Advertisement

Amebiasis pp 305-327 | Cite as

Mitosomes in Entamoeba histolytica

  • Takashi Makiuchi
  • Fumika Mi-ichi
  • Tomoyoshi Nozaki
Chapter

Abstract

Mitosomes are highly divergent, often reduced, mitochondrion-derived organelles. Mitosomes in Entamoeba histolytica possess a unique metabolic role that has not been discovered in other eukaryotes. Sulfate activation, in which sulfate is activated with two ATP molecules to form 3′-phosphoadenosine-5′-phosphosulfate, is compartmentalized in Entamoeba mitosomes. Sulfate activation is essential for the production of sulfur-containing polar lipids and proliferation of trophozoites. Besides its unique metabolic role, the mechanisms of protein and solute transport across mitosomal double membranes are also highly divergent from other eukaryotes. For instance, the translocator of the outer membrane consists of the β-barrel pore component Tom40 and the unique peripheral membrane component Tom60, the latter of which is localized to both the mitosomal outer membrane and the cytoplasm and functions as a shuttle carrier of mitosomal proteins. In this chapter, we summarize the discovery, functions, and protein transport of Entamoeba mitosomes, and also discuss remaining important biochemical and biological riddles of mitosomes, including other metabolic functions, redox control, regulation of gene expression, solute/metabolite transport, replication, and degradation.

Keywords

Intermembrane Space Entamoeba Histolytica Sulfate Activation Mitochondrial Target Signal Mitochondrial Carrier Family 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature (Lond) 326:332–333Google Scholar
  2. 2.
    Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75–77PubMedGoogle Scholar
  3. 3.
    Leipe DD, Gunderson JH, Nerad TA, Sogin ML (1993) Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59:41–48PubMedGoogle Scholar
  4. 4.
    Hashimoto T, Hasegawa M (1996) Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1alpha/Tu and 2/G. Adv Biophys 32:73–120PubMedGoogle Scholar
  5. 5.
    Müller M (1992) Energy metabolism of ancestral eukaryotes: a hypothesis based on the biochemistry of amitochondriate parasitic protists. Biosystems 28:33–40PubMedGoogle Scholar
  6. 6.
    Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci USA 92:6518–6521PubMedCentralPubMedGoogle Scholar
  7. 7.
    Soltys BJ, Gupta RS (1994) Presence and cellular distribution of a 60-kDa protein related to mitochondrial hsp60 in Giardia lamblia. J Parasitol 80:580–590PubMedGoogle Scholar
  8. 8.
    Bui ET, Bradley PJ, Johnson PJ (1996) A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 93:9651–9656PubMedCentralPubMedGoogle Scholar
  9. 9.
    Germot A, Philippe H, Le Guyader H (1996) Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc Natl Acad Sci USA 93:14614–14617PubMedCentralPubMedGoogle Scholar
  10. 10.
    Roger AJ, Clark CG, Doolittle WF (1996) A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc Natl Acad Sci USA 93:14618–14622PubMedCentralPubMedGoogle Scholar
  11. 11.
    Germot A, Philippe H, Le Guyader H (1997) Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol 87:159–168PubMedGoogle Scholar
  12. 12.
    Hirt RP, Healy B, Vossbrinck CR, Canning EU, Embley TM (1997) A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr Biol 7:995–998PubMedGoogle Scholar
  13. 13.
    Peyretaillade E, Broussolle V, Peyret P, Méténier G, Gouy M, Vivarès CP (1998) Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Mol Biol Evol 15:683–689PubMedGoogle Scholar
  14. 14.
    Morrison HG, Roger AJ, Nystul TG, Gillin FD, Sogin ML (2001) Giardia lamblia expresses a proteobacterial-like DnaK homolog. Mol Biol Evol 18:530–541PubMedGoogle Scholar
  15. 15.
    Bozner P (1997) Immunological detection and subcellular localization of Hsp70 and Hsp60 homologs in Trichomonas vaginalis. J Parasitol 83:224–229PubMedGoogle Scholar
  16. 16.
    Williams BA, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature (Lond) 418:865–869Google Scholar
  17. 17.
    Putignani L, Tait A, Smith HV, Horner D, Tovar J, Tetley L, Wastling JM (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129:1–18PubMedGoogle Scholar
  18. 18.
    Slapeta J, Keithly JS (2004) Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryot Cell 3:483–494PubMedCentralPubMedGoogle Scholar
  19. 19.
    Maralikova B, Ali V, Nakada-Tsukui K, Nozaki T, van der Giezen M, Henze K, Tovar J (2010) Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell Microbiol 12:331–342PubMedGoogle Scholar
  20. 20.
    Mi-ichi F, Makiuchi T, Furukawa A, Sato D, Nozaki T (2011) Sulfate activation in mitosomes plays an important role in the proliferation of Entamoeba histolytica. PLoS Negl Trop Dis 5:e1263PubMedCentralPubMedGoogle Scholar
  21. 21.
    Mai Z, Ghosh S, Frisardi M, Rosenthal B, Rogers R, Samuelson J (1999) Hsp60 is targeted to a cryptic mitochondrion-derived organelle (“crypton”) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19:2198–2205PubMedCentralPubMedGoogle Scholar
  22. 22.
    Hjort K, Goldberg AV, Tsaousis AD, Hirt RP, Embley TM (2010) Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos Trans R Soc Lond B Biol Sci 365:713–727PubMedCentralPubMedGoogle Scholar
  23. 23.
    Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495PubMedCentralPubMedGoogle Scholar
  24. 24.
    Margulis L (1970) Origin of eukaryotic cells; evidence and research implications for a theory of the origin and evolution of microbial, plant, and animal cells on the Precambrian earth, vol 22. Yale University Press, New Haven, p 349Google Scholar
  25. 25.
    Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447PubMedCentralPubMedGoogle Scholar
  26. 26.
    Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC et al (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature (Lond) 396:133–140Google Scholar
  27. 27.
    Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716PubMedGoogle Scholar
  28. 28.
    Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112–123PubMedCentralPubMedGoogle Scholar
  29. 29.
    Bartlett K, Eaton S (2004) Mitochondrial beta-oxidation. Eur J Biochem 271:462–469PubMedGoogle Scholar
  30. 30.
    Maechler P, Carobbio S, Rubi B (2006) In beta-cells, mitochondria integrate and generate metabolic signals controlling insulin secretion. Int J Biochem Cell Biol 38:696–709PubMedGoogle Scholar
  31. 31.
    Susin SA, Lorenzo HK, Zamzami N (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature (Lond) 397:441–446Google Scholar
  32. 32.
    Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol 529:57–68PubMedCentralPubMedGoogle Scholar
  33. 33.
    Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25:352–356PubMedGoogle Scholar
  34. 34.
    van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525–530PubMedCentralPubMedGoogle Scholar
  35. 35.
    Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32:1013–1021PubMedGoogle Scholar
  36. 36.
    Regoes A, Zourmpanou D, León-Avila G, van der Giezen M, Tovar J, Hehl AB (2005) Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem 280:30557–30563PubMedGoogle Scholar
  37. 37.
    Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature (Lond) 426:172–176Google Scholar
  38. 38.
    Sutak R, Dolezal P, Fiumera HL, Hrdy I, Dancis A, Delgadillo-Correa M, Johnson PJ, Müller M, Tachezy J (2004) Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc Natl Acad Sci USA 101:10368–10373PubMedCentralPubMedGoogle Scholar
  39. 39.
    Goldberg AV, Molik S, Tsaousis AD, Neumann K, Kuhnke G, Delbac F, Vivares CP, Hirt RP, Lill R, Embley TM (2008) Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature (Lond) 452:624–628Google Scholar
  40. 40.
    Tsaousis AD, Ollagnier de Choudens S, Gentekaki E, Long S, Gaston D, Stechmann A, Vinella D, Py B, Fontecave M, Barras F, Lukeš J, Roger AJ (2012) Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc Natl Acad Sci USA 109:10426–10431PubMedCentralPubMedGoogle Scholar
  41. 41.
    Wawrzyniak I, Roussel M, Diogon M, Couloux A, Texier C, Tan KS, Vivarès CP, Delbac F, Wincker P, El Alaoui H (2008) Complete circular DNA in the mitochondria-like organelles of Blastocystis hominis. Int J Parasitol 38:1377–1382PubMedGoogle Scholar
  42. 42.
    Barberà MJ, Ruiz-Trillo I, Tufts JY, Bery A, Silberman JD, Roger AJ (2010) Sawyeria marylandensis (Heterolobosea) has a hydrogenosome with novel metabolic properties. Eukaryot Cell 9:1913–1924PubMedCentralPubMedGoogle Scholar
  43. 43.
    Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236:729–739PubMedCentralPubMedGoogle Scholar
  44. 44.
    Gill EE, Diaz-Triviño S, Barberà MJ, Silberman JD, Stechmann A, Gaston D, Tamas I, Roger AJ (2007) Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol Microbiol 66:1306–1320PubMedGoogle Scholar
  45. 45.
    Morada M, Smid O, Hampl V, Sutak R, Lam B, Rappelli P, Dessì D, Fiori PL, Tachezy J, Yarlett N (2011) Hydrogenosome-localization of arginine deiminase in Trichomonas vaginalis. Mol Biochem Parasitol 176:51–54PubMedCentralPubMedGoogle Scholar
  46. 46.
    Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, Xie Y, Loo JA, Johnson PJ (2011) The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol 41:1421–1434PubMedGoogle Scholar
  47. 47.
    Jedelský PL, Doležal P, Rada P, Pyrih J, Smíd O, Hrdý I, Sedinová M, Marcinčiková M, Voleman L, Perry AJ, Beltrán NC, Lithgow T, Tachezy J (2011) The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One 6:e17285PubMedCentralPubMedGoogle Scholar
  48. 48.
    Mogi T, Kita K (2010) Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 59:305–312PubMedGoogle Scholar
  49. 49.
    Pérez-Brocal V, Clark CG (2008) Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content and genome organization. Mol Biol Evol 25:2475–2482PubMedCentralPubMedGoogle Scholar
  50. 50.
    Stechmann A, Hamblin K, Pérez-Brocal V, Gaston D, Richmond GS, van der Giezen M, Clark CG, Roger AJ (2008) Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18:580–585PubMedCentralPubMedGoogle Scholar
  51. 51.
    Mi-ichi F, Yousuf MA, Nakada-Tsukui K, Nozaki T (2009) Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci USA 106:21731–21736PubMedCentralPubMedGoogle Scholar
  52. 52.
    Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:1–14Google Scholar
  53. 53.
    Brunold C, Schiff JA (1976) Studies of sulfate utilization of algae: 15. Enzymes of assimilatory sulfate reduction in Euglena and their cellular localization. Plant Physiol 57:430–436PubMedCentralPubMedGoogle Scholar
  54. 54.
    Saidha T, Na SQ, Li JY, Schiff JA (1988) A sulphate metabolizing centre in Euglena mitochondria. Biochem J 253:533–539PubMedCentralPubMedGoogle Scholar
  55. 55.
    Venkatachalam KV (2003) Human 3′-phosphoadenosine 5′-phosphosulfate (PAPS) synthase: biochemistry, molecular biology and genetic deficiency. IUBMB Life 55:1–11PubMedGoogle Scholar
  56. 56.
    Schwartz NB, Lyle S, Ozeran JD, Li H, Deyrup A, Ng K, Westley J (1998) Sulfate activation and transport in mammals: system components and mechanisms. Chem Biol Interact 109:143–151PubMedGoogle Scholar
  57. 57.
    Schwartz NB (2005) PAPS and sulfoconjugation human cystolic sulfotransferases. Taylor & Francis, London, pp 43–57Google Scholar
  58. 58.
    Heinonen JK (2001) Biological role of inorganic pyrophosphate. Kluwer Academic, Boston/Dordrecht/LondonGoogle Scholar
  59. 59.
    Bakker-Grunwald T, Geilhorn B (1992) Sulfate metabolism in Entamoeba histolytica. Mol Biochem Parasitol. 53:71–78Google Scholar
  60. 60.
    Bradley ME, Rest JS, Li WH, Schwartz NB (2009) Sulfate activation enzymes: phylogeny and association with pyrophosphatase. J Mol Evol 68:1–13PubMedGoogle Scholar
  61. 61.
    Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M, Bauer M, Zibat A, Lombardot T, Becker I, Amann J, Gellner K, Teeling H, Leuschner WD, Glöckner FO, Lupas AN, Amann R, Klenk HP (2004) The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6:887–902PubMedGoogle Scholar
  62. 62.
    Gómez-García MR, Losada M, Serrano A (2006) A novel subfamily of monomeric inorganic pyrophosphatases in photosynthetic eukaryotes. Biochem J 395:211–221PubMedCentralPubMedGoogle Scholar
  63. 63.
    Kunji ER, Robinson AJ (2010) Coupling of proton and substrate translocation in the transport cycle of mitochondrial carriers. Curr Opin Struct Biol 20:440–447PubMedGoogle Scholar
  64. 64.
    Chan KW, Slotboom DJ, Cox S, Embley TM, Fabre O, van der Giezen M, Harding M, Horner DS, Kunji ER, León-Avila G, Tovar J (2005) A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr Biol 15:737–742PubMedGoogle Scholar
  65. 65.
    Dolezal P, Dagley MJ, Kono M, Wolynec P, Likić VA, Foo JH, Sedinová M, Tachezy J, Bachmann A, Bruchhaus I, Lithgow T (2010) The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6:e1000812PubMedCentralPubMedGoogle Scholar
  66. 66.
    Black PN, DiRusso CC (2007) Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation. Biochim Biophys Acta 1771:286–298PubMedGoogle Scholar
  67. 67.
    Soupene E, Kuypers FA (2008) Mammalian long-chain acyl-CoA synthetases. Exp Biol Med (Maywood) 233:507–521Google Scholar
  68. 68.
    Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 100:13207–13212PubMedCentralPubMedGoogle Scholar
  69. 69.
    Zou Z, Tong F, Faergeman NJ, Børsting C, Black PN, DiRusso CC (2003) Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex. J Biol Chem 278:16414–16422PubMedGoogle Scholar
  70. 70.
    Athenstaedt K, Zweytick D, Jandrositz A, Kohlwein SD, Daum G (1999) Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J Bacteriol 181:6441–6448PubMedCentralPubMedGoogle Scholar
  71. 71.
    Natter K, Leitner P, Faschinger A, Wolinski H, McCraith S, Fields S, Kohlwein SD (2005) The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol Cell Proteomics 4:662–672PubMedGoogle Scholar
  72. 72.
    Zhan T, Poppelreuther M, Ehehalt R, Füllekrug J (2012) Overexpressed FATP1, ACSVL4/FATP4 and ACSL1 increase the cellular fatty acid uptake of 3T3-L1 adipocytes but are localized on intracellular membranes. PLoS One 7:e45087PubMedCentralPubMedGoogle Scholar
  73. 73.
    Nakada-Tsukui K, Tsuboi K, Furukawa A, Yamada Y, Nozaki T (2012) A novel class of cysteine protease receptors that mediate lysosomal transport. Cell Microbiol 14:1299–1317PubMedCentralPubMedGoogle Scholar
  74. 74.
    Ali V, Shigeta Y, Tokumoto U, Takahashi Y, Nozaki T (2004) An intestinal parasitic protist, Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J Biol Chem 279:16863–16874PubMedGoogle Scholar
  75. 75.
    Choi MH, Sajed D, Poole L, Hirata K, Herdman S, Torian BE, Reed SL (2005) An unusual surface peroxiredoxin protects invasive Entamoeba histolytica from oxidant attack. Mol Biochem Parasitol 143:80–89PubMedGoogle Scholar
  76. 76.
    Arias DG, Gutierrez CE, Iglesias AA, Guerrero SA (2007) Thioredoxin-linked metabolism in Entamoeba histolytica. Free Radic Biol Med 42:1496–1505PubMedGoogle Scholar
  77. 77.
    Davis PH, Zhang X, Guo J, Townsend RR, Stanley SL Jr (2006) Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Mol Microbiol 61:1523–1532PubMedGoogle Scholar
  78. 78.
    Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature (Lond) 433:865–868Google Scholar
  79. 79.
    LeGall J, Prickril BC, Moura I, Xavier AV, Moura JJ, Huynh BH (1988) Isolation and characterization of rubrerythrin, a non-heme iron protein from Desulfovibrio vulgaris that contains rubredoxin centers and a hemerythrin-like binuclear iron cluster. Biochemistry 27:1636–1642PubMedGoogle Scholar
  80. 80.
    Lehmann Y, Meile L, Teuber M (1996) Rubrerythrin from Clostridium perfringens: cloning of the gene, purification of the protein, and characterization of its superoxide dismutase function. J Bacteriol 178:7152–7158PubMedCentralPubMedGoogle Scholar
  81. 81.
    Alban PS, Popham DL, Rippere KE, Krieg NR (1998) Identification of a gene for a rubrerythrin/nigerythrin-like protein in Spirillum volutans by using amino acid sequence data from mass spectrometry and NH2-terminal sequencing. J Appl Microbiol 85:875–882PubMedGoogle Scholar
  82. 82.
    Das A, Coulter ED, Kurtz DM, Ljungdahl LG (2001) Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidoreductase-rubredoxin and rubrerythrin-type A flavoprotein-high-molecular-weight rubredoxin. J Bacteriol 183:1560–1567PubMedCentralPubMedGoogle Scholar
  83. 83.
    Sztukowska M, Bugno M, Potempa J, Travis J, Kurtz DM (2002) Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol 44:479–488PubMedGoogle Scholar
  84. 84.
    Weinberg MV, Jenney FE, Cui X, Adams MW (2004) Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol 186:7888–7895PubMedCentralPubMedGoogle Scholar
  85. 85.
    Pütz S, Gelius-Dietrich G, Piotrowski M, Henze K (2005) Rubrerythrin and peroxiredoxin: two novel putative peroxidases in the hydrogenosomes of the microaerophilic protozoon Trichomonas vaginalis. Mol Biochem Parasitol 142:212–223PubMedGoogle Scholar
  86. 86.
    Bruchhaus I, Tannich E (1994) Induction of the iron-containing superoxide dismutase in Entamoeba histolytica by a superoxide anion-generating system or by iron chelation. Mol Biochem Parasitol 67:281–288PubMedGoogle Scholar
  87. 87.
    Miriyala S, Holley AK, St. Clair DK (2011) Mitochondrial superoxide dismutase: signals of distinction. Anticancer Agents Med Chem 11:181–190PubMedCentralPubMedGoogle Scholar
  88. 88.
    Kang JM, Cheun HI, Kim J, Moon SU, Park SJ, Kim TS, Sohn WM, Na BK (2008) Identification and characterization of a mitochondrial iron-superoxide dismutase of Cryptosporidium parvum. Parasitol Res 103:787–795PubMedGoogle Scholar
  89. 89.
    Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–644PubMedCentralPubMedGoogle Scholar
  90. 90.
    Likic VA, Dolezal P, Celik N, Dagley M, Lithgow T (2010) Using hidden Markov models to discover new protein transport machines. Methods Mol Biol 619:271–284PubMedGoogle Scholar
  91. 91.
    Truscott KN, Brandner K, Pfanner N (2003) Mechanisms of protein import into mitochondria. Curr Biol 13:R326–R337PubMedGoogle Scholar
  92. 92.
    Yousuf MA, Mi-ichi F, Nakada-Tsukui K, Nozaki T (2010) Localization and targeting of an unusual pyridine nucleotide transhydrogenase in Entamoeba histolytica. Eukaryot Cell 9:926–933PubMedCentralPubMedGoogle Scholar
  93. 93.
    Brown MT, Goldstone HM, Bastida-Corcuera F, Delgadillo-Correa MG, McArthur AG, Johnson PJ (2007) A functionally divergent hydrogenosomal peptidase with protomitochondrial ancestry. Mol Microbiol 64:1154–1163PubMedGoogle Scholar
  94. 94.
    Smíd O, Matusková A, Harris SR, Kucera T, Novotný M, Horváthová L, Hrdý I, Kutejová E, Hirt RP, Embley TM, Janata J, Tachezy J (2008) Reductive evolution of the mitochondrial processing peptidases of the unicellular parasites Trichomonas vaginalis and Giardia intestinalis. PLoS Pathog 4:e1000243PubMedCentralPubMedGoogle Scholar
  95. 95.
    Dolezal P, Smíd O, Rada P, Zubácová Z, Bursać D, Suták R, Nebesárová J, Lithgow T, Tachezy J (2005) Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci USA 102:10924–10929PubMedCentralPubMedGoogle Scholar
  96. 96.
    Burri L, Williams BA, Bursac D, Lithgow T, Keeling PJ (2006) Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc Natl Acad Sci USA 103:15916–15920PubMedCentralPubMedGoogle Scholar
  97. 97.
    Tachezy J, Sánchez LB, Müller M (2001) Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18:1919–1928PubMedGoogle Scholar
  98. 98.
    Makiuchi T, Mi-ichi F, Nakada-Tsukui K, Nozaki T (2013) Novel TPR-containing subunit of TOM complex functions as cytosolic receptor for Entamoeba mitosomal transport. Sci Rep 3:1129PubMedCentralPubMedGoogle Scholar
  99. 99.
    Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N (1998) Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature (Lond) 395:516–521Google Scholar
  100. 100.
    Baker KP, Schaniel A, Vestweber D, Schatz G (1990) A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature (Lond) 348:605–609Google Scholar
  101. 101.
    Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N (2003) An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278:48520–48523PubMedGoogle Scholar
  102. 102.
    Model K, Meisinger C, Prinz T, Wiedemann N, Truscott KN, Pfanner N, Ryan MT (2001) Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat Struct Biol 8:361–370PubMedGoogle Scholar
  103. 103.
    Dagley MJ, Dolezal P, Likic VA, Smid O, Purcell AW, Buchanan SK, Tachezy J, Lithgow T (2009) The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol Biol Evol 26:1941–1947PubMedCentralPubMedGoogle Scholar
  104. 104.
    Karpenahalli MR, Lupas AN, Söding J (2007) TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinform 8:2Google Scholar
  105. 105.
    Baker MJ, Frazier AE, Gulbis JM, Ryan MT (2007) Mitochondrial protein-import machinery: correlating structure with function. Trends Cell Biol 17:456–464PubMedGoogle Scholar
  106. 106.
    Young JC, Hoogenraad NJ, Hartl FU (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41–50PubMedGoogle Scholar
  107. 107.
    Dekker PJ, Ryan MT, Brix J, Müller H, Hönlinger A, Pfanner N (1998) Preprotein translocase of the outer mitochondrial membrane: molecular dissection and assembly of the general import pore complex. Mol Cell Biol 18:6515–6524PubMedCentralPubMedGoogle Scholar
  108. 108.
    Schmidt O, Harbauer AB, Rao S, Eyrich B, Zahedi RP, Stojanovski D, Schönfisch B, Guiard B, Sickmann A, Pfanner N, Meisinger C (2011) Regulation of mitochondrial protein import by cytosolic kinases. Cell 144:227–239PubMedGoogle Scholar
  109. 109.
    Bailey K, Webb EC (1944) Purification and properties of yeast pyrophosphatase. Biochem J 38:394–398PubMedCentralPubMedGoogle Scholar
  110. 110.
    Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58:83–102PubMedGoogle Scholar
  111. 111.
    Aguilera P, Barry T, Tovar J (2008) Entamoeba histolytica mitosomes: organelles in search of a function. Exp Parasitol 118:10–16PubMedGoogle Scholar
  112. 112.
    Groot PH, Scholte HR, Hülsmann WC (1976) Fatty acid activation: specificity, localization, and function. Adv Lipid Res 14:75–126PubMedGoogle Scholar
  113. 113.
    Rostovtseva TK, Tan W, Colombini M (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37:129–142PubMedGoogle Scholar
  114. 114.
    Colombini M (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 256-257:107–115PubMedGoogle Scholar
  115. 115.
    Kmita H, Budzińska M (2000) Involvement of the TOM complex in external NADH transport into yeast mitochondria depleted of mitochondrial porin1. Biochim Biophys Acta 1509:86–94PubMedGoogle Scholar
  116. 116.
    Budzińska M, Gałgańska H, Karachitos A, Wojtkowska M, Kmita H (2009) The TOM complex is involved in the release of superoxide anion from mitochondria. J Bioenerg Biomembr 41:361–367PubMedGoogle Scholar
  117. 117.
    Lithgow T, Schneider A (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond B Biol Sci 365:799–817PubMedCentralPubMedGoogle Scholar
  118. 118.
    Schülke N, Sepuri NB, Pain D (1997) In vivo zippering of inner and outer mitochondrial membranes by a stable translocation intermediate. Proc Natl Acad Sci USA 94:7314–7319PubMedCentralPubMedGoogle Scholar
  119. 119.
    Schülke N, Sepuri NB, Gordon DM, Saxena S, Dancis A, Pain D (1999) A multisubunit complex of outer and inner mitochondrial membrane protein translocases stabilized in vivo by translocation intermediates. J Biol Chem 274:22847–22854PubMedGoogle Scholar
  120. 120.
    Ahsan MK, Lekli I, Ray D, Yodoi J, Das DK (2009) Redox regulation of cell survival by the thioredoxin superfamily: an implication of redox gene therapy in the heart. Antioxid Redox Signal 11:2741–2758PubMedCentralPubMedGoogle Scholar
  121. 121.
    Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147PubMedGoogle Scholar
  122. 122.
    Jain R, Shrimal S, Bhattacharya S, Bhattacharya A (2010) Identification and partial characterization of a dynamin-like protein, EhDLP1, from the protist parasite Entamoeba histolytica. Eukaryot Cell 9:215–223PubMedCentralPubMedGoogle Scholar
  123. 123.
    Kanki T, Klionsky DJ, Okamoto K (2011) Mitochondria autophagy in yeast. Antioxid Redox Signal 14:1989–2001PubMedCentralPubMedGoogle Scholar
  124. 124.
    Okamoto K, Kondo-Okamoto N (2012) Mitochondria and autophagy: critical interplay between the two homeostats. Biochim Biophys Acta 1820:595–600PubMedGoogle Scholar
  125. 125.
    Picazarri K, Nakada-Tsukui K, Nozaki T (2008) Autophagy during proliferation and encystation in the protozoan parasite Entamoeba invadens. Infect Immun 76:278–288PubMedCentralPubMedGoogle Scholar
  126. 126.
    Picazarri K, Nakada-Tsukui K, Sato D, Nozaki T (2008) Analysis of autophagy in the enteric protozoan parasite Entamoeba. Methods Enzymol 451:359–371PubMedGoogle Scholar
  127. 127.
    Okamoto K, Kondo-Okamoto N, Ohsumi Y (2009) Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17:87–97PubMedGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  • Takashi Makiuchi
    • 1
  • Fumika Mi-ichi
    • 2
  • Tomoyoshi Nozaki
    • 3
    • 4
  1. 1.Department of Infectious DiseasesTokai University School of MedicineKanagawaJapan
  2. 2.Department of Biomolecular Sciences, Faculty of MedicineSaga UniversitySagaJapan
  3. 3.Department of ParasitologyNational Institute of Infectious DiseasesTokyoJapan
  4. 4.Graduate School of Life and Environmental SciencesUniversity of TsukubaIbarakiJapan

Personalised recommendations