Characterization of a Leishmania stage-specific mitochondrial membrane protein that enhances the activity of cytochrome c oxidase and its role in virulence

Molecular Microbiology

Volumn 77, Issue 2, 2010, Pages 399-414

  Dey, Ranadhir ^a   Meneses, Claudio ^b   Salotra, Poonam ^c   Kamhawi, Shaden ^b   Nakhasi, Hira L ^a   Duncan, Robert ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c SAFDARJUNG HOSPITAL CAMPUS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN LDP27; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN; PROTOZOAL RNA;

AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENETIC CODE; HUMAN; HUMAN CELL; KINETOPLASTIDA; LEISHMANIA DONOVANI; MOUSE; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATIVE PHOSPHORYLATION; PARASITE SURVIVAL; PARASITE VIRULENCE; PRIORITY JOURNAL; PROMASTIGOTE; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; LEISHMANIA; MACROPHAGE; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; SEQUENCE ALIGNMENT; VIRULENCE;

HEXAPODA; MUS; PROTOZOA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; GENE DELETION; GENETIC COMPLEMENTATION TEST; HUMANS; LEISHMANIA; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; OXIDATIVE PHOSPHORYLATION; PROTOZOAN PROTEINS; RNA, PROTOZOAN; SEQUENCE ALIGNMENT; VIRULENCE;

EID: 77954354604     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07214.x     Document Type: Article

References (68)

1. Akopyants, N.S., Matlib, R.S., Bukanova, E.N., Smeds, M.R., Brownstein, B.H., Stormo, G.D. Beverley, S.M. (2004) Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Mol Biochem Parasitol 136 : 71 86.
2. Alexander, J., Coombs, G.H. Mottram, J.C. (1998) Leishmania mexicana cysteine proteinase-deficient mutants have attenuated virulence for mice and potentiate a Th1 response. J Immunol 161 : 6794 6801.
3. Alexander, J., Satoskar, A.R. Russell, D.G. (1999) Leishmania species: models of intracellular parasitism. J Cell Sci 112 (Part 18 2993 3002.
4. Allemann, N. Schneider, A. (2000) ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Mol Biochem Parasitol 111 : 87 94.
5. Bates, P.A. (2007) Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol 37 : 1097 1106.
6. Bates, P.A. (2008) Leishmania sand fly interaction: progress and challenges. Curr Opin Microbiol 11 : 340 344.
7. Bochud-Allemann, N. Schneider, A. (2002) Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J Biol Chem 277 : 32849 32854.
8. Boitz, J.M., Yates, P.A., Kline, C., Gaur, U., Wilson, M.E., Ullman, B. Roberts, S.C. (2009) Leishmania donovani ornithine decarboxylase is indispensable for parasite survival in the mammalian host. Infect Immun 77 : 756 763.
9. Burchmore, R.J. Barrett, M.P. (2001) Life in vacuoles - nutrient acquisition by Leishmania amastigotes. Int J Parasitol 31 : 1311 1320.
10. Cermakova, P., Verner, Z., Man, P., Lukes, J. Horvath, A. (2007) Characterization of the NADH:ubiquinone oxidoreductase (complex I) in the trypanosomatid Phytomonas serpens (Kinetoplastida). FEBS J 274 : 3150 3158.
11. Charest, H. Matlashewski, G. (1994) Developmental gene expression in Leishmania donovani: differential cloning and analysis of an amastigote-stage-specific gene. Mol Cell Biol 14 : 2975 2984.
12. Cruz, A., Coburn, C.M. Beverley, S.M. (1991) Double targeted gene replacement for creating null mutants. Proc Natl Acad Sci USA 88 : 7170 7174.
13. Cunningham, M.L., Titus, R.G., Turco, S.J. Beverley, S.M. (2001) Regulation of differentiation to the infective stage of the protozoan parasite Leishmania major by tetrahydrobiopterin. Science 292 : 285 287.
14. David, K.K., Sasaki, M., Yu, S.W., Dawson, T.M. Dawson, V.L. (2006) EndoG is dispensable in embryogenesis and apoptosis. Cell Death Differ 13 : 1147 1155.
15. Debrabant, A., Lee, N., Pogue, G.P., Dwyer, D.M. Nakhasi, H.L. (2002) Expression of calreticulin P-domain results in impairment of secretory pathway in Leishmania donovani and reduced parasite survival in macrophages. Int J Parasitol 32 : 1423 1434.
16. Debrabant, A., Joshi, M.B., Pimenta, P.F.P. Dwyer, D.M. (2004) Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int J Parasitol 34 : 205 217.
17. Desjeux, P. (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27 : 305 318.
18. Dey, R., Khan, S., Pahari, S., Srivastava, N., Jadhav, M. Saha, B. (2007) Functional paradox in host-pathogen interaction dictates the fate of parasites. Future Microbiol 2 : 425 437.
19. Duncan, R. (2004) DNA microarray analysis of protozoan parasite gene expression: outcomes correlate with mechanisms of regulation. Trends Parasitol 20 : 211 215.
20. Duncan, R., Alvarez, R., Jaffe, C., Wiese, M., Klutch, M., Shakarian, A., et al. (2001) Early response gene expression during differentiation of cultured Leishmania donovani. Parasitol Res 87 : 897 906.
21. Duncan, R., Salotra, P., Goyal, N., Akopyants, N., Beverley, S. Nakhasi, H. (2004) The application of gene expression microarray technology to kinetoplastid pathogenesis. Curr Mol Med 4 : 611 621.
22. Duncan, R., Dey, R., Tomioka, K., Hairston, H., Selvapandiyan, A. Nakhasi, H.L. (2009) Biomarkers of attenuation in the Leishmania donovani centrin gene deleted cell line-requirements for safety in a live vaccine candidate. Open Parasitol 3 : 32 41.
23. Freedman, D.J. Beverley, S.M. (1993) Two more independent selectable markers for stable transfection of Leishmania. Mol Biochem Parasitol 62 : 37 44.
24. Gannavaram, S., Vedvyas, C. Debrabant, A. (2008) Conservation of the pro-apoptotic nuclease activity of endonuclease G in unicellular trypanosomatid parasites. J Cell Sci 121 : 99 109.
25. Gaur, U., Showalter, M., Hickerson, S., Dalvi, R., Turco, S.J., Wilson, M.E. Beverley, S.M. (2009) Leishmania donovani lacking the Golgi GDP-Man transporter LPG2 exhibit attenuated virulence in mammalian hosts. Exp Parasitol 122 : 182 191.
26. Goyard, S., Segawa, H., Gordon, J., Showalter, M., Duncan, R., Turco, S.J. Beverley, S.M. (2003) An in vitro system for developmental and genetic studies of Leishmania donovani phosphoglycans. Mol Biochem Parasitol 130 : 31 42.
27. Handman, E. (2001) Leishmaniasis: current status of vaccine development. Clin Microbiol Rev 14 : 229 243.
28. Hart, D.T., Vickerman, K. Coombs, G.H. (1981) Respiration of Leishmania mexicana amastigotes and promastigotes. Mol Biochem Parasitol 4 : 39 51.
29. Hellemond, J.J., Bakker, B.M. Tielens, A.G. (2005) Energy metabolism and its compartmentation in Trypanosoma brucei. Adv Microb Physiol 50 : 199 226.
30. Horvath, A., Berry, E.A., Huang, L.S. Maslov, D.A. (2000a) Leishmania tarentolae: a parallel isolation of cytochrome bc(1) and cytochrome c oxidase. Exp Parasitol 96 : 160 167.
31. Horvath, A., Kingan, T.G. Maslov, D.A. (2000b) Detection of the mitochondrially encoded cytochrome c oxidase subunit I in the trypanosomatid protozoan Leishmania tarentolae. Evidence for translation of unedited mRNA in the kinetoplast. J Biol Chem 275 : 17160 17165.
32. Horvath, A., Horakova, E., Dunajcikova, P., Verner, Z., Pravdova, E., Slapetova, I., et al. (2005) Downregulation 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 : 116 130.
33. Joshi, M., Dwyer, D.M. Nakhasi, H. (1993) Cloning and characterization of differentially expressed genes from in vitro-grown 'amastigotes' of Leishmania donovani. Mol Biochem Parasitol 58 : 345 354.
34. Kamhawi, S. (2006) Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol 22 : 439 445.
35. McConville, M.J. Handman, E. (2007) The molecular basis of Leishmania pathogenesis. Int J Parasitol 37 : 1047 1051.
36. McConville, M.J. Ralton, J.E. (1997) Developmentally regulated changes in the cell surface architecture of Leishmania parasites. Behring Inst Mitt 99 : 34 43.
37. McConville, M.J., de Souza, D., Saunders, E., Likic, V.A. Naderer, T. (2007) Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol 23 : 368 375.
38. Maslov, D.A., Zikova, A., Kyselova, I. Lukes, J. (2002) A putative novel nuclear-encoded subunit of the cytochrome c oxidase complex in trypanosomatids. Mol Biochem Parasitol 125 : 113 125.
39. Molyneux, D. Killick-Kendrick, R. (1987) Morphology, ultrastructure and life cycles. In The Leishmaniases in Biology and Medicine. Peters, W. Killick-Kendrick, R. (eds).
40. Naderer, T. McConville, M.J. (2002) Characterization of a Leishmania mexicana mutant defective in synthesis of free and protein-linked GPI glycolipids. Mol Biochem Parasitol 125 : 147 161.
41. Naderer, T. McConville, M.J. (2008) The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10 : 301 308.
42. Naderer, T., Ellis, M.A., Sernee, M.F., De Souza, D.P., Curtis, J., Handman, E. McConville, M.J. (2006) Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 103 : 5502 5507.
43. Panigrahi, A.K., Zikova, A., Dalley, R.A., Acestor, N., Ogata, Y., Anupama, A., et al. (2008) Mitochondrial complexes in Trypanosoma brucei: a novel complex and a unique oxidoreductase complex. Mol Cell Proteomics 7 : 534 545.
44. Papadopoulou, B., Roy, G., Breton, M., Kundig, C., Dumas, C., Fillion, I., et al. (2002) Reduced infectivity of a Leishmania donovani biopterin transporter genetic mutant and its use as an attenuated strain for vaccination. Infect Immun 70 : 62 68.
45. Rochette, A., Raymond, F., Corbeil, J., Ouellette, M. Papadopoulou, B. (2009) Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum. Mol Biochem Parasitol 165 : 32 47.
46. Sacks, D.L. Perkins, P.V. (1984) Identification of an infective stage of Leishmania promastigotes. Science 223 : 1417 1419.
47. Santhamma, K.R. Bhaduri, A. (1995) Characterization of the respiratory chain of Leishmania donovani promastigotes. Mol Biochem Parasitol 75 : 43 53.
48. Santos, D.O., Coutinho, C.E., Madeira, M.F., Bottino, C.G., Vieira, R.T., Nascimento, S.B., et al. (2008) Leishmaniasis treatment - a challenge that remains: a review. Parasitol Res 103 : 1 10.
49. Saxena, A., Lahav, T., Holland, N., Aggarwal, G., Anupama, A., Huang, Y., et al. (2007) Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Mol Biochem Parasitol 152 : 53 65.
50. Selvapandiyan, A., Duncan, R., Debrabant, A., Bertholet, S., Sreenivas, G., Negi, N.S., et al. (2001) Expression of a mutant form of Leishmania donovani centrin reduces the growth of the parasite. J Biol Chem 276 : 43253 43261.
51. Selvapandiyan, A., Debrabant, A., Duncan, R., Muller, J., Salotra, P., Sreenivas, G., et al. (2004) Centrin gene disruption impairs stage-specific basal body duplication and cell cycle progression in Leishmania. J Biol Chem 279 : 25703 25710.
52. Selvapandiyan, A., Duncan, R., Debrabant, A., Lee, N., Sreenivas, G., Salotra, P. Nakhasi, H.L. (2006) Genetically modified live attenuated parasites as vaccines for leishmaniasis. Indian J Med Res 123 : 455 466.
53. Selvapandiyan, A., Duncan, R., Mendez, J., Kumar, R., Salotra, P., Cardo, L.J. Nakhasi, H.L. (2008) A Leishmania minicircle DNA footprint assay for sensitive detection and rapid speciation of clinical isolates. Transfusion 48 : 1787 1798.
54. Selvapandiyan, A., Dey, R., Nylen, S., Duncan, R., Sacks, D. Nakhasi, H.L. (2009) Intracellular replication-deficient Leishmania donovani induces long lasting protective immunity against visceral leishmaniasis. J Immunol 183 : 1813 1820.
55. Shapira, M., McEwen, J.G. Jaffe, C.L. (1988) Temperature effects on molecular processes which lead to stage differentiation in Leishmania. EMBO J 7 : 2895 2901.
56. Spath, G.F., Garraway, L.A., Turco, S.J. Beverley, S.M. (2003a) The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci USA 100 : 9536 9541.
57. Spath, G.F., Lye, L.F., Segawa, H., Sacks, D.L., Turco, S.J. Beverley, S.M. (2003b) Persistence without pathology in phosphoglycan-deficient Leishmania major. Science 301 : 1241 1243.
58. Speijer, D., Breek, C.K., Muijsers, A.O., Groenevelt, P.X., Dekker, H., de Haan, A. Benne, R. (1996) The sequence of a small subunit of cytochrome c oxidase from Crithidia fasciculata which is homologous to mammalian subunit IV. FEBS Lett 381 : 123 126.
59. Srividya, G., Duncan, R., Sharma, P., Raju, B.V., Nakhasi, H.L. Salotra, P. (2007) Transcriptome analysis during the process of in vitro differentiation of Leishmania donovani using genomic microarrays. Parasitology 134 : 1527 1539.
60. Stewart, J., Curtis, J., Spurck, T.P., Ilg, T., Garami, A., Baldwin, T., et al. (2005) Characterisation of a Leishmania mexicana knockout lacking guanosine diphosphate-mannose pyrophosphorylase. Int J Parasitol 35 : 861 873.
61. Streit, J.A., Recker, T.J., Filho, F.G., Beverley, S.M. Wilson, M.E. (2001) Protective immunity against the protozoan Leishmania chagasi is induced by subclinical cutaneous infection with virulent but not avirulent organisms. J Immunol 166 : 1921 1929.
62. Tan, T.H., Bochud-Allemann, N., Horn, E.K. Schneider, A. (2002) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci USA 99 : 1152 1157.
63. Van Hellemond, J.J. Tielens, A.G. (1997) Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes. Mol Biochem Parasitol 85 : 135 138.
64. Vergnes, B., Sereno, D., Tavares, J., Cordeiro-da-Silva, A., Vanhille, L., Madjidian-Sereno, N., et al. (2005) Targeted disruption of cytosolic SIR2 deacetylase discloses its essential role in Leishmania survival and proliferation. Gene 363 : 85 96.
65. Volf, P. Myskova, J. (2007) Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol 23 : 91 92.
66. Zhang, W.W. Matlashewski, G. (2001) Characterization of the A2-A2rel gene cluster in Leishmania donovani: involvement of A2 in visceralization during infection. Mol Microbiol 39 : 935 948.
67. Zikova, A., Horakova, E., Jirku, M., Dunajcikova, P. Lukes, J. (2006) The effect of down-regulation of mitochondrial RNA-binding proteins MRP1 and MRP2 on respiratory complexes in procyclic Trypanosoma brucei. Mol Biochem Parasitol 149 : 65 73.
68. Zikova, A., Panigrahi, A.K., Uboldi, A.D., Dalley, R.A., Handman, E. Stuart, K. (2008) Structural and functional association of Trypanosoma brucei MIX protein with cytochrome c oxidase complex. Eukaryot Cell 7 : 1994 2003.