Trypanosoma brucei vacuolar transporter chaperone 4 (TbVtc4) is an acidocalcisome polyphosphate kinase required for in vivo infection

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 34205-34216

  Lander, Noelia ^a   Ulrich, Paul N ^a,b   Docampo, Roberto ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDOCALCISOMES; ANIONIC POLYMERS; KINASE ACTIVITY; PARENTAL CELLS; POLYCLONAL ANTIBODY; SUBCELLULAR LOCALIZATIONS; TRYPANOSOMA BRUCEI; VOLUME RECOVERY;

BIOSYNTHESIS; CELL CULTURE; CHAINS; OSMOSIS;

ENZYMES;

DOXYCYCLINE; EPITOPE; MICROORGANISM PROTEIN; POLYCLONAL ANTIBODY; POLYPHOSPHATE; TRYPANOSOMA BRUCEI VACUOLAR TRANSPORTER CHAPERONE 4; UNCLASSIFIED DRUG;

AFRICAN TRYPANOSOMIASIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EUKARYOTE; FLUORESCENCE MICROSCOPY; GENE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOREGULATION; OSMOTIC STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TBVTC4 GENE; TRYPANOSOMA BRUCEI; WILD TYPE;

ACIDOCALCISOME; ENZYME CATALYSIS; OSMOREGULATION; PARASITE; PARASITE METABOLISM; POLYPHOSPHATE; TRYPANOSOMA BRUCEI; VACUOLAR ACIDIFICATION; VACUOLAR TRANSPORTER CHAPERONE;

ANIMALS; GENE KNOCKDOWN TECHNIQUES; MICE; MOLECULAR CHAPERONES; PHOSPHOTRANSFERASES (PHOSPHATE GROUP ACCEPTOR); PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 84888355905     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.518993     Document Type: Article

References (49)

1. Rao, N. N., Gómez-Garcia, M. R., and Kornberg, A. (2009) Inorganic polyphosphate. Essential for growth and survival. Annu. Rev. Biochem. 78, 605-647
2. Moreno, S. N., and Docampo, R. (2013) Polyphosphate and its diverse functions in host cells and pathogens. PLoS Pathog. 9, e1003230
3. Ruiz, F. A., Lea, C. R., Oldfield, E., and Docampo, R. (2004) Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J. Biol. Chem. 279, 44250-44257
4. Moreno-Sanchez, D., Hernandez-Ruiz, L., Ruiz, F. A., and Docampo, R. (2012) Polyphosphate is a novel pro-inflammatory regulator of mast cells and is located in acidocalcisomes. J. Biol. Chem. 287, 28435-28444
5. Smith, S. A., Mutch, N. J., Baskar, D., Rohloff, P., Docampo, R., and Morrissey, J. H. (2006) Polyphosphate modulates blood coagulation and fibrinolysis. Proc. Natl. Acad. Sci. U. S. A. 103, 903-908
6. Müller, F., Mutch, N. J., Schenk, W. A., Smith, S. A., Esterl, L., Spronk, H. M., Schmidbauer, S., Gahl, W. A., Morrissey, J. H., and Renné, T. (2009) Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 139, 1143-1156
7. Morrissey, J. H., Choi, S. H., and Smith, S. A. (2012) Polyphosphate. An ancient molecule that links platelets, coagulation, and inflammation. Blood 119, 5972-5979
8. Wurst, H., Shiba, T., and Kornberg, A. (1995) The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 177, 898-906
9. Rodrigues, C. O., Ruiz, F. A., Vieira, M., Hill, J. E., and Docampo, R. (2002) An acidocalcisomal exopolyphosphatase from Leishmania major with high affinity for short chain polyphosphate. J. Biol. Chem. 277, 50899-50906
10. 2+-sensitive soluble exopolyphosphatase from Trypanosoma cruzi depletes polyphosphate and affects osmoregulation. J. Biol. Chem. 282, 32501-32510
11. Tammenkoski, M., Koivula, K., Cusanelli, E., Zollo, M., Steegborn, C., Baykov, A. A., and Lahti, R. (2008) Human metastasis regulator protein H-prune is a short-chain exopolyphosphatase. Biochemistry 47, 9707-9713
12. Sethuraman, A., Rao, N. N., and Kornberg, A. (2001) The endopolyphosphatase gene. Essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 98, 8542-8547
13. Hothorn, M., Neumann, H., Lenherr, E. D., Wehner, M., Rybin, V., Hassa, P. O., Uttenweiler, A., Reinhardt, M., Schmidt, A., Seiler, J., Ladurner, A. G., Herrmann, C., Scheffzek, K., and Mayer, A. (2009) Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324, 513-516
14. Cohen, A., Perzov, N., Nelson, H., and Nelson, N. (1999) A novel family of yeast chaperons involved in the distribution of V-ATPase and other membrane proteins. J. Biol. Chem. 274, 26885-26893
15. Müller, O., Bayer, M. J., Peters, C., Andersen, J. S., Mann, M., and Mayer, A. (2002) The Vtc proteins in vacuole fusion. Coupling NSF activity to V (0) trans-complex formation. EMBO J. 21, 259-269
16. Müller, O., Neumann, H., Bayer, M. J., and Mayer, A. (2003) Role of the Vtc proteins in V-ATPase stability and membrane trafficking. J. Cell Sci. 116, 1107-1115
17. 2+ signaling. Trends Cell Biol. 20, 277-286
18. Docampo, R., De Souza, W., Miranda, K., Rohloff, P., and Moreno, S. N. (2005) Acidocalcisomes. Conserved from bacteria to man. Nat. Rev. Microbiol. 3, 251-261
19. Docampo, R., and Moreno, S. N. (2011) Acidocalcisomes. Cell Calcium 50, 113-119
20. + exchange in acidic vacuoles of Trypanosoma brucei. Biochem. J. 304, 227-233
21. Huang, G., Bartlett, P. J., Thomas, A. P., Moreno, S. N., and Docampo, R. (2013) Acidocalcisomes of Trypanosoma brucei have an inositol 1, 4, 5-trisphosphate receptor that is required for growth and infectivity. Proc. Natl. Acad. Sci. U. S. A. 110, 1887-1892
22. Ruiz, F. A., Rodrigues, C. O., and Docampo, R. (2001) Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J. Biol. Chem. 276, 26114-26121
23. Li, Z. H., Alvarez, V. E., De Gaudenzi, J. G., Sant'Anna, C., Frasch, A. C., Cazzulo, J. J., and Docampo, R. (2011) Hyperosmotic stress induces aquaporindependent cell shrinkage, polyphosphate synthesis, amino acid accumulation, and global gene expression changes in Trypanosoma cruzi. J. Biol. Chem. 286, 43959-43971
24. Docampo, R., Jimenez, V., King-Keller, S., Li, Z. H., and Moreno, S. N. (2011) The role of acidocalcisomes in the stress response of Trypanosoma cruzi. Adv. Parasitol. 75, 307-324
25. Rohloff, P., and Docampo, R. (2008) A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi. Exp. Parasitol. 118, 17-24
26. Ulrich, P. N., Jimenez, V., Park, M., Martins, V. P., Atwood, J., 3rd, Moles, K., Collins, D., Rohloff, P., Tarleton, R., Moreno, S. N., Orlando, R., and Docampo, R. (2011) Identification of contractile vacuole proteins in Trypanosoma cruzi. PLoS One 6, e18013
27. Fang, J., Rohloff, P., Miranda, K., and Docampo, R. (2007) Ablation of a small transmembrane protein of Trypanosoma brucei (TbVTC1) involved in the synthesis of polyphosphate alters acidocalcisome biogenesis and function and leads to a cytokinesis defect. Biochem. J. 407, 161-170
28. Wirtz, E., and Clayton, C. (1995) Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science 268, 1179-1183
29. Wirtz, E., Leal, S., Ochatt, C., and Cross, G. A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominantnegative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99, 89-101
30. Huang, G., Fang, J., Sant'Anna, C., Li, Z. H., Wellems, D. L., Rohloff, P., and Docampo, R. (2011) Adaptor protein-3 (AP-3) complex mediates the biogenesis of acidocalcisomes and is essential for growth and virulence of Trypanosoma brucei. J. Biol. Chem. 286, 36619-36630
31. +- pyrophosphatase governs maintenance of functional acidocalcisomes and growth of the insect and mammalian forms of Trypanosoma brucei. J. Biol. Chem. 277, 37369-37376
32. Oberholzer, M., Morand, S., Kunz, S., and Seebeck, T. (2006) A vector series for rapid PCR-mediated C-terminal in situ tagging of Trypanosoma brucei genes. Mol. Biochem. Parasitol. 145, 117-120
33. Falquet, L., Pagni, M., Bucher, P., Hulo, N., Sigrist, C. J., Hofmann, K., and Bairoch, A. (2002) The PROSITE database, its status in 2002. Nucleic Acids Res. 30, 235-238
34. Claros, M. G., and Von Heijne, G. (1994) TopPred II. An improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686
35. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B. P., Carrington, M., Depledge, D. P., Fischer, S., Gajria, B., Gao, X., Gardner, M. J., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hertz-Fowler, C., Houston, R., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Logan, F. J., Miller, J. A., Mitra, S., Myler, P. J., Nayak, V., Pennington, C., Phan, I., Pinney, D. F., Ramasamy, G., Rogers, M. B., Roos, D. S., Ross, C., Sivam, D., Smith, D. F., Srinivasamoorthy, G., Stoeckert, C. J., Jr., Subramanian, S., Thibodeau, R., Tivey, A., Treatman, C., Velarde, G., and Wang, H. (2010) TriTrypDB. A functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38, D457-D462
36. Medina-Acosta, E., and Cross, G. A. (1993) Rapid isolation of DNA from trypanosomatid protozoa using a simple "mini-prep" procedure. Mol. Biochem. Parasitol. 59, 327-329
37. De Jesus, T. C., Tonelli, R. R., Nardelli, S. C., Da SilvaAugusto, L., Motta, M. C., Girard Dias, W., Miranda, K., Ulrich, P., Jimenez, V., Barquilla, A., Navarro, M., Docampo, R., and Schenkman, S. (2010) Target of rapamycin (TOR)-like 1 kinase is involved in the control of polyphosphate levels and acidocalcisome maintenance in Trypanosoma brucei. J. Biol. Chem. 285, 24131-24140
38. Kocic, I., Hirano, Y., and Hiraoka, M. (2001) Ionic basis for membrane potential changes induced by hypoosmotic stress in guinea-pig ventricular myocytes. Cardiovasc. Res. 51, 59-70
39. Herbert, W. J., and Lumsden, W. H. (1976) Trypanosoma brucei: a rapid "matching" method for estimating the host's parasitemia. Exp. Parasitol. 40, 427-431
40. Rodrigues, C. O., Scott, D. A., and Docampo, R. (1999) Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes. Mol. Cell. Biol. 19, 7712-7723
41. Rohloff, P., Rodrigues, C. O., and Docampo, R. (2003) Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium. Mol. Biochem. Parasitol. 126, 219-230
42. Scott, D. A., Docampo, R., Dvorak, J. A., Shi, S., and Leapman, R. D. (1997) In situ compositional analysis of acidocalcisomes in Trypanosoma cruzi. J. Biol. Chem. 272, 28020-28029
43. + antiporter of Saccharomyces cerevisiae. J. Biol. Chem. 282, 24284-24293
44. Rao, N. N., and Kornberg, A. (1996) Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J. Bacteriol. 178, 1394-1400
45. Moreno, B., Urbina, J. A., Oldfield, E., Bailey, B. N., Rodrigues, C. O., and Docampo, R. (2000) 31PNMRspectroscopy of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Evidence for high levels of condensed inorganic phosphates. J. Biol. Chem. 275, 28356-28362
46. Lang, F., Busch, G. L., Ritter, M., Völkl, H., Waldegger, S., Gulbins, E., and Häussinger, D. (1998) Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78, 247-306
47. Emmer, B. T., Nakayasu, E. S., Souther, C., Choi, H., Sobreira, T. J., Epting, C. L., Nesvizhskii, A. I., Almeida, I. C., and Engman, D. M. (2011) Global analysis of protein palmitoylation in African trypanosomes. Eukaryot. Cell 10, 455-463
48. Furuya, T., Kashuba, C., Docampo, R., and Moreno, S. N. (2000) A novel phosphatidylinositol-phospholipase C of Trypanosoma cruzi that is lipid modified and activated during trypomastigote to amastigote differentiation. J. Biol. Chem. 275, 6428-6438
49. De PauloMartins, V., Okura, M., Maric, D., Engman, D. M., Vieira, M., Docampo, R., and Moreno, S. N. (2010) Acylation-dependent export of Trypanosoma cruzi phosphoinositide-specific phospholipase C to the outer surface of amastigotes. J. Biol. Chem. 285, 30906-30917