Downregulation of mitochondrial porin inhibits cell growth and alters respiratory phenotype in Trypanosoma brucei

Eukaryotic Cell

Volumn 8, Issue 9, 2009, Pages 1418-1428

  Singha, Ujjal K ^a   Sharma, Shvetank ^a   Chaudhuri, Minu ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUROQUINOL OXIDASE; OXIDOREDUCTASE; PROTOZOAL PROTEIN; VOLTAGE DEPENDENT ANION CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL RESPIRATION; CHEMISTRY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; CELL RESPIRATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TRYPANOSOMA BRUCEI BRUCEI; VOLTAGE-DEPENDENT ANION CHANNELS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 69949188844     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00132-09     Document Type: Article

References (56)

1. Abu-Hamad, S., S. Sivan, and V. Shosham-Barmatz. 2006. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc. Natl. Acad. Sci. USA 103:5787-5792.
2. Allemann, N., and A. Schneider. 2000. ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 111: 87-94.
3. 3. Bagos, P. G., T. D. Liakopoulos, I. C. Spyropoulos, and A. J. Hamodrakas. 2004. PRED-TMββ: a web-server for predicting the topology of β-barrel outer membrane proteins. Nucleic Acids Res. 32:W400-W404. (Pubitemid 38997367)
4. Baxevanis, A. D. 2008. Searching NCBI databases using Entrez, chapter 1. In Current protocols in bioinformatics, unit 1.3. Wiley, Hoboken, NJ.
5. Bayrhuber, M., T. Meins, M. Habeck, S. Backer, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, and K. Zeth. 2008. Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 105:15370-15375.
6. Berriman, M., et al. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
7. Besteiro, S., M. P. L. Barrett, L. Riviere, and F. Bringaud. 2005. Energy generation in the insect stages of of Trypanosoma brucei: metabolism in flux. Trends Parasitol. 21:185-191.
8. 8. Biebinger, S., L. E. Wirtz, P. Lorenz, and C. Clayton. 1997. Vectors for inducible expression of toxic gene products in bloodstream and procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 85:99-112. (Pubitemid 27168008)
9. 9. Bochud-Allemann, N., and A. Schneider. 2002. Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J. Biol. Chem. 277:32849-32854. (Pubitemid 34984796)
10. Brown, S. V., P. Hosking, J. Li, and N. Williams. 2006. ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryot. Cell 5:45-53.
11. Chaudhuri, M., W. U. Ajayi, and G. C. Hill. 1998. Biochemical and molecular properties of the Trypanosoma brucei alternative oxidase. Mol. Biochem. Parasitol. 95:53-68.
12. 12. Chaudhuri, M. 2001. Cloning and characterization of a novel serine/threonine protein phosphatase type 5 from Trypanosoma brucei. Gene 266:1-13. (Pubitemid 32268651)
13. Chaudhuri, M., and F. E. Nargang. 2003. Import and assembly of Neurospora crassa Tom40 into mitochondria of Trypanosoma brucei in vivo. Curr. Genet. 44:85-94.
14. Chaudhuri, M., R. D. Ott, L. Saha, S. Williams, and G. C. Hill. 2005. The trypanosome alternative oxidase exists as a monomer in Trypanosoma brucei mitochondria. Parasitol. Res. 96:178-183.
15. 15. Chaudhuri, M., R. D. Ott, and G. C. Hill. 2006. Trypanosome alternative oxidase: from molecule to function. Trends Parasitol. 22:484-491. (Pubitemid 44333289)
16. Colombini, M., E. Blachly-Dyson, and M. Forte. 1996. VDAC, a channel in the outer membrane. Ion Channels 4:169-202.
17. De Pinto, V., S. Reina, F. Guarino, and A. Messina. 2008. Structure of the voltage dependent anion channel: state of the art. J. Bioenerg. Biomembr. 40:139-147.
18. Effron, P. N., A. F. Torri, D. M. Engman, J. E. Donelson, and P. T. Englund. 1993. A mitochondrial heat shock protein from Crithidia fasciculata. Mol. Biochem. Parasitol. 59:191-200.
19. Elkeles, A., K. M. Devos, D. Graur, M. Zizi, and A. Breiman. 1995. Mutiple cDNAs of wheat voltage-dependent anion channels: isolation, differential expression, mapping and evolution. Plant Mol. Biol. 29:109-124.
20. 20. Higgins, D. G., J. D. Thompson, and T. J. Gibson. 1996. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266:383-402. (Pubitemid 26165878)
21. Khalid, S., P. J. Bond, T. Carpenter, and M. S. P. Sansom. 2008. OmpA: gating and dynamics via molecular dynamics simulations. Biochim. Biophys. Acta 1778:1871-1880.
22. 22. Kmita, H., M. Budzinska, and M. O. Stobienia. 2003. Modulation of the voltage-dependent anion-selective channel by cytoplasmic proteins from wild type and the channel depleted cells of Saccharomyces cerevisiae. Acta Biochim. Pol. 50:415-424. (Pubitemid 37034695)
23. Kmita, H., N. Antos, M. Wojtkowska, and L. Hryniewiecka. 2004. Processes underlying the upregulation of Tom proteins in S. cerevisiae mitochondria depleted of the VDAC channel. J. Bioenerg. Biomembr. 36:187-193.
24. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239-253.
25. Krauskopf, A., O. Eriksson, W. J. Craigen, M. A. Forte, and P. Bernardi. 2006. Properties of the permeability transition in VDAC-/- mitochondria. Biochim. Biophys. Acta 1757:590-595.
26. 26. Krimmer, T., D. Rapaport, M. T. Ryan, C. Mesinger, C. K. Kassenbrock, E. Blachly-Dyson, M. Forte, M. G. Douglas, W. Neupert, F. E. Nargang, and N. Pfanner. 2001. Biogenesis of porin of the outer mitochondrial membrane involves an import pathway via receptors and the general import pore of the TOM complex. J. Cell Biol. 152:289-300. (Pubitemid 34285599)
27. Laemmli, U. K. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680-685.
28. Lemasters, J. J., and E. Holmuhamedov. 2006. Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim. Biophys. Acta 1762:181-190.
29. 29. Liu, B., Y. Liu, S. A. Motyka, E. E. Agbo, and P. T. Englund. 2005. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 21:363369. (Pubitemid 40968137)
30. Lukes, J., H. Hashimi, and A. Zikova. 2005. Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr. Genet. 48:277-299.
31. Maslov, D. A., A. Zinkova, I. Kyselova, and J. Lukes. 2002. A putative novel nuclear-encoded subunit of the cytochrome coxidase complex in trypanosomatids. Mol. Biochem. Parasitol. 125:113-125.
32. Niederweis, M. 2003. Mycobacterial porins-new channel proteins in unique outer membranes. Mol. Microbiol. 49:1167-1177.
33. Nolan, D. P., and H. P. Voorheis. 1992. The mitochondrion in bloodstream forms of Trypanosoma brucei is energized by the electrogenic pumping of protons catalysed by the FIFO-ATPase. Eur. J. Biochem. 209:207-216.
34. Priest, J. W., and S. L. Hajduk. 1994. Developmental regulation of Trypanosoma brucei cytochrome c reductase during bloodstream to procyclic differentiation. Mol. Biochem. Parasitol. 65:291-304.
35. Pusnik, M., F. Charriere, P. Maser, R. Waller, M. J. Dagley, T. Lithgow, and A. Schneider. 2009. The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol. Biol. Evol. 26:671-680.
36. 36. Randall, A., J. Cheng, M. Sweredoski, and P. Baldi. 2008. TMBPro: secondary structure, beta contact and tertiary structure prediction of transmembrane beta-barrel proteins. Bioinformatics 24:513-520. (Pubitemid 351256295)
37. Sambrook, J., E. Fritsch, and T. Maniatis. 1994. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Schneider, A., N. Bouzaidi-Tiali, A. L. Chanez, and L. Bulliard. 2007. ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Methods Mol. Biol. 372:379-387.
39. 39. Schnaufer, A., D. G. Clark-Walker, A. G. Steinberg, and K. Stuart. 2005. The Fl-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J. 24:4029-4040. (Pubitemid 41752872)
40. Schulz, G. E. 2002. The structure of bacterial outer membrane proteins. Biochim. Biophys. Acta 1565:308-317.
41. Shoshan-Barmatz, V., A. Israelson, D. Brdiczka, and S. S. Sheu. 2006. The voltage-dependent anion channel (VDAC): function in intracellular signaling, cell life and cell death. Curr. Pharm. Des. 12:2249-2270.
42. Simpson, A. G., J. R. Stevens, and J. Lukes. 2006. The evolution and diversity of kinetoplastid flagellates. Trends Parasitol. 22:168-174.
43. Singha, U. K., E. Peprah, S. Williams, R. Walker, L. Saha, and M. Chaudhuri. 2008. Characterization of the mitochondrial inner membrane translocator Tim17 from Trypanosoma brucei. Mol. Biochem. Parasitol. 159: 30-43.
44. Smith, S. G., V. Mahon, M. A. Lambert, and R. P. Fagan. 2007. A molecular swiss army knife: OmpA structure, function and expression. FEMS Microbiol. Lett. 273:1-11.
45. Stuart, K. D., A. Schnaufer, N. L. Ernst, and A. K. Panigrahi. 2005. Complex management: RNA editing in trypanosomes. Trends Biochem. 30:97-105.
46. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from Polyacrylamide gels to nitrocellulose sheets: procedures and some application. Proc. Natl. Acad. Sci. USA 76:4350-4354.
47. 47. Tsujimoto, Y., and S. Shimizu. 2007. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12:835-840. (Pubitemid 46653286)
48. 2+ accumulation in Trypanosoma brucei bloodstream and procyclic trypomastigotes mitochondria. Mol. Biochem. Parasitol. 56:251-257.
49. Walker, R., L. Saha, G. C. Hill, and M. Chaudhuri. 2005. The effect of over-expression of the alternative oxidase in the procyclic forms of Trypanosoma brucei. Mol. Biochem. Parasitol. 139:153-162.
50. 50. Wickstead, B., K. Ersfeld, and K. Gull. 2002. Targeting of a tetracyclineinducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol. Biochem. Parasitol. 125:211-216. (Pubitemid 35449262)
51. Wittig, L, H. P. Braun, and H. Schagger. 2006. Blue native PAGE. Nat. Protoc. 1:418-428.
52. Woods, A., T. Sherwin, R. Sasse, T. H. MacRae, A. J. Baines, and K. Gull. 1989. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93: 491-500.
53. World Health Organization. 2009. Report on infectious diseases. World Health Organization, Geneva, Switzerland, www.who.int/tropics/trypanosomiasis -african/en/.
54. Yehezkel, G., S. Abu-Hamad, and V. Shoshan-Barmatz. 2007. An N-terminal nucleotide-binding site in VDACl: Involvement in regulating mitochondrial function. J. Cell. Physiol. 212:551-561.
55. 55. Zalk, R., A. Israelson, E. S. Garty, H. Azoulay-Zohar, and V. ShoshanBarmatz. 2005. Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem. J. 386:73-83. (Pubitemid 40289226)
56. 56. Ziková, A., E. Horakova, M. Jirku, P. Dunajcikova, and J. Lukes. 2006. The effect of down-regulation of mitochondrial RNA-binding proteins MRPl and MRP2 on respiratory complex in procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 149:65-73. (Pubitemid 44037843)