Glycan–glycan interactions determine <i>Leishmania</i> attachment to the midgut of permissive sand fly vectors

Hall, Amy R.; Blakeman, Jamie T; Eissa, Ahmed M.; Chapman, Paul; Morales-García, Ana L.; Stennett, Laura; Martín, Oihane; Giraud, Émilie; Dockrell, David H.; Cameron, Neil R.; Wiese, Martin; Yakob, Laith; Rogers, Matthew E.; Geoghegan, Mark

doi:10.1039/d0sc03298k

Cited by 8 publications

(6 citation statements)

References 63 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Conversely, P. argentipes and P. orientalis are known to be permissive vectors susceptible to multiple Leishmania spp. under laboratory conditions [ 33 ] in which promastigotes attach via a different, glycan-mediated, mechanism [ 39 ]. In both of these sand fly species, the highest infection rates and highest intensities of infections were recorded for L .…”

Section: Discussionmentioning

confidence: 99%

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

et al. 2022

View full text Add to dashboard Cite

Background Species belonging to the subgenus Sauroleishmania are parasites of reptiles, and traditionally considered to be non-pathogenic to mammals. Knowledge of the development of these parasites in sand flies and their mechanism of transmission is currently lacking. The main aim of this study was to test the susceptibility of various sand fly species to infection by two Sauroleishmania species, focusing on the localization of parasites in the sand fly intestinal tract. Methods The development of Leishmania (Sauroleishmania [S.]) adleri and Leishmania (S.) hoogstraali was studied in six sand fly species (Phlebotomus orientalis, P. argentipes, P. sergenti, P. papatasi, P. duboscqi, Sergentomyia schwetzi). Sand flies were fed through a chick-skin membrane on blood containing Sauroleishmania promastigotes, and they were dissected at various time intervals post blood meal (PBM). Guts were examined microscopically for the presence of parasites, and the intensity and localizations of infections were recorded. Morphological forms of both Sauroleishmania species developing in P. orientalis were analyzed. Experimental infections of geckos using sand fly-derived promastigotes were also performed, and the reptiles were repeatedly examined for Sauroleishmania infection by xenodiagnosis and PCR analysis. Results High infection rates for both Sauroleishmania species were observed in P. orientalis and P. argentipes, with the parasites migrating anteriorly and undergoing a peripylarian type of development, including colonization of the stomodeal valve. Conversely, the development of L. (S.) adleri in P. sergenti, P. papatasi and Se. schwetzi was restricted to the sand fly hindgut (hypopylarian type of development). Five morphological forms were distinguished for both Sauroleishmania species developing in P. orientalis. All experimentally infected geckos scored negative for Sauroleishmania based on xenodiagnosis and molecular analysis. Conclusions The results showed that Sauroleishmania promastigotes can undergo either a peripylarian or hypopylarian type of development in the sand fly intestinal tract, depending on the sand fly species infected. We demonstrated that P. argentipes and P. orientalis, two sand fly species known as permissive vectors for mammalian parasites of subgenus Leishmania, are also highly susceptible to Sauroleishmania as the parasites developed mature late-stage infections, including colonization of the sand fly stomodeal valve. Thus, the role of Phlebotomus sand flies in transmission of Sauroleishmania should be reconsidered and further investigated. Graphical Abstract

show abstract

Section: Discussionmentioning

confidence: 99%

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

et al. 2022

View full text Add to dashboard Cite

show abstract

“…The midgut life cycle after a single blood meal Decades of research had established the occurrence of a complex developmental process that involves several well-defined morphological and functional Leishmania stages in the sand fly [1]. Based on experimental studies conducted after a single blood meal, the life cycle of Leishmania parasites in the sand fly midgut was established as follows: amastigotes differentiate into procyclic promastigotes; this parasite stage then transforms to nectomonad promastigotes, large forms that escape the deteriorating peritrophic matrix (PM) and anchor to the insect midgut [1,19,20]. Anchoring to the midgut wall is a crucial event in the parasite life cycle and determines vector competence for restrictive sand fly vectors through parasite lipophosphoglycan (LPG)midgut receptor-specific interactions [1,19].…”

Section: The Critical Role Of Sand Fly Behavior and Blood Acquisition In Leishmania Developmentmentioning

confidence: 99%

“…Based on experimental studies conducted after a single blood meal, the life cycle of Leishmania parasites in the sand fly midgut was established as follows: amastigotes differentiate into procyclic promastigotes; this parasite stage then transforms to nectomonad promastigotes, large forms that escape the deteriorating peritrophic matrix (PM) and anchor to the insect midgut [1,19,20]. Anchoring to the midgut wall is a crucial event in the parasite life cycle and determines vector competence for restrictive sand fly vectors through parasite lipophosphoglycan (LPG)midgut receptor-specific interactions [1,19]. This is less clear for permissive vectors, in which attachment has been proposed to occur through other interactions with O-glycans bearing N-acetyl-D-galactosamine residues that are common on the midgut surface of permissive sand fly vectors [1,19].…”

Section: The Critical Role Of Sand Fly Behavior and Blood Acquisition In Leishmania Developmentmentioning

confidence: 99%

“…Anchoring to the midgut wall is a crucial event in the parasite life cycle and determines vector competence for restrictive sand fly vectors through parasite lipophosphoglycan (LPG)midgut receptor-specific interactions [1,19]. This is less clear for permissive vectors, in which attachment has been proposed to occur through other interactions with O-glycans bearing N-acetyl-D-galactosamine residues that are common on the midgut surface of permissive sand fly vectors [1,19]. However, blocking LuloG, an O-linked glycoprotein in the midgut of Lu.…”

Section: The Critical Role Of Sand Fly Behavior and Blood Acquisition In Leishmania Developmentmentioning

confidence: 99%

See 1 more Smart Citation

Leishmaniasis: the act of transmission

Serafim

Coutinho-Abreu

Dey

et al. 2021

Trends in Parasitology

View full text Add to dashboard Cite

“…Glycans are an important component of both the glycocalyx of cells mucosal surfaces as well as the surface of most bacteria [16]. The existence of glycan-glycan interactions opens for new mechanisms of bacterial adhesion to biological surfaces including mucosal surfaces, as documented in recent publications [17,18]. The role of glycan-glycan interactions in bacterial adhesion has also been reviewed [15,19].…”

Section: Introductionmentioning

confidence: 99%

Elucidating bacterial adhesion to mucosal surface by an original AFM approach

et al. 2021

View full text Add to dashboard Cite

Background Fish skin represents an ancient vertebrate mucosal surface, sharing characteristics with other mucosal surfaces including those of the intestine. The skin mucosa is continuously exposed to microbes in the surrounding water and is therefore important in the first line defense against environmental pathogens by preventing bacteria from accessing the underlying surfaces. Understanding the microbe-host interactions at the fish skin mucosa is highly relevant in order to understand and control infection, commensalism, colonization, persistence, infection, and disease. Here we investigate the interactions between the pathogenic bacteria Aeromonas salmonicida (A. salmonicida) and Yersinia ruckeri (Y. ruckeri), respectively, and the skin mucosal surface of Atlantic salmon fry using AFM force spectroscopy. Results The results obtained revealed that when retracting probes functionalized with bacteria from surfaces coated with immobilized mucins, isolated from salmon mucosal surfaces, rupture events reflecting the disruption of adhesive interactions were observed, with rupture strengths centered around 200 pN. However, when retracting probes functionalized with bacteria from the intact mucosal surface of salmon fish fry no adhesive interactions could be detected. Furthermore, rheological measurements revealed a near fluid-like behavior for the fish fry skin mucus. Taken together, the experimental data indicate that the adhesion between the mucin molecules within the mucous layer may be significantly weaker than the interaction between the bacteria and the mucin molecules. The bacteria, immobilized on the AFM probe, do bind to individual mucins in the mucosal layer, but are released from the near fluid mucus with little resistance upon retraction of the AFM probe, to which they are immobilized. Conclusion The data provided in the current paper reveal that A. salmonicida and Y. ruckeri do bind to the immobilized mucins. However, when retracting the bacteria from intact mucosal surfaces, no adhesive interactions are detected. These observations suggest a mechanism underlying the protective function of the mucosal surface based on the clearing of potential threats by adhering them to loosely attached mucus that is subsequently released from the fish skin.

show abstract

Glycan–glycan interactions determine Leishmania attachment to the midgut of permissive sand fly vectors

Abstract: Direct glycan-glycan interactions are increasingly implicated in survival and pathogenicity of bacteria. Here, we show that they can be exploited by protozoan parasites in their insect hosts. Force spectroscopy revealed...

Cited by 8 publications

References 63 publications

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

Leishmaniasis: the act of transmission

Elucidating bacterial adhesion to mucosal surface by an original AFM approach

Contact Info

Product

Resources

About