Exosome Secretion by the Parasitic Protozoan Leishmania within the Sand Fly Midgut

Cell Reports

Volumn 13, Issue 5, 2015, Pages 957-967

  Atayde, Vanessa Diniz ^a,b   Aslan, Hamide ^c,d   Townsend, Shannon ^c   Hassani, Kasra ^a   Kamhawi, Shaden ^c   Olivier, Martin ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d Selahaddin Eyyubi University   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE CARRIER; DISEASE EXACERBATION; EXOSOME; FEMALE; FLAGELLUM; FLY BITE; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA INFANTUM; LEISHMANIA MAJOR; MIDGUT; MOUSE; MULTIVESICULAR BODY; NONHUMAN; PARASITE TRANSMISSION; PHLEBOTOMINAE; PRIORITY JOURNAL; SECRETION (PROCESS); SKIN LEISHMANIASIS; ANIMAL; INTESTINE; LEISHMANIA; METABOLISM; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; PSYCHODIDAE;

ANIMALS; CYTOKINES; EXOSOMES; INTESTINES; LEISHMANIA; LEISHMANIASIS, CUTANEOUS; MICE; PSYCHODIDAE;

EID: 84947431830     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.058     Document Type: Article

References (45)

1. Bendtsen J.D., Jensen L.J., Blom N., Von Heijne G., Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 2004, 17:349-356.
2. Bhatnagar S., Schorey J.S. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J. Biol. Chem. 2007, 282:25779-25789.
3. Bhatnagar S., Shinagawa K., Castellino F.J., Schorey J.S. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 2007, 110:3234-3244.
4. Boaventura V.S., Santos C.S., Cardoso C.R., de Andrade J., Dos Santos W.L., Clarêncio J., Silva J.S., Borges V.M., Barral-Netto M., Brodskyn C.I., Barral A. Human mucosal leishmaniasis: neutrophils infiltrate areas of tissue damage that express high levels of Th17-related cytokines. Eur. J. Immunol. 2010, 40:2830-2836.
5. Bobrie A., Théry C. Unraveling the physiological functions of exosome secretion by tumors. OncoImmunology 2013, 2:e22565.
6. Bobrie A., Colombo M., Raposo G., Théry C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011, 12:1659-1668.
7. Field M.C., Carrington M. The trypanosome flagellar pocket. Nat. Rev. Microbiol. 2009, 7:775-786.
8. Gomes R., Oliveira F. The immune response to sand fly salivary proteins and its influence on leishmania immunity. Front. Immunol. 2012, 3:110.
9. Götz S., García-Gómez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talón M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36:3420-3435.
10. Hassani K., Olivier M. Immunomodulatory impact of leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. PLoS Negl. Trop. Dis. 2013, 7:e2185.
11. Hassani K., Antoniak E., Jardim A., Olivier M. Temperature-induced protein secretion by Leishmania mexicana modulates macrophage signalling and function. PLoS ONE 2011, 6:e18724.
12. Hassani K., Shio M.T., Martel C., Faubert D., Olivier M. Absence of metalloprotease GP63 alters the protein content of Leishmania exosomes. PLoS ONE 2014, 9:e95007.
13. Hedges S.B., Blair J.E., Venturi M.L., Shoe J.L. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 2004, 4:2.
14. Heinzel F.P., Sadick M.D., Mutha S.S., Locksley R.M. Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc. Natl. Acad. Sci. USA 1991, 88:7011-7015.
15. 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.
16. Joshi P.B., Kelly B.L., Kamhawi S., Sacks D.L., McMaster W.R. Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol. Biochem. Parasitol. 2002, 120:33-40.
17. Kamhawi S. Phlebotomine sand flies and Leishmania parasites: friends or foes?. Trends Parasitol. 2006, 22:439-445.
18. Kamhawi S., Belkaid Y., Modi G., Rowton E., Sacks D. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 2000, 290:1351-1354.
19. Kemp M., Handman E., Kemp K., Ismail A., Mustafa M.D., Kordofani A.Y., Bendtzen K., Kharazmi A., Theander T.G. The Leishmania promastigote surface antigen-2 (PSA-2) is specifically recognised by Th1 cells in humans with naturally acquired immunity to L. major. FEMS Immunol. Med. Microbiol. 1998, 20:209-218.
20. Koppers-Lalic D., Hackenberg M., Bijnsdorp I.V., van Eijndhoven M.A., Sadek P., Sie D., Zini N., Middeldorp J.M., Ylstra B., de Menezes R.X., et al. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014, 8:1649-1658.
21. Lopez Kostka S., Dinges S., Griewank K., Iwakura Y., Udey M.C., von Stebut E. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J. Immunol. 2009, 182:3039-3046.
22. Mottram J.C., Coombs G.H., Alexander J. Cysteine peptidases as virulence factors of Leishmania. Curr. Opin. Microbiol. 2004, 7:375-381.
23. Olivier M., Atayde V.D., Isnard A., Hassani K., Shio M.T. Leishmania virulence factors: focus on the metalloprotease GP63. Microbes Infect. 2012, 14:1377-1389.
24. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
25. Rafati S., Gholami E., Hassani N., Ghaemimanesh F., Taslimi Y., Taheri T., Soong L. Leishmania major heat shock protein 70 (HSP70) is not protective in murine models of cutaneous leishmaniasis and stimulates strong humoral responses in cutaneous and visceral leishmaniasis patients. Vaccine 2007, 25:4159-4169.
26. Rezende A.M., Folador E.L., Resende Dde.M., Ruiz J.C. Computational prediction of protein-protein interactions in Leishmania predicted proteomes. PLoS ONE 2012, 7:e51304.
27. Rogers M.E., Ilg T., Nikolaev A.V., Ferguson M.A., Bates P.A. Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 2004, 430:463-467.
28. Rogers M., Kropf P., Choi B.S., Dillon R., Podinovskaia M., Bates P., Müller I. Proteophosophoglycans regurgitated by Leishmania-infected sand flies target the L-arginine metabolism of host macrophages to promote parasite survival. PLoS Pathog. 2009, 5:e1000555.
29. Sacks D., Anderson C. Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol. Rev. 2004, 201:225-238.
30. Sacks D., Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002, 2:845-858.
31. Santarém N., Racine G., Silvestre R., Cordeiro-da-Silva A., Ouellette M. Exoproteome dynamics in Leishmania infantum. J. Proteomics 2013, 84:106-118.
32. Schlein Y., Jacobson R.L., Messer G. Leishmania infections damage the feeding mechanism of the sandfly vector and implement parasite transmission by bite. Proc. Natl. Acad. Sci. USA 1992, 89:9944-9948.
33. Sibley L.D. Invasion and intracellular survival by protozoan parasites. Immunol. Rev. 2011, 240:72-91.
34. Silverman J.M., Reiner N.E. Exosomes and other microvesicles in infection biology: organelles with unanticipated phenotypes. Cell. Microbiol. 2011, 13:1-9.
35. Silverman J.M., Reiner N.E. Leishmania exosomes deliver preemptive strikes to create an environment permissive for early infection. Front. Cell. Infect. Microbiol. 2011, 1:26.
36. Silverman J.M., Chan S.K., Robinson D.P., Dwyer D.M., Nandan D., Foster L.J., Reiner N.E. Proteomic analysis of the secretome of Leishmania donovani. Genome Biol. 2008, 9:R35.
37. 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.
38. Silverman J.M., Clos J., Horakova E., Wang A.Y., Wiesgigl M., Kelly I., Lynn M.A., McMaster W.R., Foster L.J., Levings M.K., Reiner N.E. Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J. Immunol. 2010, 185:5011-5022.
39. Smoot M.E., Ono K., Ruscheinski J., Wang P.L., Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27:431-432.
40. Taylor D.D., Gercel-Taylor C. The origin, function, and diagnostic potential of RNA within extracellular vesicles present in human biological fluids. Front. Genet. 2013, 4:142.
41. Théry C., Amigorena S., Raposo G., Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 2006, Chapter 3:Unit 3.22.
42. Théry C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009, 9:581-593.
43. Vanden Eijnden S., Goriely S., De Wit D., Willems F., Goldman M. IL-23 up-regulates IL-10 and induces IL-17 synthesis by polyclonally activated naive T cells in human. Eur. J. Immunol. 2005, 35:469-475.
44. Volf P., Hajmova M., Sadlova J., Votypka J. Blocked stomodeal valve of the insect vector: similar mechanism of transmission in two trypanosomatid models. Int. J. Parasitol. 2004, 34:1221-1227.
45. Warburg A. The structure of the female sand fly (Phlebotomus papatasi) alimentary canal. Trans. R. Soc. Trop. Med. Hyg. 2008, 102:161-166.