Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands.
<h4>Background</h4>Rhodnius prolixus is a blood-sucking bug vector of Trypanosoma cruzi and T. rangeli. T. cruzi is transmitted by vector feces deposited close to the wound produced by insect mouthparts, whereas T. rangeli invades salivary glands and is inoculated into the host skin. Bug...
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oai:doaj.org-article:8a2fb4638f134bb5a69ce8f3b05386ce2021-11-18T08:12:00ZGlycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands.1932-620310.1371/journal.pone.0047285https://doaj.org/article/8a2fb4638f134bb5a69ce8f3b05386ce2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23077586/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Rhodnius prolixus is a blood-sucking bug vector of Trypanosoma cruzi and T. rangeli. T. cruzi is transmitted by vector feces deposited close to the wound produced by insect mouthparts, whereas T. rangeli invades salivary glands and is inoculated into the host skin. Bug saliva contains a set of nitric oxide-binding proteins, called nitrophorins, which deliver NO to host vessels and ensure vasodilation and blood feeding. NO is generated by nitric oxide synthases (NOS) present in the epithelium of bug salivary glands. Thus, T. rangeli is in close contact with NO while in the salivary glands.<h4>Methodology/principal findings</h4>Here we show by immunohistochemical, biochemical and molecular techniques that inositolphosphate-containing glycolipids from trypanosomatids downregulate NO synthesis in the salivary glands of R. prolixus. Injecting insects with T. rangeli-derived glycoinositolphospholipids (Tr GIPL) or T. cruzi-derived glycoinositolphospholipids (Tc GIPL) specifically decreased NO production. Salivary gland treatment with Tc GIPL blocks NO production without greatly affecting NOS mRNA levels. NOS protein is virtually absent from either Tr GIPL- or Tc GIPL-treated salivary glands. Evaluation of NO synthesis by using a fluorescent NO probe showed that T. rangeli-infected or Tc GIPL-treated glands do not show extensive labeling. The same effect is readily obtained by treatment of salivary glands with the classical protein tyrosine phosphatase (PTP) inhibitor, sodium orthovanadate (SO). This suggests that parasite GIPLs induce the inhibition of a salivary gland PTP. GIPLs specifically suppressed NO production and did not affect other anti-hemostatic properties of saliva, such as the anti-clotting and anti-platelet activities.<h4>Conclusions/significance</h4>Taken together, these data suggest that trypanosomatids have overcome NO generation using their surface GIPLs. Therefore, these molecules ensure parasite survival and may ultimately enhance parasite transmission.Felipe Gazos-LopesRafael Dias MesquitaLívia Silva-CardosoRaquel SennaAlan Barbosa SilveiraWilly JablonkaCecília Oliveira CudischevitchAlan Brito CarneiroEdnildo Alcantara MachadoLuize G LimaRobson Queiroz MonteiroRoberto Henrique NussenzveigEvelize FollyAlexandre RomeiroJorick VanbeselaereLucia Mendonça-PreviatoJosé Osvaldo PreviatoJesus G ValenzuelaJosé Marcos Chaves RibeiroGeorgia Correa AtellaMário Alberto Cardoso Silva-NetoPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 10, p e47285 (2012) |
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Medicine R Science Q Felipe Gazos-Lopes Rafael Dias Mesquita Lívia Silva-Cardoso Raquel Senna Alan Barbosa Silveira Willy Jablonka Cecília Oliveira Cudischevitch Alan Brito Carneiro Ednildo Alcantara Machado Luize G Lima Robson Queiroz Monteiro Roberto Henrique Nussenzveig Evelize Folly Alexandre Romeiro Jorick Vanbeselaere Lucia Mendonça-Previato José Osvaldo Previato Jesus G Valenzuela José Marcos Chaves Ribeiro Georgia Correa Atella Mário Alberto Cardoso Silva-Neto Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| description |
<h4>Background</h4>Rhodnius prolixus is a blood-sucking bug vector of Trypanosoma cruzi and T. rangeli. T. cruzi is transmitted by vector feces deposited close to the wound produced by insect mouthparts, whereas T. rangeli invades salivary glands and is inoculated into the host skin. Bug saliva contains a set of nitric oxide-binding proteins, called nitrophorins, which deliver NO to host vessels and ensure vasodilation and blood feeding. NO is generated by nitric oxide synthases (NOS) present in the epithelium of bug salivary glands. Thus, T. rangeli is in close contact with NO while in the salivary glands.<h4>Methodology/principal findings</h4>Here we show by immunohistochemical, biochemical and molecular techniques that inositolphosphate-containing glycolipids from trypanosomatids downregulate NO synthesis in the salivary glands of R. prolixus. Injecting insects with T. rangeli-derived glycoinositolphospholipids (Tr GIPL) or T. cruzi-derived glycoinositolphospholipids (Tc GIPL) specifically decreased NO production. Salivary gland treatment with Tc GIPL blocks NO production without greatly affecting NOS mRNA levels. NOS protein is virtually absent from either Tr GIPL- or Tc GIPL-treated salivary glands. Evaluation of NO synthesis by using a fluorescent NO probe showed that T. rangeli-infected or Tc GIPL-treated glands do not show extensive labeling. The same effect is readily obtained by treatment of salivary glands with the classical protein tyrosine phosphatase (PTP) inhibitor, sodium orthovanadate (SO). This suggests that parasite GIPLs induce the inhibition of a salivary gland PTP. GIPLs specifically suppressed NO production and did not affect other anti-hemostatic properties of saliva, such as the anti-clotting and anti-platelet activities.<h4>Conclusions/significance</h4>Taken together, these data suggest that trypanosomatids have overcome NO generation using their surface GIPLs. Therefore, these molecules ensure parasite survival and may ultimately enhance parasite transmission. |
| format |
article |
| author |
Felipe Gazos-Lopes Rafael Dias Mesquita Lívia Silva-Cardoso Raquel Senna Alan Barbosa Silveira Willy Jablonka Cecília Oliveira Cudischevitch Alan Brito Carneiro Ednildo Alcantara Machado Luize G Lima Robson Queiroz Monteiro Roberto Henrique Nussenzveig Evelize Folly Alexandre Romeiro Jorick Vanbeselaere Lucia Mendonça-Previato José Osvaldo Previato Jesus G Valenzuela José Marcos Chaves Ribeiro Georgia Correa Atella Mário Alberto Cardoso Silva-Neto |
| author_facet |
Felipe Gazos-Lopes Rafael Dias Mesquita Lívia Silva-Cardoso Raquel Senna Alan Barbosa Silveira Willy Jablonka Cecília Oliveira Cudischevitch Alan Brito Carneiro Ednildo Alcantara Machado Luize G Lima Robson Queiroz Monteiro Roberto Henrique Nussenzveig Evelize Folly Alexandre Romeiro Jorick Vanbeselaere Lucia Mendonça-Previato José Osvaldo Previato Jesus G Valenzuela José Marcos Chaves Ribeiro Georgia Correa Atella Mário Alberto Cardoso Silva-Neto |
| author_sort |
Felipe Gazos-Lopes |
| title |
Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| title_short |
Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| title_full |
Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| title_fullStr |
Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| title_full_unstemmed |
Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. |
| title_sort |
glycoinositolphospholipids from trypanosomatids subvert nitric oxide production in rhodnius prolixus salivary glands. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2012 |
| url |
https://doaj.org/article/8a2fb4638f134bb5a69ce8f3b05386ce |
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