility of the epigenetic technologies available that can be cross-applied to host–pathogen studies. We conclude with recommendations and directions for future research on the burgeoning field of epigenetics as applied to host–pathogen interactions.

The Cytoplasm Affects the Epigenome in Drosophila melanogaster

“…Both mitochondria and Wolbachia have been implicated to affect the nuclear epigenome [12,32,55]. While both could, therefore, be causing the differential H3K4me3 enrichment we observed, it is interesting to note that the only significantly enriched GO category we found was related to mitochondrial function.…”

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

“…Likewise, in wild populations, resistance and tolerance may be affected by many processes that are transmitted across generations but that are not related to additive (or non-additive) genetic variance. For instance, epigenetic inheritance may contribute to the inclusive heritability of resistance and tolerance (reviewed in [56]). Similarly, parental non-genetic effects have already been shown in resistance to parasites.…”

Borna Disease Virus Phosphoprotein Modulates Epigenetic Signaling in Neurons To Control Viral Replication

“…This allows them to benefit from the epigenetic changes that they induce in the nucleus of target cells, thereby producing a favorable environment for their latent/persistent states or for reactivation (10)(11)(12)(13). This has been well described for herpesviruses, such as Kaposi's sarcoma-associated herpesvirus, for which the latency-associated nuclear antigen has been shown to interact with host chromatin modifiers and induce epigenetic reprogramming (14,15).…”