Mitosomes in Entamoeba histolytica contain a sulfate activation pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 51, 2009, Pages 21731-21736

  Mi ichi, Fumika ^a   Yousuf, Mohammad Abu ^a   Nakada Tsukui, Kumiko ^a   Nozaki, Tomoyoshi ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Anaerobic protozoa; Evolution; Mitochondria; Organelle; Proteomics

Indexed keywords

ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; ADENOSINE 5' PHOSPHOSULFATE; ADENYLYLSULFATE KINASE; CHAPERONE; INORGANIC PYROPHOSPHATASE; SODIUM; SULFATE; SULFATE ADENYLYLTRANSFERASE;

ALPHAPROTEOBACTERIA; AMEBIASIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL ORGANELLE; CENTRIFUGATION; CONTROLLED STUDY; DELTAPROTEOBACTERIA; ENTAMOEBA HISTOLYTICA; IMMUNOFLUORESCENCE; LIVER ABSCESS; MASS SPECTROMETRY; MITOCHONDRION; MITOSOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEOMICS;

CENTRIFUGATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENTAMOEBA HISTOLYTICA; FLUORESCENT ANTIBODY TECHNIQUE; ORGANELLES; PHYLOGENY; SULFATES;

ENTAMOEBA HISTOLYTICA; EUKARYOTA; PROTEOBACTERIA; PROTOZOA;

EID: 76049108776     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907106106     Document Type: Article

References (54)

1. van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56:221-231.
2. Aguilera P, Barry T, Tovar J (2008) Entamoeba histolytica mitosomes: organelles in search of a function. Exp Parasitol 118:10-16.
3. Lindmark DG, Muller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248:7724-7728.
4. Hrdy I, et al. (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618-622.
5. Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236:729-739.
6. van der Giezen M, et al. (2003) Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol Biol Evol 20:1051-1061.
7. Hackstein JH, Tjaden J, Huynen M Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50:225-245, 2006.
8. Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci USA 92:6518-6521.
9. Mai, Z, et al. (1999) Hsp60 is targeted to a cryptic mitochondrion- derived organelle ("crypton") in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19:2198-2205.
10. Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32:1013-1021.
11. Bakatselou C, Kidgell C, Clark CC (2000) A mitochondrial-type hsp70 gene of Entamoeba histolytica. Mol Biochem Parasitol 110:177-182.
12. Leon-Avila G, Tovar J (2004) Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 150:1245-1250.
13. van der Giezen M, Leon-Avila G, Tovar J (2005) Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiology 151:3107-3115.
14. Chan KW, et al. (2005) A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr Biol 15:737-742.
15. Tovar J, Cox SS, van der Giezen M (2007) A mitosome purification protocol based on percoll density gradients and its use in validating the mitosomal nature of Entamoeba histolytica mitochondrial Hsp70. Methods Mol Biol 390:167-177.
16. Tovar J, et al. (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
17. Dolezal P, et al. (2005) Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci USA 102:10924-10929.
18. 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 103:15916-15920.
19. Goldberg AV, et al. (2008) Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452:624-628.
20. Tsaousis AD, et al. (2008) A novel route for ATP acquisition by the remnant mitochondria of. Encephalitozoon cuniculi. Nature 453:553-556.
21. Henriquez FL, Richards TA, Roberts F, McLeod R, Roberts CW (2005) The unusual mitochondrial compartment of Cryptosporidium parvum. Trends Parasitol 21:68-74.
22. Gill EE, et al. (2007) Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol Microbiol 66:1306-1320.
23. Stechmann A, et al. (2008) Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18:580-585.
24. 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 279:16863-16874.
25. Nozaki T, et al. (1998) Cloning and bacterial expression of adenosine-5′-triphosphate sulfurylase from the enteric protozoan parasite Entamoeba histolytica. Biochim Biophys Acta 1429:284-291.
26. Leyh TS, Taylor JC, Markham GD (1988) The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J Biol Chem 263:2409-2416.
27. Yanagisawa K, et al. (1998) cDNA cloning, expression, and characterization of the human bifunctional ATP sulfurylase/adenosine 5′-phosphosulfate kinase enzyme. Biosci Biotechnol Biochem 62:1037-1040.
28. Capasso JM, Hirschberg CB (1984) Mechanisms of glycosylation and sulfation in the Golgi apparatus: evidence for nucleotide sugar/nucleoside monophosphate and nucleotide sulfate/nucleoside monophosphate antiports in the Golgi apparatus membrane. Proc Natl Acad Sci USA 81:7051-7055.
29. Kamiyama S, et al. (2003) Molecular cloning and identification of 3′-phosphoadenosine 5′-phosphosulfate transporter. J Biol Chem 278:25958-25963.
30. Kamiyama S, et al. (2006) Molecular cloning and characterization of a novel 3′-phosphoadenosine 5′-phosphosulfate transporter, PAPST2. J Biol Chem 281:10945-10953.
31. Guo B, Irigoyen S, Fowler TB, Versaw WK (2008) Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues. Plant Signal Behav 3:784-790.
32. Strott CA (2002) Sulfonation and molecular action. Endocr Rev 23:703-732.
33. Negishi M, et al. (2001) Structure and function of sulfotransferases. Arch Biochem Biophys 390:149-157.
34. Clark CG, et al. (2007) Structure and content of the Entamoeba histolytica genome. Adv Parasitol 65:51-190.
35. Ali V, Nozaki T (2007) Current therapeutics, their problems, and sulfur-containing-amino-acid metabolism as a novel target against infections by "amitochondriate" protozoan parasites. Clin Microbiol Rev 20:164-187.
36. Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:1-14.
37. Bradley ME, Rest JS, Li WH, Schwartz NB (2009) Sulfate activation enzymes: phylogeny and association with pyrophosphatase. J Mol Evol 68:1-13.
38. 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 57:430-436.
39. Saidha T, Na SQ, Li JY, Schiff JA (1988) A sulphate metabolizing centre in Euglena mitochondria. Biochem J 253:533-539.
40. Loftus B, et al. (2005) The genome of the protist parasite. Entamoeba histolytica Nature 433:865-868.
41. Claros MG, Vincens P (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779-786.
42. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34-36.
43. Dolezal, et al. (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313:314-318.
44. Dagley MJ, et al. (2009) The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol Biol Evol 26:1941-1947.
45. Dolezal P, et al. (2005) Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci USA 102:10924-10929.
46. Smíd O, et al. (2008) Reductive evolution of the mitochondrial processing peptidases of the unicellular parasites Trichomonas vaginalis and Giardia intestinalis. PLoS Pathog 4: e1000243.
47. Diamond LS, Mattern CF, Bartgis IL (1972) Viruses of Entamoeba histolytica. I. Identification of transmissible virus-like agents. J Virol 9:326-341.
48. Diamond LS, Harlow DR, Cunnick CC (1978) A new medium for the axenic cultivation of Entamoeba histolytica and other. Entamoeba Trans R Soc Trop Med Hyg 72:431-432.
49. Nakada-Tsukui K, Saito-Nakano Y, Ali V, Nozaki T (2005)Aretromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol Biol Cell 16:5294-5303.
50. Nozaki T, et al. (1998) Molecular cloning and characterization of the genes encoding two isoforms of cysteine synthase in the enteric protozoan parasite Entamoeba histolytica. Mol Biochem Parasitol 97:33-44.
51. Mitra BN, Saito-Nakano Y, Nakada-Tsukui K, Sato D, Nozaki T (2007) Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9:2112-2125.
52. Saito-Nakano Y, Yasuda T, Nakada-Tsukui K, Leippe M, Nozaki T (2004) Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J Biol Chem 279:49497-49507.
53. Nozaki T, et al. (1999) Characterization of the gene encoding serine acetyltransferase, a regulated enzyme of cysteine biosynthesis from the protist parasites Entamoeba histolytica and Entamoeba dispar. Regulation and possible function of the cysteine biosynthetic pathway in Entamoeba. J Biol Chem 274:32445-32452.
54. Bakker-Grunwald T, Geilhorn B (1992) Sulfate metabolism in Entamoeba histolytica. Mol Biochem Parasitol 53:71-78.