Leishmania donovani: Proteasome-mediated down-regulation of methionine adenosyltransferase

Parasitology

Volumn 138, Issue 9, 2011, Pages 1082-1092

  Pérez Pertejo, Yolanda ^a   Álvarez Velilla, Raquel ^a   Estrada, Carlos García ^a   Balaña Fouce, Rafael ^a   Reguera, Rosa M ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Leishmania spp.; methionine adenosyltransferase overexpressing strain; post translational regulation; proteasome; S adenosylmethionine; ubiquitin

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; EPOXOMICIN; LACTACYSTIN; METHIONINE ADENOSYLTRANSFERASE; MG 115; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENZYME DEGRADATION; ENZYME METABOLISM; IMMUNOPRECIPITATION; LEISHMANIA DONOVANI; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION;

ACETYLCYSTEINE; CELL CULTURE TECHNIQUES; CLONING, MOLECULAR; CYCLOHEXIMIDE; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION; IMMUNOPRECIPITATION; KINETICS; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; LEUPEPTINS; METHIONINE ADENOSYLTRANSFERASE; OLIGOPEPTIDES; PLASMIDS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; S-ADENOSYLMETHIONINE; TRANSFECTION; UBIQUITIN;

LEISHMANIA DONOVANI;

EID: 80053073787     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011000862     Document Type: Article

References (42)

1. Bacchi, C. J., Garofalo, J., Ciminelli, M., Rattendi, D., Goldberg, B., McCann, P. P. and Yarlett, N. (1993). Resistance to DL-alpha-difluoro- methylornithine by clinical isolates of Trypanosoma brucei rhodesiense. Role of S-adenosylmethionine. Biochemical Pharmacology 46, 471-481. (Pubitemid 23239998)
2. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B., Böhme, U., Hannick, L., Aslett, M. A., Shallom, J., Marcello, L., Hou, L., Wickstead, B., Alsmark, U. C., Arrowsmith, C., Atkin, R. J., Barron, A. J., Bringaud, F., Brooks, K., Carrington, M., Cherevach, I., Chillingworth, T. J., Churcher, C., Clark, L. N., Corton, C. H., Cronin, A., Davies, R. M., Doggett, J., Djikeng, A., Feldblyum, T., Field, M.C., Fraser, A., Goodhead, I., Hance, Z., Harper, D., Harris, B. R., Hauser, H., Hostetler, J., Ivens, A., Jagels, K., Johnson, D., Johnson, J., Jones, K., Kerhornou, A. X., Koo, H., Larke, N., Landfear, S., Larkin, C., Leech, V., Line, A., Lord, A., Macleod, A., Mooney, P. J., Moule, S., Martin, D. M., Morgan, G.W., Mungall, K., Norbertczak, H., Ormond, D., Pai, G., Peacock, C. S., Peterson, J., Quali, M. A., Rabbinowitsch, E., Rajandream, M. A., Reitter, C., Salzberg, S. L., Sanders, M., Schobel, S., Sharp, S., Simmonds, M., Simpson, A. J., Tallon, L., Turner, C. M., Tait, A., Tivey, A. R., Van Aken, S., Walker, D., Wanless, D., Wang, S., White, B., White, O., Whitehead, S., Woodward, J., Wortman, J., Adams, M. D., Embley, T. M., Gull, K., Ullu, E., Barry, J. D., Fairlamb, A.H., Opperdoes, F., Barrell, B. G., Donelson, J. E., Hall, N., Fraser, C. M., Melville, S. E. and El-Sayed, N. M. (2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416-422. (Pubitemid 40994676)
3. Bouzat, J. L., McNeil, L.K., Robertson, H. M., Solter, L. F., Nixon, J.E., Beever, J.E., Gaskins, H.R., Olsen, G., Subramaniam, S., Sogin, M.L. and Lewin, H.A. (2000). Phylogenomic analysis of the alpha proteasome gene family from early-diverging eukaryotes. Journal of Molecular Evolution 51, 532-543. (Pubitemid 32001972)
4. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
5. Carlton, J. M., Angiuoli, S. V., Suh, B. B., Kooij, T. W., Pertea, M., Silva, J. C., Ermolaeva, M. D., Allen, J. E., Selengut, J. D., Koo, H. L., Peterson, J.D., Pop, M., Kosack, D.S., Shumway, M.F., Bidwell, S. L., Shallom, S. J., van Aken, S. E., Riedmuller, S.B., Feldblyum, T. V., Cho, J. K., Quackenbush, J., Sedegah, M., Shoaibi, A., Cummings, L. M., Florens, L., Yates, J. R., Raine, J. D., Sinden, R. E., Harris, M. A., Cunningham, D. A., Preiser, P. R., Bergman, L. W., Vaidya, A. B., van Lin, L.H., Janse, C. J., Waters, A. P., Smith, H. O., White, O. R., Salzberg, S. L., Venter, J.C., Fraser, C. M., Hoffman, S. L., Gardner, M. J. and Carucci, D.J. (2002). Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature, London 419, 512-519.
6. Cuervo, P., de Jesús, J. B., Junqueira, M., Mendonca-Lima, L., Gonzalez, L. J., Betancourt, L., Grimaldi, G. Jr, Domoni, G.B., Fernández, O. and Cupolillo, E. (2007). Proteome analysis of Leishmania (Viannia) braziliensis by two-dimensional gel electrophoresis and mass spectrometry. Molecular and Biochemical Parasitology 154, 6-21. (Pubitemid 46894708)
7. de Diego, J. L., Katz, J. M., Marshall, P., Gutierrez, B., Manning, J. E., Nussenzweig, V. and Gonzalez, J. (2001). The ubiquitin-proteasome pathway plays an essential role in proteolysis during Trypanosoma cruzi remodeling. Biochemistry 40, 1053-1062. (Pubitemid 32108598)
8. Drummelsmith, J., Brochu, V., Girard, I., Messier, N. and Ouellette, M. (2003). Proteome mapping of the protozoan parasite Leishmania and application to the study of drug targets and resistance mechanisms. Molecular and Cellular Proteomics: MCP 2, 146-155.
9. Drummelsmith, J., Girard, I., Trudel, N. and Ouellette, M. (2004). Differential protein expression analysis of Leishmania major reveals novel roles for methionine adenosyltransferase and S-adenosylmethionine in methotrexate resistance. The Journal of Biological Chemistry 279, 33273-33280. (Pubitemid 39062974)
10. Dubessay, P., Blaineau, C., Bastien, P., Tasse, L., Van Dijk, J., Crobu, L. and Pages, M. (2006). Cell cycle-dependent expression regulation by the proteasome pathway and characterization of the nuclear targeting signal of a Leishmania major Kin-13 kinesin. Molecular Microbiology 59, 1162-1174.
11. El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A.N., Ghedin, E., Worthey, E.A., Delcher, A.L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., da Silveira, J.F., de Jong, P., Edwards, K., Englund, P. T., Fazelina, G., Feldblyum, T., Ferella, M., Frasch, A.C., Gull, K., Horn, D., Hou, L., Huang, Y., Kindlund, E., Klingbeil, M., Kluge, S., Koo, H., Lacerda, D., Levin, M.J., Lorenzi, H., Louie, T., Machado, C. R., McCulloch, R., McKenna, A., Mizuno, Y., Mottram, J. C., Nelson, S., Ochaya, S., Osoegawa, K., Pai, G., Parsons, M., Pentony, M., Pettersson, U., Pop, M., Ramirez, J. L., Rinta, J., Robertson, L., Salzberg, S. L., Sanchez, D. O., Seyler, A., Sharma, R., Shetty, J., Simpson, A.J., Sisk, E., Tammi, M. T., Tarleton, R., Teixeira, S., Van Aken, S., Vogt, C., Ward, P. N., Wickstead, B., Wortman, J., White, O., Fraser, C. M., Stuart, K. D. and Andersson, B. (2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409-415.
12. Emmerlich, V., Santarius, U., Bakker-Grunwald, T. and Scholze, H. (1999). Isolation and subunit composition of the 20S proteasome of Giardia lamblia. Molecular and Biochemical Parasitology 100, 131-134. (Pubitemid 29206680)
13. Fontecave, M., Atta, M. and Mulliez, E. (2004). S-adenosylmethionine: nothing goes to waste. Trends in Biochemical Sciences 29, 243-249. (Pubitemid 38591318)
14. Garcia-Estrada, C., Perez-Pertejo, Y., Ordonez, D., Balana-Fouce, R. and Reguera, R.M. (2007). Analysis of genetic elements regulating the methionine adenosyltransferase gene in Leishmania infantum. Gene 389, 163-173. (Pubitemid 46186785)
15. Garcia-Estrada, C., Reguera, R. M., Villa, H., Requena, J. M., Muller, S., Perez-Pertejo, Y., Balana-Fouce, R. and Ordonez, D. (2003). Identification of a gene in Leishmania infantum encoding a protein that contains aSP-RING/MIZ zinc finger domain. Biochimica et Biophysica Acta 1629, 44-52. (Pubitemid 37186777)
16. Gil, B., Pajares, M. A., Mato, J. M. and Alvarez, L. (1997). Glucocorticoid regulation of hepatic S-adenosylmethionine synthetase gene expression. Endocrinology 138, 1251-1258. (Pubitemid 27089784)
17. Gonzalez, J., Ramalho-Pinto, F.J., Frevert, U., Ghiso, J., Tomlinson, S., Scharfstein, J., Corey, E. J. and Nussenzweig, V. (1996). Proteasome activity is required for the stage-specific transformation of a protozoan parasite. The Journal of Experimental Medicine 184, 1909-1918. (Pubitemid 26404481)
18. Hellberg, A., Sommer, A. and Bruchhaus, I. (1999). Primary sequence of a putative non-ATPase subunit of the 26S proteasome from Entamoeba histolytica is similar to the human and yeast S2 subunit. Parasitology Research 85, 417-420. (Pubitemid 29156189)
19. Hicke, L., Schubert, H. L. and Hill, C. P. (2005). Ubiquitin-binding domains. Nature Reviews. Molecular Cell Biology 6, 610-621.
20. Hunter, T. (2007). The age of crosstalk: phosphorylation, ubiquitination, and beyond. Molecular Cell 28, 730-738. (Pubitemid 350217067)
21. Ivens, A. C., Peacock, C. S., Worthey, E. A., Murphy, L., Aggarwal, G., Berriman, M., Sisk, E., Rajandream, M.A., Adlem, E., Aert, R., Anupama, A., Apostolou, Z., Attipoe, P., Bason, N., Bauser, C., Beck, A., Beverley, S. M., Bianchettin, G., Borzym, K., Bothe, G., Bruschi, C. V., Collins, M., Cadag, E., Ciarloni, L., Clayton, C., Coulson, R.M., Cronin, A., Cruz, A.K., Davies, R. M., De Gaudenzi, J., Dobson, D. E., Duesterhoeft, A., Fazelina, G., Fosker, N., Frasch, A. C., Fraser, A., Fuchs, M., Gabel, C., Goble, A., Goffeau, A., Harris, D., Hertz-Fowler, C., Hilbert, H., Horn, D., Huang, Y., Klages, S., Knights, A., Kube, M., Larke, N., Litvin, L., Lord, A., Louie, T., Marra, M., Masuy, D., Matthews, K., Michaeli, S., Mottram, J. C., Muller-Auer, S., Munden, H., Nelson, S., Norbertczak, H., Oliver, K., O'neil, S., Pentony, M., Pohl, T. M., Price, C., Purnelle, B., Quail, M. A., Rabbinowitsch, E., Reinhardt, R., Rieger, M., Rinta, J., Robben, J., Robertson, L., Ruiz, J. C., Rutter, S., Saunders, D., Schafer, M., Schein, J., Schwartz, D. C., Seeger, K., Seyler, A., Sharp, S., Shin, H., Sivam, D., Squares, R., Squares, S., Tosato, V., Vogt, C., Volckaert, G., Wambutt, R., Warren, T., Wedler, H., Woodward, J., Zhou, S., Zimmermann, W., Smith, D.F., Blackwell, J. M., Stuart, K. D., Barrell, B. and Myler, P. J. (2005). The genome of the kinetoplastid parasite, Leishmania major. Science 309, 436-442. (Pubitemid 40994677)
22. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680-685.
23. Li, G. D., Li, J. L., Mugthin, M. and Ward, S. A. (2000). Molecular cloning of a gene encoding a 20S proteasome beta subunit from Plasmodium falciparum. International Journal for Parasitology 30, 729-733. (Pubitemid 30336452)
24. Mato, J. M., Alvarez, L., Ortiz, P. and Pajares, M. A. (1997). S-adenosylmethionine synthesis: molecular mechanisms and clinical implications. Pharmacology and Therapeutics 73, 265-280. (Pubitemid 27224439)
25. Mato, J. M., Corrales, F. J., Lu, S. C. and Avila, M. A. (2002). S-Adenosylmethionine: a control switch that regulates liver function. The FASEB Journal 16, 15-26. (Pubitemid 34027946)
26. Nasizadeh, S., Jeppsson, A. and Persson, L. (2003). Proteasomal degradation of a trypanosomal ornithine decarboxylase. Cellular Physiology and Biochemistry 13, 321-328. (Pubitemid 37356739)
27. Pajares, M. A., Duran, C., Corrales, F. and Mato, J.M. (1994). Protein kinase C phosphorylation of rat liver S-adenosylmethionine synthetase: dissociation and production of an active monomer. The Biochemical Journal 303, 949-955. (Pubitemid 24326034)
28. Paugam, A., Creuzet, C., Dupouy-Camet, J. and Roisin, M. P. (2001). Evidence for the existence of a proteasome in Toxoplasma gondii: intra-cellular localization and specific peptidase activities. Parasite 8, 267-273. (Pubitemid 33629566)
29. Pegg, A. E. (2006). Regulation of ornithine decarboxylase. The Journal of Biological Chemistry 281, 14529-14532. (Pubitemid 43855154)
30. Perez-Pertejo, Y., Reguera, R.M., Ordonez, D. and Balana-Fouce, R. (2006). Characterization of a methionine adenosyltransferase over-expressing strain in the trypanosomatid Leishmania donovani. Biochimica et Biophysica Acta 1760, 10-19. (Pubitemid 41790626)
31. Persson, L., Jeppsson, A. and Nasizadeh, S. (2003). Turnover of trypanosomal ornithine decarboxylases. Biochemical Society Transactions 31, 411-414. (Pubitemid 36520687)
32. Reguera, R. M., Balana-Fouce, R., Perez-Pertejo, Y., Fernandez, F. J., Garcia-Estrada, C., Cubria, J. C., Ordonez, C. and Ordonez, D. (2002). Cloning expression and characterization of methionine adenosyltransferase in Leishmania infantum promastigotes. The Journal of Biological Chemistry 277, 3158-3167. (Pubitemid 34953177)
33. Reguera, R. M., Redondo, C.M., Perez-Pertejo, Y. and Balana-Fouce, R. (2007). S-Adenosylmethionine in protozoan parasites: functions, synthesis and regulation. Molecular and Biochemical Parasitology 152, 1-10. (Pubitemid 46107702)
34. Robertson, C. D. (1999). The Leishmania mexicana proteasome. Molecular and Biochemical Parasitology 103, 49-60. (Pubitemid 29428228)
35. Silva-Jardim, I., Horta, M. F. and Ramalho-Pinto, F. J. (2004). The Leishmania chagasi proteasome: role in promastigotes growth and amasti-gotes survival within murine macrophages. Acta Tropica 91, 121-130. (Pubitemid 38952713)
36. To, W. Y. and Wang, C. C. (1997). Identification and characterization of an activated 20S proteasome in Trypanosoma brucei. FEBS Letters 404, 253-262. (Pubitemid 27113463)
37. Tryoen-Toth, P., Richert, S., Sohm, B., Mine, M., Marsac, C., Van Dorsselaer, A., Leize, E. and Florentz, C. (2003). Proteomic consequences of a human mitochondrial tRNA mutation beyond the frame of mitochondrial translation. The Journal of Biological Chemistry 278, 24314-24323. (Pubitemid 37548582)
38. Van Hellemond, J. J. and Mottram, J. C. (2000). The CYC3 gene of trypanosoma brucei encodes a cyclin with a short half-life. Molecular and Biochemical Parasitology 111, 275-282. (Pubitemid 32121671)
39. Voges, D., Zwickl, P. and Baumeister, W. (1999). The 26S proteasome: a molecular machine designed for controlled proteolysis. Annual Review of Biochemistry 68, 1015-1068. (Pubitemid 29449214)
40. Wang, S. C. and Frey, P. A. (2007). S-adenosylmethionine as an oxidant: the radical SAM superfamily. Trends in Biochemical Sciences 32, 101-110. (Pubitemid 46367690)
41. Yao, Y., Toth, C.R., Huang, L., Wong, M.L., Dias, P., Burlingame, A. L., Coffino, P. and Wang, C. C. (1999). Alpha5 subunit in Trypanosoma brucei proteasome can self-assemble to form a cylinder of four stacked heptamer rings. The Biochemical Journal 344 Pt 2, 349-358. (Pubitemid 30011589)
42. Yerlikaya, A. and Stanley, B. A. (2004). S-adenosylmethionine de-carboxylase degradation by the 26 S proteasome is accelerated by substrate-mediated transamination. The Journal of Biological Chemistry 279, 12469-12478. (Pubitemid 38445816)