Identification of virulence factors in leishmania infantum strains by a proteomic approach

Journal of Proteome Research

Volumn 13, Issue 4, 2014, Pages 1860-1872

  Da Fonseca Pires, Simone ^a   Fialho, Luiz Carlos ^a   Silva, Soraia Oliveira ^a   Melo, Maria Norma ^a   De Souza, Carolina Carvalho ^a   Tafuri, Wagner Luiz ^a   Bruna Romero, Oscar ^a   De Andrade, Hélida Monteiro ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Leishmania infantum; proteome; virulence

Indexed keywords

BETA TUBULIN; CHAPERONE; COFILIN LIKE PROTEIN; ENOLASE; HEAT SHOCK PROTEIN 70; IRON SULFUR PROTEIN; KINETOPLASTID MEMBRANE PROTEIN 11; METALLOPROTEINASE; PEROXIDASE; PEROXIDOXIN; PHOSPHOMANNOMUTASE; PROTEIN; PROTEIN 14 3 3; RAB11 PROTEIN; RIBONUCLEASE; S ADENOSYLHOMOCYSTEINE; TOXIN; TRYPAREDOXIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; PROTEOME; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL MIGRATION; CONTROLLED STUDY; DEGRADATION; ENERGY CONSUMPTION; FEMALE; HOST; LEISHMANIA INFANTUM; LEISHMANIASIS; MASS SPECTROMETRY; NONHUMAN; PARASITE SURVIVAL; PERITONEAL CAVITY; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEOMICS; STRESS; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; HAMSTER; MACROPHAGE; METABOLISM; MOUSE; PATHOGENICITY; PROCEDURES;

ANIMALS; CELLS, CULTURED; CRICETINAE; LEISHMANIA INFANTUM; MACROPHAGES; MICE; MICE, INBRED BALB C; PROTEOME; PROTEOMICS; PROTOZOAN PROTEINS; VIRULENCE FACTORS;

EID: 84898759637     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400923g     Document Type: Article

References (55)

1. Desjeux, P. Leishmaniasis: current situation and new perspectives Comp. Immunol. Microbiol. Infect. Dis. 2004, 27, 305-318
2. Alvar, J.; Aparicio, P.; Aseffa, A.; Den Boer, M.; Cañavate, C.; Dedet, J. P.; Gradoni, L.; Ter Horst, R.; López-Vélez, R.; Moreno, J. The relationship between leishmaniasis and AIDS: the second 10 years Clin. Microbiol. Rev. 2008, 21 (2) 334-359
3. Hailu, A.; Berhe, N. The performance of direct agglutination tests (DAT) in the diagnosis of visceral leishmaniasis among Ethiopian patients with HIV co-infection Ann Trop Med Parasitol. 2002, 96 (1) 25-30
4. Dye, C. The logic of visceral Leishmaniasis control Am. J. Trop. Med. Hyg. 1996, 55, 125-130
5. Berrahal, F.; Mary, C.; Roze, M.; Berenger, A.; Escoffier, K.; Lamouroux, D. Canine Leishmaniasis: identification of asymptomatic carriers by polymerase chain reaction and immunoblotting Am. J. Trop. Med. Hyg. 1996, 55, 273-277
6. Azizi, H.; Hassani, K.; Taslimi, Y.; Shateri-Najafabadi, H.; Papadopoulou, B.; Rafati, S. Searching for virulence factors in the non-pathogenic parasite to humans Leishmania tarentolae Parasitology 2009, 136, 723-735
7. Zhang, W. W.; Matlashewski, G. Screening Leishmania donovani -specific genes required for visceral infection Mol. Microbiol. 2010, 77 (2) 1-13
8. Brittingham, A.; Miller, M. A.; Donelson, J. E.; Wilson, M. E. Regulation of GP63 mRNA stability in promastigotes of virulent and attenuated Leishmania chagasi Mol. Biochem. Parasitol. 2001, 112, 51-59
9. Yao, C.; Chen, Y.; Sudan, B.; Donelson, J. E.; Wilson, M. E. Leishmania chagasi: Homogenous metacyclic promastigotes isolated by buoyant density are highly virulent in a mouse model Exp. Parasitol. 2008, 118, 129-133
10. Yao, C.; Li, Y.; Donelson, J. E.; Wilson, M. E. Proteomic examination of Leishmania chagasi plasma membrane proteins: contrast between avirulent and virulent (metacyclic) parasite forms Proteomics Clin. Appl. 2010, 4, 4-16
11. Morales, M. A.; Watanabe, R.; Dacher, M.; Chafey, P.; Osorio, Y.; Fortéa, J.; Scott, D. A.; Beverley, S. M.; Ommen, G.; Clos, J.; Hem, S.; Lenormand, P.; Rousselle, J. C.; Namane, A.; Späth, G. F. Phosphoproteome dynamics reveal heat-shock protein complexes specific to the Leishmania donovani infectious stage Proc. Natl. Acad. Sci., U. S. A. 2010, 107, 8381-8386
12. Costa, M. M.; Andrade, H. M.; Bartholomeu, D. C.; Pires, S. F.; Chapeaurouge, A. D.; Gazzinelli, R. T. Analysis of Leishmania chagasi by 2-D Difference Gel Eletrophoresis (2-D DIGE) and Immunoproteomic: Identification of Novel Candidate Antigens for Diagnostic Tests and Vaccine J. Proteome Res. 2011, 10, 2172-2184
13. Pescher, P.; Blisnick, T.; Bastin, P.; Späth, G. Quantitative proteome profiling informs on phenotypictraits that adapt Leishmania donovani for axenic and intracellular proliferation Cell. Microbiol. 2011, 13, 978-991
14. Clayton, C.; Shapira, M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias Mol. Biochem. Parasitol. 2007, 156, 93-101
15. Clayton, C. E. Life without transcriptional control? From fly to man and back again EMBO J. 2002, 21, 1881-1888
16. Giaimis, J.; Lombard, Y.; Makaya-Kumba, M.; Fonteneau, P.; Poindron, P. A new and simple method for studying the binding and ingestion steps in the phagocytosis of yeasts J. Immunol. Methods 1992, 154 (2) 185-193
17. Tafuri, W. L.; Santos, R. L.; Arantes, R. M.; Gonçalves, R.; De Melo, M. N.; Michalick, M. S.; Tafuri, W. L. An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues J. Immunol. Methods. 2004, 292, 17-23
18. Afonso, L. C.; Scott, P. Immune responses associated with susceptibility of C57BL/10 mice to Leishmania amazonensis Infect. Immun. 1993, 61, 2952-2959
19. Bretagne, S.; Durand, R.; Olivi, M.; Garin, J. F.; Sulahian, A.; Rivollet, D.; Vidaud, M.; Deniau, M. Real-time PCR as a new tool for quantifying Leishmania infantum in liver in infected mice Clin. Diagn. Lab. Immunol. 2001, 8, 828-831
20. Bruna-Romero, O.; Hafalla, C. R.; González-Aseguinolaza, G.; Sano, G. I.; Tsuji, M.; Zavala, F. Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR Int. J. Parasitol. 2001, 31, 1499-1502
21. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250 Electrophoresis 1988, 9, 255-262
22. Teixeira, S. M. R.; Otsu, K.; Hill, K. L.; Kirchhoff, L. V.; Donelson, J. E. Expression of a marker for intracellular Trypanosoma cruzi amastigotes in extracellular spheromastigotes Mol. Biochem. Parasitol. 1999, 98, 265-270
23. Di Noia, J. M.; D'orso, I.; Sanchez, D. O.; Frasch, A. C. AU-rich elements in the 3′-untranslated region of a new mucin-type gene family of Trypanosoma cruzi confers mRNA instability and modulates translation efficiency J. Biol. Chem. 2000, 275, 10218-10227
24. D'orso, I.; Frasch, A. C. TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes J. Biol. Chem. 2001, 276, 34801-34809
25. Santarém, N.; Racine, G.; Silvestre, R.; Cordeiro-da-Silva, A.; Ouellette, M. Exoproteome dynamics in Leishmania infantum J. Proteomics 2013, 12 (84) 106-118
26. Jardim, A.; Funk, V.; Caprioli, R. M.; Olafson, R. W. Isolation and structural characterization of the Leishmania donovani kinetoplastid membrane protein-11, a major immunoreactive membrane glycoprotein Biochem. J. 1995, 305, 307-313
27. Mukhopadhyay, S.; Sen, P.; Majumder, H. K.; Roy, S. Reduced expression of lipophosphoglycan (LPG) and kinetoplastid membrane protein (KMP)-11 in Leishmania donovani promastigotes in axenic culture J. Parasitol. 1998, 84, 644-647
28. Lacerda, D. I.; Cysne-Finkelstein, L.; Nunes, M. P.; De-Luca, P. M.; Genestra, M.; Da, S.; Leon, L. L.; Berrêdo-Pinho, M.; Mendonça- Lima, L.; Matos, D. C.; Medeiros, M. A.; Mendonça, S. C. Kinetoplastid membrane protein-11 exacerbates infection with Leishmania amazonensis in murine macrophages Mem. Inst. Oswaldo Cruz. 2012, 107, 238-245
29. Matos, D. C.; Faccioli, L. A.; Cysne-Finkelstein, L.; Luca, P. M.; Corte-Real, S.; Armoa, G. R. Kinetoplastid membrane protein-11 is present in promastigotes and amastigotes of Leishmania amazonensis and its surface expression increases during metacyclogenesis Mem Inst Oswaldo Cruz. 2010, 105, 341-347
30. El Fadili, K.; Drummelsmith, J.; Roy, G.; Jardim, A.; Ouellette, M. Down regulation of KMP-11 in Leishmania infantum axenic antimony resistant amastigotes as revealed by a proteomic screen Exp. Parasitol. 2009, 123 (1) 51-57
31. Swenerton, R. K.; Zhang, S.; Sajid, M.; Medzihradszky, K. F.; Craik, C. S.; Kelly, B. L.; Mckerrow, J. H. The oligopeptidase B of Leishmania regulates parasite enolase and immune evasion J. Biol. Chem. 2011, 286, 429-40
32. Vanegas, G.; Quiñones, W.; Concepción, L.; Avilán, L. Enolase as a plasminogen binding protein in Leishmania mexicana Parasitol Res. 2007, 101, 1511-1516
33. Ruhland, A.; Leal, N.; Kima, P. E. Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis Cell Microbiol. 2007, 9, 84-96
34. Rappu, P.; Shin, B. S.; Zalkin, H.; Mantsala, P. A Role for a Highly Conserved Protein of Unknown Function in Regulation of Bacillus subtilis purA by the Purine Repressor J. Bacteriol. 1999, 181, 3810-3815
35. Brotherton, M. C; Racine, G.; Ouameur, A. A; Leprohon, P.; Papadopoulou, B.; Ouellette, M. Analysis of membrane-enriched and high molecular weight proteins in Leishmania infantum promastigotes and axenic amastigotes J. Proteome Res. 2012, 11 (8) 3974-3985
36. Priest, J. W.; Hajduk, S. L. In Vitro Import of the Rieske Iron-Sulfur Protein by Trypanosome Mitochondria J. Biol. Chem. 1996, 271, 20060-20069
37. Harnisch, U.; Weiss, H.; Sebald, W. The primary structure of the iron-sulfur subunit of ubiquinol-cytochrome c reductase from Neurospora, determined by cDNA and gene sequencing Eur. J. Biochem. 1985, 149, 95-99
38. Matrangolo, F. S.; Liarte, D. B.; Andrade, L. C.; de Melo, M. F.; Andrade, J. M.; Ferreira, R. F.; Santiago, A. S.; Pirovani, C. P.; Silva-Pereira, R. A.; Murta, S. M. Comparative proteomic analysis of antimony-resistant and -susceptible Leishmania braziliensis and Leishmania infantum chagasi lines Mol. Biochem. Parasitol. 2013, 190 (2) 63-75
39. Kushawaha, R.; Gupta, R.; Amogh, A.; Sahasrabuddhe, S. Elongation factor-2, a Th1 stimulatory protein of Leishmania donovani, generates strong IFN-γ and IL-12 response in cured Leishmania -infected patients/hamsters and protects hamsters against Leishmania challenge J Immunol. 2011, 187, 6417-6427
40. Bargis-Surgey, P.; Lavergne, J. P.; Reboud, J. P. Interaction of elongation factor eEF-2 with ribosomal P proteins Eur. J. Biochem. 1999, 262, 606-611
41. Mottram, J. C.; Coombs, G. H.; Alexander, J. Cysteine peptidases as virulence factors of Leishmania Curr. Opin. Microbiol. 2004, 7, 375-381
42. Walker, J.; Vasquez, J. J.; Gomez, M. A. Identification of developmentally-regulated proteins in Leishmania panamensis by proteome profiling of promastigotes and axenic amastigotes Mol. Biochem. Parasitol. 2006, 147, 64-73
43. Kedzierski, L.; Malby, R.; Smith, B.; Handman, E. Structure of Leishmania Mexicana Phosphomannomutase Highlights Similarities with Human Isoforms J. Mol. Biol. 2006, 363, 215-227
44. Silverman, J. M.; Chan, S. K.; Robinson, D. P.; Dwyer, D. M. Proteomic analysis of the secretome of Leishmania donovani Genome Biol. 2008, 9, 1-21
45. Malygin, A. A.; Shaulo, D. D.; Karpova, G. Proteins S7, S10, S16 and S19 of the human 40S ribosomal subunit are most resistant to dissociation by salt Biochem. Biophys. Acta 2000, 1494, 213-216
46. Romao, S.; Castro, H.; Sousa, C.; Carvalho, S.; Tomás, A. The cytosolic tryparedoxin of Leishmania infantum is essential for parasite survival Int. J. Parasitol. 2009, 39, 1-9
47. Iyer, J. P.; Kaprakkaden, A.; Choudhary, M. L.; Shaha, C. Crucial role of cytosolic tryparedoxin peroxidase in Leishmania donovani survival, drug response and virulence Mol. Microbiol. 2008, 68, 372-391
48. Castro, H.; Sousa, C.; Santos, M.; Tomas, A. M. Complementary antioxidant defense by cytoplasmic and Mitochondrial peroxiredoxins in Leishmania infantum Free Radical Biol. Med. 2002, 33, 1552-1562
49. Daneshvar, H.; Wyllie, S.; Phillips, S.; Hagan, P.; Burchmore, R. Comparative proteomics profiling of a gentamicin-attenuated Leishmania infantum cell line identifies key changes in parasite thiol-redox metabolism J. Proteomics 2012, 75 (5) 1463-1471
50. Silverman, J. M.; Clos, J.; de'Oliveira, C. C.; Shirvani, O.; Fang, Y.; Wang, C.; Foster, L. J.; Reiner, N. E. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages J. Cell Sci. 2010, 123, 842-852
51. Jensen, O. N. Interpreting the protein language using proteomics Nat. Rev., Mol. Cell Biol. 2006, 7, 391-403
52. Hughes, G. J.; Frutiger, S.; Paquet, N.; Ravier, F.; Pasquali, C.; Sanchez, J. C.; James, R.; Tissot, J. D.; Bjellqvist, B.; Hochstrasser, D. Plasma protein map: an update by microsequencing Electrophoresis 1992, 13, 707-714
53. Nandan, D.; Yi, T.; Lopez, M.; Lai, C.; Reiner, N. E. Leishmania EF-1 alpha activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation J. Biol. Chem. 2002, 277, 50190-50197
54. Brotherton, M. C.; Racine, G.; Foucher, A. L.; Drummelsmith, J.; Papadopoulou, B.; Ouellette, M. Analysis of stage-specific expression of basic proteins in Leishmania infantum J. Proteome Res. 2010, 9 (8) 3842-3853
55. Lynn, M. A.; Marr, A. K.; McMaster, W. R. Differential quantitative proteomic profiling of Leishmania infantum and Leishmania mexicana density gradient separated membranous fractions J. Proteomics 2013, 82, 179-192