Organelle targeting during bacterial infection: insights from Listeria

Abstract

Listeria monocytogenes, a facultative intracellular bacterium responsible for severe foodborne infections, is now recognized as a multifaceted model in infection biology. Comprehensive studies of the molecular and cellular basis of the infection have unraveled how the bacterium crosses the intestinal and feto-placental barriers, invades several cell types in which it multiplies and moves, and spreads from cell to cell. Interestingly, although Listeria does not actively invade host cell organelles, it can interfere with their function. We discuss the effect of Listeria on the endoplasmic reticulum (ER) and the mechanisms leading to the fragmentation of the mitochondrial network and its consequences, and review the strategies used by Listeria to subvert nuclear functions, more precisely to control host gene expression at the chromatin level.

Alteration of epithelial cell lysosomal integrity induced by bacterial cholesterol-dependent cytolysins

“…Many bacterial pathogens have evolved the ability to interfere with host cell organelles (Escoll, Mondino, Rolando, & Buchrieser, 2016;Lebreton et al, 2015). Important cellular functions are compartmentalized in these organelles, such as DNA maintenance and gene expression in the nucleus, sorting of newly synthetized proteins and lipids in the ER and in the Golgi or bioenergetics and programmed cell death in mitochondria.…”

“…At the cell level, Listeria has the ability to enter and replicate in both phagocytic and nonphagocytic cells (Cossart, ; Pizarro‐Cerda, Kuhbacher, & Cossart, ). Listeria 's intracellular life cycle involves hijacking of host‐cell pathways and interference with host cell organelles (Lebreton, Stavru, & Cossart, ). Indeed, it has been reported that Listeria alters the dynamic of mitochondria fission/fusion events (Stavru, Bouillaud, Sartori, Ricquier, & Cossart, ; Stavru, Palmer, Wang, Youle, & Cossart, ), activates the endoplasmic reticulum (ER) stress responses (Pillich, Loose, Zimmer, & Chakraborty, ), and reshapes host nuclear functions by altering histone modifications and chromatin condensation (Eskandarian et al, ; Hamon et al, ; Hamon & Cossart, ; Lebreton et al, ).…”

“…The endomembrane system is a privileged target of Listeria during infection (Lebreton et al, 2015). In nonphagocytic cells, internalization of Listeria and its escape from the internalization vacuole requires tight control of the host endocytic compartments (Hamon et al, 2012;Pizarro-Cerda et al, 2012).…”

How the Study of Listeria Monocytogenes has Led to New Concepts in Biology

“…Although L. monocytogenes does not invade these host cell organelles, it has developed several strategies to interfere with their functions, i.e. by inhibiting phagosomal killing and lysosomal function, by activating the ER stress response, by modulating mitochondrial dynamics, by modulating host gene expression via interference with chromatin-based regulation (for review, [83]). …”

The Hijacking of Host Endocytic Trafficking by the Bacterial Pathogen

“…In Listeria infection, the secretion of listeriolysin (LLO) by Listeria decreases phagosomal calcium concentration and increases pH, which impedes phago-lysosomal fusion. The secreted effector, Lmo2459, blocks the maturation of the phagosome via the inhibition of Rab 5 [11]. Legionella containing vacuoles (LCV) inside phagocytic cells avoid fusion with lysosomes, yet the pathogen vacuole extensively communicates with the endosomal, secretory, and retrograde vesicle trafficking pathways, as well as with the endoplasmic reticulum (ER) [12].…”