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Toxoplasma Gondii © 2016. Published by The Company of Biologists Ltd | Journal of Cell Science (2016) 129, 1031-1045 doi:10.1242/jcs.177386 RESEARCH ARTICLE Structural and functional dissection of Toxoplasma gondii armadillo repeats only protein Christina Mueller1, Atta Samoo2,3,4,*, Pierre-Mehdi Hammoudi1,*, Natacha Klages1, Juha Pekka Kallio3,4,5, Inari Kursula2,3,4,5 and Dominique Soldati-Favre1,‡ ABSTRACT specialised membranous sac termed the parasitophorous vacuole Rhoptries are club-shaped, regulated secretory organelles that membrane (PVM). Rhoptries are positioned at the apical end of the cluster at the apical pole of apicomplexan parasites. Their parasite and adopt an elongated, club-shaped morphology with a discharge is essential for invasion and the establishment of an bulbous body and a narrow neck (Dubey et al., 1998). These intracellular lifestyle. Little is known about rhoptry biogenesis and organelles play a key role not only during invasion, but also recycling during parasite division. In Toxoplasma gondii, positioning contribute to the formation of the PVM as well as subsequent of rhoptries involves the armadillo repeats only protein (ARO) and evasion and subversion of the host cell defence mechanisms myosin F (MyoF). Here, we show that two ARO partners, ARO- (reviewed in Kemp et al., 2013). During parasite entry, only one of – interacting protein (AIP) and adenylate cyclase β (ACβ) localize to a the 10 12 rhoptries injects its contents, including the rhoptry neck rhoptry subcompartment. In absence of AIP, ACβ disappears from proteins (RONs), rhoptry bulb proteins (ROPs) and some the rhoptries. By assessing the contribution of each ARO armadillo membranous materials, into the host cell (Boothroyd and (ARM) repeat, we provide evidence that ARO is multifunctional, Dubremetz, 2008). Several RONs form a complex with apical participating not only in positioning but also in clustering of rhoptries. membrane antigen 1 (AMA-1), a protein secreted from the Structural analyses show that ARO resembles the myosin-binding micronemes, resulting in the formation of the so-called moving domain of the Caenorhabditis elegans myosin chaperone UNC-45. A junction (Besteiro et al., 2011; Straub et al., 2009). The moving conserved patch of aromatic and acidic residues denotes the putative junction is a tight apposition between the parasite and the host cell MyoF-binding site, and the overall arrangement of the ARM repeats plasma membrane, and ensures efficient propulsion of the parasite explains the dramatic consequences of deleting each of them. Finally, into the host cell, ultimately leading to the formation of the PVM Plasmodium falciparum ARO functionally complements ARO (Besteiro et al., 2011; Straub et al., 2009). Several ROPs migrate depletion and interacts with the same partners, highlighting the either to the lumen of the nascent parasitophorous vacuole, the conservation of rhoptry biogenesis in Apicomplexa. PVM, or into the cytosol or nucleus of the infected host cell where they modulate cellular functions (Butcher et al., 2011; El Hajj et al., KEY WORDS: Apicomplexa, Toxoplasma gondii, Rhoptry organelle, 2007a; Etheridge et al., 2014; Fleckenstein et al., 2012; Yamamoto Armadillo repeat et al., 2009). The signalling events leading to rhoptry secretion are poorly understood. However, it is known that rhoptry discharge INTRODUCTION occurs shortly after microneme discharge, and the microneme Unicellular pathogens belonging to the phylum Apicomplexa protein MIC8 has been implicated in rhoptry exocytosis in represent a major threat to both human and animal health. The Toxoplasma gondii (Kessler et al., 2008). most notorious member of this phylum is the causative agent of During parasite division, rhoptries are formed de novo, first human malaria, Plasmodium falciparum. Other members of appearing as globular vesicles in close proximity to the Golgi considerable medical and veterinary importance include complex, and then subsequently maturing into club-shaped Toxoplasma, Neospora, Cryptosporidium, Babesia, Eimeria and organelles localizing to the parasite apex (Fig. 1B) (Nishi et al., Sarcocystis. These organisms are unified by phylum-specific 2008; Shaw et al., 1998). The cellular and molecular mechanisms cytoskeletal structures and sets of specialized secretory organelles underlying rhoptry biogenesis, including their targeting to the termed micronemes, rhoptries and dense granules, discharge of apical pole, are currently not well understood. Previous studies which is necessary for the establishment of an obligate intracellular have, however, shown that perturbation of T. gondii proteins life cycle (reviewed in Carruthers and Sibley, 1997; Sibley, 2010). involved in vesicular trafficking, such as the dynamin-related This cycle is initiated by host cell penetration; an active process that protein B (DrpB), sortilin-like receptor (SORTLR), clathrin heavy leads to the formation of a replication-permissive niche inside a chain 1 (CHC1) or the RabGTPases Rab5A and Rab5C result either in a block of both rhoptry and microneme biogenesis and/or in mistargeting of the proteins to either of the two organelles (Breinich 1Department of Microbiology and Molecular Medicine, CMU, University of Geneva, 1 Rue Michel-Servet, CH-1211, Geneva 4, Switzerland. 2Faculty of Biochemistry et al., 2009; Kremer et al., 2013; Pieperhoff et al., 2013; Sloves and Molecular Medicine, University of Oulu, P.O. Box 5400, Oulu 90014, Finland. et al., 2012). The T. gondii armadillo repeats only protein (ARO) is a 3 Helmholtz Centre for Infection Research, Notkestrasse 85, Hamburg 22607, key factor ensuring the apical distribution of rhoptries (Beck et al., Germany. 4German Electron Synchrotron (DESY), Notkestrasse 85, Hamburg 22607, Germany. 5Department of Biomedicine, University of Bergen, Jonas Lies vei 2013; Mueller et al., 2013). Anchoring of ARO to the cytosolic face 91, Bergen 5009, Norway. of the rhoptry membrane is dependent upon acylation (Cabrera *These authors contributed equally to this work et al., 2012). Of the 18 members of the protein acyltransferases ‡ Author for correspondence ([email protected]) (PATs) identified in T. gondii, only one, DHHC7, is localized to the rhoptries and found to be responsible for palmitoylating ARO (Beck Received 13 July 2015; Accepted 7 January 2016 et al., 2013; Frenal et al., 2013). It is currently unclear at which stage Journal of Cell Science 1031 RESEARCH ARTICLE Journal of Cell Science (2016) 129, 1031-1045 doi:10.1242/jcs.177386 Fig. 1. Characterization of ACβ, an interacting partner of ARO. (A) Western blot analyses of RH and ACβ–3Ty parasite lysates using anti-Ty and the polyclonal anti-ACβ antibodies. ACβ migrates at ∼220 kDa as detected by the polyclonal antibodies, and also migrates at this position in the ACβ–3Ty strain as shown by use of anti-Ty antibodies. Several lower bands are also detected and most likely represent degradation products. Catalase was used as a loading control. (B) The scheme on the top shows a representation of an enlarged rhoptry organelle with the two sub-compartments, the bulb and neck, delimited by ROP (beige) and RON (reddish) proteins (left). The intermediate region occupied by both, ACβ and AIP (in bold) is indicated by dashed lines. ARO distributes over the entire rhoptry surface. On the right (boxed), the disappearance of the mother rhoptries and the de novo formation of daughter rhoptries during parasite cell division is illustrated. The lower panels show localization of ACβ in the ACβ–3Ty strain as assessed by immunofluorescence. Parasites were stained with anti-Ty, anti- GAP45, anti-ROP2, anti-ARO and anti-ACβ antibodies. Anti-GAP45 antibodies were used to visualize the parasites, anti-ARO antibodies were used to visualize the whole rhoptry organelle and anti-ROP2 antibodies were used to label the bulbous region of the rhoptries. ACβ localizes to the rhoptry neck region. The sketches on the right depict localization of organelles and proteins within T. gondii and the parasitophorous vacuole. (C) Transient transfection of ARO–GFP–Ty or GFP in the ACβ–3Ty strain, following co-immunoprecipitation (IP) using anti-GFP antibodies and western blot (WB) analyses using anti-Ty and anti-GFP antibodies. ARO–GFP–Ty specifically interacts with ACβ (anti-Ty staining). The negative control GFP does not co-immunoprecipitate ACβ (anti-Ty and anti-GFP staining). (D) Immunofluorescence analyses of ARO-iKO parasites grown with or without ATc for 48 h and stained with anti-ROP2 and anti-ACβ antibodies. In the absence of AROi-Ty, ACβ is no longer detected at the rhoptries. (E) Immunofluorescence analyses of the AIP–3Ty strain using anti-Ty, anti-ACβ and anti-ROP2 antibodies. ACβ perfectly colocalizes with AIP. (F) Immunofluorescence analyses of the ACβ–3Ty strain. Staining with anti-RON9 and anti-ACβ antibodies revealed that ACβ localizes to a defined intermediate region that lies between the rhoptry bulb and the rhoptry neck. Scale bars: 2 μm. Journal of Cell Science 1032 RESEARCH ARTICLE Journal of Cell Science (2016) 129, 1031-1045 doi:10.1242/jcs.177386 during rhoptry biogenesis this palmitoylation event takes place. used to generate polyclonal anti-ACβ-specific antibodies in rabbits Upon conditional depletion of ARO, rhoptries are randomly (anti-ACβ). Western blot analyses of lysates from the wild-type RH dispersed within the parasite cytosol, ablating rhoptry secretion strain and ACβ–3Ty-expressing strain using anti-ACβ sera detected a and hampering host cell invasion (Beck et al.,
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