Formation and three-dimensional architecture of Leishmania adhesion in the sand fly vector
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
Wellcome Trust - United Kingdom
221944/Z/20/Z
Wellcome Trust - United Kingdom
PubMed
37162189
PubMed Central
PMC10195081
DOI
10.7554/elife.84552
PII: 84552
Knihovny.cz E-resources
- Keywords
- Leishmania, cell adhesion, cell biology, host-parasite interaction, infectious disease, microbiology, sand fly, serial block face scanning electron microscopy, serial section electron microscopy tomography,
- MeSH
- Microscopy, Electron MeSH
- Leishmania * MeSH
- Psychodidae * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Attachment to a substrate to maintain position in a specific ecological niche is a common strategy across biology, especially for eukaryotic parasites. During development in the sand fly vector, the eukaryotic parasite Leishmania adheres to the stomodeal valve, as the specialised haptomonad form. Dissection of haptomonad adhesion is a critical step for understanding the complete life cycle of Leishmania. Nevertheless, haptomonad studies are limited, as this is a technically challenging life cycle form to investigate. Here, we have combined three-dimensional electron microscopy approaches, including serial block face scanning electron microscopy (SBFSEM) and serial tomography to dissect the organisation and architecture of haptomonads in the sand fly. We showed that the attachment plaque contains distinct structural elements. Using time-lapse light microscopy of in vitro haptomonad-like cells, we identified five stages of haptomonad-like cell differentiation, and showed that calcium is necessary for Leishmania adhesion to the surface in vitro. This study provides the structural and regulatory foundations of Leishmania adhesion, which are critical for a holistic understanding of the Leishmania life cycle.
Department of Basic Biology School of Life Science Okazaki Japan
Department of Biological and Medical Sciences Oxford Brookes University Oxford United Kingdom
Department of Parasitology Charles University Prague Czech Republic
Laboratory for Spatiotemporal Regulations National Institute for Basic Biology Okazaki Japan
doi: 10.1101/2022.10.28.514187 PubMed
See more in PubMed
Akopyants NS, Kimblin N, Secundino N, Patrick R, Peters N, Lawyer P, Dobson DE, Beverley SM, Sacks DL. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science. 2009;324:265–268. doi: 10.1126/science.1169464. PubMed DOI PMC
Bates PA. Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. International Journal for Parasitology. 2007;37:1097–1106. doi: 10.1016/j.ijpara.2007.04.003. PubMed DOI PMC
Beattie P, Gull K. Cytoskeletal architecture and components involved in the attachment of Trypanosoma congolense epimastigotes. Parasitology. 1997;115 (Pt 1):47–55. doi: 10.1017/s0031182097001042. PubMed DOI
Bloodgood RA. Flagellar Surfaces of Parasitic Protozoa and Their Role in AttachmentCiliary and Flagellar Membranes. Springer; 1990. Ciliary and Flagellar membranes. DOI
Borradori L, Sonnenberg A. Structure and function of hemidesmosomes: more than simple adhesion complexes. The Journal of Investigative Dermatology. 1999;112:411–418. doi: 10.1046/j.1523-1747.1999.00546.x. PubMed DOI
Bridges AA, Zhang H, Mehta SB, Occhipinti P, Tani T, Gladfelter AS. Septin assemblies form by diffusion-driven annealing on membranes. PNAS. 2014;111:2146–2151. doi: 10.1073/pnas.1314138111. PubMed DOI PMC
Burdett IDJ, Sullivan KH. Desmosome assembly in MDCK cells: transport of precursors to the cell surface occurs by two phases of vesicular traffic and involves major changes in centrosome and Golgi location during a Ca (2+) shift. Experimental Cell Research. 2002;276:296–309. doi: 10.1006/excr.2002.5509. PubMed DOI
Burza S, Croft SL, Boelaert M. Leishmaniasis. Lancet. 2018;392:951–970. doi: 10.1016/S0140-6736(18)31204-2. PubMed DOI
Cecílio P, Cordeiro-da-Silva A, Oliveira F. Sand flies: basic information on the vectors of leishmaniasis and their interactions with Leishmania parasites. Communications Biology. 2022;5:305. doi: 10.1038/s42003-022-03240-z. PubMed DOI PMC
Coulombe PA, Wong P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nature Cell Biology. 2004;6:699–706. doi: 10.1038/ncb0804-699. 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
Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T. Invasion of erythrocytes by malaria merozoites. Science. 1975;187:748–750. doi: 10.1126/science.803712. PubMed DOI
Ellis DS, Ormerod WE, Lumsden WHR. Filaments of Trypanosoma brucei: some notes on differences in origin and structure in two strains of Trypanosoma (Trypanozoon) brucei rhodesiense. Acta Tropica. 1976;33:151–168. PubMed
Evans DA, Ellis DS, Stamford S. Ultrastructural studies of certain aspects of the development of Trypanosoma congolense in Glossina morsitans morsitans. The Journal of Protozoology. 1979;26:557–563. doi: 10.1111/j.1550-7408.1979.tb04195.x. PubMed DOI
Friend DS. The fine structure of Giardia muris. The Journal of Cell Biology. 1966;29:317–332. doi: 10.1083/jcb.29.2.317. PubMed DOI PMC
Gadelha C, Wickstead B, McKean PG, Gull K. Basal body and flagellum mutants reveal a rotational constraint of the central pair microtubules in the axonemes of trypanosomes. Journal of Cell Science. 2006;119:2405–2413. doi: 10.1242/jcs.02969. PubMed DOI
Garrod DR, Berika MY, Bardsley WF, Holmes D, Tabernero L. Hyper-adhesion in desmosomes: its regulation in wound healing and possible relationship to cadherin crystal structure. Journal of Cell Science. 2005;118:5743–5754. doi: 10.1242/jcs.02700. PubMed DOI
Garrod D, Chidgey M. Desmosome structure, composition and function. Biochimica et Biophysica Acta - Biomembranes. 2008;1778:572–587. doi: 10.1016/j.bbamem.2007.07.014. PubMed DOI
Gossage SM, Rogers ME, Bates PA. Two separate growth phases during the development of Leishmania in sand flies: implications for understanding the life cycle. International Journal for Parasitology. 2003;33:1027–1034. doi: 10.1016/s0020-7519(03)00142-5. PubMed DOI PMC
Hall MJR, Ghosh D, Martín-Vega D, Clark B, Clatworthy I, Cheke RA, Rogers ME. Micro-Ct visualization of a promastigote secretory gel (PSG) and parasite plug in the digestive tract of the sand fly Lutzomyia longipalpis infected with Leishmania mexicana. PLOS Neglected Tropical Diseases. 2021;15:e0009682. doi: 10.1371/journal.pntd.0009682. PubMed DOI PMC
Hendry KAK. Glasgow, UK: University of Glasgow; 1987. Studies on the flagellar attachment of african trypanosomes DPhil thesis.http://theses.gla.ac.uk/id/eprint/77509
Hunter JD. Matplotlib: a 2D graphics environment. Computing in Science & Engineering. 2007;9:90–95. doi: 10.1109/MCSE.2007.55. DOI
Inbar E, Akopyants NS, Charmoy M, Romano A, Lawyer P, Elnaiem DEA, Kauffmann F, Barhoumi M, Grigg M, Owens K, Fay M, Dobson DE, Shaik J, Beverley SM, Sacks D, Heitman J. The mating competence of geographically diverse Leishmania major strains in their natural and unnatural sand fly vectors. PLOS Genetics. 2013;9:e1003672. doi: 10.1371/journal.pgen.1003672. PubMed DOI PMC
Iudin A, Korir PK, Somasundharam S, Weyand S, Cattavitello C, Fonseca N, Salih O, Kleywegt GJ, Patwardhan A. EMPIAR: the electron microscopy public image archive. Nucleic Acids Research. 2023;51:D1503–D1511. doi: 10.1093/nar/gkac1062. PubMed DOI PMC
Jensen AR, Adams Y, Hviid L. Cerebral Plasmodium falciparum malaria: the role of PfEMP1 in its pathogenesis and immunity, and pfemp1-based vaccines to prevent it. Immunological Reviews. 2020;293:230–252. doi: 10.1111/imr.12807. PubMed DOI PMC
Killick-Kendrick R, Molyneux DH, Ashford RW. Leishmania in phlebotomid sandflies I. modifications of the flagellum associated with attachment to the mid-gut and oesophageal valve of the sandfly. Proceedings of the Royal Society of London. Series B. Biological Sciences. 1974;187:409–419. doi: 10.1098/rspb.1974.0085. PubMed DOI
Killick-Kendrick R, Molyneux DH, Hommel M, Leaney AJ, Robertson ES. Leishmania in phlebotomid sandflies V. the nature and significance of infections of the pylorus and ileum of the sandfly by leishmaniae of the braziliensis complex. Proceedings of the Royal Society of London. Series B. Biological Sciences. 1977;198:191–199. doi: 10.1098/rspb.1977.0093. PubMed DOI
Kremer JR, Mastronarde DN, McIntosh JR. Computer visualization of three-dimensional image data using IMOD. Journal of Structural Biology. 1996;116:71–76. doi: 10.1006/jsbi.1996.0013. PubMed DOI
Maraghi S, Mohamed HA, Wallbanks KR, Molyneux DH. Scratched plastic as a substrate for trypanosomatid attachment. Annals of Tropical Medicine and Parasitology. 1987;81:457–458. doi: 10.1080/00034983.1987.11812145. PubMed DOI
Mastronarde DN. SerialEM: a program for automated tilt series acquisition on tecnai microscopes using prediction of specimen position. Microscopy and Microanalysis. 2003;9:1182–1183. doi: 10.1017/S1431927603445911. DOI
Mastronarde DN. Automated electron microscope tomography using robust prediction of specimen movements. Journal of Structural Biology. 2005;152:36–51. doi: 10.1016/j.jsb.2005.07.007. PubMed DOI
Molyneux DH, Killick-Kendrick R, Ashford RW. Leishmania in phlebotomid sandflies. III . The ultrastructure of Leishmania mexicana amazonens in the midgut and pharynx of Lutzomyia longipalpis. Proc R Soc B Biol Sci. 1975;190:341–357. doi: 10.1098/rspb.1975.0098. PubMed DOI
Molyneux DH, Wallbanks KR, Ingram GA. In Vitro Studies on Parasite Substrate Interactions. Host-Parasite Cellular and Molecular Interactions in Protozoal Infections. Berlin, Heidelberg: Springer; 1987. Trypanosomatid-vector interfaces; pp. 387–396. DOI
Peacock L, Ferris V, Sharma R, Sunter J, Bailey M, Carrington M, Gibson W. Identification of the meiotic life cycle stage of Trypanosoma brucei in the tsetse fly. PNAS. 2011;108:3671–3676. doi: 10.1073/pnas.1019423108. PubMed DOI PMC
Peacock L, Kay C, Bailey M, Gibson W. Shape-Shifting trypanosomes: flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus. PLOS Pathogens. 2018;14:e1007043. doi: 10.1371/journal.ppat.1007043. PubMed DOI PMC
Portman N, Gull K. The paraflagellar rod of kinetoplastid parasites: from structure to components and function. International Journal for Parasitology. 2010;40:135–148. doi: 10.1016/j.ijpara.2009.10.005. PubMed DOI PMC
Rogers ME, Chance ML, Bates PA. The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis. Parasitology. 2002;124:495–507. doi: 10.1017/s0031182002001439. PubMed DOI
Rogers ME, Hajmová M, Joshi MB, Sadlova J, Dwyer DM, Volf P, Bates PA. Leishmania chitinase facilitates colonization of sand fly vectors and enhances transmission to mice. Cellular Microbiology. 2008;10:1363–1372. doi: 10.1111/j.1462-5822.2008.01132.x. PubMed DOI PMC
Rotureau B, Van Den Abbeele J. Through the dark continent: African trypanosome development in the tsetse fly. Frontiers in Cellular and Infection Microbiology. 2013;3:53. doi: 10.3389/fcimb.2013.00053. PubMed DOI PMC
Sadlova J, Yeo M, Seblova V, Lewis MD, Mauricio I, Volf P, Miles MA. Visualisation of Leishmania donovani fluorescent hybrids during early stage development in the sand fly vector. PLOS ONE. 2011;6:e19851. doi: 10.1371/journal.pone.0019851. PubMed DOI PMC
Sádlová J, Podešvová L, Bečvář T, Bianchi C, Gerasimov ES, Saura A, Glanzová K, Leštinová T, Matveeva NS, Chmelová Ľ, Mlacovská D, Spitzová T, Vojtková B, Volf P, Yurchenko V, Kraeva N. Catalase impairs Leishmania mexicana development and virulence. Virulence. 2021;12:852–867. doi: 10.1080/21505594.2021.1896830. PubMed DOI PMC
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. Fiji: an open-source platform for biological-image analysis. Nature Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC
Schlein Y, Jacobson RL, Messer G. Leishmania infections damage the feeding mechanism of the Sandfly vector and implement parasite transmission by bite. PNAS. 1992;89:9944–9948. doi: 10.1073/pnas.89.20.9944. PubMed DOI PMC
Schmidt J, Kleffmann T, Schaub GA. Hydrophobic attachment of Trypanosoma cruzi to a superficial layer of the rectal cuticle in the bug Triatoma infestans. Parasitology Research. 1998;84:527–536. doi: 10.1007/s004360050443. PubMed DOI
Serafim TD, Coutinho-Abreu IV, Oliveira F, Meneses C, Kamhawi S, Valenzuela JG. Sequential blood meals promote Leishmania replication and reverse metacyclogenesis augmenting vector infectivity. Nature Microbiology. 2018;3:548–555. doi: 10.1038/s41564-018-0125-7. PubMed DOI PMC
Serafim TD, Iniguez E, Beatriz A, Barletta F, Doehl JSP, Short M, Lack J, Cecilio P, Nair V, Disotuar M, Wilson T, Oliveira F, Meneses C, Barillas-Mury C, Andersen J, Ribeiro JMC, Beverley SM, Kamhawi S, Valenzuela JG. Genetic Exchange in Leishmania Is Facilitated by IgM Natural Antibodies. bioRxiv. 2022 doi: 10.1101/2022.06.09.495557. DOI
Skalický T, Dobáková E, Wheeler RJ, Tesařová M, Flegontov P, Jirsová D, Votýpka J, Yurchenko V, Ayala FJ, Lukeš J. Extensive flagellar remodeling during the complex life cycle of paratrypanosoma, an early-branching trypanosomatid. PNAS. 2017;114:11757–11762. doi: 10.1073/pnas.1712311114. PubMed DOI PMC
Späth GF, Beverley SM. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Experimental Parasitology. 2001;99:97–103. doi: 10.1006/expr.2001.4656. PubMed DOI
Sunter J, Gull K. Shape, form, function and Leishmania pathogenicity: from textbook descriptions to biological understanding. Open Biology. 2017;7:170165. doi: 10.1098/rsob.170165. PubMed DOI PMC
Sunter JD, Yanase R, Wang Z, Catta-Preta CMC, Moreira-Leite F, Myskova J, Pruzinova K, Volf P, Mottram JC, Gull K. Leishmania flagellum attachment zone is critical for flagellar pocket shape, development in the sand fly, and pathogenicity in the host. PNAS. 2019;116:6351–6360. doi: 10.1073/pnas.1812462116. PubMed DOI PMC
Tetley L, Vickerman K. Differentiation in Trypanosoma brucei: host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. Journal of Cell Science. 1985;74:1–19. doi: 10.1242/jcs.74.1.1. PubMed DOI
Todorović V, Kligys KR, Dusek RL, Jones JCR, Green KJ. In: Encyclopedia of Biological Chemistry. Todorović V, editor. Academic Press; 2004. Desmosomes and Hemidesmosomes; pp. 569–576. DOI
Trinkaus-Randall V, Gipson IK. Role of calcium and calmodulin in hemidesmosome formation in vitro. The Journal of Cell Biology. 1984;98:1565–1571. doi: 10.1083/jcb.98.4.1565. PubMed DOI PMC
Vincent JFV. In: Encyclopedia of Materials: Science and Technology. Vincent JFV, editor. Elsevier Ltd; 2001. Cuticle; pp. 1924–1928. DOI
Volf P, Hajmova M, Sadlova J, Votypka J. Blocked stomodeal valve of the insect vector: similar mechanism of transmission in two trypanosomatid models. International Journal for Parasitology. 2004;34:1221–1227. doi: 10.1016/j.ijpara.2004.07.010. PubMed DOI
Volf P, Volfova V. Establishment and maintenance of sand fly colonies. Journal of Vector Ecology. 2011;36:S1–S9. doi: 10.1111/j.1948-7134.2011.00106.x. PubMed DOI
Wakid MH, Bates PA. Flagellar attachment of Leishmania promastigotes to plastic film in vitro. Experimental Parasitology. 2004;106:173–178. doi: 10.1016/j.exppara.2004.03.001. PubMed DOI
Wang Z, Beneke T, Gluenz E, Wheeler RJ. The single Flagellum of Leishmania has a fixed Polarisation of its asymmetric beat. Journal of Cell Science. 2021;133:246637. doi: 10.1242/jcs.246637. PubMed DOI PMC
Wheeler RJ, Sunter JD, Gull K. Flagellar pocket restructuring through the Leishmania life cycle involves a discrete flagellum attachment zone. Journal of Cell Science. 2016;129:854–867. doi: 10.1242/jcs.183152. PubMed DOI PMC
Whole cell reconstructions of Leishmania mexicana through the cell cycle