Evidence that transport of iron from the lysosome to the cytosol in African trypanosomes is mediated by a mucolipin orthologue

Molecular Microbiology

Volumn 89, Issue 3, 2013, Pages 420-432

  Taylor, Martin C ^a   Mclatchie, Alex P ^a   Kelly, John M ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; DEFEROXAMINE; DOXYCYCLINE; IRON; MUCOLIPIN; SALICYLHYDROXAMIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOSOL; FEMALE; GROWTH DISORDER; IN VITRO STUDY; IN VIVO STUDY; IRON TRANSPORT; LYSOSOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; CYTOSOL; DEFEROXAMINE; FEMALE; GENE DELETION; IRON; LYSOSOMES; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; RNA INTERFERENCE; SALICYLAMIDES; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRYPANOSOMA BRUCEI BRUCEI;

MAMMALIA; TRYPANOSOMA BRUCEI;

EID: 84880832960     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12285     Document Type: Article

References (59)

1. Alsford, S., and Horn, D. (2008) Single-locus targeting constructs for reliable regulated RNAi and transgene expression in Trypanosoma brucei. Mol Biochem Parasitol 161: 76-79.
2. Alsford, S., Kawahara, T., Glover, L., and Horn, D. (2005) Tagging a T. brucei RRNA locus improves stable transfection efficiency and circumvents inducible expression position effects. Mol Biochem Parasitol 144: 142-148.
3. Altarescu, G., Sun, M., Moore, D.F., Smith, J.A., Wiggs, E.A., Solomon, B.I., etal. (2002) The neurogenetics of mucolipidosis type IV. Neurology 59: 306-313.
4. Armitage, A.E., Eddowes, L.A., Gileadi, U., Cole, S., Spottiswoode, N., Selvakumar, T.A., etal. (2011) Hepcidin regulation by innate immune and infectious stimuli. Blood 118: 4129-4139.
5. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B., Carrington, M., etal. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457-D462.
6. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., etal. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
7. Boelaert, J.R., Vandecasteele, S.J., Appelberg, R., and Gordeuk, V.R. (2007) The effect of the host's iron status on tuberculosis. J Infect Dis 195: 1745-1753.
8. Breidbach, T., Scory, S., Krauth-Siegel, R.L., and Steverding, D. (2002) Growth inhibition of bloodstream forms of Trypanosoma brucei by the iron chelator deferoxamine. Int J Parasitol 32: 473-479.
9. Brenndorfer, M., and Boshart, M. (2010) Selection of reference genes for mRNA quantification in Trypanosoma brucei. Mol Biochem Parasitol 172: 52-55.
10. Brohn, F.H., and Clarkson, A.B. (1978) Quantitative effects of salycylhydroxamic acid and glycerol on Trypanosoma brucei glycolysis in vitro and in vivo. Acta Trop 35: 23-33.
11. Chaudhri, M., Steverding, D., Kittelberger, D., Tjia, S., and Overath, P. (1994) Expression of a glycosylphosphatidylinositol-anchored Trypanosoma brucei transferrin-binding protein complex in insect cells. Proc Natl Acad Sci USA 91: 6443-6447.
12. Chaudhuri, M., Ott, R.D., and Hill, G.C. (2006) Trypanosome alternative oxidase: from molecule to function. Trends Parasitol 22: 484-491.
13. Clarkson, A.B., Jr, Bienen, E.J., Pollakis, G., and Grady, R.W. (1989) Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. J Biol Chem 264: 17770-17776.
14. Docampo, R., and Lukes, J. (2012) Trypanosomes and the solution to a 50-year mitochondrial calcium mystery. Trends Parasitol 28: 31-37.
15. Dong, X.P., Cheng, X., Mills, E., Delling, M., Wang, F., Kurz, T., and Xu, H. (2008) The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 455: 992-996.
16. Dong, X.P., Shen, D., Wang, X., Dawson, T., Li, X., Zhang, Q., etal. (2010) PI(3, 5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1: 38.
17. Dufernez, F., Yernaux, C., Gerbod, D., Noel, C., Chauvenet, M., Wintjens, R., etal. (2006) The presence of four iron-containing superoxide dismutase isozymes in trypanosomatidae: characterization, subcellular localization, and phylogenetic origin in Trypanosoma brucei. Free Radic Biol Med 40: 210-225.
18. Eichelsdoerfer, J.L., Evans, J.A., Slaugenhaupt, S.A., and Cuajungco, M. (2010) Zinc dyshomeostasis is linked with the loss of mucolipidosis IV-associated TRPML1 ion channel. J Biol Chem 285: 34304-34308.
19. El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., etal. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
20. Esposito, B.P., Epsztejn, S., Breuer, W., and Cabantchik, Z.I. (2002) A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 304: 1-18.
21. Evans, D.A., and Brown, R.C. (1973) The inhibitory effects of aromatic hydroxamic acids on the cyanide-insensitive terminal oxidase of Trypanosoma brucei. Trans R Soc Trop Med Hyg 67: 258.
22. Fast, B., Kremp, K., Boshart, M., and Steverding, D. (1999) Iron-dependent regulation of transferrin receptor expression in Trypanosoma brucei. Biochem J 342 (Part 3): 691-696.
23. Gunshin, H., Fujiwara, Y., Custodio, A.O., Direnzo, C., Robine, S., and Andrews, N.C. (2005) Slc11a2 is required for intestinal iron absorption and erythropoiesis but dispensable in placenta and liver. J Clin Invest 115: 1258-1266.
24. Halliwell, B., and Gutteridge, J.M.C. (2007) Free Radicals in Biology and Medicine. Oxford: Oxford University Press.
25. Helfert, S., Estevez, A.M., Bakker, B., Michels, P., and Clayton, C. (2001) Roles of triosephosphate isomerase and aerobic metabolism in Trypanosoma brucei. Biochem J 357: 117-125.
26. Hertz-Fowler, C., Peacock, C.S., Wood, V., Aslett, M., Kerhornou, A., Mooney, P., etal. (2004) GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 32: D339-D343.
27. Hirumi, H., and Hirumi, K. (1989) Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
28. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., etal. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
29. Kabiri, M., and Steverding, D. (2000) Studies on the recycling of the transferrin receptor in Trypanosoma brucei using an inducible gene expression system. Eur J Biochem 267: 3309-3314.
30. Kakhlon, O., and Cabantchik, Z.I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes(1). Free Radic Biol Med 33: 1037-1046.
31. Kelley, R.J., Alexander, D.L., Cowan, C., Balber, A.E., and Bangs, J.D. (1999) Molecular cloning of p67, a lysosomal membrane glycoprotein from Trypanosoma brucei. Mol Biochem Parasitol 98: 17-28.
32. Kelly, S., Reed, J., Kramer, S., Ellis, L., Webb, H., Sunter, J., etal. (2007) Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Mol Biochem Parasitol 154: 103-109.
33. Krieger, S., Schwarz, W., Ariyanayagam, M.R., Fairlamb, A.H., Krauth-Siegel, R.L., and Clayton, C. (2000) Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol Microbiol 35: 542-552.
34. Kurz, T., Gustafsson, B., and Brunk, U.T. (2006) Intralysosomal iron chelation protects against oxidative stress-induced cellular damage. FEBS J 273: 3106-3117.
35. LaPlante, J.M., Falardeau, J.L., Brown, E.M., Slaugenhaupt, S.A., and Vassilev, P.M. (2011) The cation channel mucolipin-1 is a bifunctional protein that facilitates membrane remodeling via its serine lipase domain. Exp Cell Res 317: 691-705.
36. Ligtenberg, M.J., Bitter, W., Kieft, R., Steverding, D., Janssen, H., Calafat, J., and Borst, P. (1994) Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J 13: 2565-2573.
37. van Luenen, H.G., Kieft, R., Mussmann, R., Engstler, M., ter Riet, B., and Borst, P. (2005) Trypanosomes change their transferrin receptor expression to allow effective uptake of host transferrin. Mol Microbiol 58: 151-165.
38. McDermid, J.M., and Prentice, A.M. (2006) Iron and infection: effects of host iron status and the iron-regulatory genes haptoglobin and NRAMP1 (SLC11A1) on host-pathogen interactions in tuberculosis and HIV. Clin Sci (Lond) 110: 503-524.
39. Moreno, S.N., and Docampo, R. (2003) Calcium regulation in protozoan parasites. Curr Opin Microbiol 6: 359-364.
40. Mussmann, R., Engstler, M., Gerrits, H., Kieft, R., Toaldo, C.B., Onderwater, J., etal. (2004) Factors affecting the level and localization of the transferrin receptor in Trypanosoma brucei. J Biol Chem 279: 40690-40698.
41. Netz, D.J., Stith, C.M., Stumpfig, M., Kopf, G., Vogel, D., Genau, H.M., etal. (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat Chem Biol 8: 125-132.
42. Opperdoes, F.R., Aarsen, P.N., van der Meer, C., and Borst, P. (1976) Trypanosoma brucei: an evaluation of salicylhydroxamic acid as a trypanocidal drug. Exp Parasitol 40: 198-205.
43. Ott, R., Chibale, K., Anderson, S., Chipeleme, A., Chaudhuri, M., Guerrah, A., etal. (2006) Novel inhibitors of the trypanosome alternative oxidase inhibit Trypanosoma brucei brucei growth and respiration. Acta Trop 100: 172-184.
44. Pal, A., Hall, B.S., Jeffries, T.R., and Field, M.C. (2003) Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem J 374: 443-451.
45. Portugal, S., Carret, C., Recker, M., Armitage, A.E., Goncalves, L.A., Epiphanio, S., etal. (2011) Host-mediated regulation of superinfection in malaria. Nat Med 17: 732-737.
46. Pryor, P.R., Reimann, F., Gribble, F.M., and Luzio, J. (2006) Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 7: 1388-1398.
47. Ratledge, C. (2004) Iron, mycobacteria and tuberculosis. Tuberculosis (Edinb) 84: 110-130.
48. Sheftel, A.D., Zhang, A.S., Brown, C., Shirihai, O.S., and Ponka, P. (2007) Direct interorganellar transfer of iron from endosome to mitochondrion. Blood 110: 125-132.
49. Steverding, D. (1998) Bloodstream forms of Trypanosoma brucei require only small amounts of iron for growth. Parasitol Res 84: 59-62.
50. Steverding, D., Stierhof, Y.D., Chaudhri, M., Ligtenberg, M., Schell, D., Beck-Sickinger, A.G., and Overath, P. (1994) ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur J Cell Biol 64: 78-87.
51. Steverding, D., Stierhof, Y.D., Fuchs, H., Tauber, R., and Overath, P. (1995) Transferrin-binding protein complex is the receptor for transferrin uptake in Trypanosoma brucei. J Cell Biol 131: 1173-1182.
52. Steverding, D., Sexton, D.W., Wang, X., Gehrke, S.S., Wagner, G.K., and Caffrey, C.R. (2012) Trypanosoma brucei: chemical evidence that cathepsin L is essential for survival and a relevant drug target. Int J Parasitol 42: 481-488.
53. Stijlemans, B., Vankrunkelsven, A., Brys, L., Magez, S., and De, P. (2008) Role of iron homeostasis in trypanosomiasis-associated anemia. Immunobiology 213: 823-835.
54. Stijlemans, B., Vankrunkelsven, A., Brys, L., Raes, G., Magez, S., and De Baetselier, P. (2010a) Scrutinizing the mechanisms underlying the induction of anemia of inflammation through GPI-mediated modulation of macrophage activation in a model of African trypanosomiasis. Microbes Infect 12: 389-399.
55. Stijlemans, B., Vankrunkelsven, A., Caljon, G., Bockstal, V., Guilliams, M., Bosschaerts, T., etal. (2010b) The central role of macrophages in trypanosomiasis-associated anemia: rationale for therapeutical approaches. Endocr Metab Immune Disord Drug Targets 10: 71-82.
56. Taylor, M.C., and Kelly, J.M. (2010) Iron metabolism in trypanosomatids, and its crucial role in infection. Parasitology 137: 899-917.
57. Theil, E.C. (2011) Iron homeostasis and nutritional iron deficiency. J Nutr 141: 724S-728S.
58. Wilkinson, S.R., Prathalingam, S.R., Taylor, M.C., Ahmed, A., Horn, D., and Kelly, J.M. (2006) Functional characterisation of the iron superoxide dismutase gene repertoire in Trypanosoma brucei. Free Radic Biol Med 40: 198-209.
59. Wrighting, D.M., and Andrews, N.C. (2006) Interleukin-6 induces hepcidin expression through STAT3. Blood 108: 3204-3209.