Phenotypical Differences between Leishmania (Leishmania) amazonensis PH8 and LV79 Strains May Impact Survival in Mammal Host and in Phlebotomine Sand Flies
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
2018/14972-8 and 2021/08915-4 (to BSS) and 2017/26197-6 (to FTT)
Fundacao de Amparo a Pesquisa do Estado de Sao Paulo
PROEX 88882.333060/2010-01
Coordenação de Aperfeicoamento de Pessoal de Nível Superior
INCT-EM 465678/2014-9 (to YMTC)
Conselho Nacional de Desenvolvimento Científico e Tecnológico
PubMed
36839445
PubMed Central
PMC9965022
DOI
10.3390/pathogens12020173
PII: pathogens12020173
Knihovny.cz E-zdroje
- Klíčová slova
- L. (L.) amazonensis, LPG, complement, infection, sand fly, virulence,
- Publikační typ
- časopisecké články MeSH
We previously showed that L. (Leishmania) amazonensis promastigotes and amastigotes of the PH8 strain generated larger lesions in mice than LV79, and that lesion-derived amastigotes from the two strains differ in their proteomes. We recently reported that PH8 promastigotes are more phagocytized by macrophages. Promastigotes' membrane-enriched proteomes showed several differences, and samples of each strain clustered based on proteomes. In this paper, we show phenotypic differences between PH8 and LV79 promastigotes that may explain the higher virulence of PH8. We compared in vitro macrophage infections by day 4 (early) and day 6 (late stationary phase) cultures, resistance to complement, and LPG characteristics. PH8 promastigotes showed a higher infectivity and were more resistant to murine complement. LPG was different between the strains, which may influence the interaction with macrophages and survival to complement. We compared the infection of the permissive vector Lutzomyia longipalpis. PH8 was more abundant in the vector's gut 72 h after feeding, which is a moment where blood digestion is finished and the parasites are exposed to the gut environment. Our results indicate that PH8 promastigotes are more infective, more resistant to complement, and infect the permissive vector more efficiently. These data suggest that PH8 is probably better adapted to the sand fly and more prone to survive in the vertebrate host.
Biotechnology Applied to Pathogens Belo Horizonte 30000 000 MG Brazil
Department of Parasitology Faculty of Science Charles University 12844 Prague Czech Republic
Zobrazit více v PubMed
Kaye P.M., Cruz I., Picado A., Van Bocxlaer K., Croft S.L. Leishmaniasis immunopathology—Impact on design and use of vaccines, diagnostics and drugs. Semin. Immunopathol. 2020;42:247–264. doi: 10.1007/s00281-020-00788-y. PubMed DOI
Ruiz-Postigo J.A., Jain S., Mikhailov A., Maia-Elkhoury A.N., Valadas S., Warusavithana S., Osman M., Lin Z., Beshah A., Yajima A., et al. Global Leishmaniasis Surveillance: 2019–2020, a Baseline for the 2030 Roadmap. WHO; Geneva, Switzerland: 2021.
Podinovskaia M., Descoteaux A. Leishmania and the macrophage: A multifaceted interaction. Futur. Microbiol. 2015;10:111–129. doi: 10.2217/fmb.14.103. PubMed DOI
Velasquez L.G., Galuppo M.K., De Rezende E., Brandão W.N., Peron J.P., Uliana S.R.B., Duarte M.I., Stolf B.S. Distinct courses of infection with Leishmania (L.) amazonensis are observed in BALB/c, BALB/c nude and C57BL/6 mice. Parasitology. 2016;143:692–703. doi: 10.1017/S003118201600024X. PubMed DOI
de Rezende E., Kawahara R., Peña M.S., Palmisano G., Stolf B.S. Quantitative proteomic analysis of amastigotes from Leishmania (L.) amazonensis LV79 and PH8 strains reveals molecular traits associated with the virulence phenotype. PLoS Negl. Trop. Dis. 2017;11:e0006090. doi: 10.1371/journal.pntd.0006090. PubMed DOI PMC
Volpedo G., Pacheco-Fernandez T., Holcomb E.A., Cipriano N., Cox B., Satoskar A.R. Mechanisms of Immunopathogenesis in Cutaneous Leishmaniasis and Post Kala-azar Dermal Leishmaniasis (PKDL) Front. Cell. Infect. Microbiol. 2021;11:685296. doi: 10.3389/fcimb.2021.685296. PubMed DOI PMC
Cupolillo E., Medina-Acosta E., Noyes H., Momen H., Grimaldi G., Jr. A Revised Classification for Leishmania and Endotrypanum. Parasitol. Today. 2000;16:142–144. doi: 10.1016/S0169-4758(99)01609-9. PubMed DOI
Akhoundi M., Kuhls K., Cannet A., Votypka J., Marty P., Delaunay P., Sereno D. A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies. PLoS Negl. Trop. Dis. 2016;10:e0004349. doi: 10.1371/journal.pntd.0004349. PubMed DOI PMC
Espinosa O.A., Serrano M.G., Camargo E.P., Teixeira M.M.G., Shaw J.J. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018;145:430–442. doi: 10.1017/S0031182016002092. PubMed DOI
Kevric I., Cappel M.A., Keeling J.H. New World and Old World Leishmania Infections: A Practical Review. Dermatol. Clin. 2015;33:579–593. doi: 10.1016/j.det.2015.03.018. PubMed DOI
Dostálová A., Volf P. Leishmania development in sand flies: Parasite-vector interactions overview. Parasites Vectors. 2012;5:276. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC
Al-Khalaifah H.S. Major Molecular Factors Related to Leishmania Pathogenicity. Front. Immunol. 2022;13:847797. doi: 10.3389/fimmu.2022.847797. PubMed DOI PMC
Brittingham A., Morrison C.J., McMaster W.R., McGwire B.S., Chang K.P., Mosser D.M. Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J. Immunol. 1995;155:3102–3111. doi: 10.4049/jimmunol.155.6.3102. PubMed DOI
Sacks D.L., Modi G., Rowton E., Spath G., Epstein L., Turco S.J., Beverley S.M. The role of phosphoglycans in Leishmania-sand fly interactions. Proc. Natl. Acad. Sci. USA. 2000;97:406–411. doi: 10.1073/pnas.97.1.406. PubMed DOI PMC
Chang K.-P., Reed S.G., McGwire B.S., Soong L. Leishmania model for microbial virulence: The relevance of parasite multiplication and pathoantigenicity. Acta Trop. 2003;85:375–390. doi: 10.1016/S0001-706X(02)00238-3. PubMed DOI
Späth G.F., Garraway L.A., Turco S.J., Beverley S.M. The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc. Natl. Acad. Sci. USA. 2003;100:9536–9541. doi: 10.1073/pnas.1530604100. PubMed DOI PMC
Yao C., Donelson J.E., Wilson M.E. The major surface protease (MSP or GP63) of Leishmania sp. Biosynthesis, regulation of expression, and function. Mol. Biochem. Parasitol. 2003;132:1–16. doi: 10.1016/S0166-6851(03)00211-1. PubMed DOI
Svárovská A., Ant T.H., Seblová V., Jecná L., Beverley S., Volf P. Leishmania major Glycosylation Mutants Require Phosphoglycans (lpg2−) but Not Lipophosphoglycan (lpg1−) for Survival in Permissive Sand Fly Vectors. PLoS Negl. Trop. Dis. 2010;4:e580. doi: 10.1371/journal.pntd.0000580. PubMed DOI PMC
Mosser D.M., Edelson P.J. The mouse macrophage receptor for C3bi (CR3) is a major mechanism in the phagocytosis of Leish-mania promastigotes. J. Immunol. 1985;135:2785–2789. doi: 10.4049/jimmunol.135.4.2785. PubMed DOI
Atayde V.D., Hassani K., da Silva Lira Filho A., Borges A.R., Adhikari A., Martel C., Olivier M. Leishmania exosomes and other virulence factors: Impact on innate immune response and macrophage functions. Cell. Immunol. 2016;309:7–18. doi: 10.1016/j.cellimm.2016.07.013. PubMed DOI
McGwire B.S., Chang K.-P., Engman D.M. Migration through the Extracellular Matrix by the Parasitic Protozoan Leishmania Is Enhanced by Surface Metalloprotease gp63. Infect. Immun. 2003;71:1008–1010. doi: 10.1128/IAI.71.2.1008-1010.2003. PubMed DOI PMC
Puentes S.M., Sacks D.L., Da Silva R.P., Joiner K. Complement binding by two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. J. Exp. Med. 1988;167:887–902. doi: 10.1084/jem.167.3.887. PubMed DOI PMC
Sacks D.L., Brodin T.N., Turco S.J. Developmental modification of the lipophosphoglycan from Leishmania major promastigotes during metacyclogenesis. Mol. Biochem. Parasitol. 1990;42:225–233. doi: 10.1016/0166-6851(90)90165-I. PubMed DOI
Talamas-Rohana P., Wright S.D., Lennartz M.R., Russell D.G. Lipophosphoglycan from Leishmania mexicana promastigotes binds to members of the CR3, p150,95 and LFA-1 family of leukocyte integrins. J. Immunol. 1990;144:4817–4824. doi: 10.4049/jimmunol.144.12.4817. PubMed DOI
Kamhawi S., Ramalho-Ortigao M., Pham V.M., Kumar S., Lawyer P.G., Turco S.J., Barillas-Mury C., Sacks D.L., Valenzuela J.G. A role for insect galectins in parasite survival. Cell. 2004;119:329–341. doi: 10.1016/j.cell.2004.10.009. PubMed DOI
Coutinho-Abreu I.V., Oristian J., de Castro W., Wilson T.R., Meneses C., Soares R.P., Borges V.M., Descoteaux A., Kamhawi S., Valenzuela J.G. Binding of Leishmania infantum Lipophosphoglycan to the Midgut Is Not Sufficient to Define Vector Competence in Lutzomyia longipalpis Sand Flies. Msphere. 2020;5:e00594-20. doi: 10.1128/mSphere.00594-20. PubMed DOI PMC
Nogueira P.M., Assis R.R., Torrecilhas A.C., Saraiva E.M., Pessoa N.L., Campos M.A., Marialva E.F., Ríos-Velasquez C.M., Pessoa F.A., Secundino N.F., et al. Lipophosphoglycans from Leishmania amazonensis Strains Display Immunomodulatory Properties via TLR4 and Do Not Affect Sand Fly Infection. PLoS Negl. Trop. Dis. 2016;10:e0004848. doi: 10.1371/journal.pntd.0004848. PubMed DOI PMC
Nogueira P.M., Guimarães A.C., Assis R.R., Sadlova J., Myskova J., Pruzinova K., Hlavackova J., Turco S.J., Torrecilhas A.C., Volf P., et al. Lipophosphoglycan polymorphisms do not affect Leishmania amazonensis development in the permissive vectors Lutzomyia migonei and Lutzomyia longipalpis. Parasites Vectors. 2017;10:608. doi: 10.1186/s13071-017-2568-8. PubMed DOI PMC
Coelho-Finamore J., Freitas V., Assis R., Melo M., Novozhilova N., Secundino N., Pimenta P., Turco S., Soares R. Leishmania infantum: Lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. Int. J. Parasitol. 2010;41:333–342. doi: 10.1016/j.ijpara.2010.10.004. PubMed DOI
Guimarães A.C., Nogueira P.M., Silva S.D.O., Sadlova J., Pruzinova K., Hlaváčová J., Melo M.N., Soares R.P. Lower galactosylation levels of the Lipophosphoglycan from Leishmania (Leishmania) major-like strains affect interaction with Phlebotomus papatasi and Lutzomyia longipalpis. Mem. Inst. Oswaldo Cruz. 2018;113:e170333. doi: 10.1590/0074-02760170333. PubMed DOI PMC
Scorza B.M., Carvalho E.M., Wilson M.E. Cutaneous Manifestations of Human and Murine Leishmaniasis. Int. J. Mol. Sci. 2017;18:1296. doi: 10.3390/ijms18061296. PubMed DOI PMC
Silveira F.T., Lainson R., Corbett C.E.P. Clinical and immunopathological spectrum of American cutaneous leishmaniasis with special reference to the disease in Amazonian Brazil: A review. Mem. Inst. Oswaldo Cruz. 2004;99:239–251. doi: 10.1590/S0074-02762004000300001. PubMed DOI
Valdivia H.O., Almeida L.V., Roatt B.M., Reis-Cunha J.L., Pereira A.A.S., Gontijo C., Fujiwara R.T., Reis A.B., Sanders M.J., Cotton J.A., et al. Comparative genomics of canine-isolated Leishmania (Leishmania) amazonensis from an endemic focus of visceral leishmaniasis in Governador Valadares, southeastern Brazil. Sci. Rep. 2017;7:40804. doi: 10.1038/srep40804. PubMed DOI PMC
Lainson R., Shaw J.J., Silveira F., De Souza A.A.A., Braga R.R., Ishikawa E.A.Y. The dermal leishmaniases of Brazil, with special reference to the eco-epidemiology of the disease in Amazonia. Mem. Inst. Oswaldo Cruz. 1994;89:435–443. doi: 10.1590/S0074-02761994000300027. PubMed DOI
Tano F.T., Barbosa G.R., de Rezende E., Souza R.O.O., Muxel S.M., Silber A.M., Palmisano G., Stolf B.S. Proteome and morphological analysis show unexpected differences between promastigotes of Leishmania amazonensis PH8 and LV79 strains. PLoS ONE. 2022;17:e0271492. doi: 10.1371/journal.pone.0271492. PubMed DOI PMC
Soares R.P., Barron T., McCoy-Simandle K., Svobodova M., Warburg A., Turco S.J. Leishmania tropica: Intraspecific polymorphisms in lipophosphoglycan correlate with transmission by different Phlebotomus species. Exp. Parasitol. 2004;107:105–114. doi: 10.1016/j.exppara.2004.05.001. PubMed DOI
Ueno N., Wilson M.E. Receptor-mediated phagocytosis of Leishmania: Implications for intracellular survival. Trends Parasitol. 2012;28:335–344. doi: 10.1016/j.pt.2012.05.002. PubMed DOI PMC
Lincoln L.M., Ozaki M., Donelson J.E., Beetham J.K. Genetic complementation of Leishmania deficient in PSA (GP46) restores their resistance to lysis by complement. Mol. Biochem. Parasitol. 2004;137:185–189. doi: 10.1016/j.molbiopara.2004.05.004. PubMed DOI
Rego F.D., Cardoso C.D.A., Moreira P.O.L., Nogueira P.M., Araujo M.S., Borges V.M., Laurenti M.D., Bartholomeu D.C., Reis A.B., Monte-Neto R.L.D., et al. Leishmania amazonensis from distinct clinical forms/hosts has polymorphisms in Lipophosphoglycans, displays variations in immunomodulatory properties and, susceptibility to antileishmanial drugs. Cell Biol. Int. 2022;46:1947–1958. doi: 10.1002/cbin.11880. PubMed DOI PMC
Telleria E.L., Martins-Da-Silva A., Tempone A.J., Traub-Csekö Y.M. Leishmania, microbiota and sand fly immunity. Parasitology. 2018;145:1336–1353. doi: 10.1017/S0031182018001014. PubMed DOI PMC
Manzano J.I., Perea A., León-Guerrero D., Campos-Salinas J., Piacenza L., Castanys S., Gamarro F. Leishmania LABCG1 and LABCG2 transporters are involved in virulence and oxidative stress: Functional linkage with autophagy. Parasites Vectors. 2017;10:267. doi: 10.1186/s13071-017-2198-1. PubMed DOI PMC
Ong G.L., Mattes M. Mouse strains with typical mammalian levels of complement activity. J. Immunol. Methods. 1989;125:147–158. doi: 10.1016/0022-1759(89)90088-4. PubMed DOI
Cardoso C.A., Araujo G.V., Sandoval C.M., Nogueira P.M., Zúniga C., Sosa-Ochoa W.H., Laurenti M.D., Soares R.P. Lipophosphoglycans from dermotropic Leishmania infantum are more pro-inflammatory than those from viscerotropic strains. Mem. Inst. Oswaldo Cruz. 2020;115:e200140. doi: 10.1590/0074-02760200140. PubMed DOI PMC
Assis R.R., Ibraim I.C., Noronha F.S., Turco S.J., Soares R.P. Glycoinositolphospholipids from Leishmania braziliensis and L. infantum: Modulation of Innate Immune System and Variations in Carbohydrate Structure. PLoS Negl. Trop. Dis. 2012;6:e1543. doi: 10.1371/journal.pntd.0001543. PubMed DOI PMC
Paranaíba L.F., de Assis R.R., Nogueira P.M., Torrecilhas A.C., Campos J.H., Silveira A.C.D.O., Martins-Filho O.A., Pessoa N.L., Campos M.A., Parreiras P.M., et al. Leishmania enriettii: Biochemical characterisation of lipophosphoglycans (LPGs) and glycoinositolphospholipids (GIPLs) and infectivity to Cavia porcellus. Parasites Vectors. 2015;8:31. doi: 10.1186/s13071-015-0633-8. PubMed DOI PMC
Vieira T.D.S., Rugani J.N., Nogueira P.M., Torrecilhas A.C., Gontijo C.M.F., Descoteaux A., Soares R.P. Intraspecies Polymorphisms in the Lipophosphoglycan of L. braziliensis Differentially Modulate Macrophage Activation via TLR4. Front. Cell. Infect. Microbiol. 2019;9:240. doi: 10.3389/fcimb.2019.00240. PubMed DOI PMC
Proudfoot L., Nikolaev A.V., Feng G.J., Wei W.Q., Ferguson M.A., Brimacombe J.S., Liew F.Y. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA. 1996;93:10984–10989. doi: 10.1073/pnas.93.20.10984. PubMed DOI PMC
Telleria E.L., Azevedo-Brito D.A., Kykalová B., Tinoco-Nunes B., Pitaluga A.N., Volf P., Traub-Csekö Y.M. Leishmania infantum Infection Modulates the Jak-STAT Pathway in Lutzomyia longipalpis LL5 Embryonic Cells and Adult Females, and Affects Parasite Growth in the Sand Fly. Front. Trop. Dis. 2021;2:747820. doi: 10.3389/fitd.2021.747820. DOI
Telleria E.L., Sant’Anna M.R., Ortigão-Farias J.R., Pitaluga A.N., Dillon V.M., Bates P.A., Traub-Csekö Y.M., Dillon R.J. Caspar-like Gene Depletion Reduces Leishmania Infection in Sand Fly Host Lutzomyia longipalpis. J. Biol. Chem. 2012;287:12985–12993. doi: 10.1074/jbc.M111.331561. PubMed DOI PMC
Di-Blasi T., Telleria E.L., Marques C., Couto R.D.M., Da Silva-Neves M., Jančářová M., Volf P., Tempone A.J., Traub-Csekö Y.M. Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector. Front. Cell. Infect. Microbiol. 2019;9:71. doi: 10.3389/fcimb.2019.00071. PubMed DOI PMC