Lipids in host–pathogen interactions: Pathogens exploit the complexity of the host cell lipidome

Abstract

Lipids were long believed to have a structural role in biomembranes and a role in energy storage utilizing cellular lipid droplets and plasma lipoproteins. Research over the last decades has identified an additional role of lipids in cellular signaling, membrane microdomain organization and dynamics, and membrane trafficking. These properties make lipids an attractive target for pathogens to modulate host cell processes in order to allow their survival and replication. In this review we will summarize the often ingenious strategies of pathogens to modify the lipid homeostasis of host cells, allowing them to divert cellular processes. To this end pathogens take full advantage of the complexity of the lipidome. The examples are categorized in generalized and emerging principles describing the involvement of lipids in host-pathogen interactions. Several pathogens are described that simultaneously induce multiple changes in the host cell signaling and trafficking mechanisms. Elucidation of these pathogen-induced changes may have important implications for drug development. The emergence of high-throughput lipidomic techniques will allow the description of changes of the host cell lipidome at the level of individual molecular lipid species and the identification of lipid biomarkers.

Antibacterial effect of biosynthesized silver nanoparticles in Pacific white shrimp Litopenaeus vannamei (Boone) infected with necrotizing hepatopancreatitis bacterium (NHP B)

“…It is well recognized that certain bacteria inhabiting a vacuole or phagosome, are able to synthesize some proteins and toxins to form holes in the vacuole membrane of their hosts to escape from these organelles (Van der Meer-Janssen et al, 2010). The disrupted cellular membranes could facilitate the entry of nanoparticles into the host cell and several reports have demonstrated that Gram-negative bacteria show an increased susceptibility to AgNPs (Sondi & Salopek-Sondi, 2004;Radzig et al, 2013), which makes these vehicles suitable candidates as an antimicrobial agent against NHP-B.…”

Maintenance of vacuole integrity by bacterial pathogens

“…Changes in membrane lipids alter the membrane identity of the organelle affecting trafficking. Recruiting or altering lipids is also important for metabolism, membrane dynamics and the tethering of effector proteins to the vacuole [23][24][25]. Several pathogens change the phosphoinositol signature found on their vacuoles.…”

Bacterial Sphingomyelinases and Phospholipases as Virulence Factors

“…Bacterial SMases and PLases might contribute to the infection process in different hosts in several ways. Some of these enzymes hydrolyze structural membrane lipids and cause lysis of the host cells, contributing to bacterial colonization and/or dissemination and providing nutrients for pathogen survival and replication (14,15). Others generate bioactive lipids which activate endogenous mediators of cell death without inducing cellular lysis (15)(16)(17) (Fig.…”

“…Bacterial SMases and PLases may act on vacuolar lipids, contributing to transform phagosomes into a replication-permissive niche or causing phagosomal membrane disruption that allows the pathogen to reach the host cell cytoplasm and survive by evading the host immune response ( Fig. 1) (14,15,18). Bacterial PLases from enteric pathogens degrade the phospholipid-rich mucus layer overlying the gastrointestinal mucosa, whereas those from lung pathogens cleave phospholipids from pulmonary surfactant, promoting nutrient release and contributing to tissue colonization, as well as in the case of surfactant cleavage to lung dysfunction.…”

“…Products generated by bacterial SMases and PLases could hijack vesicle trafficking pathways or dysregulate signaling cascades affecting the immune response and thus promote infection establishment or progression ( Fig. 1) (14)(15)(16)(17)(18).…”