Entamoeba histolytica mitosomes: Organelles in search of a function

Experimental Parasitology

Volumn 118, Issue 1, 2008, Pages 10-16

  Aguilera, Penelope ^a   Barry, Tara ^a   Tovar, Jorge ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

m; adenosine triphosphate; Amoeba; Anaerobic metabolism; ATP; ATP transporter; Chaperone; chaperonin 60; Cpn60; Cryptosporidium; cysteine desulphurase; Dictyostelium; Energy metabolism; Entamoeba; firefly luciferase gene; flavin mononucleotide; FMN; Giardia; Hydrogenosome; iron binding scaffold protein; Iron sulphur; iron sulphur cluster; Isc; luc; Mastigamoeba; micrometer; Mitochondria; mitochondrial type Hsp70; Mitosome; mtHsp70; NAD; NADP; nicotine adenine dinucleotide; nicotine adenine dinucleotide phosphate; NifS; NifU; nitrate; NO3; Organelle; PFO; PNT; Protein import; Protist; Protozoa; pyridine nucleotide transhydrogenase; pyruvate ferredoxin oxidoreductase; Pyruvate oxidation; ribosomal ribonucleic acid; rRNA; Trichomonas

Indexed keywords

IRON SULFUR PROTEIN; PYRUVIC ACID;

CELL ORGANELLE; ENERGY METABOLISM; ENTAMOEBA; ENTAMOEBA DISPAR; ENTAMOEBA HISTOLYTICA; GENOME; MITOCHONDRION; NONHUMAN; PARASITE; PRIORITY JOURNAL; REVIEW; STATISTICAL SIGNIFICANCE; TRANSMISSION ELECTRON MICROSCOPY; TROPHOZOITE;

AEROBIOSIS; ANAEROBIOSIS; ANIMALS; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; GENOME, PROTOZOAN; HUMANS; INTESTINE, LARGE; IRON-SULFUR PROTEINS; MITOCHONDRIA; ORGANELLES; OXYGEN CONSUMPTION; PHYLOGENY; PROTOZOAN PROTEINS; PYRUVIC ACID; SYMBIOSIS;

CRYPTOSPORIDIUM; DICTYOSTELIUM; ENTAMOEBA; ENTAMOEBA HISTOLYTICA; GIARDIA; MASTIGAMOEBA; PROTISTA; PROTOZOA; TRICHOMONAS;

EID: 37349117643     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2007.08.004     Document Type: Review

References (52)

1. Adl S.M., Simpson A.G., Farmer M.A., Andersen R.A., Anderson O.R., Barta J.R., Bowser S.S., Brugerolle G., Fensome R.A., Fredericq S., James T.Y., Karpov S., Kugrens P., Krug J., Lane C.E., Lewis L.A., Lodge J., Lynn D.H., Mann D.G., McCourt R.M., Mendoza L., Moestrup O., Mozley-Standridge S.E., Nerad T.A., Shearer C.A., Smirnov A.V., Spiegel F.W., and Taylor M.F. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52 (2005) 399-451
2. Ali V., Shigeta Y., Tokumoto U., Takahashi Y., and Nozaki T. An intestinal parasitic protist, Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulphur cluster assembly under anaerobic conditions. Journal of Biological Chemistry 279 (2004) 16863-16874
3. Avron B., and Chayen A. Biochemistry of Entamoeba: a review. Cell Biochemistry and Function 6 (1988) 71-86
4. Bapteste E., Brinkmann H., Lee J.A., Moore D.V., Sensen C.W., Gordon P., Durufle L., Gaasterland T., Lopez P., Müller M., and Philippe H. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proceedings of the National Academy of Science USA 99 (2002) 1414-1419
5. Carlton J.M., Hirt R.P., Silva J.C., Delcher A.L., Schatz M., Zhao Q., Wortman J.R., Bidwell S.L., Alsmark U.C., Besteiro S., Sicheritz-Ponten T., Noel C.J., Dacks J.B., Foster P.G., Simillion C., Van de P.Y., Miranda-Saavedra D., Barton G.J., Westrop G.D., Muller S., Dessi D., Fiori P.L., Ren Q., Paulsen I., Zhang H., Bastida-Corcuera F.D., Simoes-Barbosa A., Brown M.T., Hayes R.D., Mukherjee M., Okumura C.Y., Schneider R., Smith A.J., Vanacova S., Villalvazo M., Haas B.J., Pertea M., Feldblyum T.V., Utterback T.R., Shu C.L., Osoegawa K., de Jong P.J., Hrdy I., Horvathova L., Zubacova Z., Dolezal P., Malik S.B., Logsdon Jr. J.M., Henze K., Gupta A., Wang C.C., Dunne R.L., Upcroft J.A., Upcroft P., White O., Salzberg S.L., Tang P., Chiu C.H., Lee Y.S., Embley T.M., Coombs G.H., Mottram J.C., Tachezy J., Fraser-Liggett C.M., and Johnson P.J. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315 (2007) 207-212
6. Chan K.W., Slotboom D.J., Cox S., Embley T.M., Fabre O., van der Giezen M., Harding M., Horner D.S., Kunji E.R., León-Avila G., and Tovar J. A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Current Biology 15 (2005) 737-742
7. Clark C.G., and Roger A.J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proceedings of the National Academy of Science USA 92 (1995) 6518-6521
8. Clemens D.L., and Johnson P.J. Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Molecular and Biochemical Parasitology 106 (2000) 307-313
9. Dolezal P., Smid O., Rada P., Zubacova Z., Sutak R., Nebesarova J., and Tachezy J. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proceedings of the National Academy of Science USA 102 (2005) 10924-10929
10. Embley T.M. Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philosophical Transactions of the Royal Society of London, Series B Biological Sciences 361 (2006) 1055-1067
11. Embley T.M., and Martin W. Eukaryotic evolution, changes and challenges. Nature 440 (2006) 623-630
12. Embley T.M., van der Giezen M., Horner D.S., Dyal P.L., Bell S., and Foster P.G. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55 (2003) 387-395
13. Ghosh S., Field J., Rogers R., Hickman M., and Samuelson J. The Entamoeba histolytica mitochondrion-derived organelle (crypton) contains double-stranded DNA and appears to be bound by a double membrane. Infection and Immunity 68 (2000) 4319-4322
14. Gray M.W., Burger G., and Lang B.F. Mitochondrial evolution. Science 283 (1999) 1476-1481
15. Gribaldo S., and Philippe H. Ancient phylogenetic relationships. Theoretical Population Biology 61 (2002) 391-408
16. Hirt R.P., and Horner D.S. Organelles, Genomes and Eukaryote Phylogeny (2004), CRC Press, Boca Raton, FL
17. LaGier M.J., Tachezy J., Stejskal F., Kutisova K., and Keithly J.S. Mitochondrial-type iron-sulphur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology 149 (2003) 3519-3530
18. León-Avila G., and Tovar J. Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 150 (2004) 1245-1250
19. Lill R., and Muhlenhoff U. Iron-sulphur protein biogenesis in eukaryotes: components and mechanisms. Annual Review of Cellular and Developmental Biology 22 (2006) 457-486
20. Loftus B., Anderson I., Davies R., Alsmark U.C., Samuelson J., Amedeo P., Roncaglia P., Berriman M., Hirt R.P., Mann B.J., Nozaki T., Suh B., Pop M., Duchene M., Ackers J., Tannich E., Leippe M., Hofer M., Bruchhaus I., Willhoeft U., Bhattacharya A., Chillingworth T., Churcher C., Hance Z., Harris B., Harris D., Jagels K., Moule S., Mungall K., Ormond D., Squares R., Whitehead S., Quail M.A., Rabbinowitsch E., Norbertczak H., Price C., Wang Z., Guillen N., Gilchrist C., Stroup S.E., Bhattacharya S., Lohia A., Foster P.G., Sicheritz-Ponten T., Weber C., Singh U., Mukherjee C., El Sayed N.M., Petri Jr. W.A., Clark C.G., Embley T.M., Barrell B., Fraser C.M., and Hall N. The genome of the protist parasite Entamoeba histolytica. Nature 433 (2005) 865-868
21. Lucattini R., Likic V.A., and Lithgow T. Bacterial proteins predisposed for targeting to mitochondria. Molecular Biology and Evolution 21 (2004) 652-658
22. Mai Z., Ghosh S., Frisardi M., Rosenthal B., Rogers R., and Samuelson J. Hsp60 is targeted to a cryptic mitochondrion-derived organelle ("crypton") in the microaerophilic protozoan parasite Entamoeba histolytica. Molecular and Cellular Biology 19 (1999) 2198-2205
23. Martin W., and Müller M. Origin of Mitochondria and Hydrogenosomes (2007), Springer-Verlag, Heidelberg
24. McLaughlin J., and Aley S. The biochemistry and functional morphology of the Entamoeba. Journal of Protozoology 32 (1985) 221-240
25. Okada M., Huston C.D., Mann B.J., Petri Jr. W.A., Kita K., and Nozaki T. Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryotic Cell 4 (2005) 827-831
26. Okada M., Huston C.D., Oue M., Mann B.J., Petri Jr. W.A., Kita K., and Nozaki T. Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Molecular and Biochemical Parasitology 145 (2006) 171-183
27. Putignani L., Tait A., Smith H.V., Horner D., Tovar J., Tetley L., and Wastling J.M. Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129 (2004) 1-18
28. Reeves R.E. Metabolism of Entamoeba histolytica Schaudinn, 1903. Advances in Parasitology 23 (1984) 105-142
29. Reeves R.E., Warren L.G., Susskind B., and Lo H.S. An energy-conserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. Journal of Biological Chemistry 252 (1977) 726-731
30. Regoes A., Zourmpanou D., León-Avila G., van der Giezen M., Tovar J., and Hehl A.B. Protein import, replication, and inheritance of a vestigial mitochondrion. Journal of Biological Chemistry 280 (2005) 30557-30563
31. Riordan C.E., Ault J.G., Langreth S.G., and Keithly J.S. Cryptosporidium parvum Cpn60 targets a relict organelle. Current Genetics 44 (2003) 138-147
32. Risgaard-Petersen N., Langezaal A.M., Ingvardsen S., Schmid M.C., Jetten M.S., op den Camp H.J., Derksen J.W., Pina-Ochoa E., Eriksson S.P., Nielsen L.P., Revsbech N.P., Cedhagen T., and van der Zwaan G.J. Evidence for complete denitrification in a benthic foraminifer. Nature 443 (2006) 93-96
33. Rodríguez M.A., García-Pérez R.M., Mendoza L., Sánchez T., Guillén N., and Orozco E. The pyruvate:ferredoxin oxidoreductase enzyme is located in the plasma membrane and in a cytoplasmic structure in Entamoeba. Microbial Pathogenesis 25 (1998) 1-10
34. Silberman J.D., Clark C.G., Diamond L.S., and Sogin M.L. Phylogeny of the genera Entamoeba and Endolimax as deduced from small-subunit ribosomal RNA sequences. Molecular Biology and Evolution 16 (1999) 1740-1751
35. Slapeta J., and Keithly J.S. Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryotic Cell 3 (2004) 483-494
36. Sogin M.L. Early evolution and the origin of eukaryotes. Current Opinion in Genetics and Development 1 (1991) 457-463
37. Stanley Jr. S.L. Amoebiasis. Lancet 361 (2003) 1025-1034
38. Sutak R., Dolezal P., Fiumera H.L., Hrdy I., Dancis A., Delgadillo-Correa M., Johnson P.J., Müller M., and Tachezy J. Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proceedings of the National Academy of Science USA 101 (2004) 10368-10373
39. Tachezy J., Sánchez L.B., and Müller M. Mitochondrial type iron-sulphur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Molecular Biology and Evolution 18 (2001) 1919-1928
40. Tielens A.G., Rotte C., van Hellemond J.J., and Martin W. Mitochondria as we don′t know them. Trends in Biochemical Sciences 27 (2002) 564-572
41. Tovar J. Mitosomes of Parasitic Protozoa: Biology and Evolutionary Significance. In: Martin W.F., and Müller M. (Eds). Origin of Mitochondria and Hydrogenosomes (2007), Heidelberg, Springer-Verlag 277-300
42. Tovar J., Cox S.S.E., and van der Giezen M. A mitosome purification protocol based on Percoll density gradients and its use in validating the mitosomal nature of Entamoeba histolytica mitochondrial Hsp70. In: van der Giezen M. (Ed). Protein Targeting Protocols (2007), Humana Press, Totowa, NJ 167-178
43. Tovar J., Fischer A., and Clark C.G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Molecular Microbiology 32 (1999) 1013-1021
44. Tovar J., León-Avila G., Sánchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M., and Lucocq J.M. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426 (2003) 172-176
45. van der Giezen M., Cox S., and Tovar J. The iron-sulphur cluster assembly genes iscS and iscU of Entamoeba histolytica were acquired by horizontal gene transfer. BMC Evolutionary Biology 4 (2004) 7
46. van der Giezen M., León-Avila G., and Tovar J. Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiology 151 (2005) 3107-3115
47. van der Giezen M., and Tovar J. Degenerate mitochondria. EMBO Reports 6 (2005) 525-530
48. van der Giezen M., Tovar J., and Clark C.G. Mitochondrion-derived organelles in protists and fungi. International Review of Cytology 244 (2005) 177-227
49. Williams B.A., and Keeling P.J. Cryptic organelles in parasitic protists and fungi. Advances in Parasitology 54 (2003) 9-68
50. Williams B.A.P., Hirt R.P., Lucocq J.M., and Embley T.M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418 (2002) 865-869
51. Yamaguchi M., and Hatefi Y. Mitochondrial energy-linked nicotinamide nucleotide transhydrogenase. Membrane topography of the bovine enzyme. Journal of Biological Chemistry 266 (1991) 5728-5735
52. Yu Y., and Samuelson J. Primary structure of an Entamoeba histolytica nicotinamide nucleotide transhydrogenase. Molecular and Biochemical Parasitology 68 (1994) 323-328