Trypanosome lytic factor-1 initiates oxidation-stimulated osmotic lysis of trypanosoma brucei brucei

Journal of Biological Chemistry

Volumn 291, Issue 6, 2016, Pages 3063-3075

  Greene, Amy Styer ^a   Hajduk, Stephen L ^a  

^a University of Georgia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; CELL MEMBRANES; FREE RADICALS; LIPOPROTEINS; OXIDATION; PEROXIDES;

EVOLVED RESISTANCES; HIGH DENSITY LIPOPROTEIN; HYPOTONIC STRESS; IRON-CONTAINING; LIPOPHILIC ANTIOXIDANTS; OXIDATIVE PROCESS; P-PHENYLENE DIAMINES; TRYPANOSOMA BRUCEI;

OSMOSIS;

APOLIPOPROTEIN; HAPTOGLOBIN; HEMOGLOBIN; HIGH DENSITY LIPOPROTEIN; ION CHANNEL; LIPID PEROXIDASE; N,N' DIPHENYL 1,4 PHENYLENEDIAMINE; PEROXIDE; THIOL; TRANSFERRIN; APOL1 PROTEIN, HUMAN; FREE RADICAL; PROTOZOAL PROTEIN; TLF1 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; INNATE IMMUNITY; NONHUMAN; OSMOSIS; OSMOTIC STRESS; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE; DRUG EFFECTS; GENE SILENCING; GENETICS; HUMAN; METABOLISM; OSMOTIC PRESSURE; OXIDATION REDUCTION REACTION;

APOLIPOPROTEINS; CELL MEMBRANE; FREE RADICALS; GENE KNOCKDOWN TECHNIQUES; HUMANS; LIPOPROTEINS, HDL; OSMOTIC PRESSURE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84958093245     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.680371     Document Type: Article

References (63)

1. Harrington, J. M., Howell, S., and Hajduk, S. L. (2009) Membrane permeabilization by trypanosome lytic factor, a cytolytic human high density lipoprotein. J. Biol. Chem. 284, 13505-13512.
2. Pérez-Morga, D., Vanhollebeke, B., Paturiaux-Hanocq, F., Nolan, D. P., Lins, L., Homblé, F., Vanhamme, L., Tebabi, P., Pays, A., Poelvoorde, P., Jacquet, A., Brasseur, R., and Pays, E. (2005) Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309, 469-472.
3. Nielsen, M. J., Petersen, S. V., Jacobsen, C., Oxvig, C., Rees, D., Møller, H. J., and Moestrup, S. K. (2006) Haptoglobin-related protein is a highaffinity hemoglobin-binding plasma protein. Blood 108, 2846-2849.
4. Andersen, C. B., Torvund-Jensen, M., Nielsen, M. J., de Oliveira, C. L., Hersleth, H. P., Andersen, N. H., Pedersen, J. S., Andersen, G. R., and Moestrup, S. K. (2012) Structure of the haptoglobin-haemoglobin complex. Nature 489, 456-459.
5. Vanhollebeke, B., De Muylder, G., Nielsen, M. J., Pays, A., Tebabi, P., Dieu, M., Raes, M., Moestrup, S. K., and Pays, E. (2008) A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 320, 677-681.
6. Higgins, M. K., Tkachenko, O., Brown, A., Reed, J., Raper, J., and Carrington, M. (2013) Structure of the trypanosome haptoglobin-hemoglobin receptor and implications for nutrient uptake and innate immunity. Proc. Natl. Acad. Sci. U.S.A. 110, 1905-1910.
7. Thomson, R., and Finkelstein, A. (2015) Human trypanolytic factor APOL1 forms pH-gated cation-selective channels in planar lipid bilayers: relevance to trypanosome lysis. Proc. Natl. Acad. Sci. U.S.A. 112, 2894-2899.
8. Vanwalleghem, G., Fontaine, F., Lecordier, L., Tebabi, P., Klewe, K., Nolan, D. P., Yamaryo-Botté, Y., Botté, C., Kremer, A., Burkard, G. S., Rassow, J., Roditi, I., Pérez-Morga, D., and Pays, E. (2015) Coupling of lysosomal and mitochondrial membrane permeabilization in trypanolysis by APOL1. Nat. Commun. 6, 8078.
9. Rifkin, M. R. (1984) Trypanosoma brucei: biochemical and morphological studies of cytotoxicity caused by normal human serum. Exp. Parasitol. 58, 81-93.
10. Raper, J., Portela, M. P., Lugli, E., Frevert, U., and Tomlinson, S. (2001) Trypanosome lytic factors: novel mediators of human innate immunity. Curr. Opin. Microbiol. 4, 402-408.
11. Shimamura, M., Hager, K. M., and Hajduk, S. L. (2001) The lysosomal targeting and intracellular metabolism of trypanosome lytic factor by Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 115, 227-237.
12. Vanhollebeke, B., Lecordier, L., Perez-Morga, D., Amiguet-Vercher, A., and Pays, E. (2007) Human serum lyses Trypanosoma brucei by triggering uncontrolled swelling of the parasite lysosome. J. Eukaryot. Microbiol. 54, 448-451.
13. Widener, J., Nielsen, M. J., Shiflett, A., Moestrup, S. K., and Hajduk, S. (2007) Hemoglobin is a co-factor of human trypanosome lytic factor. Plos Pathog. 3, 1250-1261.
14. 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.
15. Molina-Portela Mdel, P., Lugli, E. B., Recio-Pinto, E., and Raper, J. (2005) Trypanosome lytic factor, a subclass of high-density lipoprotein, forms cation-selective pores in membranes. Mol. Biochem. Parasitol. 144, 218-226.
16. Bishop, J. R., Shimamura, M., and Hajduk, S. L. (2001) Insight into the mechanism of trypanosome lytic factor-1 killing of Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 118, 33-40.
17. Smith, A. B., Esko, J. D., and Hajduk, S. L. (1995) Killing of trypanosomes by the human haptoglobin-related protein. Science 268, 284-286.
18. Molina Portela, M. P., Raper, J., and Tomlinson, S. (2000) An investigation into the mechanism of trypanosome lysis by human serum factors. Mol.Biochem. Parasitol. 110, 273-282.
19. Diechtierow, M., and Krauth-Siegel, R. L. (2011) A tryparedoxin-dependent peroxidase protects African trypanosomes from membrane damage. Free Radic. Biol. Med. 51, 856-868.
20. Hiller, C., Nissen, A., Benítez, D., Comini, M. A., and Krauth-Siegel, R. L. (2014) Cytosolic peroxidases protect the lysosome of bloodstream African trypanosomes from iron-mediated membrane damage. Plos Pathog. 10, e1004075.
21. DeJesus, E., Kieft, R., Albright, B., Stephens, N. A., and Hajduk, S. L. (2013) A single amino acid substitution in the group 1 Trypanosoma brucei gambiense haptoglobin-hemoglobin receptor abolishes TLF-1 binding. Plos Pathog. 9, e1003317.
22. Shiflett, A. M., Bishop, J. R., Pahwa, A., and Hajduk, S. L. (2005) Human high density lipoproteins are platforms for the assembly of multi-component innate immune complexes. J. Biol. Chem. 280, 32578-32585.
23. Dolai, S., Pal, S., Yadav, R. K., and Adak, S. (2011) Endoplasmic reticulum stress-induced apoptosis in Leishmania through Ca2-dependent and caspase-independent mechanism. J. Biol. Chem. 286, 13638-13646.
24. Ascoli, F., Fanelli, M. R., and Antonini, E. (1981) Preparation and properties of apohemoglobin and reconstituted hemoglobins. Methods Enzymol. 76, 72-87.
25. Lustbader, J. W., Arcoleo, J. P., Birken, S., and Greer, J. (1983) Hemoglobin- binding site on haptoglobin probed by selective proteolysis. J. Biol. Chem. 258, 1227-1234.
26. Keij, J. F., Bell-Prince, C., and Steinkamp, J. A. (1999) Simultaneous analysis of relative DNA and glutathione content in viable cells by phaseresolved flow cytometry. Cytometry 35, 48-54.
27. Ariyanayagam, M. R., and Fairlamb, A. H. (2001) Ovothiol and trypanothione as antioxidants in trypanosomatids. Mol. Biochem. Parasitol. 115, 189-198.
28. Penketh, P. G., and Klein, R. A. (1986) Hydrogen peroxide metabolism in Trypanosoma brucei. Mol. Biochem. Parasitol. 20, 111-121.
29. Cossarizza, A., Ferraresi, R., Troiano, L., Roat, E., Gibellini, L., Bertoncelli, L., Nasi, M., and Pinti, M. (2009) Simultaneous analysis of reactive oxygen species and reduced glutathione content in living cells by polychromatic flow cytometry. Nat. Protoc. 4, 1790-1797.
30. Reczek, C. R., and Chandel, N. S. (2015) ROS-dependent signal transduction. Curr Opin. Cell Biol. 33, 8-13.
31. Waks, M., and Beychok, S. (1974) Induced conformational states in human apohemoglobin on binding of haptoglobin 1-1. Effect of added heme as a probe of frozen structures. Biochemistry 13, 15-22.
32. Niki, E., and Noguchi, N. (2000) Evaluation of antioxidant capacity. What capacity is being measured by which method? IUBMB Life 50, 323-329.
33. Niki, E. (2010) Assessment of antioxidant capacity in vitro and in vivo. Free Radic. Biol. Med. 49, 503-515.
34. Hajduk, S. L., Hager, K., and Esko, J. D. (1992) High-density lipoproteinmediated lysis of trypanosomes. Parasitol. Today 8, 95-98.
35. Uzcategui, N. L., Szallies, A., Pavlovic-Djuranovic, S., Palmada, M., Figarella, K., Boehmer, C., Lang, F., Beitz, E., and Duszenko, M. (2004) Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J. Biol. Chem. 279, 42669-42676.
36. Vanhollebeke, B., Nielsen, M. J., Watanabe, Y., Truc, P., Vanhamme, L., Nakajima, K., Moestrup, S. K., and Pays, E. (2007) Distinct roles of haptoglobin- related protein and apolipoprotein L-I in trypanolysis by human serum. Proc. Natl. Acad. Sci. U.S.A. 104, 4118-4123.
37. Hansen, D. B., Friis, M. B., Hoffmann, E. K., and Lambert, I. H. (2012) Downregulation of the taurine transporter TauT during hypo-osmotic stress in NIH3T3 mouse fibroblasts. J. Membr. Biol. 245, 77-87.
38. Díaz-Elizondo, J., Chiong, M., Rojas-Rivera, D., Olea-Azar, C., Kwon, H. M., and Lavandero, S. (2006) Reactive oxygen species inhibit hyposmotic stress-dependent volume regulation in cultured rat cardiomyocytes. Biochem. Biophys. Res. Commun. 350, 1076-1081.
39. Rojas-Rivera, D., Díaz-Elizondo, J., Parra, V., Salas, D., Contreras, A., Toro, B., Chiong, M., Olea-Azar, C., and Lavandero, S. (2009) Regulatory volume decrease in cardiomyocytes is modulated by calcium influx and reactive oxygen species. FEBS Lett. 583, 3485-3492.
40. Roggy, J. L., and Bangs, J. D. (1999) Molecular cloning and biochemical characterization of a VCP homolog in African trypanosomes. Mol. Biochem. Parasitol. 98, 1-15.
41. Defrise-Quertain, F., Fraser-L'Hostis, C., Coral, D., and Deshusses, J. (1996) Kinetic study of the plasma-membrane potential in procyclic and bloodstream forms of Trypanosoma brucei brucei using the fluorescent probe bisoxonol. Biochem. J. 314, 595-601.
42. Wright, V. P., Reiser, P. J., and Clanton, T. L. (2009) Redox modulation of global phosphatase activity and protein phosphorylation in intact skeletal muscle. J. Physiol. 587, 5767-5781.
43. Cosentino-Gomes, D., Russo-Abrahão, T., Fonseca-de-Souza, A. L., Ferreira, C. R., Galina, A., and Meyer-Fernandes, J. R. (2009) Modulation of Trypanosoma rangeli ecto-phosphatase activity by hydrogen peroxide. Free Radic. Biol. Med. 47, 152-158.
44. Tamma, G., Ranieri, M., Di Mise, A., Centrone, M., Svelto, M., and Valenti, G. (2014) Glutathionylation of the aquaporin-2 water channel: A novel post-translational modification modulated by the oxidative stress. J. Biol. Chem. 289, 27807-27813.
45. Lambert, I. H., Klausen, T. K., Bergdahl, A., Hougaard, C., and Hoffmann, E. K. (2009) ROS activate KCl cotransport in nonadherent Ehrlich ascites cells but K- And Cl- channels in adherent Ehrlich Lettre and NIH3T3 cells. Am. J. Physiol. Cell Physiol. 297, C198-C206.
46. Lambert, I. H. (2003) Reactive oxygen species regulate swelling-induced taurine efflux in NIH3T3 mouse fibroblasts. J. Membr. Biol. 192, 19-32.
47. Zhu, L., Zuo, W., Yang, H., Zhang, H., Luo, H., Ye, D., Lin, X., Mao, J., Feng, J., Chen, L., and Wang, L. (2013) Involvement of volume-activated chloride channels in H2O 2 preconditioning against oxidant-induced injury through modulating cell volume regulation mechanisms and membrane permeability in PC12 cells. Mol. Neurobiol. 48, 205-216.
48. Bienert, G. P., and Chaumont, F. (2014) Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys Acta 1840, 1596-1604.
49. Adragna, N. C., Di Fulvio, M., and Lauf, P. K. (2004) Regulation of K-Cl cotransport: from function to genes. J. Membr. Biol. 201, 109-137.
50. Bursell, J. D., Kirk, J., Hall, S. T., Gero, A. M., and Kirk, K. (1996) Volumeregulatory amino acid release from the protozoan parasite Crithidia luciliae. J. Membr. Biol. 154, 131-141.
51. Ren, Z., Raucci, F. J. Jr., Browe, D. M., and Baumgarten, C. M. (2008) Regulation of swelling-activated Cl- current by angiotensin II signalling and NADPH oxidase in rabbit ventricle. Cardiovasc. Res. 77, 73-80.
52. Lutje, V., Seixas, J., and Kennedy, A. (2010) Chemotherapy for secondstage human African trypanosomiasis. Cochrane Database Syst. Rev. CD006201.
53. Vincent, I. M., Creek, D. J., Burgess, K., Woods, D. J., Burchmore, R. J., and Barrett, M. P. (2012) Untargeted metabolomics reveals a lack of synergy between nifurtimox and eflornithine against Trypanosoma brucei. PLoS Negl. Trop. Dis. 6, e1618.
54. Priotto, G., Kasparian, S., Mutombo, W., Ngouama, D., Ghorashian, S., Arnold, U., Ghabri, S., Baudin, E., Buard, V., Kazadi-Kyanza, S., Ilunga, M., Mutangala, W., Pohlig, G., Schmid, C., Karunakara, U., Torreele, E., and Kande, V. (2009) Nifurtimox-eflornithine combination therapy for second- stage African Trypanosoma brucei gambiense trypanosomiasis: A multicentre, randomised, phase III, non-inferiority trial. Lancet 374, 56-64.
55. Meshnick, S. R., Blobstein, S. H., Grady, R. W., and Cerami, A. (1978) An approach to the development of new drugs for African trypanosomiasis. J. Exp. Med. 148, 569-579.
56. Fairlamb, A. H., Henderson, G. B., and Cerami, A. (1989) Trypanothione is the primary target for arsenical drugs against African trypanosomes. Proc. Natl. Acad. Sci. U.S.A. 86, 2607-2611.
57. Steverding, D., and Sexton, D.W.(2013) Trypanocidal activity of salinomycin is due to sodium influx followed by cell swelling. Parasit Vectors 6, 78.
58. Bassarak, B., Uzcátegui, N. L., Schönfeld, C., and Duszenko, M. (2011) Functional characterization of three aquaglyceroporins from Trypanosoma brucei in osmoregulation and glycerol transport. Cell Physiol. Biochem. 27, 411-420.
59. Eintracht, J., Maathai, R., Mellors, A., and Ruben, L. (1998) Calcium entry in Trypanosoma brucei is regulated by phospholipase A2 and arachidonicacid. Biochem. J. 336, 659-666.
60. 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.
61. Jimenez, V., Paredes, R., Sosa, M. A., and Galanti, N. (2008) Natural programmed cell death in T. cruzi epimastigotes maintained in axenic cultures. J. Cell Biochem. 105, 688-698.
62. Irigoín, F., Inada, N. M., Fernandes, M. P., Piacenza, L., Gadelha, F. R., Vercesi, A. E., and Radi, R. (2009) Mitochondrial calcium overload triggers complement-dependent superoxide-mediated programmed cell death in Trypanosoma cruzi. Biochem. J. 418, 595-604.
63. D'hondt, J., Van Meirvenne, N., Moens, L., and Kondo, M. (1979) Ca2- is essential cofactor for trypanocidal activity of normal human serum. Nature 282, 613-615.