Mitochondrial dynamics in parasitic protists
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
31751405
PubMed Central
PMC6871780
DOI
10.1371/journal.ppat.1008008
PII: PPATHOGENS-D-19-00930
Knihovny.cz E-zdroje
- MeSH
- mitochondriální dynamika * MeSH
- parazitární nemoci epidemiologie parazitologie patofyziologie MeSH
- paraziti patogenita MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
The shape and number of mitochondria respond to the metabolic needs during the cell cycle of the eukaryotic cell. In the best-studied model systems of animals and fungi, the cells contain many mitochondria, each carrying its own nucleoid. The organelles, however, mostly exist as a dynamic network, which undergoes constant cycles of division and fusion. These mitochondrial dynamics are driven by intricate protein machineries centered around dynamin-related proteins (DRPs). Here, we review recent advances on the dynamics of mitochondria and mitochondrion-related organelles (MROs) of parasitic protists. In contrast to animals and fungi, many parasitic protists from groups of Apicomplexa or Kinetoplastida carry only a single mitochondrion with a single nucleoid. In these groups, mitochondrial division is strictly coupled to the cell cycle, and the morphology of the organelle responds to the cell differentiation during the parasite life cycle. On the other hand, anaerobic parasitic protists such as Giardia, Entamoeba, and Trichomonas contain multiple MROs that have lost their organellar genomes. We discuss the function of DRPs, the occurrence of mitochondrial fusion, and mitophagy in the parasitic protists from the perspective of eukaryote evolution.
Zobrazit více v PubMed
Friedman JR, Nunnari J. Mitochondrial form and function. Nature. 2014;505: 335–43. 10.1038/nature12985 PubMed DOI PMC
Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol. 2014;15: 634–46. 10.1038/nrm3877 PubMed DOI PMC
Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337: 1062–1065. 10.1126/science.1219855 PubMed DOI PMC
Gilkerson RW, Schon EA, Hernandez E, Davidson MM. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J Cell Biol. 2008;181: 1117–1128. 10.1083/jcb.200712101 PubMed DOI PMC
Labbé K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol. 2014;30: 357–91. 10.1146/annurev-cellbio-101011-155756 PubMed DOI
Ingerman E, Perkins EM, Marino M, Mears JA, McCaffery JM, Hinshaw JE, et al. Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol. 2005;170: 1021–1027. 10.1083/jcb.200506078 PubMed DOI PMC
Kalia R, Wang RY-R, Yusuf A, Thomas PV., Agard DA, Shaw JM, et al. Structural basis of mitochondrial receptor binding and constriction by DRP1. Nature. 2018;558: 401–405. 10.1038/s41586-018-0211-2 PubMed DOI PMC
Liu R, Chan DC. The mitochondrial fission receptor Mff selectively recruits oligomerized Drp1. Mol Biol Cell. 2015;26: 4466–77. 10.1091/mbc.E15-08-0591 PubMed DOI PMC
Mozdy AD, McCaffery JM, Shaw JM. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol. 2000;151: 367–80. 10.1083/jcb.151.2.367 PubMed DOI PMC
Griffin EE, Graumann J, Chan DC. The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J Cell Biol. 2005;170: 237–248. 10.1083/jcb.200503148 PubMed DOI PMC
Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science. 2011;334: 358–62. 10.1126/science.1207385 PubMed DOI PMC
Murley A, Lackner LL, Osman C, West M, Voeltz GK, Walter P, et al. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife. 2013;2: e00422 10.7554/eLife.00422 PubMed DOI PMC
Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, et al. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science. 2009;325: 477–81. 10.1126/science.1175088 PubMed DOI PMC
Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol. 2003;160: 189–200. 10.1083/jcb.200211046 PubMed DOI PMC
Hales KG, Fuller MT. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 1997;90: 121–9. 10.1016/s0092-8674(00)80319-0 PubMed DOI
Sesaki H, Jensen RE. Ugo1p links the Fzo1p and Mgm1p GTPases for mitochondrial fusion. J Biol Chem. 2004;279: 28298–28303. 10.1074/jbc.M401363200 PubMed DOI
Abrams AJ, Hufnagel RB, Rebelo A, Zanna C, Patel N, Gonzalez MA, et al. Mutations in SLC25A46, encoding a UGO1-like protein, cause an optic atrophy spectrum disorder. Nat Genet. 2015;47: 926–932. 10.1038/ng.3354 PubMed DOI PMC
Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12: 9–14. 10.1038/nrm3028 PubMed DOI PMC
Cowman AF, Berry D, Baum J. The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J Cell Biol. 2012;198: 961–71. 10.1083/jcb.201206112 PubMed DOI PMC
Cowman AF, Healer J, Marapana D, Marsh K. Malaria: biology and disease. Cell. 2016;167: 610–624. 10.1016/j.cell.2016.07.055 PubMed DOI
Ke H, Lewis IA, Morrisey JM, McLean KJ, Ganesan SM, Painter HJ, et al. Genetic investigation of tricarboxylic acid metabolism during the Plasmodium falciparum life cycle. Cell Rep. 2015;11: 164–74. 10.1016/j.celrep.2015.03.011 PubMed DOI PMC
Krungkrai J, Prapunwattana P, Krungkrai SR. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite. 2000;7: 19–26. 10.1051/parasite/2000071019 PubMed DOI
van Dooren GG, Marti M, Tonkin CJ, Stimmler LM, Cowman AF, McFadden GI. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol. 2005;57: 405–419. 10.1111/j.1365-2958.2005.04699.x PubMed DOI
Kohler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJM, et al. A plastid of probable green algal origin in apicomplexan parasites. Science. 1997;275: 1485–1489. 10.1126/science.275.5305.1485 PubMed DOI
Hopkins J, Fowler R, Krishna S, Wilson I, Mitchell G, Bannister L. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist. 1999;150: 283–295. 10.1016/S1434-4610(99)70030-1 PubMed DOI
Arisue N, Hashimoto T. Phylogeny and evolution of apicoplasts and apicomplexan parasites. Parasitol Int. 2015;64: 254–259. 10.1016/j.parint.2014.10.005 PubMed DOI
Lim L, McFadden GI. The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci. 2010;365: 749–63. 10.1098/rstb.2009.0273 PubMed DOI PMC
Stanway RR, Mueller N, Zobiak B, Graewe S, Froehlke U, Zessin PJM, et al. Organelle segregation into Plasmodium liver stage merozoites. Cell Microbiol. 2011;13: 1768–1782. 10.1111/j.1462-5822.2011.01657.x PubMed DOI
Stanway RR, Witt T, Zobiak B, Aepfelbacher M, Heussler VT. GFP-targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites. Biol Cell. 2009;101: 415–435. 10.1042/BC20080202 PubMed DOI
Okamoto N, Spurck TP, Goodman CD, McFadden GI. Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryot Cell. 2009;8: 128–132. 10.1128/EC.00267-08 PubMed DOI PMC
Goodman CD, Siregar JE, Mollard V, Vega-Rodriguez J, Syafruddin D, Matsuoka H, et al. Parasites resistant to the antimalarial atovaquone fail to transmit by mosquitoes. Science. 2016;352: 349–353. 10.1126/science.aad9279 PubMed DOI PMC
Li H, Han Z, Lu Y, Lin Y, Zhang L, Wu Y, et al. Isolation and functional characterization of a dynamin-like gene from Plasmodium falciparum. Biochem Biophys Res Commun. 2004;320: 664–671. 10.1016/j.bbrc.2004.06.010 PubMed DOI
Charneau S, Dourado Bastos IM, Mouray E, Ribeiro BM, Santana JM, Grellier P, et al. Characterization of PfDYN2, a dynamin-like protein of Plasmodium falciparum expressed in schizonts. Microbes Infect. 2007;9: 797–805. 10.1016/j.micinf.2007.02.020 PubMed DOI
Breinich MS, Ferguson DJP, Foth BJ, van Dooren GG, Lebrun M, Quon D V, et al. A dynamin is required for the biogenesis of secretory organelles in Toxoplasma gondii. Curr Biol. 2009;19: 277–286. 10.1016/j.cub.2009.01.039 PubMed DOI PMC
van Dooren GG, Stimmler LM, McFadden GI. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev. 2006;30: 596–630. 10.1111/j.1574-6976.2006.00027.x PubMed DOI
Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30: 1217–58. 10.1016/s0020-7519(00)00124-7 PubMed DOI PMC
Melo EJL, Attias M, De Souza W. The single mitochondrion of tachyzoites of Toxoplasma gondii. J Struct Biol. 2000;130: 27–33. 10.1006/jsbi.2000.4228 PubMed DOI
Francia ME, Striepen B. Cell division in apicomplexan parasites. Nat Rev Microbiol. 2014;12: 125–136. 10.1038/nrmicro3184 PubMed DOI
Nishi M, Hu K, Murray JM, Roos DS. Organellar dynamics during the cell cycle of Toxoplasma gondii. J Cell Sci. 2008;121: 1559–68. 10.1242/jcs.021089 PubMed DOI PMC
van Dooren GG, Reiff SB, Tomova C, Meissner M, Humbel BM, Striepen B. A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii. Curr Biol. 2009;19: 267–276. 10.1016/j.cub.2008.12.048 PubMed DOI PMC
Heredero-Bermejo I, Varberg JM, Charvat R, Jacobs K, Garbuz T, Sullivan WJ, et al. TgDrpC, an atypical dynamin-related protein in Toxoplasma gondii, is associated with vesicular transport factors and parasite division. Mol Microbiol. 2019;111: 46–64. 10.1111/mmi.14138 PubMed DOI PMC
Melatti C, Pieperhoff M, Lemgruber L, Pohl E, Sheiner L, Meissner M. A unique dynamin-related protein is essential for mitochondrial fission in Toxoplasma gondii. PLoS Pathog. 2019;15: e1007512 10.1371/journal.ppat.1007512 PubMed DOI PMC
Harding CR, Meissner M. The inner membrane complex through development of Toxoplasma gondii and Plasmodium. Cell Microbiol. 2014;16: 632–641. 10.1111/cmi.12285 PubMed DOI PMC
Ovciarikova J, Lemgruber L, Stilger KL, Sullivan WJ, Sheiner L. Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii. Sci Rep. 2017;7: 42746 10.1038/srep42746 PubMed DOI PMC
Ghosh D, Walton JL, Roepe PD, Sinai AP. Autophagy is a cell death mechanism in Toxoplasma gondii. Cell Microbiol. 2012;14: 589–607. 10.1111/j.1462-5822.2011.01745.x PubMed DOI PMC
Besteiro S, Brooks CF, Striepen B, Dubremetz J-F. Autophagy protein Atg3 is essential for maintaining mitochondrial integrity and for normal intracellular development of Toxoplasma gondii. tachyzoites. PLoS Pathog. 2011;7: e1002416 10.1371/journal.ppat.1002416 PubMed DOI PMC
Simarro PP, Cecchi G, Franco JR, Paone M, Diarra A, Ruiz-Postigo JA, et al. Estimating and mapping the population at risk of sleeping sickness. PLoS Negl Trop Dis. 2012;6: e1859 10.1371/journal.pntd.0001859 PubMed DOI PMC
Verner Z, Basu S, Benz C, Dixit S, Dobáková E, Faktorová D, et al. Malleable mitochondrion of Trypanosoma brucei. Int Rev Cell Mol Biol. 2015;315: 73–151. 10.1016/bs.ircmb.2014.11.001 PubMed DOI
Trindade S, Rijo-Ferreira F, Carvalho T, Pinto-Neves D, Guegan F, Aresta-Branco F, et al. Trypanosoma brucei parasites occcupy and functionally adapt to the adipose tissue in mice. Cell Host Microbe. 2016;19: 837–848. 10.1016/j.chom.2016.05.002 PubMed DOI PMC
Jakob M, Hoffmann A, Amodeo S, Peitsch C, Zuber B, Ochsenreiter T. Mitochondrial growth during the cell cycle of Trypanosoma brucei bloodstream forms. Sci Rep. 2016;6: 36565 10.1038/srep36565 PubMed DOI PMC
Lukes J, Guilbride DL, Votýpka J, Zíková A, Benne R, Englund PT. Kinetoplast DNA network: evolution of an improbable structure. Eukaryot Cell. 2002;1: 495–502. 10.1128/EC.1.4.495-502.2002 PubMed DOI PMC
Ogbadoyi EO, Robinson DR, Gull K. A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol Biol Cell. 2003;14: 1769–1779. 10.1091/mbc.E02-08-0525 PubMed DOI PMC
Woodward R, Gull K. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J Cell Sci. 1990;95 (Pt 1): 49–57. PubMed
Robinson DR, Gull K. Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature. 1991;352: 731–733. 10.1038/352731a0 PubMed DOI
Hoffmann A, Käser S, Jakob M, Amodeo S, Peitsch C, Týc Í, et al. Molecular model of the mitochondrial genome segregation machinery in Trypanosoma brucei. Proc Natl Acad Sci. 2018;115: 1–10. PubMed PMC
Chanez A-L, Hehl AB, Engstler M, Schneider A. Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J Cell Sci. 2006;119: 2968–74. 10.1242/jcs.03023 PubMed DOI
Schneider A, Ochsenreiter T. Failure is not an option–mitochondrial genome segregation in trypanosomes. J Cell Sci. 2018;131: jcs221820 10.1242/jcs.221820 PubMed DOI
Morgan GW, Goulding D, Field MC. The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem. 2004;279: 10692–701. 10.1074/jbc.M312178200 PubMed DOI
Benz C, Stříbrná E, Hashimi H, Lukeš J. Dynamin-like proteins in Trypanosoma brucei: A division of labour between two paralogs? PLoS ONE. 2017;12: e0177200 10.1371/journal.pone.0177200 PubMed DOI PMC
Vanwalleghem G, Fontaine F, Lecordier L, Tebabi P, Klewe K, Nolan DP, et al. Coupling of lysosomal and mitochondrial membrane permeabilization in trypanolysis by APOL1. Nat Commun. 2015;6: 8078 10.1038/ncomms9078 PubMed DOI PMC
Shaw JM, Nunnari J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 2002;12: 178–84. 10.1016/s0962-8924(01)02246-2 PubMed DOI PMC
Peacock L, Ferris V, Bailey M, Gibson W. Mating compatibility in the parasitic protist Trypanosoma brucei. Parasit Vectors. 2014;7: 78 10.1186/1756-3305-7-78 PubMed DOI PMC
Esseiva AC, Chanez A-L, Bochud-Allemann N, Martinou J-C, Hemphill A, Schneider A. Temporal dissection of Bax-induced events leading to fission of the single mitochondrion in Trypanosoma brucei. EMBO Rep. 2004;5: 268–273. 10.1038/sj.embor.7400095 PubMed DOI PMC
DiMaio J, Ruthel G, Cannon JJ, Malfara MF, Povelones ML. The single mitochondrion of the kinetoplastid parasite Crithidia fasciculata is a dynamic network. PLoS ONE. 2018;13: e0202711 10.1371/journal.pone.0202711 PubMed DOI PMC
Bouchemal K, Bories C, Loiseau PM. Strategies for prevention and treatment of Trichomonas vaginalis infections. Clin Microbiol Rev. 2017;30: 811–825. 10.1128/CMR.00109-16 PubMed DOI PMC
Lindmark DG, Müller M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem. 1973;248: 7724–7729. PubMed
Dyall SD, Johnson PJ. Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol. 2000;3: 404–11. 10.1016/s1369-5274(00)00112-0 PubMed DOI
Bradley PJ, Lahti CJ, Plümper E, Johnson PJ. Targeting and translocation of proteins into the hydrogenosome of the protist Trichomonas: similarities with mitochondrial protein import. EMBO J. 1997;16: 3484–93. 10.1093/emboj/16.12.3484 PubMed DOI PMC
Kulda J. Trichomonads, hydrogenosomes and drug resistance. Int J Parasitol. 1999;29: 199–212. 10.1016/s0020-7519(98)00155-6 PubMed DOI
Benchimol M, Johnson PJ, Souza W. Morphogenesis of the hydrogenosome: An ultrastructural study. Biol Cell. 1996;87: 197–205. PubMed
Benchimol M. Hydrogenosomes under microscopy. Tissue Cell. 2009;41: 151–168. 10.1016/j.tice.2009.01.001 PubMed DOI
Morin-Adeline V, Šlapeta J. The past, present and future of fluorescent protein tags in anaerobic protozoan parasites. Parasitology. 2016;143: 260–275. 10.1017/S0031182015001663 PubMed DOI
Martincová E, Voleman L, Najdrová V, De Napoli M, Eshar S, Gualdron M, et al. Live imaging of mitosomes and hydrogenosomes by HaloTag technology. PLoS ONE. 2012;7: e36314 10.1371/journal.pone.0036314 PubMed DOI PMC
Wexler-Cohen Y, Stevens GC, Barnoy E, van der Bliek AM, Johnson PJ. A dynamin-related protein contributes to Trichomonas vaginalis hydrogenosomal fission. FASEB J. 2014;28: 1113–1121. 10.1096/fj.13-235473 PubMed DOI PMC
Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 2003;426: 172–176. 10.1038/nature01945 PubMed DOI
Pyrihová E, Motyčková A, Voleman L, Wandyszewska N, Fišer R, Seydlová G, et al. A Single Tim translocase in the mitosomes of Giardia intestinalis illustrates convergence of protein import machines in anaerobic eukaryotes. Genome Biol Evol. 2018;10: 2813–2822. 10.1093/gbe/evy215 PubMed DOI PMC
Jedelský PL, Doležal P, Rada P, Pyrih J, Smíd O, Hrdý I, et al. The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS ONE. 2011;6: e17285 10.1371/journal.pone.0017285 PubMed DOI PMC
Rout S, Zumthor JP, Schraner EM, Faso C, Hehl AB. An interactome-centered protein discovery approach reveals novel components involved in mitosome function and homeostasis in Giardia lamblia. PLoS Pathog. 2016;12: e1006036 10.1371/journal.ppat.1006036 PubMed DOI PMC
Regoes A. Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem. 2005;280: 30557–30563. 10.1074/jbc.M500787200 PubMed DOI
Midlej V, Penha L, Silva R, de Souza W, Benchimol M. Mitosomal chaperone modulation during the life cycle of the pathogenic protist Giardia intestinalis. Eur J Cell Biol. 2016;95: 531–542. 10.1016/j.ejcb.2016.08.005 PubMed DOI
Voleman L, Najdrová V, Ástvaldsson Á, Tůmová P, Einarsson E, Švindrych Z, et al. Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum. BMC Biol. 2017;15: 27 10.1186/s12915-017-0361-y PubMed DOI PMC
Gaechter V, Schraner E, Wild P, Hehl AB. The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic. 2008;9: 57–71. 10.1111/j.1600-0854.2007.00657.x PubMed DOI
Wideman JG, Gawryluk RMR, Gray MW, Dacks JB. The ancient and widespread nature of the ER-mitochondria encounter structure. Mol Biol Evol. 2013;30: 2044–9. 10.1093/molbev/mst120 PubMed DOI
Tovar J, Fischer A, Clark CG. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol. 1999;32: 1013–21. 10.1046/j.1365-2958.1999.01414.x PubMed DOI
Mi-ichi F, Yousuf MA, Nakada-Tsukui K, Nozaki T. Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci. 2009;106: 21731–21736. 10.1073/pnas.0907106106 PubMed DOI PMC
Mi-ichi F, Miyamoto T, Takao S, Jeelani G, Hashimoto T, Hara H, et al. Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. Proc Natl Acad Sci. 2015;112: E2884–E2890. 10.1073/pnas.1423718112 PubMed DOI PMC
Jain R, Shrimal S, Bhattacharya S, Bhattacharya A. Identification and partial characterization of a dynamin-like protein, EhDLP1, from the protist parasite Entamoeba histolytica. Eukaryot Cell. 2010;9: 215–223. 10.1128/EC.00214-09 PubMed DOI PMC
Makiuchi T, Santos HJ, Tachibana H, Nozaki T. Hetero-oligomer of dynamin-related proteins participates in the fission of highly divergent mitochondria from Entamoeba histolytica. Sci Rep. 2017;7: 13439 10.1038/s41598-017-13721-5 PubMed DOI PMC
Kazama M, Ogiwara S, Makiuchi T, Yoshida K, Nakada-Tsukui K, Nozaki T, et al. Behavior of DNA-lacking mitochondria in Entamoeba histolytica revealed by organelle transplant. Sci Rep. 2017;7: 44273 10.1038/srep44273 PubMed DOI PMC
Roger AJ, Muñoz-Gómez SA, Kamikawa R. The origin and diversification of mitochondria. Curr Biol. 2017;27: R1177–R1192. 10.1016/j.cub.2017.09.015 PubMed DOI
Leger MM, Petrů M, Žárský V, Eme L, Vlček Č, Harding T, et al. An ancestral bacterial division system is widespread in eukaryotic mitochondria. Proc Natl Acad Sci U S A. 2015;112: 10239–46. 10.1073/pnas.1421392112 PubMed DOI PMC
Purkanti R, Thattai M. Ancient dynamin segments capture early stages of host-mitochondrial integration. Proc Natl Acad Sci U S A. 2015;112: 2800–5. 10.1073/pnas.1407163112 PubMed DOI PMC
Maeda-Sano K, Sato S, Ueda T, Yui R, Ito K, Hata M, et al. Visualization of mitochondrial and apicoplast nucleoids in the human malaria parasite Plasmodium falciparum by SYBR green I and PicoGreen staining. Cytologia (Tokyo). 2009;74: 449–455.
Matsuzaki M, Kikuchi T, Kita K, Kojima S, Kuroiwa T. Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma. 2001;218: 180–91. PubMed
van der Laan M, Bohnert M, Wiedemann N, Pfanner N. Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends Cell Biol. 2012;22: 185–92. 10.1016/j.tcb.2012.01.004 PubMed DOI
Wideman JG, Muñoz-Gómez SA. The evolution of ERMIONE in mitochondrial biogenesis and lipid homeostasis: An evolutionary view from comparative cell biology. Biochim Biophys Acta. 2016; PubMed
Kaurov I, Vancová M, Schimanski B, Cadena LR, Heller J, Bílý T, et al. The diverged Trypanosome MICOS complex as a hub for mitochondrial cristae shaping and protein import. Curr Biol. 2018;28: 3393–3407.e5. 10.1016/j.cub.2018.09.008 PubMed DOI
Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004;304: 441–445. 10.1126/science.1094786 PubMed DOI
Schnarwiler F, Niemann M, Doiron N, Harsman A, Kaser S, Mani J, et al. Trypanosomal TAC40 constitutes a novel subclass of mitochondrial β-barrel proteins specialized in mitochondrial genome inheritance. Proc Natl Acad Sci. 2014;111: 7624–7629. 10.1073/pnas.1404854111 PubMed DOI PMC
Niemann M, Wiese S, Mani J, Chanfon A, Jackson C, Meisinger C, et al. Mitochondrial outer membrane proteome of Trypanosoma brucei reveals novel factors required to maintain mitochondrial morphology. Mol Cell Proteomics. 2013;12: 515–28. 10.1074/mcp.M112.023093 PubMed DOI PMC
Williams RAM, Smith TK, Cull B, Mottram JC, Coombs GH. ATG5 is essential for ATG8-dependent autophagy and mitochondrial homeostasis in Leishmania major. PLoS Pathog. 2012;8: e1002695 10.1371/journal.ppat.1002695 PubMed DOI PMC
Benchimol M. Hydrogenosome autophagy: An ultrastructural and cytochemical study. Biol Cell. 1999;91: 165–174. 10.1016/s0248-4900(99)80039-2 PubMed DOI
Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, et al. Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes. J Eukaryot Microbiol. 2019;66: 4–119. 10.1111/jeu.12691 PubMed DOI PMC