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Autophagy in Dictyostelium Genes and Pathways, Cell Death and Infection REVIEW Autophagy 6:6, 686-701; August 16, 2010; © 2010 Landes Bioscience Autophagy in Dictyostelium Genes and pathways, cell death and infection Javier Calvo-Garrido,1 Sergio Carilla-Latorre,1 Yuzuru Kubohara,2 Natalia Santos-Rodrigo,1 Ana Mesquita,1 Thierry Soldati,3 Pierre Golstein4-6 and Ricardo Escalante1,* 1I nstituto de Investigaciones Biomédicas “Alberto Sols” (CSIC-UAM); Arturo Duperier 4; Madrid, Spain; 2I nstitute for Molecular & Cellular Regulation; Gunma University; Maebashi, Japan; 3Départment de Biochimie; Faculté des Sciences; Université de Genève; Sciences II; Genève-4, Switzerland; 4Centre d’Immunologie de Marseille-Luminy (CIML); Aix-Marseille Université; 5ISR N E M; 6CN RS; Faculté des Sciences de Luminy; Marseille, France Key words: Dictyostelium, social amoeba, autophagy, autophagic cell death, autophagy and infection, Vmp1, Atg proteins Since Dictyostelium cells undergo development in the absence The use of simple organisms to understand the molecular and cellular function of complex processes is instrumental of any source of external nutrients they need to mobilize resources for the rapid development of biomedical research. A to be able to respond to the high cell activity required for aggre- remarkable example has been the discovery in S. cerevisiae of gation and morphogenesis. This mobilization is in part achieved a group of proteins involved in the pathways of autophagy. by glycogenolysis and autophagy, the degradation and turnover Orthologues of these proteins have been identified in of the cells’ own biomolecules. Autophagy is essential for devel- humans and experimental model organisms. Interestingly, opment in many different systems.7-9 Three types of autophagy some mammalian autophagy proteins do not seem to have have been described, chaperone-mediated autophagy, microau- homologues in yeast but are present in Dictyostelium, a social tophagy and macroautophagy. In the first one, specific proteins amoeba with two distinctive life phases, a unicellular stage are recognized by chaperones that mediate their translocation in nutrient-rich conditions that differentiates upon starvation across the limiting membrane of the lysosome into the lumen into a multicellular stage that depends on autophagy. This for their degradation.10 This form of selective autophagy plays review focuses on the identification and annotation of the putative Dictyostelium autophagy genes and on the role an important role in the cell’s response to stress and the pres- of autophagy in development, cell death and infection by ence of damaged proteins. In contrast, microautophagy consists bacterial pathogens. of the invagination or protrusion/septation of the lysosome mem- brane, thus capturing the cargo and delivering it into the lyso- somal lumen, again for degradation.11 We will focus our review on the third type, macroautophagy (referred to as autophagy Introducing Dictyostelium, A Suitable Model hereafter), a mechanistically different degradative process char- to Study Autophagy acterized by the formation of double-membrane vesicles called autophagosomes that engulf part of the cytosol or even organ- Dictyostelium discoideum is a simple eukaryote that lives in the elles. The outer membrane of the autophagosomes subsequently soil and feeds on bacteria by phagocytosis. The individual cells fuses with lysosomes, forming autolysosomes where the contents divide by binary fission as long as food is present, however, when and inner membrane of the autophagosome are degraded and the bacteria are exhausted, starvation triggers a process of chemotaxis simple molecular constituents recycled. This form of autophagy driven by cyclic-AMP (cAMP).1-3 The resulting cell aggregate is is essential for temporary cell survival under starvation condi- surrounded by a complex extracellular matrix of protein, cellu- tions. Autophagy is also induced in other circumstances such lose and polysaccharides that isolates it from the environment. as for the elimination of protein aggregates or defective organ- This cellular association behaves like a true multicellular organ- elles or in response to intracellular bacteria, and it is therefore of ism undergoing different stages of development accomplished by immense importance in diverse pathological processes as well as the coordination of morphogenesis and cellular differentiation. in aging.12-14 The origin of the autophagosomal membrane and Eventually, the aggregates give rise to fruiting bodies, each formed the mechanism mediating its expansion and maturation are not by a cellular stalk that supports a mass of spores. The latter will yet completely understood. germinate when environmental conditions are adequate.4-6 The In mammals and Dictyostelium, nascent autophagosomes life cycle of the experimental model species Dictyostelium discoi- originate in the cytoplasm from multiple origins, in contrast deum and representative pictures of each stage are illustrated in with S. cerevisiae, where these structures are concentrated in a Figure 1. single location of the cytoplasm (named the PAS or phagophore assembly site). These autophagosomes appear in Dictyostelium *Correspondence to: Ricardo Escalante; Email: [email protected] and higher organisms as a punctate pattern in the cytoplasm Submitted: 04/10/10; Revised: 05/27/10; Accepted: 05/28/10 when they are analyzed by fluorescence microscopy using specific Previously published online: autophagosome markers like GFP-Atg8/LC3.15,16 At the molecu- www.landesbioscience.com/journals/autophagy/article/12513 lar level, several proteins involved in autophagosome formation 686 Autophagy Volume 6 Issue 6 REVIEW REVIEW Figure 1. Dictyostelium life cycle. Representative pictures of vegetative and developmental stages are shown. In the wild, Dictyostelium amoeba feed on soil bacteria by phagocytosis but most laboratory strains are also able to grow in liquid axenic media by macropinocytosis. It is important to point out that cells are haploid throughout these vegetative and developmental cycles and this facilitates the generation of knockout strains. (named Atg for autophagy-related) have historically been identi- use of comparative genomics to identify relevant genes conserved fied, primarily in the yeastS. cerevisiae. They are grouped in func- in the human genome.37,39 tional complexes required for the origin, elongation, completion and degradation of the autophagosome membrane, although the General Autophagy Mechanisms and Evolutionarily precise mechanisms of action of many of these proteins and the Conserved Autophagy Genes: way in which they are regulated temporally are not yet completely Induction of Autophagy and the Atg1 Complex understood (reviewed in ref. 12, 17–19). Two different complexes containing the protein kinase Atg1 and the lipid kinase Vps34 are We will now examine the potential of Dictyostelium as a model necessary for induction and nucleation of autophagosomes and for autophagy by describing the proteins that are known to be to recruit other proteins to the assembly site. Vesicle expansion involved in this complex process in other systems and the extent to and completion require two ubiquitin-like conjugation systems which they have been conserved in Dictyostelium. Figure 2 shows involving Atg8 and Atg12. Other proteins like Atg2, Atg9 and a scheme of autophagosome formation and conserved proteins Atg18 play a role in membrane traffic and the biogenesis of the that can be identified in the Dictyostelium genome by comparison autophagosome. Many of these autophagy proteins are conserved with the available information in yeast and mammalian systems. in evolution and can be recognized in Dictyostelium by sequence Autophagy induction and its regulation must be tightly con- homology analysis as described in detail below. trolled by the energy and nutritional status of the cell. The nutri- Despite its simplicity, Dictyostelium shows striking similari- ent sensor TOR (target of rapamycin) belongs to a protein family ties with higher eukaryotes in many biological aspects including of conserved serine/threonine kinases known as phosphatidylino- chemotaxis,2,3,20-22 developmental signaling pathways,4,23,24 the sitol kinase-related kinases. TOR receives a wide variety of intra- response to bacterial infections,25-28 the response to therapeutic and extracellular signals such as nutrients, energy, growth factors, drugs29-32 and programmed cell death including autophagic cell calcium and amino acids.40,41 TOR associates with different pro- death (reviewed in ref. 33). The Dictyostelium genome has been teins to form two complexes and only one of them, TORC1, is fully sequenced34 and carefully annotated (http://dictybase.org/) primarily involved in autophagy. The S. cerevisiae TORC1 con- and it is amenable to a wide range of molecular genetic techniques tains Tor1 or 2, Kog1, Tco89 and Lst8 and is sensitive to rapamy- including the generation of mutants by homologous recombina- cin. As in higher eukaryotes, the Dictyostelium genome codes for tion and random genetic screens,6,33,35-38 that have facilitated the proteins highly similar to Tor, Kog1 (also known as Raptor) and www.landesbioscience.com Autophagy 687 Figure 2. Autophagosome formation and putative signaling pathways in Dictyostelium. The phagophore is a double membrane whose origin is still a matter of debate. This membrane enlarges and finally engulfs parts of the cytoplasm. After fusion with lysosomes the content is degraded and recycled. The predicted Dictyostelium autophagic proteins have been
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