Mitochondrial dynamics in parasitic protists

Autoři: Luboš Voleman aff001;  Pavel Doležal aff001
Působiště autorů: Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic aff001
Vyšlo v časopise: Mitochondrial dynamics in parasitic protists. PLoS Pathog 15(11): e32767. doi:10.1371/journal.ppat.1008008
Kategorie: Review
doi: 10.1371/journal.ppat.1008008


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.

Klíčová slova:

Cell cycle and cell division – Cellular structures and organelles – Mitochondria – Parasitic life cycles – Protists – Toxoplasma gondii – Trypanosoma – Parasitic cell cycles


1. Friedman JR, Nunnari J. Mitochondrial form and function. Nature. 2014;505: 335–43. doi: 10.1038/nature12985 24429632

2. Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol. 2014;15: 634–46. doi: 10.1038/nrm3877 25237825

3. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337: 1062–1065. doi: 10.1126/science.1219855 22936770

4. 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. doi: 10.1083/jcb.200712101 18573913

5. Labbé K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol. 2014;30: 357–91. doi: 10.1146/annurev-cellbio-101011-155756 25288115

6. 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. doi: 10.1083/jcb.200506078 16186251

7. 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. doi: 10.1038/s41586-018-0211-2 29899447

8. Liu R, Chan DC. The mitochondrial fission receptor Mff selectively recruits oligomerized Drp1. Mol Biol Cell. 2015;26: 4466–77. doi: 10.1091/mbc.E15-08-0591 26446846

9. 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. doi: 10.1083/jcb.151.2.367 11038183

10. 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. doi: 10.1083/jcb.200503148 16009724

11. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science. 2011;334: 358–62. doi: 10.1126/science.1207385 21885730

12. 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. doi: 10.7554/eLife.00422 23682313

13. 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. doi: 10.1126/science.1175088 19556461

14. 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. doi: 10.1083/jcb.200211046 12527753

15. Hales KG, Fuller MT. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 1997;90: 121–9. doi: 10.1016/s0092-8674(00)80319-0 9230308

16. Sesaki H, Jensen RE. Ugo1p links the Fzo1p and Mgm1p GTPases for mitochondrial fusion. J Biol Chem. 2004;279: 28298–28303. doi: 10.1074/jbc.M401363200 15087460

17. 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. doi: 10.1038/ng.3354 26168012

18. Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12: 9–14. doi: 10.1038/nrm3028 21179058

19. 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. doi: 10.1083/jcb.201206112 22986493

20. Cowman AF, Healer J, Marapana D, Marsh K. Malaria: biology and disease. Cell. 2016;167: 610–624. doi: 10.1016/j.cell.2016.07.055 27768886

21. 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. doi: 10.1016/j.celrep.2015.03.011 25843709

22. Krungkrai J, Prapunwattana P, Krungkrai SR. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite. 2000;7: 19–26. doi: 10.1051/parasite/2000071019 10743643

23. 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. doi: 10.1111/j.1365-2958.2005.04699.x 15978074

24. 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. doi: 10.1126/science.275.5305.1485 9045615

25. 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. doi: 10.1016/S1434-4610(99)70030-1 10575701

26. Arisue N, Hashimoto T. Phylogeny and evolution of apicoplasts and apicomplexan parasites. Parasitol Int. 2015;64: 254–259. doi: 10.1016/j.parint.2014.10.005 25451217

27. Lim L, McFadden GI. The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci. 2010;365: 749–63. doi: 10.1098/rstb.2009.0273 20124342

28. 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. doi: 10.1111/j.1462-5822.2011.01657.x 21801293

29. 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. doi: 10.1042/BC20080202 19143588

30. Okamoto N, Spurck TP, Goodman CD, McFadden GI. Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryot Cell. 2009;8: 128–132. doi: 10.1128/EC.00267-08 18996983

31. 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. doi: 10.1126/science.aad9279 27081071

32. 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. doi: 10.1016/j.bbrc.2004.06.010 15240099

33. 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. doi: 10.1016/j.micinf.2007.02.020 17533148

34. 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. doi: 10.1016/j.cub.2009.01.039 19217293

35. van Dooren GG, Stimmler LM, McFadden GI. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev. 2006;30: 596–630. doi: 10.1111/j.1574-6976.2006.00027.x 16774588

36. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30: 1217–58. doi: 10.1016/s0020-7519(00)00124-7 11113252

37. Melo EJL, Attias M, De Souza W. The single mitochondrion of tachyzoites of Toxoplasma gondii. J Struct Biol. 2000;130: 27–33. doi: 10.1006/jsbi.2000.4228 10806088

38. Francia ME, Striepen B. Cell division in apicomplexan parasites. Nat Rev Microbiol. 2014;12: 125–136. doi: 10.1038/nrmicro3184 24384598

39. Nishi M, Hu K, Murray JM, Roos DS. Organellar dynamics during the cell cycle of Toxoplasma gondii. J Cell Sci. 2008;121: 1559–68. doi: 10.1242/jcs.021089 18411248

40. 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. doi: 10.1016/j.cub.2008.12.048 19217294

41. 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. doi: 10.1111/mmi.14138 30362624

42. 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. doi: 10.1371/journal.ppat.1007512 30947298

43. Harding CR, Meissner M. The inner membrane complex through development of Toxoplasma gondii and Plasmodium. Cell Microbiol. 2014;16: 632–641. doi: 10.1111/cmi.12285 24612102

44. Ovciarikova J, Lemgruber L, Stilger KL, Sullivan WJ, Sheiner L. Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii. Sci Rep. 2017;7: 42746. doi: 10.1038/srep42746 28202940

45. Ghosh D, Walton JL, Roepe PD, Sinai AP. Autophagy is a cell death mechanism in Toxoplasma gondii. Cell Microbiol. 2012;14: 589–607. doi: 10.1111/j.1462-5822.2011.01745.x 22212386

46. 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. doi: 10.1371/journal.ppat.1002416 22144900

47. 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. doi: 10.1371/journal.pntd.0001859 23145192

48. 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. doi: 10.1016/bs.ircmb.2014.11.001 25708462

49. 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. doi: 10.1016/j.chom.2016.05.002 27237364

50. 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. doi: 10.1038/srep36565 27874016

51. 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. doi: 10.1128/EC.1.4.495-502.2002 12455998

52. 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. doi: 10.1091/mbc.E02-08-0525 12802053

53. 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.

54. Robinson DR, Gull K. Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature. 1991;352: 731–733. doi: 10.1038/352731a0 1876188

55. 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.

56. 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. doi: 10.1242/jcs.03023 16787942

57. Schneider A, Ochsenreiter T. Failure is not an option–mitochondrial genome segregation in trypanosomes. J Cell Sci. 2018;131: jcs221820. doi: 10.1242/jcs.221820 30224426

58. 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. doi: 10.1074/jbc.M312178200 14670954

59. 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. doi: 10.1371/journal.pone.0177200 28481934

60. 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. doi: 10.1038/ncomms9078 26307671

61. Shaw JM, Nunnari J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 2002;12: 178–84. doi: 10.1016/s0962-8924(01)02246-2 11978537

62. Peacock L, Ferris V, Bailey M, Gibson W. Mating compatibility in the parasitic protist Trypanosoma brucei. Parasit Vectors. 2014;7: 78. doi: 10.1186/1756-3305-7-78 24559099

63. 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. doi: 10.1038/sj.embor.7400095 14968134

64. 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. doi: 10.1371/journal.pone.0202711 30592713

65. Bouchemal K, Bories C, Loiseau PM. Strategies for prevention and treatment of Trichomonas vaginalis infections. Clin Microbiol Rev. 2017;30: 811–825. doi: 10.1128/CMR.00109-16 28539504

66. 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. 4750424

67. Dyall SD, Johnson PJ. Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol. 2000;3: 404–11. doi: 10.1016/s1369-5274(00)00112-0 10972502

68. 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. doi: 10.1093/emboj/16.12.3484 9218791

69. Kulda J. Trichomonads, hydrogenosomes and drug resistance. Int J Parasitol. 1999;29: 199–212. doi: 10.1016/s0020-7519(98)00155-6 10221623

70. Benchimol M, Johnson PJ, Souza W. Morphogenesis of the hydrogenosome: An ultrastructural study. Biol Cell. 1996;87: 197–205. 9075329

71. Benchimol M. Hydrogenosomes under microscopy. Tissue Cell. 2009;41: 151–168. doi: 10.1016/j.tice.2009.01.001 19297000

72. Morin-Adeline V, Šlapeta J. The past, present and future of fluorescent protein tags in anaerobic protozoan parasites. Parasitology. 2016;143: 260–275. doi: 10.1017/S0031182015001663 26653973

73. 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. doi: 10.1371/journal.pone.0036314 22558433

74. 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. doi: 10.1096/fj.13-235473 24297697

75. 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. doi: 10.1038/nature01945 14614504

76. 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. doi: 10.1093/gbe/evy215 30265292

77. 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. doi: 10.1371/journal.pone.0017285 21390322

78. 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. doi: 10.1371/journal.ppat.1006036 27926928

79. Regoes A. Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem. 2005;280: 30557–30563. doi: 10.1074/jbc.M500787200 15985435

80. 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. doi: 10.1016/j.ejcb.2016.08.005 27608965

81. 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. doi: 10.1186/s12915-017-0361-y 28372543

82. 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. doi: 10.1111/j.1600-0854.2007.00657.x 17892527

83. 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. doi: 10.1093/molbev/mst120 23813918

84. 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. doi: 10.1046/j.1365-2958.1999.01414.x 10361303

85. 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. doi: 10.1073/pnas.0907106106 19995967

86. 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. doi: 10.1073/pnas.1423718112 25986376

87. 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. doi: 10.1128/EC.00214-09 19915078

88. 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. doi: 10.1038/s41598-017-13721-5 29044162

89. 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. doi: 10.1038/srep44273 28287148

90. Roger AJ, Muñoz-Gómez SA, Kamikawa R. The origin and diversification of mitochondria. Curr Biol. 2017;27: R1177–R1192. doi: 10.1016/j.cub.2017.09.015 29112874

91. 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. doi: 10.1073/pnas.1421392112 25831547

92. 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. doi: 10.1073/pnas.1407163112 25691734

93. 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.

94. 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. 11770434

95. 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. doi: 10.1016/j.tcb.2012.01.004 22386790

96. 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;

97. 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. doi: 10.1016/j.cub.2018.09.008 30415698

98. 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. doi: 10.1126/science.1094786 15044751

99. 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. doi: 10.1073/pnas.1404854111 24821793

100. 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. doi: 10.1074/mcp.M112.023093 23221899

101. 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. doi: 10.1371/journal.ppat.1002695 22615560

102. Benchimol M. Hydrogenosome autophagy: An ultrastructural and cytochemical study. Biol Cell. 1999;91: 165–174. doi: 10.1016/s0248-4900(99)80039-2 10425703

103. 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. doi: 10.1111/jeu.12691 30257078

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Inhibitory karboanhydrázy v léčbě glaukomu
Autoři: MUDr. Petr Výborný, CSc., FEBO

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