Probing for primary functions of prohibitin in Trypanosoma brucei

International Journal for Parasitology

Volumn 40, Issue 1, 2010, Pages 73-83

  Týč, Jiří ^a   Faktorová, Drahomíra ^a   Kriegová, Eva ^a   Jirků, Milan ^a   Vávrová, Zuzana ^a   Maslov, Dmitri A ^b   Lukeš, Julius ^a  

^a INSTITUTE OF PARASITOLOGY   (Czech Republic)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mitochondrial translation; Mitochondrion; Morphology; Prohibitin; Trypanosoma

Indexed keywords

MITOCHONDRIAL DNA; PROHIBITIN; PROHIBITIN 1; PROHIBITIN 2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

EUKARYOTE; FLAGELLATE; MEMBRANE; MITOCHONDRION; MORPHOLOGY; PROTEIN; RNA;

ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLAGELLATE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ANIMALS; DNA, MITOCHONDRIAL; MEMBRANE POTENTIALS; MITOCHONDRIA; PHYLOGENY; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, MESSENGER; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; MASTIGOPHORA (FLAGELLATES); TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 72149100176     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.07.008     Document Type: Article

References (48)

1. Acín-Pérez R., Fernández-Silva P., Peleato M.L., Pérez-Martos A., and Enriquez J.A. Respiratory active mitochondrial supercomplexes. Mol. Cell 32 (2008) 529-539
2. Artal-Sanz M., Tsang W.Y., Willems E.M., Grivell L.A., Lemire B.D., van der Spek H., and Nijtmans L.G. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J. Biol. Chem. 278 (2003) 32091-32099
3. Berger K.H., and Yaffe M.P. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol. Cell. Biol. 18 (1998) 4043-4052
4. Birner R., Nebauer R., Schneiter R., and Daum G. Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine biosynthetic machinery with the prohibitin complex of Saccharomyces cerevisiae. Mol. Biol. Cell 14 (2003) 370-383
5. Bourges I., Ramus C., de Camaret B.M., Beugnot R., Remacle C., Cardol P., Hofhaus G., and Issartel J.P. Structural organization of mitochondrial human complex I: role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem. J. 383 (2004) 491-499
6. Brinkmann H., and Philippe H. The diversity of eukaryotes and the root of the eukaryotic tree. Adv. Exp. Med. Biol. 607 (2007) 20-37
7. Coates P.J., Jamieson D.J., Smart K., Prescott A.R., and Hall P.A. The prohibitin family of mitochondrial proteins regulate replicative lifespan. Curr. Biol. 7 (1997) 607-610
8. Coates P.J., Nenutil R., McGregor A., Picksley S.M., Crouch D.H., Hall P.A., and Wright E.G. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp. Cell Res. 265 (2001) 262-273
9. Fisk J.C., Ammerman M.L., Presnyak V., and Read L.K. TbRGG2, an essential RNA editing accessory factor in two Trypanosoma brucei life cycle stages. J. Biol. Chem. 283 (2008) 23016-23025
10. Fusaro G., Dasgupta P., Rastogi S., Joshi B., and Chellappan S. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. J. Biol. Chem. 278 (2003) 47853-47861
11. Gamble S.C., Chotai D., Odontiadis M., Dard D.A., Brooke G.N., Powell S.M., Reebye V., Varela-Carver A., Kawano Y., Waxman J., and Bevan C.L. Prohibitin, a protein downregulated by androgens, prepresses androgen receptor activity. Oncogene 26 (2007) 1757-1768
12. Gluenz E., Shaw M.K., and Gull K. Structural asymmetry and discrete nucleic acid subdomains in the Trypanosoma brucei kinetoplast. Mol. Microbiol. 64 (2007) 1529-1539
13. Grams J., Morris J.C., Drew M.E., Wang Z.F., Englund P.T., and Hajduk S.L. A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J. Biol. Chem. 277 (2002) 16952-16959
14. Gregory-Bass R.C., Olatinwo M., Xu W., Matthews R., Stiles J.K., Thomas K., Liu D., Tsang B., and Thompson W.E. Prohibitin silencing reverses stabilization of mitochondrial integrity and chemoresistance in ovarian cancer cells by increasing their sensitivity to apoptosis. Int. J. Cancer 122 (2008) 1923-1930
15. Hashimi H., Zíková A., Panigrahi A.K., Stuart K.D., and Lukeš J. TbRGG1, a component of a novel multi-protein complex involved in kinetoplastid RNA editing. RNA 14 (2008) 970-980
16. Hashimi H., Čičová Z., Novotná L., Wen Y.-Z., and Lukeš J. Kinetoplastid guide RNA biogenesis is dependent on subunits of the mitochondrial RNA binding complex 1 and mitochondrial RNA polymerase. RNA 15 (2009) 588-599
17. Horváth A., Berry E.A., and Maslov D.A. Translation of the edited mRNA for cytochrome b in trypanosome mitochondria. Science 287 (2000) 1639-1640
18. Horváth A., Neboháčová M., Lukeš J., and Maslov D.A. Unusual polypeptide synthesis in the kinetoplastid-mitochondria from Leishmania tarentolae. J. Biol. Chem. 277 (2002) 7222-7230
19. Horváth A., Horáková E., Dunajčíková P., Verner Z., Pravdová E., Šlapetová I., Cuninková L., and Lukeš J. Down-regulation of the nuclear-encoded subunits of the complexes III and IV disrupts their respective complexes but not complex I in procyclic Trypanosoma brucei. Mol. Microbiol. 58 (2005) 116-130
20. Ikonen E., Fiedler K., Parton R.G., and Simons K. Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett. 358 (1995) 273-277
21. Kasashima K., Sumitani M., Satoh M., and Endo H. Human prohibitin 1 maintains the organization and stability of the mitochondrial nucleoids. Exp. Cell Res. 314 (2008) 988-996
22. Kasashima K., Ohta E., Kagawa Y., and Endo H. Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2. J. Biol. Chem. 281 (2006) 36401-36410
23. Keeling P.J., Burger G., Durnford D.G., Lang B.F., Lee R.W., Pearlman R.E., Roger J., and Gray M.W. The tree of eukaryotes. Trends Ecol. Evol. 20 (2005) 670-676
24. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., and Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007) 2947-2948
25. Long S., Jirků M., Mach J., Ginger M.L., Sutak R., Richardson D., Tachezy J., and Lukeš J. Ancestral roles of eukaryotic frataxin: mitochondrial frataxin function and heterologous expression of hydrogenosomal Trichomonas homologs in trypanosomes. Mol. Microbiol. 69 (2008) 94-109
26. Manjeshwar S., Branam D.E., Lerner M.R., Brackett D.J., and Jupe E.R. Tumor suppression by the prohibitin gene 3′ untranslated region RNA in human breast cancer. Cancer Res. 63 (2003) 5251-5256
27. McClung J.K., Danner D.B., Steward D.A., Smith J.R., Schneider E.L., Lumpkin C.K., Dell'Orco R.T., and Nuell M.J. Isolation of a cDNA that hybrid selects antiproliferative mRNA from rat liver. Biochem. Biophys. Res. Commun. 164 (1989) 1316-1322
28. Merkwirth C., Dargazanli S., Tatsuta T., Geimer S., Lower B., Wunderlich F.T., von Kleist-Retzow J.C., Waisman A., Westermann B., and Langer T. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphologenesis in mitochondria. Genes Dev. 22 (2008) 476-488
29. Merkwirth C., and Langer T. Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta 1793 (2009) 27-32
30. Mishra S., Murphy L.C., Nyomba B.L.G., and Murphy L.J. Prohibitin: a potential target for new therapeutics. Trends Mol. Med. 11 (2005) 192-197
31. Neboháčová M., Maslov D.A., Falick A.M., and Simpson L. The effect of RNA interference down-regulation of RNA editing 3′-terminal uridylyl transferase (TUTase) 1 on mitochondrial de novo protein synthesis and stability of respiratory complexes in Trypanosoma brucei. J. Biol. Chem. 279 (2005) 7819-7825
32. Nijtmans L.G.J., de Jong L., Artal-Sanz M., Coates P.J., Berden J.A., Back J.W., Muijsers A.O., van der Spek H., and Grivell L.A. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 19 (2000) 2444-2451
33. 0-ATP synthase. Mol. Biol. Cell 18 (2007) 627-633
34. Opperdoes F.R., and Michels P.A. Complex I of Trypanosomatidae: does it exist?. Trends Parasitol. 24 (2008) 310-317
35. Park S.E., Xu J., Frolova A., Liao L., O'Malley B.W., and Katzenellenbogen B.S. Genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo. Mol. Cell Biol. 25 (2005) 1989-1999
36. Ross J.A., Nagy Z.S., and Kirken R.A. The PHB1/2 phosphocomplex is required for mitochondrial homeostasis and survival of human T cells. J. Biol. Chem. 283 (2008) 4699-4713
37. Schleicher M., Shepherd B.R., Suarez Y., Fernandez-Hernando C., Yu J., Pan Y., Acevedo L.M., Shadel G.S., and Sessa W.C. Prohibitin-1 maintains the angiogenic capacity of endothelial cells by regulating mitochondrial function and senescence. J. Cell. Biol. 180 (2008) 101-112
38. Schneider A., Charriere F., Pusnik M., and Horn E.K. Isolation of mitochondria from procyclic Trypanosoma brucei. Methods Mol. Biol. 372 (2007) 67-80
39. Schumacher M.A., Karamooz E., Zíková A., Trantírek L., and Lukeš J. Crystal structures of Trypanosoma brucei MRP1/MRP2 guide-RNA-binding complex reveals RNA matchmaking mechanism. Cell 126 (2006) 701-711
40. Smalla K.H., Mikhaylova M., Sahin J., Bernstein H.G., Bogerts B., Schmitt A., van der Schors R., Smit A.B., Li K.W., Gundelfinger E.D., and Kreutz M.R. A comparison of the synaptic proteome in human chronic schizophrenia and rat ketamine psychosis suggest that prohibitin is involved in the synaptic pathology of schizophrenia. Mol. Psychiatry 13 (2008) 878-896
41. Smíd O., Horáková E., Vilímová V., Hrdý I., Cammack R., Horváth A., Lukeš J., and Tachezy J. Knock-downs of mitochondrial iron-sulfur cluster assembly proteins IscS and IscU down-regulate the active mitochondrion of procyclic Trypanosoma brucei. J. Biol. Chem. 281 (2006) 28679-28686
42. Steglich G., Neupert W., and Langer T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol. Cell. Biol. 19 (1999) 3435-3442
43. Sun Q.J., Miao M.Y., Jia X., Guo W., Wang L.H., Yao Z.Z., Liu C.L., and Jiao B.H. Subproteomic analysis of the mitochondrial proteins in rats 24 h after partial hepatectomy. J. Cell. Biochem. 105 (2008) 176-184
44. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
45. Tatsuta T., Model K., and Langer T. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell 16 (2005) 248-259
46. Theiss A.L., Idell R.D., Srinivasan S., Klapproth J.M., Jones D.P., Merlin D., and Sitaraman S.V. Prohibitin protects against oxidative stress in intestinal epithelial cells. FASEB J. 58 (2007) 197-206
47. Vondrušková E., van den Burg J., Zíková A., Ernst N.L., Stuart K., Benne R., and Lukeš J. RNA interference analyses suggest a transcript-specific regulatory role for mitochondrial RNA-binding proteins MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J. Biol. Chem. 280 (2005) 2429-2438
48. Zíková A., Horáková E., Jirků M., Dunajčíková P., and Lukeš J. The effect of down-regulation of mitochondrial RNA-binding proteins MRP1 and MRP2 on respiratory complexes in procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 149 (2006) 65-73