Cellular Growth and Mitochondrial Ultrastructure of Leishmania (Viannia) braziliensis Promastigotes Are Affected by the Iron Chelator 2,2-Dipyridyl

PLoS Neglected Tropical Diseases

Volumn 7, Issue 10, 2013, Pages

  Mesquita Rodrigues, Camila ^a   Menna Barreto, Rubem F S ^a   Sabóia Vahia, Leonardo ^a   Da Silva, Silvia A G ^b   de Souza, Elen M ^a   Waghabi, Mariana C ^a   Cuervo, Patrícia ^a   De Jesus, José B ^a,c  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c Fed Univ Sao Joao Del Rey   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

2, 2' BIPYRIDINE; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IRON DEPLETION; LEISHMANIA BRAZILIENSIS; MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION SWELLING; NICK END LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; TWO DIMENSIONAL ELECTROPHORESIS; ULTRASTRUCTURE;

2,2'-DIPYRIDYL; CELL DEATH; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHELATING AGENTS; CYTOPLASMIC VESICLES; DNA FRAGMENTATION; GENE EXPRESSION; GOLGI APPARATUS; HUMANS; IN SITU NICK-END LABELING; IRON; LEISHMANIA BRAZILIENSIS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PROTOZOAN PROTEINS;

EID: 84887291914     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002481     Document Type: Article

References (58)

1. Grimaldi G Jr, Tesh RB, (1993) Leishmaniases of the New World: current concepts and implications for future research. Clin Microbiol Rev 6: 230-250.
2. Turetz ML, Machado PR, Ko AI, Alves F, Bittencourt A, et al. (2002) Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis 186: 829-1834.
3. Marsden PD, (1986) Mucosal leishmaniasis ("espundia" Escomel, 1911). Trans R Soc Trop Med Hyg 80: 859-876.
4. Taylor MC, Kelly JM, (2010) Iron in trypanosomatids, and its crucial role in infection. Parasitology 137: 899-917.
5. Tripodi KE, Menendez Bravo SM, Cricco JA, (2011) Role of heme and heme-proteins in trypanosomatid essential metabolic pathways. Enzyme Res 2011: 873230.
6. Sen G, Mukhopadhyay S, Ray M, Biswas T, (2008) Quercetin interferes with iron metabolism in Leishmania donovani and targets ribonucleotide reductase to exert leishmanicidal activity. J Antimicrob Chemother 61: 1066-1075.
7. Wilson ME, Britigan BE, (1998) Iron acquisition by parasitic protozoa. Parasitol Today 14: 348-353.
8. Voyiatzaki CS, Soteriadou KP, (1992) Identification and isolation of the Leishmania transferrin receptor. J Biol Chem 267: 9112-9117.
9. Wilson ME, Vorhies RW, Andersen KA, Brotigan BE, (1994) Acquisition of iron from transferrin and lactoferrin by the protozoan Leishmania chagasi. Infect Immun 2: 3262-3269.
10. Sengputa S, Tripathi J, Tandon R, Raje M, Roy RP, et al. (1999) Hemoglobin endocytosis in Leishmania is mediated through a 46 kDa protein located in the flagellar pocket. J Biol Chem 274: 2758-2765.
11. Krishnamurthy G, Vikram R, Singh SB, Patel N, Agarwal S, et al. (2005) Hemoglobin receptor in Leishmania is a hexokinase located in the flagellar pocket. J Biol Chem 280: 5884-5891.
12. Huynh C, Sacks DL, Andrews NW, (2006) A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J Exp Med 203: 2363-2375.
13. Flannery AR, Huynh C, Mittra B, Mortara RA, Andrews NW, (2011) LFR1 Ferric Iron Reductase of Leishmania amazonensis is essential for the generation of infective parasite forms. J Biol Chem 286: 23266-23279.
14. Soteriadou K, Papavassiliou P, Voyiatzaki C, Boelart J, (1995) Effect of iron on the in vitro growth of Leishmania promastigotes. J Antimicrob Chemother 35: 23-29.
15. Atkinson CT, Bayne MT, Gordeuk VR, Brittenham GM, Aikawa M, (1991) Stage-specific ultrastructural effects of desferrioxamine on Plasmodium falciparum in vitro. Am J Trop Med Hyg 45: 593-601.
16. Breidbach T, Scory S, Krauth-Siegel RL, Steverding D, (2002) Growth inhibition of bloodstream forms of Trypanosoma brucei by the iron chelator deferoxamine. Int J Parasitol 32: 473-479.
17. Merschjohann K, Steverding D, (2006) In vitro growth inhibition of bloodstream forms of Trypanosoma brucei and Trypanosoma congolense by iron chelators. Kinetoplastid Biol Dis 5: 1-5.
18. Lehker MW, Arroyo R, Alderete JF, (1991) The regulation by iron of the synthesis of adhesins and cytoadherence levels in the protozoan Trichomonas vaginalis. J Exp Med 174: 311-318.
19. Melo-Braga M, Rocha-Azevedo R, Silva-Filho FC, (2003) Tritrichomonas foetus: the role played by iron during parasite interaction with epithelial cells. Exp Parasitol 105: 111-120.
20. De Jesus JB, Cuervo P, Junqueira M, Britto C, Silva-Filho FC, et al. (2007) A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis. Proteomics 7: 1961-1972.
21. Breuer W, Epsztejn S, Cabantchik ZI, (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron (II). J Biol Chem 270: 24209-24215.
22. Romeo AM, Christen L, Niles EG, Kosman DJ, (2001) Intracellular chelation of iron by bipyridyl inhibits DNA virus replication: ribonucleotide reductase maturation as a probe of intracellular iron pools. J Biol Chem 276: 24301-24308.
23. Thompson CC, Carabeo RA, (2011) An optimal method of iron starvation of the obligate intracellular pathogen, Chlamydia trachomatis. Front Microbiol 2: 20.
24. Cuervo P, De Jesus JB, Junqueira M, Mendonca-Lima L, Gonzàlez LJ, et al. (2007) Proteome analysis of Leishmania (Viannia) braziliensis by two-dimensional gel electrophoresis and mass spectrometry. Mol Biochem Parasitol 154: 6-21.
25. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: 211-215.
26. Taylor CF, Paton NW, Lilley KS, Binz PA, Julian RK Jr, et al. (2007) The minimum information about a proteomics experiment (MIAPE). Nat Biotechnol 25: 887-893.
27. Willems E, Leyns L, Vandesompele J, (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379: 127-129.
28. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-22.
29. Loo VG, Lalonde RG, (1984) Role of iron in intracellular growth of Trypanosoma cruzi. Infect Immun 45: 726-730.
30. De Jesus JB, Cuervo P, Junqueira M, Britto C, Silva-Filho FC, et al. (2007) A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis. Proteomics 7: 1961-1972.
31. Lee J, Park SJ, Yong TS, (2008) Effect of iron on adherence and citotoxicity of Entamoeba histolytica to CHO cell monolayers. Korean J Parasitol 46: 37-40.
32. Salzman TA, Stella AM, De Xifra EAW, Baffle AMDC, Docampo R, et al. (1982) Porphyrin biosynthesis in parasitic hemoflagellates: Functional and defective enzymes in Trypanosoma cruzi. Comp Biochem Physiol 72B: 663-667.
33. Chang CS, Chang KP, (1985) Heme requirement and acquisition by extracellular and intracellular stages of Leishmania mexicana amazonensis. Mol Biochem Parasitol 16: 267-276.
34. Sah JF, Ito H, Kolli BK, Peterson DA, Sassa S, et al. (2002) Genetic rescue of Leishmania deficiency in porphyrin biosynthesis creates mutants suitable for analysis of cellular events in uroporphyria and for photodynamic therapy. J Biol Chem 207: 14902-14909.
35. Le NTV, Richardson DR, (2002) The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim Biophys Acta 1603: 31-46.
36. Rodvien R, Tavassoli M, Crosby WH, (1974) The structure of spleen in experimentally induced iron deficiency anaemia. Am J Pathol 75: 243-254.
37. Jarvis JH, Jacobs A, (1974) Morphological abnormalities in lymphocyte mitochondria associates with iron deficiency anaemia. J Clin Pathol 27: 973-979.
38. Levi S, Rovida E, (2009) The role of iron in mitochondrial function. Biochim Biophys Acta 1790: 629-636.
39. Yoon YS, Byun HO, Cho H, Kim BK, Toon G, (2003) Complex II defect via down regulation of iron-sulfur subunit induces mitochondrial dysfunction and cell cycle delay in iron chelation-induced senescence associated growth arrest. J Biol Chem 278: 51577-51586.
40. Mehta A, Shaha C, (2004) Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition. Complex inhibition results in increased pentamidine citotoxicity. J Biol Chem 279: 11798-11813.
41. Ly JD, Grubb DR, Lawen A, (2003) The mitochondrial membrane potential (ΔΨm) in apoptosis; an update. Apoptosis 8: 115-128.
42. Mittra B, Cortez M, Haydock A, Ramasamy G, Myler PJ, et al. (2013) Iron uptake controls the generation of Leishmania infective forms through regulation of ROS levels. J Exp Med 210: 401-416.
43. Proto WR, Coombs GH, Mottram JC, (2013) Cell death in parasitic protozoa: regulated or incidental? Nat Rev Microbiol 11: 58-66.
44. Li S, Crooks PA, Wei X, de Leon J, (2004) Toxicity of dipyridyl compounds and related compounds. Crit Rev Toxicol 34: 447-460.
45. Livnat-Levanon N, Glickman MH, (2011) Ubiquitin-proteasome system and mitochondria - reciprocity. Biochim Biophys Acta 1809: 80-87.
46. Shang F, Taylor A, (2011) Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 51: 5-16.
47. Subota I, Rotureau B, Blisnick T, Ngwabyt S, Durand-Dubief M, et al. (2011) ALBA proteins are stage-regulated during Trypanosome development in the tsetse fly and participate in differentiation. Mol Biol Cell 22: 4205-4219.
48. Mani J, Güttinger A, Schimanski B, Heller M, Acosta-Serrano A, et al. (2011) Alba-domain proteins of Trypanosoma brucei are cytoplasmic RNA-binding proteins that interact with the translation machinery. PLOS One 6: 1-16.
49. DiPetrillo CG, Smith EF, (2010) Pcdp1 is a central apparatus protein that binds Ca2+-calmodulin and regulates ciliary motility. J Cell Biol 89: 601-612.
50. Eid JE, Sollner-Webb B, (1991) Homologous recombination in the tandem calmodulin genes of Trypanosoma brucei yelds multiple products: compensation for deleterious deletions by gene amplification. Genes Dev 11: 2024-2032.
51. Lee MG, Chen JF, Ho AW, D'Alesandro PA, Van der Ploeg LH, (1990) A putative flagellar Ca2+- binding protein of the flagellum of trypanosomatid protozoan parasites. Nucleic Acids Res 18: 4252.
52. Ridgley E, Webster P, Patton C, Ruben L, (2000) Calmodulin-binding properties of the paraflagellar rod complex from Trypanosoma brucei. Mol Biochem Parasitol 109: 195-201.
53. Portman N, Lacomble S, Thomas B, McKean PG, Gull K, (2009) Combining RNA interference mutants and comparative proteomics to identify protein components and dependences in a eukaryotic flagellum. J Biol Chem 284: 5610-5619.
54. Grasso JA, Bruno M, Yates MA, Wei L, Epstein PM, (1990) Calmodulin dependence of transferrin receptor recycling in rat reticulocytes. Biochem J 266: 261-272.
55. McNicoll F, Drummelsmith J, Müller M, Madore E, Boilard, et al, (2006) A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 6: 3567-3581.
56. Haile S, Dupé A, Papadopoulou B, (2008) Deadenylation-independent stage-specific mRNA degradation in Leishmania. Nucleic Acids Res 36: 1634-1644.
57. Gonçalves RL, Barreto RF, Polycarpo CR, Gadelha FR, Castro SL, et al. (2011) A comparative assessment of mitochondrial function in epimastigotes and bloodstream trypomastigotes of Trypanosoma cruzi. J Bioenerg Biomembr 43: 651-661.
58. Van Hellemond JJ, Tielens AGM, (1998) Differences in energy metabolism between Trypanosomatidae. Parasitol Today 14: 265-271.