Danger signals - damaged-self recognition across the tree of life.

Martin Heil,Walter G Land

doi:10.3389/fpls.2014.00578

Abstract

Multicellular organisms suffer injury and serve as hosts for microorganisms. Therefore, they require mechanisms to detect injury and to distinguish the self from the non-self and the harmless non-self (microbial mutualists and commensals) from the detrimental non-self (pathogens). Danger signals are “damage-associated molecular patterns” (DAMPs) that are released from the disrupted host tissue or exposed on stressed cells. Seemingly ubiquitous DAMPs are extracellular ATP or extracellular DNA, fragmented cell walls or extracellular matrices, and many other types of delocalized molecules and fragments of macromolecules that are released when pre-existing precursors come into contact with enzymes from which they are separated in the intact cell. Any kind of these DAMPs enable damaged-self recognition, inform the host on tissue disruption, initiate processes aimed at restoring homeostasis, such as sealing the wound, and prepare the adjacent tissues for the perception of invaders. In mammals, antigen-processing and -presenting cells such as dendritic cells mature to immunostimulatory cells after the perception of DAMPs, prime naïve T-cells and elicit a specific adaptive T-/B-cell immune response. We discuss molecules that serve as DAMPs in multiple organisms and their perception by pattern recognition receptors (PRRs). Ca2+-fluxes, membrane depolarization, the liberation of reactive oxygen species and mitogen-activated protein kinase (MAPK) signaling cascades are the ubiquitous molecular mechanisms that act downstream of the PRRs in organisms across the tree of life. Damaged-self recognition contains both homologous and analogous elements and is likely to have evolved in all eukaryotic kingdoms, because all organisms found the same solutions for the same problem: damage must be recognized without depending on enemy-derived molecules and responses to the non-self must be directed specifically against detrimental invaders.

Highlights

Multicellular organisms across the tree of life share as common problems injury and infection, against which they must initiate immunity to maintain metabolic homeostasis and integrity
Attempts to understand the inducible responses in plants to herbivory or infection by pathogens generally focus on the detection of the non-self: specific prokaryotic molecules such as flagellin or chitin are perceived as microbe- associated molecular patterns (MAMPs/PAMPs), whereas molecules from the saliva, regurgitate or oviposition fluids of herbivores are perceived as herbivore-associated molecular patterns (HAMPs), to mount adequate resistance responses (Jones and Dangl, 2006; Wu and Baldwin, 2010; Zipfel, 2014)
We suggest to divide mammalian damage-associated molecular patterns” (DAMPs) into five classes (Table 1) because they are sensed by distinct members of five families of pattern recognition receptors (PRRs): Tolllike receptors (TLRs) (Kawai and Akira, 2010), receptor for advanced glycation endproducts (RAGE; Lee and Park, 2013), NOD-like receptors (NLRs; Zhong et al, 2013), RIG-I-like receptors (RLRs; Wu and Chen, 2014), and AIM2-like receptors (ALRs; Wu and Chen, 2014)

Summary

INTRODUCTION

Multicellular organisms across the tree of life share as common problems injury and infection, against which they must initiate immunity to maintain metabolic homeostasis and integrity. Attempts to understand the inducible responses in plants to herbivory or infection by pathogens generally focus on the detection of the non-self: specific prokaryotic molecules such as flagellin or chitin are perceived as microbe- (or pathogen-) associated molecular patterns (MAMPs/PAMPs), whereas molecules from the saliva, regurgitate or oviposition fluids of herbivores are perceived as herbivore-associated molecular patterns (HAMPs), to mount adequate resistance responses (Jones and Dangl, 2006; Wu and Baldwin, 2010; Zipfel, 2014). There are more than one million species of arthropods described, the majority of which are considered herbivores, but we know only a handful of insect-derived elicitors of plant resistance responses (Wu and Baldwin, 2010). Female organisms must tolerate invasion by pollen or sperm, which are genetically nonself, and females in most species carry the embryo for a certain www.frontiersin.org

Heil and Land

Class V

CONCLUSION