Peptide-targeted delivery of a pH sensor for quantitative measurements of intraglycosomal pH in live Trypanosoma brucei

Biochemistry

Volumn 52, Issue 21, 2013, Pages 3629-3637

  Lin, Sheng ^a   Morris, Meredith T ^a   Ackroyd, P Christine ^a   Morris, James C ^a   Christensen, Kenneth A ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVIRONMENTAL CONDITIONS; KINETOPLASTID PARASITE; PEROXISOMAL TARGETING SEQUENCES; PHYSIOLOGICAL CONDITION; PROTOZOAN PARASITES; QUANTITATIVE MEASUREMENT; RATIOMETRIC FLUORESCENT SENSORS; SUBCELLULAR COMPARTMENTS;

ACIDIFICATION; DEXTRAN; FLUORESCENCE; GLUCOSE; MOLECULAR BIOLOGY; PEPTIDES;

PROBES;

DEXTRAN; FLUORESCEIN; FLUORESCENT DYE; GLUCOSE;

ACIDIFICATION; AMINO ACID SEQUENCE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ENDOCYTOSIS; GLYCOSOME; IMMUNOFLUORESCENCE; KINETOPLASTIDA; LYSOSOME; NONHUMAN; PEROXISOMAL TARGETING SIGNAL; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSOR; TRYPANOSOMA BRUCEI;

ANIMALS; FLOW CYTOMETRY; HYDROGEN-ION CONCENTRATION; MICROBODIES; SUBCELLULAR FRACTIONS; TRYPANOSOMA BRUCEI BRUCEI;

KINETOPLASTIDA; PROTOZOA; TRYPANOSOMA BRUCEI;

EID: 84878341330     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400029m     Document Type: Article

References (43)

1. Beard, C. B. (2009) Forgotten People, Forgotten Diseases: The Neglected Tropical Diseases and Their Impact on Global Health and Development Emerging Infect. Dis. 15, 510-511
2. Barrett, M. P., Burchmore, R. J. S., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J., and Krishna, S. (2003) The trypanosomiases Lancet 362, 1469-1480
3. Steverding, D. (2008) The history of African trypanosomiasis Parasites Vectors 1, 3
4. Coley, A. F., Dodson, H. C., Morris, M. T., and Morris, J. C. (2011) Glycolysis in the African Trypanosome: Targeting Enzymes and Their Subcellular Compartments for Therapeutic Development Mol. Biol. Int. 2011, 1-10
5. Opperdoes, F. R. (1987) Compartmentation of carbohydrate metabolism in trypanosomes Annu. Rev. Microbiol. 41, 127-151
6. Dodson, H. C., Morris, M. T., and Morris, J. C. (2011) Glycerol 3-phosphate alters Trypanosoma brucei hexokinase activity in response to environmental change J. Biol. Chem. 286, 33150-33157
7. Reddy, J. K. and Mannaerts, G. P. (1994) Peroxisomal Lipid Metabolism Annu. Rev. Nutr. 14, 343-370
8. Walton, P. A., Gould, S. J., Feramisco, J. R., and Subramani, S. (1992) Transport of microinjected proteins into peroxisomes of mammalian cells: Inability of Zellweger cell lines to import proteins with the SKL tripeptide peroxisomal targeting signal Mol. Cell. Biol. 12, 531-541
9. Gould, S. J., Keller, G. A., Hosken, N., Wilkinson, J., and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes J. Cell Biol. 108, 1657-1664
10. Jankowski, A., Kim, J. H., Collins, R. F., Daneman, R., Walton, P., and Grinstein, S. (2001) In Situ Measurements of the pH of Mammalian Peroxisomes Using the Fluorescent Protein pHluorin J. Biol. Chem. 276, 48748-48753
11. Dansen, T. B., Pap, E. H. W., Wanders, R. J., and Wirtz, K. W. (2001) Targeted fluorescent probes in peroxisome function Histochem. J. 33, 65-69
12. Walton, P. A., Hill, P. E., and Subramani, S. (1995) Import of stably folded proteins into peroxisomes Mol. Biol. Cell 6, 675-683
13. Milagros Camara, M. d. L., Bouvier, L. A., Miranda, M. R., and Pereira, C. A. (2012) Identification and validation of Trypanosoma cruzi 's glycosomal adenylate kinase containing a peroxisomal targeting signal Exp. Parasitol. 130, 408-411
14. Costa-Pinto, D., Trindade, L. S., McMahon-Pratt, D., and Traub-Cseko, Y. M. (2001) Cellular trafficking in trypanosomatids: A new target for therapies? Int. J. Parasitol. 31, 536-543
15. Subramani, S. (1998) Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement Physiol. Rev. 78, 171-188
16. Wang, Z., Morris, J. C., Drew, M. E., and Englund, P. T. (2000) Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters J. Biol. Chem. 275, 40174-40179
17. Wirtz, E., Leal, S., Ochatt, C., and Cross, G. A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei Mol. Biochem. Parasitol. 99, 89-101
18. Nolan, D. P., Jackson, D. G., Biggs, M. J., Brabazon, E. D., Pays, A., Van Laethem, F., Paturiaux-Hanocq, F., Elliott, J. F., Elliot, J. F., Voorheis, H. P., and Pays, E. (2000) Characterization of a novel alanine-rich protein located in surface microdomains in Trypanosoma brucei J. Biol. Chem. 275, 4072-4080
19. Hager, K. M., Pierce, M. A., Moore, D. R., Tytler, E. M., Esko, J. D., and Hajduk, S. L. (1994) Endocytosis of a cytotoxic human high density lipoprotein results in disruption of acidic intracellular vesicles and subsequent killing of African trypanosomes J. Cell Biol. 126, 155-167
20. Fernando, L. P., Kandel, P. K., Yu, J., McNeill, J., Ackroyd, P. C., and Christensen, K. A. (2010) Mechanism of cellular uptake of highly fluorescent conjugated polymer nanoparticles Biomacromolecules 11, 2675-2682
21. Webster, P. and Grab, D. J. (1988) Intracellular colocalization of variant surface glycoprotein and transferrin-gold in Trypanosoma brucei J. Cell Biol. 106, 279-288
22. Brickman, M. J., Cook, J. M., and Balber, A. E. (1995) Low temperature reversibly inhibits transport from tubular endosomes to a perinuclear, acidic compartment in African trypanosomes J. Cell Sci. 108 (Part 11) 3611-3621
23. Coppens, I., Baudhuin, P., Opperdoes, F. R., and Courtoy, P. J. (1993) Role of acidic compartments in Trypanosoma brucei, with special reference to low-density lipoprotein processing Mol. Biochem. Parasitol. 58, 223-232
24. Hannaert, V., Albert, M.-A., Rigden, D. J., da Silva Giotto, M. T., Thiemann, O., Garratt, R. C., Van Roy, J., Opperdoes, F. R., and Michels, P. A. M. (2003) Kinetic characterization, structure modelling studies and crystallization of Trypanosoma brucei enolase Eur. J. Biochem. 270, 3205-3213
25. Poole, B. and Ohkuma, S. (1981) Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages J. Cell Biol. 90, 665-669
26. McCann, A. K., Schwartz, K. J., and Bangs, J. D. (2008) A determination of the steady state lysosomal pH of bloodstream stage African trypanosomes Mol. Biochem. Parasitol. 159, 146-149
27. Wendland, M. and Subramani, S. (1993) Cytosol-dependent peroxisomal protein import in a permeabilized cell system J. Cell Biol. 120, 675-685
28. Field, M. C., Menon, A. K., and Cross, G. A. (1992) Developmental variation of glycosylphosphatidylinositol membrane anchors in Trypanosoma brucei. In vitro biosynthesis of intermediates in the construction of the GPI anchor of the major procyclic surface glycoprotein J. Biol. Chem. 267, 5324-5329
29. Richmond, G. S., Gibellini, F., Young, S. A., Major, L., Denton, H., Lilley, A., and Smith, T. K. (2010) Lipidomic analysis of bloodstream and procyclic form Trypanosoma brucei Parasitology 137, 1357-1392
30. Langreth, S. G. and Balber, A. E. (1975) Protein uptake and digestion in bloodstream and culture forms of Trypanosoma brucei J. Protozool. 22, 40-53
31. Coppens, I., Opperdoes, F. R., Courtoy, P. J., and Baudhuin, P. (1987) Receptor-mediated endocytosis in the bloodstream form of Trypanosoma brucei J. Protozool. 34, 465-473
32. Boucrot, E., Saffarian, S., Zhang, R., and Kirchhausen, T. (2010) Roles of AP-2 in Clathrin-Mediated Endocytosis PLoS One 5, e10597
33. Schaible, U. E., Schlesinger, P. H., Steinberg, T. H., Mangel, W. F., Kobayashi, T., and Russell, D. G. (1999) Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes J. Cell Sci. 112 (Part 5) 681-693
34. Vickerman, K. and Tetley, L. (1978) Biology and ultrastructure of trypanosomes in relation to pathogenesis. Conference on Recent Advances in the Knowledge of Pathogenicity of Trypanosomes, November 20-23, Nairobi, Kenya.
35. Huybrechts, S. J., Van Veldhoven, P. P., Brees, C., Mannaerts, G. P., Los, G. V., and Fransen, M. (2009) Peroxisome dynamics in cultured mammalian cells Traffic 10, 1722-1733
36. Clayton, C. E. (1988) Most proteins, including fructose bisphosphate aldolase, are stable in the procyclic trypomastigote form of Trypanosoma brucei Mol. Biochem. Parasitol. 28, 43-46
37. Dansen, T. B., Wirtz, K. W., Wanders, R. J., and Pap, E. H. (2000) Peroxisomes in human fibroblasts have a basic pH Nat. Cell Biol. 2, 51-53
38. ter Kuile, B. H. (1997) Adaptation of metabolic enzyme activities of Trypanosoma brucei promastigotes to growth rate and carbon regimen J. Bacteriol. 179, 4699-4705
39. Omura, T. (1998) Mitochondria-Targeting Sequence, a Multi-Role Sorting Sequence Recognized at All Steps of Protein Import into Mitochondria J. Biochem. 123, 1010-1016
40. Kjer-Nielsen, L., van Vliet, C., Erlich, R., Toh, B. H., and Gleeson, P. A. (1999) The Golgi-targeting sequence of the peripheral membrane protein p230 J. Cell Sci. 112 (Part 11) 1645-1654
41. Liu, X. and Zheng, X. F. S. (2007) Endoplasmic Reticulum and Golgi Localization Sequences for Mammalian Target of Rapamycin Mol. Biol. Cell 18, 1073-1082
42. 2+-indicator dyes Cell Calcium 27, 97-106
43. 2+ measurement with Indo-1 in substrate-attached cells: Advantages and special considerations Cell Calcium 11, 487-500