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Research Article

More than just exosomes: distinct Leishmania infantum extracellular products potentiate the establishment of infection

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Article: 1541708 | Received 18 Jun 2018, Accepted 23 Oct 2018, Published online: 08 Nov 2018

References

  • Naderer T, McConville MJ. Intracellular growth and pathogenesis of Leishmania parasites. Essays Biochem. 2011;51:81–15. bse0510081 [pii]. PubMed PMID: 22023443; eng.
  • WHO. Leishmaniasis, Fact sheet N°375 2014. [cited 2015 Jan 19].
  • Cecilio P, Oliveira F, Cordeiro-da-Silva A. Vaccines for human leishmaniasis: where do we stand and what is still missing? In: Afrin F, editor. Leishmaniases as re-emerging diseases. Rijeka: IntechOpen; 2018: 59–93.
  • Loria-Cervera EN, Andrade-Narvaez FJ. Animal models for the study of leishmaniasis immunology. Rev Inst Med Trop Sao Paulo. 2014 Jan–Feb;56(1): 1–11.
  • Cecilio P, Perez-Cabezas B, Santarem N, et al. Deception and manipulation: the arms of leishmania, a successful parasite. Front Immunol. 2014;5:480. PubMed PMID: 25368612; PubMed Central PMCID: PMC4202772. eng
  • Teixeira C, Gomes R, Oliveira F, et al. Characterization of the early inflammatory infiltrate at the feeding site of infected sand flies in mice protected from vector-transmitted Leishmania major by exposure to uninfected bites. PLoS Negl Trop Dis. 2014 Apr;8(4):e2781. PubMed PMID: 24762408; PubMed Central PMCID: PMCPMC3998922.
  • Rogers ME, Corware K, Muller I, et al. Leishmania infantum proteophosphoglycans regurgitated by the bite of its natural sand fly vector, Lutzomyia longipalpis, promote parasite establishment in mouse skin and skin-distant tissues. Microbes Infect. 2010 Oct;12(11):875–879. PubMed PMID: 20561596; eng.
  • Atayde VD, Aslan H, Townsend S, et al. Exosome secretion by the parasitic protozoan leishmania within the sand fly midgut. Cell Rep. 2015 Nov 3;13(5):957–967. PubMed PMID: 26565909; PubMed Central PMCID: PMC4644496. eng.
  • Santarem N, Racine G, Silvestre R, et al. Exoproteome dynamics in Leishmania infantum. J Proteomics. 2013 Jun 12;84:106–118. PubMed PMID: 23558030; eng.
  • Halle M, Gomez MA, Stuible M, et al. The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. J Biol Chem. 2009 Mar 13;284(11):6893–6908. PubMed PMID: 19064994; PubMed Central PMCID: PMC2652307. eng.
  • Jaramillo M, Gomez MA, Larsson O, et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe. 2011 Apr 21;9(4):331–341. PubMed PMID: 21501832; eng.
  • Silverman JM, Clos J, de’Oliveira CC, et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci. 2010 Mar 15;123(Pt 6):842–852. PubMed PMID: 20159964; eng.
  • Silverman JM, Reiner NE. Leishmania exosomes deliver preemptive strikes to create an environment permissive for early infection. Front Cell Infect Microbiol. 2011;1:26. . PubMed PMID: 22919591; PubMed Central PMCID: PMC3417360. eng
  • Atayde VD, Hassani K, Da Silva Lira Filho A, et al. Leishmania exosomes and other virulence factors: impact on innate immune response and macrophage functions. Cell Immunol. 2016 Nov;309:7–18. PubMed PMID: 27499212.
  • Marshall S, Kelly PH, Bk S, et al. Extracellular release of virulence factor major surface protease via exosomes in Leishmania infantum promastigotes. Parasit Vectors. 2018 Jun 19;11(1):355. PubMed PMID: 29921321; PubMed Central PMCID: PMCPMC6006689.
  • Carvalho LP, Passos S, Dutra WO, et al. Effect of LACK and KMP11 on IFN-gamma production by peripheral blood mononuclear cells from cutaneous and mucosal leishmaniasis patients. Scand J Immunol. 2005 Apr;61(4):337–342. PubMed PMID: 15853916; eng.
  • Nandan D, Yi T, Lopez M, et al. Leishmania EF-1alpha activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. J Biol Chem. 2002 Dec 20;277(51):50190–50197. PubMed PMID: 12384497; eng.
  • Nandan D, Tran T, Trinh E, et al. Identification of leishmania fructose-1,6-bisphosphate aldolase as a novel activator of host macrophage Src homology 2 domain containing protein tyrosine phosphatase SHP-1. Biochem Biophys Res Commun. 2007 Dec 21;364(3):601–607. PubMed PMID: 18028878; eng.
  • Yanez-Mo M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066. PubMed PMID: 25979354; PubMed Central PMCID: PMC4433489. eng
  • Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol. 2015 Oct;31(10):477–489. PubMed PMID: 26433251; PubMed Central PMCID: PMCPMC4685040
  • Santarem N, Cunha J, Silvestre R, et al. The impact of distinct culture media in Leishmania infantum biology and infectivity. Parasitology. 2014 Feb;141(2):192–205. PubMed PMID: 24007671; eng.
  • Consortium E-T, Van Deun J, Mestdagh P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017 Feb 28;14(3):228–232. PubMed PMID: 28245209.
  • Edwards JC, Sedgwick AD, Willoughby DA. The formation of a structure with the features of synovial lining by subcutaneous injection of air: an in vivo tissue culture system. J Pathol. 1981 Jun;134(2):147–156. PubMed PMID: 7019400.
  • Matte C, Marquis JF, Blanchette J, et al. Peroxovanadium-mediated protection against murine leishmaniasis: role of the modulation of nitric oxide. Eur J Immunol. 2000 Sep;30(9):2555–2564. PubMed PMID: 11009089.
  • Matte C, Olivier M. Leishmania-induced cellular recruitment during the early inflammatory response: modulation of proinflammatory mediators. J Infect Dis. 2002 Mar 1;185(5):673–681. PubMed PMID: 11865425; eng.
  • Bm N, Silvestre R, Resende M, et al. Activation of phosphatidylinositol 3-kinase/Akt and impairment of nuclear factor-kappaB: molecular mechanisms behind the arrested maturation/activation state of Leishmania infantum-infected dendritic cells. Am J Pathol. 2010 Dec;177(6):2898–2911. PubMed PMID: 21037075; PubMed Central PMCID: PMC2993270. eng.
  • Faria J, Loureiro I, Santarem N, et al. Disclosing the essentiality of ribose-5-phosphate isomerase B in Trypanosomatids. Sci Rep. 2016;6:26937. PubMed PMID: 27230471; PubMed Central PMCID: PMC4882579. eng.
  • Cunha J, Carrillo E, Sanchez C, et al. Characterization of the biology and infectivity of Leishmania infantum viscerotropic and dermotropic strains isolated from HIV+ and HIV- patients in the murine model of visceral leishmaniasis. Parasit Vectors. 2013;6:122. PubMed PMID: 23622683; PubMed Central PMCID: PMCPMC3649922
  • Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A. 2012 Apr;81(4):343–350. PubMed PMID: 22213571; PubMed Central PMCID: PMCPMC3987771
  • Perez-Cabezas B, Cecilio P, Robalo AL, et al. Interleukin-27 early impacts Leishmania infantum infection in mice and correlates with active visceral disease in humans. Front Immunol. 2016;7:478. PubMed PMID: 27867384; PubMed Central PMCID: PMC5095612. eng
  • Silvestre R, Cordeiro-Da-Silva A, Santarem N, et al. SIR2-deficient Leishmania infantum induces a defined IFN-gamma/IL-10 pattern that correlates with protection. J Immunol. 2007 Sep 1;179(5):3161–3170. PubMed PMID: 17709531.
  • Mathivanan S, Ji H, Rj S. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010 Sep 10;73(10):1907–1920. S1874-3919(10)00184-3 [pii]. PubMed PMID: 20601276; eng.
  • Hassani K, Shio MT, Martel C, et al. Absence of metalloprotease GP63 alters the protein content of leishmania exosomes. PLoS One. 2014;9(4):e95007. PubMed PMID: 24736445; PubMed Central PMCID: PMC3988155. eng
  • Kordelas L, Rebmann V, Ak L, et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia. 2014 Apr;28(4):970–973. PubMed PMID: 24445866; eng.
  • Lambertz U, Oviedo Ovando ME, Vasconcelos EJ, et al. Small RNAs derived from tRNAs and rRNAs are highly enriched in exosomes from both old and new world Leishmania providing evidence for conserved exosomal RNA packaging. BMC Genomics. 2015;16:151. PubMed PMID: 25764986; PubMed Central PMCID: PMC4352550. eng
  • Kimblin N, Peters N, Debrabant A, et al. Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):10125–10130. PubMed PMID: 18626016; PubMed Central PMCID: PMC2481378. eng.
  • Maia C, Seblova V, Sadlova J, et al. Experimental transmission of Leishmania infantum by two major vectors: a comparison between a viscerotropic and a dermotropic strain. PLoS Negl Trop Dis. 2011 Jun;5(6):e1181. PubMed PMID: 21695108; PubMed Central PMCID: PMCPMC3114756.
  • Stamper LW, Patrick RL, Fay MP, et al. Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis. 2011 Aug;5(8):e1288. PubMed PMID: 21886852; PubMed Central PMCID: PMCPMC3160291.
  • Doehl JSP, Bright Z, Dey S, et al. Skin parasite landscape determines host infectiousness in visceral leishmaniasis. Nat Commun. 2017 Jul 5;8(1):57. PubMed PMID: 28680146; PubMed Central PMCID: PMCPMC5498584.
  • Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009 Apr;22(2): 240–273. Table of Contents.
  • Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013 Mar;13(3): 159–175.
  • de Veer MJ, Curtis JM, Baldwin TM, et al. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and toll-like receptor 2 signaling. Eur J Immunol. 2003 Oct;33(10):2822–2831. PubMed PMID: 14515266; eng.
  • Becker I, Salaiza N, Aguirre M, et al. Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol Biochem Parasitol. 2003 Aug 31;130(2):65–74. PubMed PMID: 12946842; eng.
  • Kavoosi G, Ardestani SK, Kariminia A, et al. Leishmania major lipophosphoglycan: discrepancy in toll-like receptor signaling. Exp Parasitol. 2010 Feb;124(2):214–218. PubMed PMID: 19769970; eng.
  • Campos MA, Almeida IC, Takeuchi O, et al. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J Immunol. 2001 Jul 1;167(1):416–423. PubMed PMID: 11418678; eng.
  • Almeida IC, Gazzinelli RT. Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. J Leukoc Biol. 2001 Oct;70(4):467–477. PubMed PMID: 11590183; eng
  • Almeida IC, Camargo MM, Procopio DO, et al. Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents. Embo J. 2000 Apr 3;19(7):1476–1485. PubMed PMID: 10747016; PubMed Central PMCID: PMC310217. eng.
  • Silvestre R, Silva AM, Cordeiro-da-Silva A, et al. The contribution of Toll-like receptor 2 to the innate recognition of a Leishmania infantum silent information regulator 2 protein. Immunology. 2009 Dec;128(4):484–499. PubMed PMID: 19930041; PubMed Central PMCID: PMC2792133. eng.
  • van Zandbergen G, Hermann N, Laufs H, et al. Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes. Infect Immun. 2002 Aug;70(8):4177–4184. PubMed PMID: 12117926; PubMed Central PMCID: PMC128123. eng.
  • Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol. 2008 May;8(5):349–361. PubMed PMID: 18437155; PubMed Central PMCID: PMC2744593. eng. .
  • Vance RE, Hong S, Gronert K, et al. The opportunistic pathogen Pseudomonas aeruginosa carries a secretable arachidonate 15-lipoxygenase. Proc Natl Acad Sci U S A. 2004 Feb 17;101(7):2135–2139. PubMed PMID: 14766977; PubMed Central PMCID: PMC357064. eng.
  • Bannenberg GL, Aliberti J, Hong S, et al. Exogenous pathogen and plant 15-lipoxygenase initiate endogenous lipoxin A4 biosynthesis. J Exp Med. 2004 Feb 16;199(4):515–523. PubMed PMID: 14970178; PubMed Central PMCID: PMC2211821. eng.
  • Wenzel A, Van Zandbergen G. Lipoxin A4 receptor dependent leishmania infection. Autoimmunity. 2009 May;42(4):331–333. PubMed PMID: 19811292; eng
  • van Zandbergen G, Bollinger A, Wenzel A, et al. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13837–13842. PubMed PMID: 16945916; PubMed Central PMCID: PMCPMC1564231.
  • Gyorgy B, Szabo TG, Pasztoi M, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011 Aug;68(16):2667–2688. PubMed PMID: 21560073; PubMed Central PMCID: PMCPMC3142546.
  • Chaput N, Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol. 2011 Sep;33(5):419–440. PubMed PMID: 21174094
  • Birge RB, Boeltz S, Kumar S, et al. Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer. Cell Death Differ. 2016 Jun;23(6):962–978. PubMed PMID: 26915293; PubMed Central PMCID: PMCPMC4987730.
  • Hochreiter-Hufford A, Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol. 2013 Jan 01;5(1):a008748. PubMed PMID: 23284042; PubMed Central PMCID: PMCPMC3579390.
  • Park SY, Kim IS. Engulfment signals and the phagocytic machinery for apoptotic cell clearance. Exp Mol Med. 2017 May 12;49(5):e331. PubMed PMID: 28496201; PubMed Central PMCID: PMCPMC5454446.
  • Santarem N, Silvestre R, Tavares J, et al. Immune response regulation by leishmania secreted and nonsecreted antigens. J Biomed Biotechnol. 2007;2007(6):85154. PubMed PMID: 17710243; PubMed Central PMCID: PMC1940321. eng
  • Chang KP, Reed SG, McGwire BS, et al. Leishmania model for microbial virulence: the relevance of parasite multiplication and pathoantigenicity. Acta Trop. 2003 Mar;85(3):375–390. S0001706X02002383 [pii]. PubMed PMID: 12659975; eng.
  • Gomez MA, Contreras I, Halle M, et al. Leishmania GP63 alters host signaling through cleavage-activated protein tyrosine phosphatases. Sci Signal. 2009;2(90):ra58. PubMed PMID: 19797268; eng.
  • Contreras I, Gomez MA, Nguyen O, et al. Leishmania-induced inactivation of the macrophage transcription factor AP-1 is mediated by the parasite metalloprotease GP63. PLoS Pathog. 2010;6(10):e1001148. PubMed PMID: 20976196; PubMed Central PMCID: PMC2954837. eng
  • Descoteaux A, Matlashewski G, Turco SJ. Inhibition of macrophage protein kinase C-mediated protein phosphorylation by Leishmania donovani lipophosphoglycan. J Immunol. 1992 Nov 1;149(9):3008–3015. PubMed PMID: 1383336; eng
  • Lodge R, Descoteaux A. Modulation of phagolysosome biogenesis by the lipophosphoglycan of Leishmania. Clin Immunol. 2005 Mar;114(3): 256–265.
  • Dermine JF, Goyette G, Houde M, et al. Leishmania donovani lipophosphoglycan disrupts phagosome microdomains in J774 macrophages. Cell Microbiol. 2005 Sep;7(9):1263–1270. PubMed PMID: 16098214; eng.
  • Olekhnovitch R, Ryffel B, Muller AJ, et al. Collective nitric oxide production provides tissue-wide immunity during Leishmania infection. J Clin Invest. 2014 Apr;124(4):1711–1722. PubMed PMID: 24614106; PubMed Central PMCID: PMC3973105. eng.