Sustained rhoptry docking and discharge requires Toxoplasma gondii intraconoidal microtubule-associated proteins

被引:9
作者
Dos Santos Pacheco, Nicolas [1 ]
Puig, Albert [1 ]
Guerin, Amandine [2 ]
Martinez, Matthew [3 ]
Maco, Bohumil [1 ]
Tosetti, Nicolo [1 ]
Delgado-Betancourt, Estefania [1 ]
Lunghi, Matteo [1 ]
Striepen, Boris [2 ]
Chang, Yi-Wei [3 ,4 ]
Soldati-Favre, Dominique [1 ]
机构
[1] Univ Geneva, Fac Med, Dept Microbiol & Mol Med, Geneva, Switzerland
[2] Univ Penn, Sch Vet Med, Dept Pathobiol, Philadelphia, PA 19104 USA
[3] Univ Penn, Perelman Sch Med, Dept Biochem & Biophys, Philadelphia, PA 19014 USA
[4] Univ Penn, Inst Struct Biol, Perelman Sch Med, Philadelphia, PA 19104 USA
基金
瑞士国家科学基金会; 美国国家卫生研究院; 欧洲研究理事会;
关键词
CORTICAL MICROTUBULES; CONOID EXTRUSION; HOST-CELLS; INVASION; CYTOSKELETON; ORGANELLES; SECRETION; VISUALIZATION; EXPRESSION;
D O I
10.1038/s41467-023-44631-y
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
In Apicomplexa, rhoptry discharge is essential for invasion and involves an apical vesicle (AV) docking one or two rhoptries to a macromolecular secretory apparatus. Toxoplasma gondii is armed with 10-12 rhoptries and 5-6 microtubule-associated vesicles (MVs) presumably for iterative rhoptry discharge. Here, we have addressed the localization and functional significance of two intraconoidal microtubule (ICMT)-associated proteins instrumental for invasion. Mechanistically, depletion of ICMAP2 leads to a dissociation of the ICMTs, their detachment from the conoid and dispersion of MVs and rhoptries. ICMAP3 exists in two isoforms that contribute to the control of the ICMTs length and the docking of the two rhoptries at the AV, respectively. This study illuminates the central role ICMTs play in scaffolding the discharge of multiple rhoptries. This process is instrumental for virulence in the mouse model of infection and in addition promotes sterile protection against T. gondii via the release of key effectors inducing immunity.
引用
收藏
页数:15
相关论文
共 72 条
[1]   An Alveolata secretory machinery adapted to parasite host cell invasion [J].
Aquilini, Eleonora ;
Cova, Marta Mendonca ;
Mageswaran, Shrawan Kumar ;
Dos Santos Pacheco, Nicolas ;
Sparvoli, Daniela ;
Penarete-Vargas, Diana Marcela ;
Najm, Rania ;
Graindorge, Arnault ;
Suarez, Catherine ;
Maynadier, Marjorie ;
Berry-Sterkers, Laurence ;
Urbach, Serge ;
Fahy, Pilar Ruga ;
Guerin, Amandine N. ;
Striepen, Boris ;
Dubremetz, Jean-Francois ;
Chang, Yi-Wei ;
Turkewitz, Aaron P. ;
Lebrun, Maryse .
NATURE MICROBIOLOGY, 2021, 6 (04) :425-+
[2]   A Comprehensive Subcellular Atlas of the Toxoplasma Proteome via hyperLOPIT Provides Spatial Context for Protein Functions [J].
Barylyuk, Konstantin ;
Koreny, Ludek ;
Ke, Huiling ;
Butterworth, Simon ;
Crook, Oliver M. ;
Lassadi, Imen ;
Gupta, Vipul ;
Tromer, Eelco ;
Mourier, Tobias ;
Stevens, Tim J. ;
Breckels, Lisa M. ;
Pain, Arnab ;
Lilley, Kathryn S. ;
Waller, Ross F. .
CELL HOST & MICROBE, 2020, 28 (05) :752-+
[3]   A Novel Family of Toxoplasma IMC Proteins Displays a Hierarchical Organization and Functions in Coordinating Parasite Division [J].
Beck, Josh R. ;
Rodriguez-Fernandez, Imilce A. ;
de Leon, Jessica Cruz ;
Huynh, My-Hang ;
Carruthers, Vern B. ;
Morrissette, Naomi S. ;
Bradley, Peter J. .
PLOS PATHOGENS, 2010, 6 (09)
[4]   Biogenesis and discharge of the rhoptries: Key organelles for entry and hijack of host cells by the Apicomplexa [J].
Ben Chaabene, Rouaa ;
Lentini, Gaelle ;
Soldati-Favre, Dominique .
MOLECULAR MICROBIOLOGY, 2021, 115 (03) :453-465
[5]   Kiss and spit:: the dual roles of Toxoplasma rhoptries [J].
Boothroyd, John C. ;
Dubremetz, Jean-Francois .
NATURE REVIEWS MICROBIOLOGY, 2008, 6 (01) :79-88
[6]   Visualization of cell microtubules in their native state [J].
Bouchet-Marquis, Cedric ;
Zuber, Benoit ;
Glynn, Anne-Marie ;
Eltsov, Mikhail ;
Grabenbauer, Markus ;
Goldie, Kenneth N. ;
Thomas, Daniel ;
Frangakis, Achilleas S. ;
Dubochet, Jacques ;
Chretien, Denis .
BIOLOGY OF THE CELL, 2007, 99 (01) :45-53
[7]   Conditional Knockdown of Proteins Using Auxin-inducible Degron (AID) Fusions in Toxoplasma gondii [J].
Brown, Kevin M. ;
Long, Shaojun ;
Sibley, L. David .
BIO-PROTOCOL, 2018, 8 (04)
[8]  
Brown KM, 2017, MBIO, V8, DOI [10.1128/mBio.00375-17, 10.1128/mbio.00375-17]
[9]   Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion [J].
Burrell, Alana ;
Marugan-Hernandez, Virginia ;
Wheeler, Richard ;
Moreira-Leite, Flavia ;
Ferguson, David J. P. ;
Tomley, Fiona M. ;
Vaughan, Sue .
PLOS PATHOGENS, 2022, 18 (07)
[10]   Secretion of micronemal proteins is associated with toxoplasma invasion of host cells [J].
Carruthers, VB ;
Giddings, OK ;
Sibley, LD .
CELLULAR MICROBIOLOGY, 1999, 1 (03) :225-235