Mitochondrial shape and function in trypanosomes requires the outer membrane protein, TbLOK1

Molecular Microbiology

Volumn 87, Issue 4, 2013, Pages 713-729

  Povelones, Megan L ^a,c   Tiengwe, Calvin ^a   Gluenz, Eva ^b   Gull, Keith ^b   Englund, Paul T ^a   Jensen, Robert E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINETOPLAST DNA; LOSS OF KINETOPLAST DNA 1 PROTEIN; MITOCHONDRIAL PROTEIN; OUTER MEMBRANE PROTEIN; RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL FUNCTION; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CONTROLLED STUDY; GENE LIBRARY; GENE SEGREGATION; GENE SILENCING; GENETIC TRANSCRIPTION; LOSS OF KINETOPLAST DNA 1 GENE; MICROBIAL GROWTH; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL GENE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL SHAPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; RNA INTERFERENCE; STRUCTURE ANALYSIS; TRYPANOSOMA BRUCEI;

DNA, KINETOPLAST; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

TRYPANOSOMA BRUCEI;

EID: 84873482694     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12089     Document Type: Article

References (74)

1. Abelovska, L. (2011) Mitochondria as protean organelles: membrane processes that influence mitochondrial shape in yeast. Gen Physiol Biophys 30 Spec No: S13-S24.
2. Baines, A., and Gull, K. (2008) WCB is a C2 domain protein defining the plasma membrane - sub-pellicular microtubule corset of kinetoplastid parasites. Protist 159: 115-125.
3. Bakshi, R.P., and Shapiro, T.A. (2004) RNA interference of Trypanosoma brucei topoisomerase IB: both subunits are essential. Mol Biochem Parasitol 136: 249-255.
4. Berger, K.H., Sogo, L.F., and Yaffe, M.P. (1997) Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J Cell Biol 136: 545-553.
5. Boldogh, I.R., Nowakowski, D.W., Yang, H.C., Chung, H., Karmon, S., Royes, P., and Pon, L.A. (2003) A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol Biol Cell 14: 4618-4627.
6. Bringaud, F., Biteau, N., Melville, S.E., Hez, S., El-Sayed, N.M., Leech, V., etal. (2002) A new, expressed multigene family containing a hot spot for insertion of retroelements is associated with polymorphic subtelomeric regions of Trypanosoma brucei. Eukaryot Cell 1: 137-151.
7. Brun, R., and Schonenberger (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36: 289-292.
8. Chacinska, A., Koehler, C.M., Milenkovic, D., Lithgow, T., and Pfanner, N. (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
9. Chanez, A.L., Hehl, A.B., Engstler, M., and Schneider, A. (2006) Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J Cell Sci 119: 2968-2974.
10. Chaudhuri, M., Ajayi, W., and Hill, G.C. (1998) Biochemical and molecular properties of the Trypanosoma brucei alternative oxidase. Mol Biochem Parasitol 95: 53-68.
11. Claros, M.G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241: 779-786.
12. Clayton, A.M., Guler, J.L., Povelones, M.L., Gluenz, E., Gull, K., Smith, T.K., etal. (2011) Depletion of mitochondrial acyl carrier protein in bloodstream-form Trypanosoma brucei causes a kinetoplast segregation defect. Eukaryot Cell 10: 286-292.
13. Detke, S., and Elsabrouty, R. (2008) Identification of a mitochondrial ATP synthase-adenine nucleotide translocator complex in Leishmania. Acta Trop 105: 16-20.
14. Dimmer, K.S., Jakobs, S., Vogel, F., Altmann, K., and Westermann, B. (2005) Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J Cell Biol 168: 103-115.
15. Downey, N., Hines, J.C., Sinha, K.M., and Ray, D.S. (2005) Mitochondrial DNA ligases of Trypanosoma brucei. Eukaryot Cell 4: 765-774.
16. Effron, P.N., Torri, A.F., Engman, D.M., Donelson, J.E., and Englund, P.T. (1993) A mitochondrial heat shock protein from Crithidia fasciculata. Mol Biochem Parasitol 59: 191-200.
17. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
18. Englund, P.T., Agbo, E.E., Lindsay, M.E., Liu, B., Liu, Y., Motyka, S.A., etal. (2005) RNAi libraries and kinetoplast DNA. Biochem Soc Trans 33: 1409-1412.
19. Esseiva, A.C., Chanez, A.L., Bochud-Allemann, N., Martinou, J.C., Hemphill, A., and Schneider, A. (2004) Temporal dissection of Bax-induced events leading to fission of the single mitochondrion in Trypanosoma brucei. EMBO Rep 5: 268-273.
20. Fridberg, A., Olson, C.L., Nakayasu, E.S., Tyler, K.M., Almeida, I.C., and Engman, D.M. (2008) Sphingolipid synthesis is necessary for kinetoplast segregation and cytokinesis in Trypanosoma brucei. J Cell Sci 121: 522-535.
21. Fujiki, Y., Fowler, S., Shio, H., Hubbard, A.L., and Lazarow, P.B. (1982) Polypeptide and phospholipid composition of the membrane of rat liver peroxisomes: comparison with endoplasmic reticulum and mitochondrial membranes. J Cell Biol 93: 103-110.
22. Gibellini, F., Hunter, W.N., and Smith, T.K. (2009) The ethanolamine branch of the Kennedy pathway is essential in the bloodstream form of Trypanosoma brucei. Mol Microbiol 73: 826-843.
23. Gluenz, E., Shaw, M.K., and Gull, K. (2007) Structural asymmetry and discrete nucleic acid subdomains in the Trypanosoma brucei kinetoplast. Mol Microbiol 64: 1529-1539.
24. Gluenz, E., Povelones, M.L., Englund, P.T., and Gull, K. (2011) The kinetoplast duplication cycle in Trypanosoma brucei is orchestrated by cytoskeleton-mediated cell morphogenesis. Mol Cell Biol 31: 1012-1021.
25. Grams, J., Morris, J.C., Drew, M.E., Wang, Z., Englund, P.T., and Hajduk, S.L. (2002) A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J Biol Chem 277: 16952-16959.
26. Guler, J.L., Kriegova, E., Smith, T.K., Lukes, J., and Englund, P.T. (2008) Mitochondrial fatty acid synthesis is required for normal mitochondrial morphology and function in Trypanosoma brucei. Mol Microbiol 67: 1125-1142.
27. Hirumi, H., and Hirumi, K. (1989) Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
28. Hobbs, A.E., Srinivasan, M., McCaffery, J.M., and Jensen, R.E. (2001) Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J Cell Biol 152: 401-410.
29. Ishihara, N., Jofuku, A., Eura, Y., and Mihara, K. (2003) Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem Biophys Res Commun 301: 891-898.
30. Jensen, R.E. (2005) Control of mitochondrial shape. Curr Opin Cell Biol 17: 384-388.
31. Kornmann, B., and Walter, P. (2010) ERMES-mediated ER-mitochondria contacts: molecular hubs for the regulation of mitochondrial biology. J Cell Sci 123: 1389-1393.
32. Kornmann, B., Osman, C., and Walter, P. (2011) The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc Natl Acad Sci USA 108: 14151-14156.
33. Levy, M., Toury, R., and Andre, J. (1966) [Purification and enzymatic characterization of the external membrane of mitochondria]. C R Acad Sci Hebd Seances Acad Sci D 263: 1766-1769.
34. Li, Z., Lindsay, M.E., Motyka, S.A., Englund, P.T., and Wang, C.C. (2008) Identification of a bacterial-like HslVU protease in the mitochondria of Trypanosoma brucei and its role in mitochondrial DNA replication. PLoS Pathog 4: e1000048.
35. Lineberger, B., Dawicki, D.D., Agarwal, K.C., Kessimian, N., and Steiner, M. (1989) Permeabilization of platelets: an investigation of biochemical, ultrastructural and functional aspects. Biochim Biophys Acta 1012: 36-45.
36. Liu, B., Liu, Y., Motyka, S.A., Agbo, E.E., and Englund, P.T. (2005) Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol 21: 363-369.
37. Liu, B., Wang, J., Yaffe, N., Lindsay, M.E., Zhao, Z., Zick, A., etal. (2009) Trypanosomes have six mitochondrial DNA helicases with one controlling kinetoplast maxicircle replication. Mol Cell 35: 490-501.
38. Lukes, J., Hashimi, H., and Zikova, A. (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48: 277-299.
39. Morgan, G.W., Goulding, D., and Field, M.C. (2004) The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem 279: 10692-10701.
40. Morris, J.C., Wang, Z., Drew, M.E., and Englund, P.T. (2002) Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO J 21: 4429-4438.
41. Morton, D.J., Hoppel, C., and Cooper, C. (1968) The action of digitonin on rat liver mitochondria. Electron microscopy. Biochem J 107: 377-380.
42. Motyka, S.A., Drew, M.E., Yildirir, G., and Englund, P.T. (2006) Overexpression of a cytochrome b5 reductase-like protein causes kinetoplast DNA loss in Trypanosoma brucei. J Biol Chem 281: 18499-18506.
43. Nakai, K., and Horton, P. (1999) psort: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36.
44. Ntambi, J.M., and Englund, P.T. (1985) A gap at a unique location in newly replicated kinetoplast DNA minicircles from Trypanosoma equiperdum. J Biol Chem 260: 5574-5579.
45. Ogbadoyi, E.O., Robinson, D.R., and Gull, K. (2003) A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol Biol Cell 14: 1769-1779.
46. Osman, C., Voelker, D.R., and Langer, T. (2011) Making heads or tails of phospholipids in mitochondria. J Cell Biol 192: 7-16.
47. Otera, H., and Mihara, K. (2011) Molecular mechanisms and physiologic functions of mitochondrial dynamics. J Biochem (Tokyo) 149: 241-251.
48. Perez-Moreno, G., Sealey-Cardona, M., Rodrigues-Poveda, C., Gelb, M.H., Ruiz-Perez, L.M., Castillo-Acosta, V., etal. (2012) Endogenous sterol biosynthesis is important for mitochondrial function and cell morphology in procyclic forms of Trypanosoma brucei. Int J Parasitol 42: 975-989.
49. Pitts, K.R., Yoon, Y., Krueger, E.W., and McNiven, M.A. (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol Biol Cell 10: 4403-4417.
50. Plutner, H., Davidson, H.W., Saraste, J., and Balch, W.E. (1992) Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the P58 containing compartment. J Cell Biol 119: 1097-1116.
51. Poot, M., Zhang, Y.Z., Kramer, J.A., Wells, K.S., Jones, L.J., Hanzel, D.K., etal. (1996) Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 44: 1363-1372.
52. Priest, J.W., and Hajduk, S.L. (1994) Developmental regulation of mitochondrial biogenesis in Trypanosoma brucei. J Bioenerg Biomembr 26: 179-191.
53. Pusnik, M., Charriere, F., Maser, P., Waller, R.F., Dagley, M.J., Lithgow, T., and Schneider, A. (2009) The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol Biol Evol 26: 671-680.
54. Rieder, S.E., Banta, L.M., Kohrer, K., McCaffery, J.M., and Emr, S.D. (1996) Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol Biol Cell 7: 985-999.
55. Schnaitman, C., Erwin, V.G., and Greenawalt, J.W. (1967) The submitochondrial localization of monoamine oxidase. An enzymatic marker for the outer membrane of rat liver mitochondria. J Cell Biol 32: 719-735.
56. Schneider, A., Bouzaidi-Tiali, N., Chanez, A.L., and Bulliard, L. (2007a) ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Methods Mol Biol 372: 379-387.
57. Schneider, A., Charriere, F., Pusnik, M., and Horn, E.K. (2007b) Isolation of mitochondria from procyclic Trypanosoma brucei. Methods Mol Biol 372: 67-80.
58. Sharma, S., Singha, U.K., and Chaudhuri, M. (2010) Role of Tob55 on mitochondrial protein biogenesis in Trypanosoma brucei. Mol Biochem Parasitol 174: 89-100.
59. Shlomai, J. (2004) The structure and replication of kinetoplast DNA. Curr Mol Med 4: 623-647.
60. Siegel, T.N., Hekstra, D.R., Wang, X., Dewell, S., and Cross, G.A. (2010) Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res 38: 4946-4957.
61. Signorell, A., Gluenz, E., Rettig, J., Schneider, A., Shaw, M.K., Gull, K., and Butikofer, P. (2009) Perturbation of phosphatidylethanolamine synthesis affects mitochondrial morphology and cell-cycle progression in procyclic-form Trypanosoma brucei. Mol Microbiol 72: 1068-1079.
62. Sogo, L.F., and Yaffe, M.P. (1994) Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J Cell Biol 126: 1361-1373.
63. Stephens, J.L., Lee, S.H., Paul, K.S., and Englund, P.T. (2007) Mitochondrial fatty acid synthesis in Trypanosoma brucei. J Biol Chem 282: 4427-4436.
64. Stuart, K.D., Schnaufer, A., Ernst, N.L., and Panigrahi, A.K. (2005) Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30: 97-105.
65. Toulmay, A., and Prinz, W.A. (2011) Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr Opin Cell Biol 23: 458-463.
66. Vickerman, K. (1985) Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull 41: 105-114.
67. Wang, Z., and Englund, P.T. (2001) RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J 20: 4674-4683.
68. Wang, Z., Morris, J.C., Drew, M.E., and Englund, P.T. (2000) Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J Biol Chem 275: 40174-40179.
69. Wang, Z., Drew, M.E., Morris, J.C., and Englund, P.T. (2002) Asymmetrical division of the kinetoplast DNA network of the trypanosome. EMBO J 21: 4998-5005.
70. Westermann, B. (2008) Molecular machinery of mitochondrial fusion and fission. J Biol Chem 283: 13501-13505.
71. Wirtz, E., and Clayton, C. (1995) Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science 268: 1179-1183.
72. Wirtz, E., Hoek, M., and Cross, G.A. (1998) Regulated processive transcription of chromatin by T7 RNA polymerase in Trypanosoma brucei. Nucleic Acids Res 26: 4626-4634.
73. Youngman, M.J., Hobbs, A.E., Burgess, S.M., Srinivasan, M., and Jensen, R.E. (2004) Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids. J Cell Biol 164: 677-688.
74. Zhao, Z., Lindsay, M.E., Roy Chowdhury, A., Robinson, D.R., and Englund, P.T. (2008) p166, a link between the trypanosome mitochondrial DNA and flagellum, mediates genome segregation. EMBO J 27: 143-154.