Localization and targeting of an unusual pyridine nucleotide transhydrogenase in Entamoeba histolytica

Eukaryotic Cell

Volumn 9, Issue 6, 2010, Pages 926-933

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

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE;

ANIMAL; ARTICLE; CELL VACUOLE; CHO CELL; CRICETULUS; ENTAMOEBA HISTOLYTICA; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; HAMSTER; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN TRANSPORT; CHO CELL LINE;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENTAMOEBA HISTOLYTICA; FLUORESCENT ANTIBODY TECHNIQUE; NADP TRANSHYDROGENASE; PROTEIN TRANSPORT; VACUOLES; NADP TRANSHYDROGENASES;

AMOEBA (GENUS); BACTERIA (MICROORGANISMS); ENTAMOEBA HISTOLYTICA; EUKARYOTA; PROTOZOA;

EID: 77953770989     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00011-10     Document Type: Article

References (52)

1. Aguilera, P., T. Barry, and J. Tovar. 2008. Entamoeba histolytica mitosomes: organelles in search of a function. Exp. Parasitol. 118:10-16.
2. Bakatselou, C., C. Kidgell, and C. C. Clark. 2000. A mitochondrial-type hsp70 gene of Entamoeba histolytica. Mol. Biochem. Parasitol. 110:177-182.
3. Bizouarn, T., O. Fjellstrom, J. Meuller, M. Axelsson, A. Bergkvist, C. Johansson, G. Karlsson, and J. Rydstrom. 2000. Proton translocating nicotinamide nucleotide transhydrogenase from E. coli. Mechanism of action deduced from its structural and catalytic properties. Biochim. Biophys. Acta 1457:211-228.
4. Bogdan, C., M. Rollinghoff, and A. Diefenbach. 2000. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12:64-76.
5. Bucci, C., P. Thomsen, P. Nicoziani, J. McCarthy, and B. van Deurs. 2000. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11:467-480.
6. Carlton, J. M., S. V. Angiuoli, and D. J. Carucci. 2002. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii. Nature 419:512-519.
7. Chan, K. W., D. J. Slotboom, S. Cox, T. M. Embley, O. Fabre, M. van der Giezen, M. Harding, D. S. Horner, E. R. Kunji, G. Leon-Avila, and J. Tovar. 2005. A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr. Biol. 15:737-742.
8. Clark, C. G., and A. J. Roger. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. U. S. A. 92: 6518-6521.
9. Diamond, L. S., D. R. Harlow, and C. C. Cunnick. 1978. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 72:431-432.
10. Gardner, M. J., and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
11. Gill, E. E., S. Diaz-Triviño, M. J. Barberà, J. D. Silberman, A. Stechmann, D. Gaston, I. Tamas, and A. J. Roger. 2007. Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol. Micro-biol. 66:1306-1320.
12. Hall, N., M. Karras, and R. E. Sinden. 2005. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307:82-86.
13. Hiltpold, A., M. Frey, A. Hulsmeier, and P. Kohler. 2000. Glycosylation and palmitoylation are common modifications of Giardia variant surface proteins. Mol. Biochem. Parasitol. 109:61-65.
14. Hoek, J. B., and J. Rydstrom. 1988. Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem. J. 254:1-10.
15. Jackson, J. B. 1991. The proton-translocating nicotinamide adenine dinucleotide transhydrogenase. J. Bioenerg. Biomembr. 23:715-741.
16. Jackson, J. B., S. J. Peake, and S. A. White. 1999. Structure and mechanism of proton-translocating transhydrogenase. FEBS Lett. 464:1-8.
17. Kramer, R. A., L. A. Tomchak, S. J. McAndrew, K. Becker, D. Hug, L. Pasamontes, and M. Humbelin. 1993. An Eimeria tenella gene encoding a protein with homology to the nucleotide transhydrogenases of Escherichia coli and bovine mitochondria. Mol. Biochem. Parasitol. 60:327-331.
18. Lee, Y.-N., L.-K. Chen, H.-C. Ma, H.-H. Yang, H.-P. Li, and S.-Y. Lo. 2005. Thermal aggregation of SARS-CoV membrane protein. J. Virol. Methods 129:152-161.
19. Leon-Avila, G., and J. Tovar. 2004. Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organeller genome. Microbiology 150:1245-1250.
20. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macro-phage function. Annu. Rev. Immunol. 15:323-350.
21. Mai, Z., S. Ghosh, M. Frisardi, B. Rosenthal, R. Rogers, and J. Samuelson. 1999. Hsp60 is targeted to a cryptic mitochondrion-derived organelle ("crypton") in the microaerophilic protozoan parasite Entamoeba histolytica. Mol. Cell. Biol. 19:2198-2205.
22. Mann, B. J., B. E. Torian, T. S. Vedvick, and W. A. Petri, Jr. 1991. Sequence of a cysteine-rich galactose-specific lectin of Entamoeba histolytica. Proc. Natl. Acad. Sci. U. S. A. 88:3248-3252.
23. Mann, B. J., C. Y. Chung, J. M. Dodson, L. S. Ashley, L. L. Braga, and T. L. Snodgrass. 1993. Neutralizing monoclonal antibody epitopes of the Entamoeba histolytica galactose adhesin map to the cysteine-rich extracellular domain of the 170-kilodalton subunit. Infect. Immun. 61:1772-1778.
24. Maralikova, B., V. Ali, K. Nakada-Tsukui, T. Nozaki, M. van der Giezen, K. Henze, and J. Tovar. 2010. Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell. Microbiol. 12: 331-342.
25. McLane, M. W., G. Hatzidimitriou, J. Yuan, U. McCann, and G. Ricaurte. 2007. Heating induces aggregation and decreases detection of serotonin transporter protein on Western blots. Synapse 61:875-876.
26. Meza, I. 1992. Entamoeba histolytica: phylogenetic consideration. Arch. Med. Res. 23:1-5.
27. Mi-ichi, F., M. A. Yousuf, K. Nakada-Tsukui, and T. Nozaki. 2009. Mito-somes in Entamoeba histolytica contain a sulphate activation pathway. Proc. Natl. Acad. Sci. U. S. A. 106:21731-21736.
28. Mitra, B. N., Y. Saito-Nakano, K. Nakada-Tsukui, D. Sato, and T. Nozaki. 2007. Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell. Microbiol. 9:2112-2125.
29. Nakada-Tsukui, K., Y. Saito-Nakano, V. Ali, and T. Nozaki. 2005. A retromerlike 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.
30. Nakada-Tsukui, K., H. Okada, B. N. Mitra, and T. Nozaki. 2009. Phosphatidylinositol-phosphates mediate cytoskeletal reorganization during phagocytosis via a unique modular protein consisting of RhoGEF/DH and FYVE domains in the parasitic protozoon Entamoeba histolytica. Cell. Microbiol. 11:1471-1491.
31. Nozaki, T., T. Asai, L. B. Sanchez, S. Kobayashi, and M. Nakazawa. 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.
32. Nozaki, T., T. Asai, S. Kobayashi, F. Ikegami, M. Noji, K. Saito, and T. Takeuchi. 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.
33. Okada, M., C. D. Huston, B. J. Mann, W. A. Petri Jr., K. Kita, and T. Nozaki. 2005. Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot. Cell 4:827-831.
34. Okada, M., C. D. Huston, M. Oue, B. J. Mann, W. A. Petri Jr., K. Kita, and T. Nozaki. 2006. Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Mol. Biochem. Parasitol. 145: 171-183.
35. Riordan, C. E., J. G. Ault, S. G. Langreth, and J. S. Keithly. 2003. Cryptosporidium parvum Cpn60 targets a relict organelle. Curr. Genet. 44:138-147.
36. Roger, A. J., S. G. Svard, J. Tovar, C. G. Clark, M. W. Smith, F. D. Gillin, and M. L. Sogin. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harboured an endosymbiont related to the progenitor of mitochondria. Proc. Natl. Acad. Sci. U. S. A. 95:229-234.
37. Saito-Nakano, Y., T. Yasuda, K. Nakada-Tsukui, M. Leippe, and T. Nozaki. 2004. Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J. Biol. Chem. 279:49497-49507.
38. Salgado, M., J. C. Villagómez-Castro, R. Rocha-Rodríguez, M. Sabanero-López, M. A. Ramos, A. Alagón, E. López-Romero, and R. Sánchez-López. 2005. Entamoeba histolytica: biochemical and molecular insights into the activities within microsomal fractions. Exp. Parasitol. 110:363-373.
39. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Sazanov, L. A., and J. B. Jackson. 1994. Proton-translocating transhydrogenase and NAD-and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett. 344:109-116.
41. Stanley, S. L., Jr. 2003. Amoebiasis. Lancet 361:1025-1034.
42. Tokoro, M., T. Asai, S. Kobayashi, T. Takeuchi, and T. Nozaki. 2003. Identification and characterization of two isoenzymes of methioninelyase from Entamoeba histolytica: a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protist that lacks forward and reverse trans-sulfuration pathways. J. Biol. Chem. 278:42717-42727.
43. Tovar, J., A. Fischer, and C. G. Clark. 1999. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32:1013-1021.
44. Tovar, J., G. Leon-Avila, L. B. Sanchez, R. Sutak, J. Tachezy, and M. van der Giezen. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
45. Tovar, J., S. S. E. Cox, and M. van der Giezen. 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.
46. van der Giezen, M. 2009. Hydrogenosomes and mitosomes: conservation and evolution of functions. J. Eukaryot. Microbiol. 56:221-231.
47. van der Giezen, M., G. Leon-Avila, and J. Tovar. 2005. Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiology 151:3107-3115.
48. Vermeulen, A. N., J. J. Kok, P. Van Den Boogart, R. Dijkema, and J. A. J. Claessens. 1993. Eimeria refractile body proteins contain two potentially functional characteristics: transhydrogenase and carbohydrate transport. FEMS Microbiol. Lett. 110:223-229.
49. Weston, C. J., J. D. Venning, and J. B. Jackson. 2002. The membrane-peripheral subunits of transhydrogenase from Entamoeba histolytica are functional only when dimerized. J. Biol. Chem. 277:26163-26170.
50. Weston, C. J., S. A. White, and J. B. Jackson. 2001. The unusual transhydrogenase of Entamoeba histolytica. FEBS Lett. 488:51-54.
51. Williams, B. A., R. P. Hirt, J. M. Lucocq, and T. M. Embley. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.
52. Yu, Y., and J. Samuelson. 1994. Primary structure of an Entamoeba histolytica nicotinamide nucleotide transhydrogenase. Mol. Biochem. Parasitol. 68:323-328.