Hide-and-Seek: A Game Played between Parasitic Protists and Their Hosts

. 2021 Nov 25 ; 9 (12) : . [epub] 20211125

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34946036

Grantová podpora
project CePaViP, grant No. CZ.02.1.01/0.0/0.0/16_019/0000759 ERD Funds
GPP506/10/P372 Czech Science Foundation
GBP505/12/G112 Czech Science Foundation

Odkazy

PubMed 34946036
PubMed Central PMC8707157
DOI 10.3390/microorganisms9122434
PII: microorganisms9122434
Knihovny.cz E-zdroje

After invading the host organism, a battle occurs between the parasitic protists and the host's immune system, the result of which determines not only whether and how well the host survives and recovers, but also the fate of the parasite itself. The exact weaponry of this battle depends, among others, on the parasite localisation. While some parasitic protists do not invade the host cell at all (extracellular parasites), others have developed successful intracellular lifestyles (intracellular parasites) or attack only the surface of the host cell (epicellular parasites). Epicellular and intracellular protist parasites have developed various mechanisms to hijack host cell functions to escape cellular defences and immune responses, and, finally, to gain access to host nutrients. They use various evasion tactics to secure the tight contact with the host cell and the direct nutrient supply. This review focuses on the adaptations and evasion strategies of parasitic protists on the example of two very successful parasites of medical significance, Cryptosporidium and Leishmania, while discussing different localisation (epicellular vs. intracellular) with respect to the host cell.

Zobrazit více v PubMed

Ratcliffe M.J.H. Encyclopedia of Immunobiology. 1st ed. Academic Press; Oxford, UK: 2016. p. 3126.

Briceño A.L., Contreras Z.P., Vera D.D., Briceño R.M., Pru E.P. Tissue culture to assess bacterial enteropathogenicity. In: Ceccherini-Nelli L., Matteoli B., editors. Biomedical Tissue Culture. IntechOpen; Rijeka, Croatia: 2012. pp. 203–220.

Valigurová A., Jirků M., Koudela B., Gelnar M., Modrý D., Šlapeta J. Cryptosporidia: Epicellular parasites embraced by the host cell membrane. Int. J. Parasitol. 2008;38:913–922. doi: 10.1016/j.ijpara.2007.11.003. PubMed DOI

Valigurová A., Hofmannová L., Koudela B., Vávra J. An ultrastructural comparison of the attachment sites between Gregarina steini and Cryptosporidium muris. J. Eukaryot. Microbiol. 2007;54:495–510. doi: 10.1111/j.1550-7408.2007.00291.x. PubMed DOI

Valigurová A., Paskerova G.G., Diakin A., Kováčiková M., Simdyanov T.G. Protococcidian Eleutheroschizon duboscqi, an unusual apicomplexan interconnecting gregarines and cryptosporidia. PLoS ONE. 2015;10:e0125063. doi: 10.1371/journal.pone.0125063. PubMed DOI PMC

Dubremetz J.F., Garcia-Reguet N., Conseil V., Fourmaux M.N. Apical organelles and host-cell invasion by Apicomplexa. Int. J. Parasitol. 1998;28:1007–1013. doi: 10.1016/S0020-7519(98)00076-9. PubMed DOI

Bargieri D., Lagal V., Andenmatten N., Tardieux I., Meissner M., Ménard R. Host cell invasion by apicomplexan parasites: The junction conundrum. PLoS Pathog. 2014;10:e1004273. doi: 10.1371/journal.ppat.1004273. PubMed DOI PMC

Umemiya R., Fukuda M., Fujisaki K., Matsui T. Electron microscopic observation of the invasion process of Cryptosporidium parvum in severe combined immunodeficiency mice. J. Parasitol. 2005;91:1034–1039. doi: 10.1645/GE-508R.1. PubMed DOI

Borowski H., Thompson R.C., Armstrong T., Clode P.L. Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology. 2010;137:13–26. doi: 10.1017/S0031182009990837. PubMed DOI

Marcial M.A., Madara J.L. Cryptosporidium: Cellular localization, structural analysis of absorptive cell-parasite membrane-membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology. 1986;90:583–594. doi: 10.1016/0016-5085(86)91112-1. PubMed DOI

Barta J.R., Thompson R.C.A. What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends Parasitol. 2006;22:463–468. doi: 10.1016/j.pt.2006.08.001. PubMed DOI

Carreno R.A., Martin D.S., Barta J.R. Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitol. Res. 1999;85:899–904. doi: 10.1007/s004360050655. PubMed DOI

Clode P.L., Koh W.H., Thompson R.C.A. Life without a host cell: What is Cryptosporidium? Trends Parasitol. 2015;31:614–624. doi: 10.1016/j.pt.2015.08.005. PubMed DOI

Melicherová J., Hofmannová L., Valigurová A. Response of cell lines to actual and simulated inoculation with Cryptosporidium proliferans. Eur. J. Protistol. 2018;62:101–121. doi: 10.1016/j.ejop.2017.12.003. PubMed DOI

Ryan U., Paparini A., Monis P., Hijjawi N. It’s official-Cryptosporidium is a gregarine: What are the implications for the water industry? Water Res. 2016;105:305–313. doi: 10.1016/j.watres.2016.09.013. PubMed DOI

Lumb R., Smith K., Odonoghue P.J., Lanser J.A. Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue-culture cells. Parasitol. Res. 1988;74:531–536. doi: 10.1007/BF00531630. PubMed DOI

Koudela B., Vitovec J., Sterba J., Milacek P. An unusual localization of developmental stages of Cryptosporidium parvum Tyzzer, 1912 in the cells of small intestine of a gnotobiotic piglet. Folia Parasitol. 1989;36:219–222. PubMed

Valentini E., Cherchi S., Possenti A., Dubremetz J.F., Pozio E., Spano F. Molecular characterisation of a Cryptosporidium parvum rhoptry protein candidate related to the rhoptry neck proteins TgRON1 of Toxoplasma gondii and PfASP of Plasmodium falciparum. Mol. Biochem. Parasitol. 2012;183:94–99. doi: 10.1016/j.molbiopara.2012.02.004. PubMed DOI

Singh P., Mirdha B.R., Srinivasan A., Rukmangadachar L.A., Singh S., Sharma P., Gururao H., Luthra K. Identification of invasion proteins of Cryptosporidium parvum. World J. Microbiol. Biotechnol. 2015;31:1923–1934. doi: 10.1007/s11274-015-1936-9. PubMed DOI

Guérin A., Roy N.H., Kugler E.M., Berry L., Burkhardt J.K., Shin J.-B., Striepen B. Cryptosporidium rhoptry effector protein ROP1 injected during invasion targets the host cytoskeletal modulator LMO7. Cell Host Microbe. 2021;29:1407–1420. doi: 10.1016/j.chom.2021.07.002. PubMed DOI PMC

Beyer T.V., Svezhova N.V., Sidorenko N.V., Khokhlov S.E. Cryptosporidium parvum (Coccidia, Apicomplexa): Some new ultrastructural observations on its endogenous development. Eur. J. Protistol. 2000;36:151–159. doi: 10.1016/S0932-4739(00)80034-6. DOI

Forney J.R., DeWald D.B., Yang S.G., Speer C.A., Healey M.C. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect. Immun. 1999;67:844–852. doi: 10.1128/IAI.67.2.844-852.1999. PubMed DOI PMC

Landsberg J.H., Paperna I. Ultrastructural study of the coccidian Cryptosporidium sp. from stomachs of juvenile cichlid fish. Dis. Aquat. Organ. 1986;2:13–20. doi: 10.3354/dao002013. DOI

O’Hara S.P., Small A.J., Chen X.M., LaRusso N.F. Host cell actin remodeling in response to Cryptosporidium. Subcell. Biochem. 2008;47:92–100. PubMed

Perkins M.E., Riojas Y.A., Wu T.W., Le Blancq S.M. CpABC, a Cryptosporidium parvum ATP-binding cassette protein at the host-parasite boundary in intracellular stages. Proc. Natl. Acad. Sci. USA. 1999;96:5734–5739. doi: 10.1073/pnas.96.10.5734. PubMed DOI PMC

Tzipori S., Griffiths J.K. Natural history and biology of Cryptosporidium parvum. Adv. Parasitol. 1998;40:5–36. doi: 10.1016/S0065-308X(08)60116-5. PubMed DOI

Dyková I., Lom J. Fish coccidia: Critical notes on life cycles, classification and pathogenicity. J. Fish. Dis. 1981;4:487–505. doi: 10.1111/j.1365-2761.1981.tb01161.x. DOI

Lukes J. Life cycle of Goussia pannonica (Molnar, 1989) (Apicomplexa, Eimeriorina), an extracytoplasmic coccidium from the white bream Blicca bjoerkna. J. Protozool. 1992;39:484–494. doi: 10.1111/j.1550-7408.1992.tb04836.x. DOI

Molnar K., Baska F. Light and electron microscopic studies on Epieimeria anguillae (Léger & Hollande, 1922), a coccidium parasitizing the European eel, Anguilla anguilla L. J. Fish Dis. 1986;9:99–110.

Valigurová A., Florent I. Nutrient acquisition and attachment strategies in basal lineages: A tough nut to crack in the evolutionary puzzle of Apicomplexa. Microorganisms. 2021;9:1430. doi: 10.3390/microorganisms9071430. PubMed DOI PMC

Bartošová-Sojková P., Oppenheim R.D., Soldati-Favre D., Lukeš J. Epicellular apicomplexans: Parasites “on the way in”. PLoS Pathog. 2015;11:e1005080. doi: 10.1371/journal.ppat.1005080. PubMed DOI PMC

Lovy J., Friend S.E. Intestinal coccidiosis of anadromous and landlocked alewives, Alosa pseudoharengus, caused by Goussia ameliae n. sp. and G. alosii n. sp. (Apicomplexa: Eimeriidae) Int. J. Parasitol. Parasites Wildl. 2015;4:159–170. doi: 10.1016/j.ijppaw.2015.02.003. PubMed DOI PMC

Carruthers V.B., Tomley F.M. Microneme proteins in apicomplexans. Subcell. Biochem. 2008;47:33–45. doi: 10.1007/978-0-387-78267-6_2. PubMed DOI PMC

Ben Chaabene R., Lentini G., Soldati-Favre D. Biogenesis and discharge of the rhoptries: Key organelles for entry and hijack of host cells by the Apicomplexa. Mol. Microbiol. 2021;115:453–465. doi: 10.1111/mmi.14674. PubMed DOI

Dogga S.K., Bartošová-Sojková P., Lukeš J., Soldati-Favre D. Phylogeny, Morphology, and metabolic and invasive capabilities of epicellular fish coccidium Goussia janae. Protist. 2015;166:659–676. doi: 10.1016/j.protis.2015.09.003. PubMed DOI

Bonnin A., Dubremetz J.F., Camerlynck P. Characterization of microneme antigens of Cryptosporidium parvum (Protozoa, Apicomplexa) Infect. Immun. 1991;59:1703–1708. doi: 10.1128/iai.59.5.1703-1708.1991. PubMed DOI PMC

Melicherová J., Ilgová J., Kváč M., Sak B., Koudela B., Valigurová A. Life cycle of Cryptosporidium muris in two rodents with different responses to parasitization. Parasitology. 2014;141:287–303. doi: 10.1017/S0031182013001637. PubMed DOI

Huang B.Q., Chen X.M., LaRusso N.F. Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: A morphologic study. J. Parasitol. 2004;90:212–221. doi: 10.1645/GE-3204. PubMed DOI

Mele R., Morales M.A.G., Tosini F., Pozio E. Cryptosporidium parvum at different developmental stages modulates host cell apoptosis in vitro. Infect. Immun. 2004;72:6061–6067. doi: 10.1128/IAI.72.10.6061-6067.2004. PubMed DOI PMC

McCole D.F., Eckmann L., Laurent F., Kagnoff M.F. Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infect. Immun. 2000;68:1710–1713. doi: 10.1128/IAI.68.3.1710-1713.2000. PubMed DOI PMC

Sasahara T., Maruyama H., Aoki M., Kikuno R., Sekiguchi T., Takahashi A., Satoh Y., Kitasato H., Takayama Y., Inoue M. Apoptosis of intestinal crypt epithelium after Cryptosporidium parvum infection. J. Infect. Chemother. 2003;9:278–281. doi: 10.1007/s10156-003-0259-1. PubMed DOI

Widmer G., Yang Y.L., Bonilla R., Tanriverdi S., Ciociola K.M. Preferential infection of dividing cells by Cryptosporidium parvum. Parasitology. 2006;133:131–138. doi: 10.1017/S0031182006000151. PubMed DOI

Ojcius D.M., Perfettini J.L., Bonnin A., Laurent F. Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect. 1999;1:1163–1168. doi: 10.1016/S1286-4579(99)00246-4. PubMed DOI

Chen X.M., Levine S.A., Tietz P., Krueger E., McNiven M.A., Jefferson D.M., Mahle M., LaRusso N.F. Cryptosporidium parvum is cytopathic for cultured human biliary epithelia via an apoptotic mechanism. Hepatology. 1998;28:906–913. doi: 10.1002/hep.510280402. PubMed DOI

Widmer G., Corey E.A., Stein B., Griffiths J.K., Tzipori S. Host cell apoptosis impairs Cryptosporidium parvum development in vitro. J. Parasitol. 2000;86:922–928. doi: 10.1645/0022-3395(2000)086[0922:HCAICP]2.0.CO;2. PubMed DOI

Chen X.M., Gores G.J., Paya C.V., LaRusso N.F. Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. Am. J. Physiol. 1999;277:G599–G608. doi: 10.1152/ajpgi.1999.277.3.G599. PubMed DOI

Crawford C.K., Kol A. The mucosal innate immune response to Cryptosporidium parvum, a global one health issue. Front. Cell. Infect. Microbiol. 2021;11:451. doi: 10.3389/fcimb.2021.689401. PubMed DOI PMC

Petry F., Jakobi V., Tessema T.S. Host immune response to Cryptosporidium parvum infection. Exp. Parasitol. 2010;126:304–309. doi: 10.1016/j.exppara.2010.05.022. PubMed DOI

Quach J., Chadee K., Mead J.R., Singer S.M. Immunity to intestinal protozoa: Entamoeba, Cryptosporidium, and Giardia. In: Ratcliffe M.J.H., editor. Encyclopedia of Immunobiology. Academic Press; Oxford, UK: 2016. pp. 133–141.

Barakat F.M., McDonald V., Di Santo J.P., Korbel D.S. Roles for NK cells and an NK cell-independent source of intestinal gamma interferon for innate immunity to Cryptosporidium parvum infection. Infect. Immun. 2009;77:5044–5049. doi: 10.1128/IAI.00377-09. PubMed DOI PMC

Choudhry N., Korbel D.S., Edwards L.A., Bajaj-Elliott M., McDonald V. Dysregulation of interferon-γ-mediated signalling pathway in intestinal epithelial cells by Cryptosporidium parvum infection. Cell. Microbiol. 2009;11:1354–1364. doi: 10.1111/j.1462-5822.2009.01336.x. PubMed DOI

Zaalouk T.K., Bajaj-Elliott M., George J.T., McDonald V. Differential regulation of defensin gene expression during Cryptosporidium parvum infection. Infect. Immun. 2004;72:2772–2779. doi: 10.1128/IAI.72.5.2772-2779.2004. PubMed DOI PMC

Wang Y., Gong A.-Y., Ma S., Chen X., Li Y., Su C.-J., Norall D., Chen J., Strauss-Soukup J.K., Chen X.-M. Delivery of parasite RNA transcripts into infected epithelial cells during Cryptosporidium infection and its potential impact on host gene transcription. J. Infect. Dis. 2016;215:636–643. doi: 10.1093/infdis/jiw607. PubMed DOI PMC

Ashigbie P.G., Shepherd S., Steiner K.L., Amadi B., Aziz N., Manjunatha U.H., Spector J.M., Diagana T.T., Kelly P. Use-case scenarios for an anti-Cryptosporidium therapeutic. PLoS Negl. Trop. Dis. 2021;15:e0009057. doi: 10.1371/journal.pntd.0009057. PubMed DOI PMC

Alvarez-Pellitero P., Quiroga M.I., Sitjà-Bobadilla A., Redondo M.J., Palenzuela O., Padrós F., Vázquez S., Nieto J.M. Cryptosporidium scophthalmi n. sp. (Apicomplexa: Cryptosporidiidae) from cultured turbot Scophthalmus maximus. Light and electron microscope description and histopathological study. Dis. Aquat. Organ. 2004;62:133–145. doi: 10.3354/dao062133. PubMed DOI

Alvarez-Pellitero P., Sitja-Bobadilla A. Cryptosporidium molnari n. sp. (Apicomplexa: Cryptosporidiidae) infecting two marine fish species, Sparus aurata L. and Dicentrarchus labrax L. Int. J. Parasitol. 2002;32:1007–1021. doi: 10.1016/S0020-7519(02)00058-9. PubMed DOI

Liebler E.M., Pohlenz J.F., Woodmansee D.B. Experimental intrauterine infection of adult BALB/c mice with Cryptosporidium sp. Infect. Immun. 1986;54:255–259. doi: 10.1128/iai.54.1.255-259.1986. PubMed DOI PMC

Kennedy G.A., Kreitner G.L., Strafuss A.C. Cryptosporidiosis in three pigs. J. Am. Vet. Med. Assoc. 1977;170:348–350. PubMed

Dillon A., Lo D.D. M Cells: Intelligent engineering of mucosal immune surveillance. Front. Immunol. 2019;10:1499. doi: 10.3389/fimmu.2019.01499. PubMed DOI PMC

Wang M., Gao Z., Zhang Z., Pan L., Zhang Y. Roles of M cells in infection and mucosal vaccines. Hum. Vaccin Immunother. 2014;10:3544–3551. doi: 10.4161/hv.36174. PubMed DOI PMC

De Sablet T., Potiron L., Marquis M., Bussière F.I., Lacroix-Lamandé S., Laurent F. Cryptosporidium parvum increases intestinal permeability through interaction with epithelial cells and IL-1β and TNFα released by inflammatory monocytes. Cell. Microbiol. 2016;18:1871–1880. doi: 10.1111/cmi.12632. PubMed DOI

Allain T., Amat C.B., Motta J.-P., Manko A., Buret A.G. Interactions of Giardia sp. with the intestinal barrier: Epithelium, mucus, and microbiota. Tissue Barriers. 2017;5:e1274354. doi: 10.1080/21688370.2016.1274354. PubMed DOI PMC

Koh W.H., Geurden T., Paget T., O’Handley R., Steuart R.F., Thompson R.C., Buret A.G. Giardia duodenalis assemblage-specific induction of apoptosis and tight junction disruption in human intestinal epithelial cells: Effects of mixed infections. J. Parasitol. 2013;99:353–358. doi: 10.1645/GE-3021.1. PubMed DOI

Hernández-Sánchez J., Liñan R.F., del Rosario Salinas-Tobón M., Ortega-Pierres G. Giardia duodenalis: Adhesion-deficient clones have reduced ability to establish infection in Mongolian gerbils. Exp. Parasitol. 2008;119:364–372. doi: 10.1016/j.exppara.2008.03.010. PubMed DOI

Sousa M.C., Gonçalves C.A., Bairos V.A., Poiares-Da-Silva J. Adherence of Giardia lamblia trophozoites to Int-407 human intestinal cells. Clin. Diagn. Lab. Immunol. 2001;8:258–265. doi: 10.1128/CDLI.8.2.258-265.2001. PubMed DOI PMC

Brandborg L.L., Tankersley C.B., Gottieb S., Barancik M., Sartor V.E. Histological demonstration of mucosal invasion by Giardia lamblia in man. Gastroenterology. 1967;52:143–150. doi: 10.1016/S0016-5085(67)80001-5. PubMed DOI

Reynoso-Robles R., Ponce-Macotela M., Rosas-López L.E., Ramos-Morales A., Martínez–Gordillo M.N., González-Maciel A. The invasive potential of Giardia intestinalis in an in vivo model. Sci. Rep. 2015;5:15168. doi: 10.1038/srep15168. PubMed DOI PMC

Saha T.K., Ghosh T.K. Invasion of small intestinal mucosa by Giardia lamblia in man. Gastroenterology. 1977;72:402–405. doi: 10.1016/S0016-5085(77)80247-3. PubMed DOI

Owen R.L., Nemanic P.C., Stevens D.P. Ultrastructural observations on giardiasis in a murine model. I. Intestinal distribution, attachment, and relationship to the immune system of Giardia muris. Gastroenterology. 1979;76:757–769. doi: 10.1016/S0016-5085(79)80176-6. PubMed DOI

Bannister L.H. The interactions of intracellular Protista and their host cells, with special reference to heterotrophic organisms. Proc. R. Soc. Lond. Ser. B Biol. Sci. 1979;204:141–163. doi: 10.1098/rspb.1979.0019. PubMed DOI

Mathur V., Kolísko M., Hehenberger E., Irwin N.A.T., Leander B.S., Kristmundsson A., Freeman M.A., Keeling P.J. Multiple independent origins of apicomplexan-like parasites. Curr. Biol. 2019;29:2936–2941.e2935. doi: 10.1016/j.cub.2019.07.019. PubMed DOI

Janouskovec J., Paskerova G.G., Miroliubova T.S., Mikhailov K.V., Birley T., Aleoshin V.V., Simdyanov T.G. Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles. eLife. 2019;8:e49662. doi: 10.7554/eLife.49662. PubMed DOI PMC

Benajiba M.H., Marques A., Lom J., Bouix G. Ultrastructure and sporogony of Eimeria (syn. Epieimeria) anguillae (Apicomplexa) in the Eel (Anguilla anguilla) J. Eukaryot. Microbiol. 1994;41:215–222. doi: 10.1111/j.1550-7408.1994.tb01500.x. DOI

Eli A., Briyai O.F., Abowei J.F.N. A review of some parasite diseases of African fish gut lumen Protozoa, coccidioses, Cryptosporidium infections, Haemoprotozoa, Haemosporidia. Res. J. Appl. Sci. Eng. Technol. 2012;4:1438–1447.

Chaves M.M., Lee S.H., Kamenyeva O., Ghosh K., Peters N.C., Sacks D. The role of dermis resident macrophages and their interaction with neutrophils in the early establishment of Leishmania major infection transmitted by sand fly bite. PLoS Pathog. 2020;16:e1008674. doi: 10.1371/journal.ppat.1008674. PubMed DOI PMC

Peters N.C., Egen J.G., Secundino N., Debrabant A., Kimblin N., Kamhawi S., Lawyer P., Fay M.P., Germain R.N., Sacks D. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science. 2008;321:970–974. doi: 10.1126/science.1159194. PubMed DOI PMC

Regli I.B., Passelli K., Hurrell B.P., Tacchini-Cottier F. Survival Mechanisms Used by Some Leishmania Species to Escape Neutrophil Killing. Front. Immunol. 2017;8:1558. doi: 10.3389/fimmu.2017.01558. PubMed DOI PMC

Gueirard P., Laplante A., Rondeau C., Milon G., Desjardins M. Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell. Microbiol. 2008;10:100–111. doi: 10.1111/j.1462-5822.2007.01018.x. PubMed DOI

Cecílio P., Pérez-Cabezas B., Santarém N., Maciel J., Rodrigues V., Cordeiro da Silva A. Deception and manipulation: The arms of Leishmania, a successful parasite. Front. Immunol. 2014;5:480. doi: 10.3389/fimmu.2014.00480. PubMed DOI PMC

Real F., Florentino P.T., Reis L.C., Ramos-Sanchez E.M., Veras P.S., Goto H., Mortara R.A. Cell-to-cell transfer of Leishmania amazonensis amastigotes is mediated by immunomodulatory LAMP-rich parasitophorous extrusions. Cell. Microbiol. 2014;16:1549–1564. doi: 10.1111/cmi.12311. PubMed DOI PMC

Thomas S.A., Nandan D., Kass J., Reiner N.E. Countervailing, time-dependent effects on host autophagy promote intracellular survival of Leishmania. J. Biol. Chem. 2018;293:2617–2630. doi: 10.1074/jbc.M117.808675. PubMed DOI PMC

Getti G.T., Cheke R.A., Humber D.P. Induction of apoptosis in host cells: A survival mechanism for Leishmania parasites? Parasitology. 2008;135:1391–1399. doi: 10.1017/S0031182008004915. PubMed DOI

Salei N., Hellberg L., Köhl J., Laskay T. Enhanced survival of Leishmania major in neutrophil granulocytes in the presence of apoptotic cells. PLoS ONE. 2017;12:e0171850. doi: 10.1371/journal.pone.0171850. PubMed DOI PMC

Pacheco-Fernandez T., Volpedo G., Verma C., Satoskar A.R. Understanding the immune responses involved in mediating protection or immunopathology during leishmaniasis. Biochem. Soc. Trans. 2021;49:297–311. doi: 10.1042/BST20200606. PubMed DOI

Sacks D.L. The null hypothesis of IFN-γ and monocyte function in leishmaniasis. Cell Host Microbe. 2020;27:683–684. doi: 10.1016/j.chom.2020.04.014. PubMed DOI

Carneiro M.B., Lopes M.E., Hohman L.S., Romano A., David B.A., Kratofil R., Kubes P., Workentine M.L., Campos A.C., Vieira L.Q., et al. Th1-Th2 cross-regulation controls early Leishmania infection in the skin by modulating the size of the permissive monocytic host cell reservoir. Cell Host Microbe. 2020;27:752–768. doi: 10.1016/j.chom.2020.03.011. PubMed DOI

Laskay T., van Zandbergen G., Solbach W. Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: Apoptosis as infection-promoting factor. Immunobiology. 2008;213:183–191. doi: 10.1016/j.imbio.2007.11.010. PubMed DOI

van Zandbergen G., Klinger M., Mueller A., Dannenberg S., Gebert A., Solbach W., Laskay T. Cutting Edge: Neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J. Immunol. 2004;173:6521–6525. doi: 10.4049/jimmunol.173.11.6521. PubMed DOI

Ritter U., Frischknecht F., van Zandbergen G. Are neutrophils important host cells for Leishmania parasites? Trends Parasitol. 2009;25:505–510. doi: 10.1016/j.pt.2009.08.003. PubMed DOI

Wanderley J.L.M., Pinto da Silva L.H., Deolindo P., Soong L., Borges V.M., Prates D.B., de Souza A.P.A., Barral A., Balanco J.M.d.F., do Nascimento M.T.C., et al. Cooperation between apoptotic and viable metacyclics enhances the pathogenesis of Leishmaniasis. PLoS ONE. 2009;4:e5733. doi: 10.1371/journal.pone.0005733. PubMed DOI PMC

Van Zandbergen G., Bollinger A., Wenzel A., Kamhawi S., Voll R., Klinger M., Müller A., Hölscher C., Herrmann M., Sacks D., et al. Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc. Natl. Acad. Sci. USA. 2006;103:13837–13842. doi: 10.1073/pnas.0600843103. PubMed DOI PMC

El-Hani C., Borges V., Wanderley J.L., Barcinski M. Apoptosis and apoptotic mimicry in Leishmania: An evolutionary perspective. Front. Cell. Infect. Microbiol. 2012;2:96. doi: 10.3389/fcimb.2012.00096. PubMed DOI PMC

Wanderley J.L.M., DaMatta R.A., Barcinski M.A. Apoptotic mimicry as a strategy for the establishment of parasitic infections: Parasite- and host-derived phosphatidylserine as key molecule. Cell Commun. Signal. 2020;18:10. doi: 10.1186/s12964-019-0482-8. PubMed DOI PMC

Terrazas C., Oghumu S., Jha B.K., Natarajan G., Drew M., Denkers E.Y., Satoskar A.R., McGwire B.S. Subverting immunity from the inside: Strategies of intracellular survival–protozoans. In: Ratcliffe M.J.H., editor. Encyclopedia of Immunobiology. Academic Press; Oxford, UK: 2016. pp. 83–93.

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

Carneiro M.B., Peters N.C. The paradox of a phagosomal lifestyle: How innate host cell-Leishmania amazonensis interactions lead to a progressive chronic disease. Front. Immunol. 2021;12:3468. doi: 10.3389/fimmu.2021.728848. PubMed DOI PMC

Courret N., Fréhel C., Gouhier N., Pouchelet M., Prina E., Roux P., Antoine J.C. Biogenesis of Leishmania-harbouring parasitophorous vacuoles following phagocytosis of the metacyclic promastigote or amastigote stages of the parasites. J. Cell Sci. 2002;115:2303–2316. doi: 10.1242/jcs.115.11.2303. PubMed DOI

Lerm M., Holm Å., Seiron Å., Särndahl E., Magnusson K.-E., Rasmusson B. Leishmania donovani requires functional Cdc42 and Rac1 to prevent phagosomal maturation. Infect. Immun. 2006;74:2613–2618. doi: 10.1128/IAI.74.5.2613-2618.2006. PubMed DOI PMC

Winberg M.E., Rasmusson B., Sundqvist T. Leishmania donovani: Inhibition of phagosomal maturation is rescued by nitric oxide in macrophages. Exp. Parasitol. 2007;117:165–170. doi: 10.1016/j.exppara.2007.04.004. PubMed DOI

Holm Å., Tejle K., Magnusson K.-E., Descoteaux A., Rasmusson B. Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: Correlation with impaired translocation of PKCalpha and defective phagosome maturation. Cell. Microbiol. 2001;3:439–447. doi: 10.1046/j.1462-5822.2001.00127.x. PubMed DOI

Kumar G.A., Karmakar J., Mandal C., Chattopadhyay A. Leishmania donovani internalizes into host cells via caveolin-mediated endocytosis. Sci. Rep. 2019;9:12636. doi: 10.1038/s41598-019-49007-1. PubMed DOI PMC

Matte C., Casgrain P.-A., Séguin O., Moradin N., Hong W.J., Descoteaux A. Leishmania major promastigotes evade LC3-associated phagocytosis through the action of GP63. PLoS Pathog. 2016;12:e1005690. doi: 10.1371/journal.ppat.1005690. PubMed DOI PMC

Paixão A.R., Dias B.R.S., Palma L.C., Tavares N.M., Brodskyn C.I., de Menezes J.P.B., Veras P.S.T. Investigating the phagocytosis of Leishmania using confocal microscopy. J. Vis. Exp. 2021;173:e62459. doi: 10.3791/62459. PubMed DOI

Azevedo E., Oliveira L.T., Castro Lima A.K., Terra R., Dutra P.M.L., Salerno V.P. Interactions between Leishmania braziliensis and macrophages are dependent on the cytoskeleton and myosin Va. J. Parasitol. Res. 2012;2012:275436. doi: 10.1155/2012/275436. PubMed DOI PMC

Young J., Kima P.E. The Leishmania parasitophorous vacuole membrane at the parasite-host interface. Yale. J. Biol. Med. 2019;92:511–521. PubMed PMC

Canton J., Ndjamen B., Hatsuzawa K., Kima P.E. Disruption of the fusion of Leishmania parasitophorous vacuoles with ER vesicles results in the control of the infection. Cell. Microbiol. 2012;14:937–948. doi: 10.1111/j.1462-5822.2012.01767.x. PubMed DOI

Antoine J.C., Lang T., Prina E., Courret N., Hellio R. H-2M molecules, like MHC class II molecules, are targeted to parasitophorous vacuoles of Leishmania-infected macrophages and internalized by amastigotes of L. amazonensis and L. mexicana. J. Cell Sci. 1999;112 Pt 15:2559–2570. doi: 10.1242/jcs.112.15.2559. PubMed DOI

Ndjamen B., Kang B.-H., Hatsuzawa K., Kima P.E. Leishmania parasitophorous vacuoles interact continuously with the host cell’s endoplasmic reticulum; parasitophorous vacuoles are hybrid compartments. Cell. Microbiol. 2010;12:1480–1494. doi: 10.1111/j.1462-5822.2010.01483.x. PubMed DOI PMC

Antoine J.C., Prina E., Lang T., Courret N. The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends Microbiol. 1998;6:392–401. doi: 10.1016/S0966-842X(98)01324-9. PubMed DOI

Okuda K., Tong M., Dempsey B., Moore K.J., Gazzinelli R.T., Silverman N. Leishmania amazonensis engages CD36 to drive parasitophorous vacuole maturation. PLoS Pathog. 2016;12:e1005669. doi: 10.1371/journal.ppat.1005669. PubMed DOI PMC

Batista M.F., Nájera C.A., Meneghelli I., Bahia D. The parasitic intracellular lifestyle of trypanosomatids: Parasitophorous vacuole development and survival. Front. Cell Dev. Biol. 2020;8:396. doi: 10.3389/fcell.2020.00396. PubMed DOI PMC

Martínez-López M., Soto M., Iborra S., Sancho D. Leishmania hijacks myeloid cells for immune escape. Front. Microbiol. 2018;9:883. doi: 10.3389/fmicb.2018.00883. PubMed DOI PMC

Matte C., Arango Duque G., Descoteaux A. Leishmania donovani metacyclic promastigotes impair phagosome properties in inflammatory monocytes. Infect. Immun. 2021;89:e0000921. doi: 10.1128/IAI.00009-21. PubMed DOI PMC

da Silva M.F.L., Zampieri R.A., Muxel S.M., Beverley S.M., Floeter-Winter L.M. Leishmania amazonensis arginase compartmentalization in the glycosome is important for parasite infectivity. PLoS ONE. 2012;7:e34022. doi: 10.1371/journal.pone.0034022. PubMed DOI PMC

Boitz J.M., Gilroy C.A., Olenyik T.D., Paradis D., Perdeh J., Dearman K., Davis M.J., Yates P.A., Li Y., Riscoe M.K., et al. Arginase is essential for survival of Leishmania donovani promastigotes but not intracellular amastigotes. Infect. Immun. 2017;85:e00554-16. doi: 10.1128/IAI.00554-16. PubMed DOI PMC

Bichiou H., Bouabid C., Rabhi I., Guizani-Tabbane L. Transcription factors interplay orchestrates the immune-metabolic response of Leishmania infected macrophages. Front. Cell. Infect. Microbiol. 2021;11:660415. doi: 10.3389/fcimb.2021.660415. PubMed DOI PMC

Torrecilhas A.C., Soares R.P., Schenkman S., Fernández-Prada C., Olivier M. Extracellular vesicles in trypanosomatids: Host cell communication. Front. Cell. Infect. Microbiol. 2020;10:750. doi: 10.3389/fcimb.2020.602502. PubMed DOI PMC

Liévin-Le Moal V., Loiseau P.M. Leishmania hijacking of the macrophage intracellular compartments. FEBS J. 2016;283:598–607. doi: 10.1111/febs.13601. PubMed DOI

Wanderley J.L., Moreira M.E., Benjamin A., Bonomo A.C., Barcinski M.A. Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L) amazonensis in mammalian hosts. J. Immunol. 2006;176:1834–1839. doi: 10.4049/jimmunol.176.3.1834. PubMed DOI

Wanderley J.L.M., Deolindo P., Carlsen E., Portugal A.B., DaMatta R.A., Barcinski M.A., Soong L. CD4+ T cell-dependent macrophage activation modulates sustained PS exposure on intracellular amastigotes of Leishmania amazonensis. Front. Cell. Infect. Microbiol. 2019;9:105. doi: 10.3389/fcimb.2019.00105. PubMed DOI PMC

Rittig M.G., Bogdan C. Leishmania-host-cell interaction: Complexities and alternative views. Parasitol. Today. 2000;16:292–297. doi: 10.1016/S0169-4758(00)01692-6. PubMed DOI

Bidri M., Vouldoukis I., Mossalayi M.D., Debré P., Guillosson J.J., Mazier D., Arock M. Evidence for direct interaction between mast cells and Leishmania parasites. Parasite Immunol. 1997;19:475–483. doi: 10.1046/j.1365-3024.1997.d01-153.x. PubMed DOI

Naqvi N., Srivastava R., Selvapandiyan A., Puri N. Host mast cells in leishmaniasis: Friend or foe? Trends Parasitol. 2020;36:952–956. doi: 10.1016/j.pt.2020.09.010. PubMed DOI

Rodríguez N.E., Wilson M.E. Eosinophils and mast cells in leishmaniasis. Immunol. Res. 2014;59:129–141. doi: 10.1007/s12026-014-8536-x. PubMed DOI PMC

Hurrell B.P., Beaumann M., Heyde S., Regli I.B., Müller A.J., Tacchini-Cottier F. Frontline Science: Leishmania mexicana amastigotes can replicate within neutrophils. J. Leukoc. Biol. 2017;102:1187–1198. doi: 10.1189/jlb.4HI0417-158R. PubMed DOI

Passelli K., Billion O., Tacchini-Cottier F. The impact of neutrophil recruitment to the skin on the pathology induced by Leishmania infection. Front. Immunol. 2021;12:446. doi: 10.3389/fimmu.2021.649348. PubMed DOI PMC

Desjardins M., Descoteaux A. Phagocytosis of Leishmania: Interaction with the host and intracellular trafficking. In: Gordon S., editor. Advances in Cellular and Molecular Biology of Membranes and Organelles. Volume 6. JAI Elsevier; Amsterdam, The Netherlands: 1999. pp. 297–316.

Cavalcante-Costa V.S., Costa-Reginaldo M., Queiroz-Oliveira T., Oliveira A.C.S., Couto N.F., Dos Anjos D.O., Lima-Santos J., Andrade L.O., Horta M.F., Castro-Gomes T. Leishmania amazonensis hijacks host cell lysosomes involved in plasma membrane repair to induce invasion in fibroblasts. J. Cell Sci. 2019;132:jcs226183. doi: 10.1242/jcs.226183. PubMed DOI

Silva M. Classical labeling of bacterial pathogens according to their lifestyle in the host: Inconsistencies and alternatives. Front. Microbiol. 2012;3:71. doi: 10.3389/fmicb.2012.00071. PubMed DOI PMC

Pacakova L., Harant K., Volf P., Lestinova T. Three types of Leishmania mexicana amastigotes: Proteome comparison by quantitative proteomic analysis. 2021 unpublished work. PubMed PMC

Holzer T.R., McMaster W.R., Forney J.D. Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol. Biochem. Parasitol. 2006;146:198–218. doi: 10.1016/j.molbiopara.2005.12.009. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...