Evolution, dynamics and specialized functions of glycosomes in metabolism and development of trypanosomatids

Current Opinion in Microbiology

Volumn 22, Issue , 2014, Pages 79-87

  Szöör, Balázs ^a   Haanstra, Jurgen R ^b,c   Gualdrón López, Melisa ^d,e   Michels, Paul A M ^a,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSIDAD DE LOS ANDES   (Venezuela)

^e FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOLYTIC ENZYME; PHOSPHOPROTEIN PHOSPHATASE;

DEGRADATION KINETICS; ENZYME KINETICS; EVOLUTIONARY ADAPTATION; GLYCOSOME; KINETOPLASTID LIFE CYCLE STAGE; KINETOPLASTIDA; LEISHMANIA; LIFE CYCLE STAGE; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; PARASITE DEVELOPMENT; PARASITE METABOLISM; PARASITE PHENOMENA AND FUNCTIONS; PARASITISM; PEROXISOME; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TURNOVER TIME; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBODY; PHYSIOLOGY; TRYPANOSOMATIDAE;

LIFE CYCLE STAGES; MICROBODIES; TRYPANOSOMATINA;

EID: 84907959214     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.09.006     Document Type: Review

References (51)

1. Bringaud F., Rivière L., Coustou V. Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 2006, 149:1-9.
2. Saunders E.C., De Souza D.P., Naderer T., Sernee M.F., Ralton J.E., Doyle M.A., Macrae J.I., Chambers J.L., Heng J., Nahid A., Likic V.A., McConville M.J. Central carbon metabolism of Leishmania parasites. Parasitology 2010, 137:1303-1313.
3. Maugeri D.A., Cannata J.J., Cazzulo J.J. Glucose metabolism in Trypanosoma cruzi. Essays Biochem 2011, 51:15-30.
4. Colasante C., Ellis M., Ruppert T., Voncken F. Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 2006, 6:3275-3293.
5. Gualdrón-López M., Brennand A., Hannaert V., Quiñones W., Cáceres A.J., Bringaud F., Concepción J.L., Michels P.A. When, how and why glycolysis became compartmentalised in the Kinetoplastea. A new look at an ancient organelle. Int J Parasitol 2012, 42:1-20.
6. Gualdrón-López M., Michels P.A.M., Quiñones W., Cáceres A.J., Avilán L., Concepción J.L. The function of glycosomes in the metabolism of trypanosomatid parasites and the promise of glycosomal proteins as drug targets. Trypanosomatid Diseases: Molecular Routes to Drug Discovery 2013, 121-151. Wiley-VCH Verlag GmbH & Co. KGaA. T. Jäger, O. Koch, L. Flohé (Eds.).
7. Barros-Alvarez X., Gualdrón-López M., Acosta H., Cáceres A.J., Graminha M.A., Michels P.A., Concepción J.L., Quiñones W. Glycosomal targets for anti-trypanosomatid drug discovery. Curr Med Chem 2014, 21:1679-1706.
8. Deramchia K., Morand P., Biran M., Millerioux Y., Mazet M., Wargnies M., Franconi J.M., Bringaud F. Contribution of pyruvate phosphate dikinase in the maintenance of the glycosomal ATP/ADP balance in the Trypanosoma brucei procyclic form. J Biol Chem 2014, 289:17365-17378.
9. Opperdoes F.R., Szikora J.P. In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol Biochem Parasitol 2006, 147:193-206.
10. Colasante C., Voncken F., Manful T., Ruppert T., Tielens A.G., van Hellemond J.J., Clayton C. Proteins and lipids of glycosomal membranes from Leishmania tarentolae and Trypanosoma brucei. F1000 Res 2013, 2:27. 10.12688/f1000research.2-27.v1.
11. Guerra D.G., Decottignies A., Bakker B.M., Michels P.A. The mitochondrial FAD-dependent glycerol-3-phosphate dehydrogenase of Trypanosomatidae and the glycosomal redox balance of insect stages of Trypanosoma brucei and Leishmania spp. Mol Biochem Parasitol 2006, 149:155-169.
12. Naderer T., Ellis M.A., Sernee M.F., De Souza D.P., Curtis J., Handman E., McConville M.J. Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci U S A 2006, 103:5502-5507.
13. Bakker B.M., Mensonides F.I., Teusink B., van Hoek P., Michels P.A., Westerhoff H.V. Compartmentation protects trypanosomes from the dangerous design of glycolysis. Proc Natl Acad Sci U S A 2000, 97:2087-2092.
14. Furuya T., Kessler P., Jardim A., Schnaufer A., Crudder C., Parsons M. Glucose is toxic to glycosome-deficient trypanosomes. Proc Natl Acad Sci U S A 2002, 99:14177-14182.
15. Kessler P.S., Parsons M. Probing the role of compartmentation of glycolysis in procyclic form Trypanosoma brucei: RNA interference studies of PEX14, hexokinase, and phosphofructokinase. J Biol Chem 2005, 280:9030-9036.
16. Haanstra J.R., van Tuijl A., Kessler P., Reijnders W., Michels P.A., Westerhoff H.V., Parsons M., Bakker B.M. Compartmentation prevents a lethal turbo-explosion of glycolysis in trypanosomes. Proc Natl Acad Sci U S A 2008, 105:17718-17723.
17. Urbaniak M.D., Güther M.L., Ferguson M.A. Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLOS ONE 2012, 7:e36619.
18. Urbaniak M.D., Martin D.M., Ferguson M.A. Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 2013, 12:2233-2244.
19. Misset O., Bos O.J., Opperdoes F.R. Glycolytic enzymes of Trypanosoma brucei. Simultaneous purification, intraglycosomal concentrations and physical properties. Eur J Biochem 1986, 157:441-453.
20. Clayton C.E. Most proteins, including fructose bisphosphate aldolase, are stable in the procyclic trypomastigote form of Trypanosoma brucei. Mol Biochem Parasitol 1988, 28:43-46.
21. Albert M.A., Haanstra J.R., Hannaert V., Van Roy J., Opperdoes F.R., Bakker B.M., Michels P.A. Experimental and in silico analyses of glycolytic flux control in bloodstream form Trypanosoma brucei. J Biol Chem 2005, 280:28306-28315.
22. Bellu A.R., Kiel J.A. Selective degradation of peroxisomes in yeasts. Microsc Res Tech 2003, 61:161-170.
23. Manjithaya R., Nazarko T.Y., Farré J.C., Subramani S. Molecular mechanism and physiological role of pexophagy. FEBS Lett 2010, 584:1367-1373.
24. Herman M., Pérez-Morga D., Schtickzelle N., Michels P.A. Turnover of glycosomes during life-cycle differentiation of Trypanosoma brucei. Autophagy 2008, 4:294-308.
25. Brennand A., Gualdrón-López M., Coppens I., Rigden D.J., Ginger M.L., Michels P.A. Autophagy in parasitic protists: unique features and drug targets. Mol Biochem Parasitol 2011, 177:83-99.
26. Michels P.A., Rigden D.J. Evolutionary analysis of fructose 2,6-bisphosphate metabolism. IUBMB Life 2006, 58:133-141.
27. Szöör B., Ruberto I., Burchmore R., Matthews K.R. A novel phosphatase cascade regulates differentiation in Trypanosoma brucei via a glycosomal signaling pathway. Genes Dev 2010, 24:1306-1316.
28. Nolan D.P., Rolin S., Rodriguez J.R., Van Den Abbeele J., Pays E. Slender and stumpy bloodstream forms of Trypanosoma brucei display a differential response to extracellular acidic and proteolytic stress. Eur J Biochem 2000, 267:18-27.
29. Szöör B., Wilson J., McElhinney H., Tabernero L., Matthews K.R. Protein tyrosine phosphatase TbPTP1: a molecular switch controlling life cycle differentiation in trypanosomes. J Cell Biol 2006, 175:293-303.
30. Brun R., Schönenberger M. Stimulating effect of citrate and cis-aconitate on the transformation of Trypanosoma brucei bloodstream forms to procyclic forms in vitro. Z Parasitenkd 1981, 66:17-24.
31. Dean S., Marchetti R., Kirk K., Matthews K.R. A surface transporter family conveys the trypanosome differentiation signal. Nature 2009, 459:213-217.
32. Güther M.L., Urbaniak M.D., Tavendale A., Prescott A., Ferguson M.A. High-confidence glycosome proteome for procyclic form Trypanosoma brucei by epitope-tag organelle enrichment and SILAC proteomics. J Proteome Res 2014, 13:2796-2806.
33. Morris J.C., Wang Z., Drew M.E., Englund P.T. Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO J 2002, 21:4429-4438.
34. Galland N., Michels P.A. Comparison of the peroxisomal matrix protein import system of different organisms. Exploration of possibilities for developing inhibitors of the import system of trypanosomatids for anti-parasite chemotherapy. Eur J Cell Biol 2010, 89:621-637.
35. Rucktäschel R., Girzalsky W., Erdmann R. Protein import machineries of peroxisomes. Biochim Biophys Acta 2011, 1808:892-900.
36. Gualdrón-López M., Brennand A., Avilán L., Michels P.A. Translocation of solutes and proteins across the glycosomal membrane of trypanosomes; possibilities and limitations for targeting with trypanocidal drugs. Parasitology 2013, 140:1-20.
37. Smith J.J., Aitchison J.D. Peroxisomes take shape. Nat Rev Mol Cell Biol 2013, 14:803-817.
38. Hettema E.H., Erdmann R., van der Klei I., Veenhuis M. Evolving models for peroxisome biogenesis. Curr Opin Cell Biol 2014, 29:25-30.
39. Gabaldón T. Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 2010, 365:765-773.
40. Makiuchi T., Annoura T., Hashimoto M., Hashimoto T., Aoki T., Nara T. Compartmentalization of a glycolytic enzyme in Diplonema, a non-kinetoplastid euglenozoan. Protist 2011, 162:482-489.
41. Martin W. Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 2010, 365:847-855.
42. Opperdoes F.R., Borst P. Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett 1977, 80:360-364.
43. Opperdoes F.R. Compartmentation of carbohydrate metabolism in trypanosomes. Annu Rev Microbiol 1987, 41:127-151.
44. Aman R.A., Kenyon G.L., Wang C.C. Cross-linking of the enzymes in the glycosome of Trypanosoma brucei. J Biol Chem 1985, 260:6966-6973.
45. Flegontov P., Votýpka J., Skalický T., Logacheva M.D., Penin A.A., Tanifuji G., Onodera N.T., Kondrashov A.S., Volf P., Archibald J.M., Lukeš J. Paratrypanosoma is a novel early-branching trypanosomatid. Curr Biol 2013, 23:1787-1793.
46. Lukeš J., Skalický T., Týč J., Votýpka J., Yurchenko V. Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasitol 2014, 195:115-122.
47. Mazet M., Morand P., Biran M., Bouyssou G., Courtois P., Daulouède S., Millerioux Y., Franconi J.M., Vincendeau P., Moreau P., Bringaud F. Revisiting the central metabolism of the bloodstream forms of Trypanosoma brucei: production of acetate in the mitochondrion is essential for parasite viability. PLoS Negl Trop Dis 2013, 7(12):e2587.
48. Aman R.A., Wang C.C. An improved purification of glycosomes from the procyclic trypomastigotes of Trypanosoma brucei. Mol Biochem Parasitol 1986, 21:211-220.
49. Hart D.T., Misset O., Edwards S.W., Opperdoes F.R. A comparison of the glycosomes (microbodies) isolated from Trypanosoma brucei bloodstream form and cultured procyclic trypomastigotes. Mol Biochem Parasitol 1984, 12:25-35.
50. Haanstra J.R. The power of network-based drug design and the interplay between metabolism and gene expression in Trypanosoma brucei 2009, 271. (Ph.D. thesis), VU University Amsterdam, Amsterdam.
51. Bringaud F., Baltz D., Baltz T. Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: pyruvate phosphate dikinase. J Biol Chem 1998, 95:7963-7968.