The different facets of organelle interplay-an overview of organelle interactions.

Michael Schrader,Luis F Godinho,Markus Islinger,Joseph L Costello

doi:10.3389/fcell.2015.00056

Abstract

Membrane-bound organelles such as mitochondria, peroxisomes, or the endoplasmic reticulum (ER) create distinct environments to promote specific cellular tasks such as ATP production, lipid breakdown, or protein export. During recent years, it has become evident that organelles are integrated into cellular networks regulating metabolism, intracellular signaling, cellular maintenance, cell fate decision, and pathogen defence. In order to facilitate such signaling events, specialized membrane regions between apposing organelles bear distinct sets of proteins to enable tethering and exchange of metabolites and signaling molecules. Such membrane associations between the mitochondria and a specialized site of the ER, the mitochondria associated-membrane (MAM), as well as between the ER and the plasma membrane (PAM) have been partially characterized at the molecular level. However, historical and recent observations imply that other organelles like peroxisomes, lysosomes, and lipid droplets might also be involved in the formation of such apposing membrane contact sites. Alternatively, reports on so-called mitochondria derived-vesicles (MDV) suggest alternative mechanisms of organelle interaction. Moreover, maintenance of cellular homeostasis requires the precise removal of aged organelles by autophagy—a process which involves the detection of ubiquitinated organelle proteins by the autophagosome membrane, representing another site of membrane associated-signaling. This review will summarize the available data on the existence and composition of organelle contact sites and the molecular specializations each site uses in order to provide a timely overview on the potential functions of organelle interaction.

Highlights

In eukaryotic cells sophisticated membrane-bound organelles have evolved which enable the cell to compartmentalize specialized biochemical reactions in specific locations within the cell (Figure 1)
Organelle interaction depends on the total number of organelles which is regulated by organelle biogenesis/formation, membrane dynamics and autophagic processes
We address processes of organelle interaction with a particular focus on membrane contact sites emerging at the cross roads of organelle research and intracellular signaling

Summary

Introduction

In eukaryotic cells sophisticated membrane-bound organelles have evolved which enable the cell to compartmentalize specialized biochemical reactions in specific locations within the cell (Figure 1). Cooperative functions of organelle networks include (1) metabolic interaction, (2) intracellular signaling, (3) cellular maintenance, (4) regulation of programmed cell death/cell survival, and (5) pathogen defence. Organelle interaction depends on the total number of organelles which is regulated by organelle biogenesis/formation, membrane dynamics and autophagic processes. These processes involve membrane contact sites, for example ER-mitochondria contacts which are supposed to contribute to mitochondrial division [see Sections The Mitochondriaassociated Membrane of the ER (MAM) and Interplay between Peroxisomes and Mitochondria] or interactions with lysosomes during autophagy (see Section Lysosomal Interactions and Autophagy). Membrane contacts between organelles have been reported in early ultrastructural studies, their important functions in intracellular signaling, metabolite transport/metabolism, organelle dynamics and transport is just beginning to emerge. A growing number of proteins with potential tethering functions are being identified in yeast and mammals

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Conclusion