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Experimental parasitology2018; 195; 24-33; doi: 10.1016/j.exppara.2018.09.017

Lipoproteins from vertebrate host blood plasma are involved in Trypanosoma cruzi epimastigote agglutination and participate in interaction with the vector insect, Rhodnius prolixus.

Abstract: Chagas disease, infecting ca. 8 million people in Central and South America, is mediated by the protozoan parasite, Trypanosoma cruzi. The parasite is transmitted by the bite of blood sucking triatomine insects, such as Rhodnius prolixus, that had previously fed on parasite-infected vertebrate blood and voided their contaminated feces and urine into the wound. The stages of the parasite life cycle in both the insect vector and human host are well-known, but determinants of infection in the insect gut are complex and enigmatic. This paper examines the possible role of the R. prolixus gut agglutinins in the parasite life cycle. The results, derived from gut extracts made from R. prolixus fed on various diets with different vertebrate blood components, and cross adsorption experiments, showed for the first time that R. prolixus has two distinct gut agglutinins originating from their vertebrate blood meal, one for T. cruzi (the parasite agglutinin, PA) and the other for the erythrocytes (the hemagglutinin, HA). Again, uniquely, the results also demonstrate that these two agglutinins are derived, respectively, from the plasma and erythrocyte components of the vertebrate blood. Subsequent experiments, examining in more detail the nature of the plasma components forming the T. cruzi PA, used fractionated extracts of the vertebrate plasma (high density lipoprotein, HDL; low density lipoprotein, LDL, and delipidated plasma) in agglutination assays. The results confirmed the identity of the PA as a high density lipoprotein (HDL) in the plasma of the vertebrate blood meal which agglutinates parasites in the R. prolixus gut. In addition, the use of single or double labeled HDL in fluorescence and confocal microscopy showed the interaction of the labeled HDL with the parasite surface and its internalization at later times. Finally, results of T. cruzi parasitization of R. prolixus, incorporating various vertebrate blood components, resulted in highly significant increases in infectivity in the presence of HDL from the 2nd day of infection, thus confirming the important role of this molecule in T. cruzi infection of R. prolixus.
Publication Date: 2018-09-24 PubMed ID: 30261188DOI: 10.1016/j.exppara.2018.09.017Google Scholar: Lookup
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  • Journal Article

Summary

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This study explores the role of high-density lipoprotein (HDL) from vertebrate host blood in promoting the infection of the insect Rhodnius prolixus by the parasite Trypanosoma cruzi, which causes Chagas disease. The evidence suggests that HDL enhances the parasites’ ability to infect the insect, leading to a higher rate of transmission of the disease.

Background and Objective

  • Chagas disease, which affects about 8 million people in Central and South America, is caused by a protozoan parasite, Trypanosoma cruzi.
  • The parasite’s transmission is through the bite of blood-sucking triatomine insects, such as Rhodnius prolixus.
  • While the stages of the parasite’s life cycle in both the insect vector and human host are understood, the factors influencing the parasite’s infection within the insect gut remain unclear.
  • This research investigates the potential role of gut agglutinins in Rhodnius prolixus in the life cycle of the parasite.

Methodology

  • The researchers examined gut extracts from Rhodnius prolixus that were fed on various diets involving different components of vertebrate blood.
  • They conducted cross-adsorption experiments and utilized agglutination assays with fractionated extracts of vertebrate plasma.
  • The team used fluorescence and confocal microscopy with singly or doubly labeled HDL to trace the interaction between the labeled HDL and the parasite.
  • Experiments regarding the parasitization of Rhodnius prolixus by Trypanosoma cruzi were carried out with different vertebrate blood components.

Findings

  • It was found that Rhodnius prolixus has two distinct types of agglutinins in its gut; one for Trypanosoma cruzi (termed the parasite agglutinin or PA) and the other for erythrocytes (referred to as the hemagglutinin or HA).
  • These gut agglutinins are derived from the plasma and erythrocyte components of the blood meal the insect consumes.
  • The identity of the PA was determined to be high-density lipoprotein (HDL) found in the plasma of the vertebrate blood meal.
  • The HDL binds to the surface of the parasite and is internalized over time. This facilitates the infection of Rhodnius prolixus by enhancing the parasites’ capacity to adhere and multiply in the insect’s gut.

Conclusion

  • The results highlight the significant role of HDL in increasing the infectivity of Trypanosoma cruzi in Rhodnius prolixus, in turn promoting the transmission of Chagas disease.
  • This finding is critical to understanding the complex interactions within the insect vector that influence the prevalence of this disease.

Cite This Article

APA
Moreira CJC, De Cicco NNT, Galdino TS, Feder D, Gonzalez MS, Miguel RB, Coura JR, Castro HC, Azambuja P, Atella GC, Ratcliffe NA, Mello CB. (2018). Lipoproteins from vertebrate host blood plasma are involved in Trypanosoma cruzi epimastigote agglutination and participate in interaction with the vector insect, Rhodnius prolixus. Exp Parasitol, 195, 24-33. https://doi.org/10.1016/j.exppara.2018.09.017

Publication

ISSN: 1090-2449
NlmUniqueID: 0370713
Country: United States
Language: English
Volume: 195
Pages: 24-33
PII: S0014-4894(18)30012-2

Researcher Affiliations

Moreira, Carlos José De Carvalho
  • Laboratory of Parasitic Diseases- IOC/ FIOCRUZ, Rio de Janeiro, Brazil.
De Cicco, Nuccia Nicole Theodoro
  • Laboratory of Lipid and Lipoprotein Biochemistry, Institute of Medical Biochemistry- UFRJ, Rio de Janeiro, Brazil.
Galdino, Tainah Silva
  • Laboratório Interdisciplinar de Pesquisas Médicas, IOC/FIOCRUZ, Rio de Janeiro, Brazil.
Feder, Denise
  • Laboratório de Biologia de Insetos - UFF, Niterói, RJ, Brazil.
Gonzalez, Marcelo Salabert
  • Laboratório de Biologia de Insetos - UFF, Niterói, RJ, Brazil.
Miguel, Renata Bortolasse
  • Laboratory of Parasitic Diseases- IOC/ FIOCRUZ, Rio de Janeiro, Brazil.
Coura, José Rodrigues
  • Laboratory of Parasitic Diseases- IOC/ FIOCRUZ, Rio de Janeiro, Brazil.
Castro, Helena Carla
  • Laboratório de Antibióticos, Bioquímica e Modelagem Molecular, - UFF, Niterói, RJ, Brazil.
Azambuja, Patricia
  • Laboratory of Biochemistry and Physiology of Insects- IOC/FIOCRUZ, Rio de Janeiro, Brazil.
Atella, Georgia Corrêa
  • Laboratory of Lipid and Lipoprotein Biochemistry, Institute of Medical Biochemistry- UFRJ, Rio de Janeiro, Brazil.
Ratcliffe, Norman Arthur
  • Laboratório de Biologia de Insetos - UFF, Niterói, RJ, Brazil; Department of Biosciences, Swansea University, Singleton Park, Swansea, SA28PP, Wales, UK.
Mello, Cicero Brasileiro
  • Laboratório de Biologia de Insetos - UFF, Niterói, RJ, Brazil. Electronic address: cicerobrasileiro@id.uff.br.

MeSH Terms

  • Agglutination
  • Agglutinins / blood
  • Agglutinins / physiology
  • Animals
  • Chagas Disease / blood
  • Chagas Disease / parasitology
  • Chagas Disease / transmission
  • Chickens
  • Erythrocytes / chemistry
  • Erythrocytes / parasitology
  • Hemagglutination
  • Horses
  • Humans
  • Insect Vectors / parasitology
  • Lipoproteins / blood
  • Lipoproteins / physiology
  • Rabbits
  • Rhodnius / parasitology
  • Sheep
  • Trypanosoma cruzi / physiology

Citations

This article has been cited 3 times.
  1. Gumiel M, de Mattos DP, Vieira CS, Moraes CS, Moreira CJC, Gonzalez MS, Teixeira-Ferreira A, Waghabi M, Azambuja P, Carels N. Proteome of the Triatomine Digestive Tract: From Catalytic to Immune Pathways; Focusing on Annexin Expression.. Front Mol Biosci 2020;7:589435.
    doi: 10.3389/fmolb.2020.589435pubmed: 33363206google scholar: lookup
  2. O'Neal AJ, Butler LR, Rolandelli A, Gilk SD, Pedra JH. Lipid hijacking: a unifying theme in vector-borne diseases.. Elife 2020 Oct 29;9.
    doi: 10.7554/eLife.61675pubmed: 33118933google scholar: lookup
  3. Cámara MLM, Balouz V, Centeno Cameán C, Cori CR, Kashiwagi GA, Gil SA, Macchiaverna NP, Cardinal MV, Guaimas F, Lobo MM, de Lederkremer RM, Gallo-Rodriguez C, Buscaglia CA. Trypanosoma cruzi surface mucins are involved in the attachment to the Triatoma infestans rectal ampoule.. PLoS Negl Trop Dis 2019 May;13(5):e0007418.
    doi: 10.1371/journal.pntd.0007418pubmed: 31107901google scholar: lookup