Deciphering the Leishmania exoproteome: What we know and what we can learn

FEMS Immunology and Medical Microbiology

Volumn 58, Issue 1, 2010, Pages 27-38

  Corrales, Rosa Milagros ^a   Sereno, Denis ^a   Mathieu Daudé, Françoise ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Leishmania secretome; Secreted virulence factors; Secretion mechanisms

Indexed keywords

BACTERIAL PROTEIN; PROTEOME;

CONFERENCE PAPER; EXTRACELLULAR SPACE; HOST PARASITE INTERACTION; LEISHMANIA; LIFE CYCLE; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEOMICS;

ANIMALS; HOST-PARASITE INTERACTIONS; HUMANS; LEISHMANIA; LEISHMANIASIS; LIFE CYCLE STAGES; MACROPHAGES; PROTEOME; PROTOZOAN PROTEINS; PSYCHODIDAE; VIRULENCE FACTORS;

EID: 74549190006     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2009.00608.x     Document Type: Conference Paper

References (102)

1. Ambit A, Fasel N, Coombs GH Mottram JC (2008) An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ 15 : 113 122.
2. Antelmann H, Tjalsma H, Voigt B, Ohlmeier S, Bron S, van Dijl JM Hecker M (2001) A proteomic view on genome-based signal peptide predictions. Genome Res 11 : 1484 1502.
3. Balu B, Shoue DA, Fraser MJ Jr. Adams JH (2005) High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. P Natl Acad Sci USA 102 : 16391 16396.
4. Bates PA (2007) Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol 37 : 1097 1106.
5. Bendtsen JD, Jensen LJ, Blom N, Von Heijne G Brunak S (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17 : 349 356.
6. Beverley SM, Akopyants NS, Goyard S et al 2002) Putting the Leishmania genome to work: functional genomics by transposon trapping and expression profiling. Philos T Roy Soc B 357 : 47 53.
7. Bottger A, Strasser D, Alexandrova O et al 2006) Genetic screen for signal peptides in Hydra reveals novel secreted proteins and evidence for non-classical protein secretion. Eur J Cell Biol 85 : 1107 1117.
8. Campbell K, Popov V Soong L (2004) Identification and molecular characterization of a gene encoding a protective Leishmania amazonensis Trp-Asp (WD) protein. Infect Immun 72 : 2194 2202.
9. Chaput N, Flament C, Viaud S et al 2006) Dendritic cell derived-exosomes: biology and clinical implementations. J Leukocyte Biol 80 : 471 478.
10. Charras GT (2008) A short history of blebbing. J Microsc 231 : 466 478.
11. Chenik M, Lakhal S, Ben Khalef N, Zribi L, Louzir H Dellagi K (2006) Approaches for the identification of potential excreted/secreted proteins of Leishmania major parasites. Parasitology 132 : 493 509.
12. Chevallet M, Diemer H, Van Dorssealer A, Villiers C Rabilloud T (2007) Toward a better analysis of secreted proteins: the example of the myeloid cells secretome. Proteomics 7 : 1757 1770.
13. Chowdhury I, Tharakan B Bhat GK (2008) Caspases - an update. Comp Biochem Phys B 151 : 10 27.
14. Clayton C, Hausler T Blattner J (1995) Protein trafficking in kinetoplastid protozoa. Microbiol Rev 59 : 325 344.
15. Coler RN, Goto Y, Bogatzki L, Raman V Reed SG (2007) Leish-111f, a recombinant polyprotein vaccine that protects against visceral Leishmaniasis by elicitation of CD4+ T cells. Infect Immun 75 : 4648 4654.
16. Croft SL, Sundar S Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19 : 111 126.
17. Denny PW, Gokool S, Russell DG, Field MC Smith DF (2000) Acylation-dependent protein export in Leishmania. J Biol Chem 275 : 11017 11025.
18. Deponte M (2008) Programmed cell death in protists. Biochim Biophys Acta 1783 : 1396 1405.
19. Duboise SM, Vannier-Santos MA, Costa-Pinto D et al 1994) The biosynthesis, processing, and immunolocalization of Leishmania pifanoi amastigote cysteine proteinases. Mol Biochem Parasit 68 : 119 132.
20. Ellis M, Sharma DK, Hilley JD, Coombs GH Mottram JC (2002) Processing and trafficking of Leishmania mexicana GP63. Analysis using GP18 mutants deficient in glycosylphosphatidylinositol protein anchoring. J Biol Chem 277 : 27968 27974.
21. Field MC, Natesan SK, Gabernet-Castello C Koumandou VL (2007) Intracellular trafficking in the trypanosomatids. Traffic 8 : 629 639.
22. Flinn HM, Rangarajan D Smith DF (1994) Expression of a hydrophilic surface protein in infective stages of Leishmania major. Mol Biochem Parasit 65 : 259 270.
23. Foth B, Piani A, Curtis JM, Ilg T, McConville M Handman E (2002) Leishmania major proteophosphoglycans exist as membrane-bound and soluble forms and localise to the cell membrane, the flagellar pocket and the lysosome. Int J Parasitol 32 : 1701 1708.
24. Gevaert K, Impens F, Ghesquiere B, Van Damme P, Lambrechts A Vandekerckhove J (2008) Stable isotopic labeling in proteomics. Proteomics 8 : 4873 4885.
25. Gopfert U, Goehring N, Klein C Ilg T (1999) Proteophosphoglycans of Leishmania mexicana. Molecular cloning and characterization of the Leishmania mexicana ppg2 gene encoding the proteophosphoglycans aPPG and pPPG2 that are secreted by amastigotes and promastigotes. Biochem J 344 : 787 795.
26. Grebaut P, Chuchana P, Brizard JP et al 2009) Identification of total and differentially expressed excreted-secreted proteins from Trypanosoma congolense strains exhibiting different virulence and pathogenicity. Int J Parasitol 39 : 1137 1150.
27. Grimmond SM, Miranda KC, Yuan Z et al 2003) The mouse secretome: functional classification of the proteins secreted into the extracellular environment. Genome Res 13 : 1350 1359.
28. Hajmova M, Chang KP, Kolli B Volf P (2004) Down-regulation of gp63 in Leishmania amazonensis reduces its early development in Lutzomyia longipalpis. Microbes Infect 6 : 646 649.
29. Hathout Y (2007) Approaches to the study of the cell secretome. Expert Rev Proteomic 4 : 239 248.
30. Helms MJ, Ambit A, Appleton P, Tetley L, Coombs GH Mottram JC (2006) Bloodstream form Trypanosoma brucei depend upon multiple metacaspases associated with RAB11-positive endosomes. J Cell Sci 119 : 1105 1117.
31. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306 : 1934 1937.
32. Holzmuller P, Grebaut P, Peltier JB et al 2008) Secretome of animal trypanosomes. Ann NY Acad Sci 1149 : 337 342.
33. Horwitz MA, Harth G, Dillon BJ Maslesa-Galic S (2005) Enhancing the protective efficacy of Mycobacterium bovis BCG vaccination against tuberculosis by boosting with the Mycobacterium tuberculosis major secretory protein. Infect Immun 73 : 4676 4683.
34. Ilg T (2000) Proteophosphoglycans of Leishmania. Parasitol Today 16 : 489 497.
35. Ilg T, Stierhof YD, Craik D, Simpson R, Handman E Bacic A (1996) Purification and structural characterization of a filamentous, mucin-like proteophosphoglycan secreted by Leishmania parasites. J Biol Chem 271 : 21583 21596.
36. Jacobs KA, Collins-Racie LA, Colbert M et al 1997) A genetic selection for isolating cDNAs encoding secreted proteins. Gene 198 : 289 296.
37. Jaffe CL Dwyer DM (2003) Extracellular release of the surface metalloprotease, gp63, from Leishmania and insect trypanosomatids. Parasitol Res 91 : 229 237.
38. Jazin EE, Luquetti AO, Rassi A Frasch AC (1991) Shift of excretory-secretory immunogens of Trypanosoma cruzi during human Chagas' disease. Infect Immun 59 : 2189 2191.
39. Joshi MB Dwyer DM (2007) Molecular and functional analyses of a novel class I secretory nuclease from the human pathogen, Leishmania donovani. J Biol Chem 282 : 10079 10095.
40. Joshi MB, Rogers ME, Shakarian AM, Yamage M, Al-Harthi SA, Bates PA Dwyer DM (2005) Molecular characterization, expression, and in vivo analysis of LmexCht1: the chitinase of the human pathogen, Leishmania mexicana. J Biol Chem 280 : 3847 3861.
41. Joshi PB, Kelly BL, Kamhawi S, Sacks DL McMaster WR (2002) Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol Biochem Parasit 120 : 33 40.
42. Keller M, Ruegg A, Werner S Beer HD (2008) Active caspase-1 is a regulator of unconventional protein secretion. Cell 132 : 818 831.
43. Kima PE (2007) The amastigote forms of Leishmania are experts at exploiting host cell processes to establish infection and persist. Int J Parasitol 37 : 1087 1096.
44. Kinseth MA, Anjard C, Fuller D, Guizzunti G, Loomis WF Malhotra V (2007) The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 130 : 524 534.
45. Klee EW (2008) The zebrafish secretome. Zebrafish 5 : 131 138.
46. Klee EW Sosa CP (2007) Computational classification of classically secreted proteins. Drug Discov Today 12 : 234 240.
47. Klein RD, Gu Q, Goddard A Rosenthal A (1996) Selection for genes encoding secreted proteins and receptors. P Natl Acad Sci USA 93 : 7108 7113.
48. Kulkarni MM, McMaster WR, Kamysz E, Kamysz W, Engman DM McGwire BS (2006) The major surface-metalloprotease of the parasitic protozoan, Leishmania, protects against antimicrobial peptide-induced apoptotic killing. Mol Microbiol 62 : 1484 1497.
49. Lane CS (2005) Mass spectrometry-based proteomics in the life sciences. Cell Mol Life Sci 62 : 848 869.
50. Latterich M, Abramovitz M Leyland-Jones B (2008) Proteomics: new technologies and clinical applications. Eur J Cancer 44 : 2737 2741.
51. Lee N, Gannavaram S, Selvapandiyan A Debrabant A (2007) Characterization of metacaspases with trypsin-like activity and their putative role in programmed cell death in the protozoan parasite Leishmania. Eukaryot Cell 6 : 1745 1757.
52. Lee SA, Wormsley S, Kamoun S, Lee AF, Joiner K Wong B (2003) An analysis of the Candida albicans genome database for soluble secreted proteins using computer-based prediction algorithms. Yeast 20 : 595 610.
53. Lemesre JL, Holzmuller P, Goncalves RB, Bourdoiseau G, Hugnet C, Cavaleyra M Papierok G (2007) Long-lasting protection against canine visceral leishmaniasis using the LiESAp-MDP vaccine in endemic areas of France: double-blind randomised efficacy field trial. Vaccine 25 : 4223 4234.
54. Lodge R Descoteaux A (2005) Modulation of phagolysosome biogenesis by the lipophosphoglycan of Leishmania. Clin Immunol 114 : 256 265.
55. Lynn MA McMaster WR (2008) Leishmania: conserved evolution - diverse diseases. Trends Parasitol 24 : 103 105.
56. McConville MJ, Mullin KA, Ilgoutz SC Teasdale RD (2002) Secretory pathway of trypanosomatid parasites. Microbiol Mol Biol R 66 : 122 154.
57. McGwire BS, O'Connell WA, Chang KP Engman DM (2002) Extracellular release of the glycosylphosphatidylinositol (GPI)-linked Leishmania surface metalloprotease, gp63, is independent of GPI phospholipolysis: implications for parasite virulence. J Biol Chem 277 : 8802 8809.
58. McMahon-Pratt D Alexander J (2004) Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol Rev 201 : 206 224.
59. Merlen T, Sereno D, Brajon N, Rostand F Lemesre JL (1999) Leishmania spp.: completely defined medium without serum and macromolecules (CDM/LP) for the continuous in vitro cultivation of infective promastigote forms. Am J Trop Med Hyg 60 : 41 50.
60. Mottram JC, Coombs GH Alexander J (2004) Cysteine peptidases as virulence factors of Leishmania. Curr Opin Microbiol 7 : 375 381.
61. Naderer T McConville MJ (2008) The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10 : 301 308.
62. Nene V Bishop R (2001) Trapping parasite secretory proteins in baker's yeast. Trends Parasitol 17 : 407 409.
63. Nickel W Rabouille C (2009) Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Bio 10 : 148 155.
64. Nickel W Seedorf M (2008) Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annu Rev Cell Dev Bi 24 : 287 308.
65. Nilsson T Warren G (1994) Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr Opin Cell Biol 6 : 517 521.
66. Olivier M, Gregory DJ Forget G (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 18 : 293 305.
67. Ortiz D, Sanchez MA, Pierce S, Herrmann T, Kimblin N, Archie Bouwer HG Landfear SM (2007) Molecular genetic analysis of purine nucleobase transport in Leishmania major. Mol Microbiol 64 : 1228 1243.
68. Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA Walton JD (2007) Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7 : 3171 3183.
69. Peters C, Stierhof YD Ilg T (1997a) Proteophosphoglycan secreted by Leishmania mexicana amastigotes causes vacuole formation in macrophages. Infect Immun 65 : 783 786.
70. Peters C, Kawakami M, Kaul M, Ilg T, Overath P Aebischer T (1997b) Secreted proteophosphoglycan of Leishmania mexicana amastigotes activates complement by triggering the mannan binding lectin pathway. Eur J Immunol 27 : 2666 2672.
71. Pickart MA, Klee EW, Nielsen AL et al 2006) Genome-wide reverse genetics framework to identify novel functions of the vertebrate secretome. PLoS ONE 1 : e104.
72. Prudovsky I, Tarantini F, Landriscina M et al 2008) Secretion without Golgi. J Cell Biochem 103 : 1327 1343.
73. Qu Y, Franchi L, Nunez G Dubyak GR (2007) Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 179 : 1913 1925.
74. Reece ST Kaufmann SH (2008) Rational design of vaccines against tuberculosis directed by basic immunology. Int J Med Microbiol 298 : 143 150.
75. Rogers ME Bates PA (2007) Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog 3 : e91.
76. Rogers ME, Ilg T, Nikolaev AV, Ferguson MA Bates PA (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430 : 463 467.
77. Rogers ME, Hajmova M, Joshi MB, Sadlova J, Dwyer DM, Volf P Bates PA (2008) Leishmania chitinase facilitates colonization of sand fly vectors and enhances transmission to mice. Cell Microbiol 10 : 1363 1372.
78. Rothman JE Orci L (1992) Molecular dissection of the secretory pathway. Nature 355 : 409 415.
79. Samant M, Gupta R, Kumari S et al 2009) Immunization with the DNA-encoding N-terminal domain of proteophosphoglycan of Leishmania donovani generates Th1-Type immunoprotective response against experimental visceral leishmaniasis. J Immunol 183 : 470 479.
80. Santarem N, Silvestre R, Tavares J, Silva M, Cabral S, Maciel J Cordeiro-da-Silva A (2007) Immune response regulation by leishmania secreted and nonsecreted antigens. J Biomed Biotechnol 2007 : 85154.
81. Santos AL, Branquinha MH D'Avila-Levy CM (2006) The ubiquitous gp63-like metalloprotease from lower trypanosomatids: in the search for a function. An Acad Bras Cienc 78 : 687 714.
82. Schatz G Dobberstein B (1996) Common principles of protein translocation across membranes. Science 271 : 1519 1526.
83. Schotman H, Karhinen L Rabouille C (2008) dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell 14 : 171 182.
84. Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, Foster LJ Reiner NE (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9 : R35.
85. Simpson AG, Stevens JR Lukes J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22 : 168 174.
86. Simpson JC, Mateos A Pepperkok R (2007) Maturation of the mammalian secretome. Genome Biol 8 : 211.
87. Simpson RJ, Jensen SS Lim JW (2008) Proteomic profiling of exosomes: current perspectives. Proteomics 8 : 4083 4099.
88. Smyth D, McManus DP, Smout MJ, Laha T, Zhang W Loukas A (2003) Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infect Immun 71 : 2548 2554.
89. Stegmayer C, Kehlenbach A, Tournaviti S et al 2005) Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J Cell Sci 118 : 517 527.
90. Stuart K, Brun R, Croft S et al 2008) Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest 118 : 1301 1310.
91. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J Amigorena S (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166 : 7309 7318.
92. Tjalsma H, Bolhuis A, Jongbloed JD, Bron S van Dijl JM (2000) Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol Mol Biol R 64 : 515 547.
93. Tobin JF Wirth DF (1993) Mutational analysis of a signal sequence required for protein secretion in Leishmania major. Mol Biochem Parasit 62 : 243 249.
94. Tonui WK, Mejia JS, Hochberg L et al 2004) Immunization with Leishmania major exogenous antigens protects susceptible BALB/c mice against challenge infection with L. major. Infect Immun 72 : 5654 5661.
95. Tournaviti S, Hannemann S, Terjung S et al 2007) SH4-domain-induced plasma membrane dynamization promotes bleb-associated cell motility. J Cell Sci 120 : 3820 3829.
96. Tournaviti S, Pietro ES, Terjung S et al 2009) Reversible phosphorylation as a molecular switch to regulate plasma membrane targeting of acylated SH4 domain proteins. Traffic 10 : 1047 1060.
97. van Ooij C, Tamez P, Bhattacharjee S et al 2008) The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog 4 : e1000084.
98. Webb JR, Campos-Neto A, Ovendale PJ, Martin TI, Stromberg EJ, Badaro R Reed SG (1998) Human and murine immune responses to a novel Leishmania major recombinant protein encoded by members of a multicopy gene family. Infect Immun 66 : 3279 3289.
99. Xue H, Lu B Lai M (2008) The cancer secretome: a reservoir of biomarkers. J Transl Med 6 : 52.
100. Yamane H, Lee SJ, Kim BD, Tao R Rose JK (2005) A coupled yeast signal sequence trap and transient plant expression strategy to identify genes encoding secreted proteins from peach pistils. J Exp Bot 56 : 2229 2238.
101. Yokoyama-Yasunaka JK, Pral EM, Oliveira Junior OC, Alfieri SC Stolf AM (1994) Trypanosoma cruzi: identification of proteinases in shed components of trypomastigote forms. Acta Trop 57 : 307 315.
102. Zwickl H, Traxler E, Staettner S et al 2005) A novel technique to specifically analyze the secretome of cells and tissues. Electrophoresis 26 : 2779 2785.