Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T08:22:49.679Z Has data issue: false hasContentIssue false
  • English
  • Français

An overview on Leishmania (Mundinia) enriettii: biology, immunopathology, LRV and extracellular vesicles during the host–parasite interaction

Published online by Cambridge University Press:  10 December 2017

Larissa F. Paranaiba ,
Lucélia J. Pinheiro ,
Diego H. Macedo ,
Armando Menezes-Neto ,
Ana C. Torrecilhas ,
Wagner L. Tafuri  and
Rodrigo P. Soares
Larissa F. Paranaiba
Affiliation:
Departamento de Parasitologia, Universidade Federal de Minas Gerais – UFMG, Av. Antônio Carlos, 6627 – Pampulha, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Lucélia J. Pinheiro
Affiliation:
Departamento de Patologia Geral, Universidade Federal de Minas Gerais – UFMG, Av Antônio Carlos, 6627 – Pampulha, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Diego H. Macedo
Affiliation:
Centro de Pesquisas René Rachou/Fundação Oswaldo Cruz – CpqRR/FIOCRUZ, Av. Augusto de Lima, 1715 – Barro Preto, 30.190-009, Belo Horizonte, Minas Gerais, Brazil
Armando Menezes-Neto
Affiliation:
Centro de Pesquisas René Rachou/Fundação Oswaldo Cruz – CpqRR/FIOCRUZ, Av. Augusto de Lima, 1715 – Barro Preto, 30.190-009, Belo Horizonte, Minas Gerais, Brazil
Ana C. Torrecilhas
Affiliation:
Departamento de Farmácia, Universidade Federal de São Paulo – UNIFESP, Av. São Nicolau, 210, 09913-030, Diadema, São Paulo, Brazil
Wagner L. Tafuri
Affiliation:
Departamento de Patologia Geral, Universidade Federal de Minas Gerais – UFMG, Av Antônio Carlos, 6627 – Pampulha, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Rodrigo P. Soares*
Affiliation:
Centro de Pesquisas René Rachou/Fundação Oswaldo Cruz – CpqRR/FIOCRUZ, Av. Augusto de Lima, 1715 – Barro Preto, 30.190-009, Belo Horizonte, Minas Gerais, Brazil
*
Author for correspondence: Rodrigo P. Soares, E-mail: rsoares@cpqrr.fiocruz.br
Get access Rights & Permissions [Opens in a new window]

Abstract

One of the Leishmania species known to be non-infective to humans is Leishmania (Mundinia) enriettii whose vertebrate host is the guinea pig Cavia porcellus. It is a good model for cutaneous leishmaniasis, chemotherapeutic and molecular studies. In the last years, an increased interest has emerged concerning the L. (Mundinia) subgenus after the finding of Leishmania (M.) macropodum in Australia and with the description of other new/putative species such as L. (M.) martiniquensis and ‘L. (M.) siamensis’. This review focused on histopathology, glycoconjugates and innate immunity. The presence of Leishmania RNA virus and shedding of extracellular vesicles by the parasite were also evaluated.

Keywords

Leishmania (Mundinia) enriettiiL. (Mundinia) subgenusChemotherapyImmunopathologyInnate immunityGlycobiologyExtracellular vesiclesRNA virus
Type
Special Issue Review
Information
Parasitology , Volume 145 , Special Issue 10: Parasites and their (endo)symbiotic microbes , September 2018 , pp. 1265 - 1273
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

These authors contributed equally to this work.

References

Adaui, V, Lye, L, Akopyants, N, Zimic, M, Llanos-Cuentas, A, Garcia, L, Maes, I, De Doncker, S, Dobson, D, Arevalo, J, Dujardin, J and Beverley, S (2016) Association of the endobiont double-stranded RNA virus LRV1 With treatment failure for human leishmaniasis caused by Leishmania braziliensis in Peru and Bolivia. The Journal of Infectious Diseases 213, 112–121.Google Scholar
Aebischer, T, Bennett, CL, Pelizzola, M, Vizzardelli, C, Pavelka, N, Urbano, M, Capozzoli, M, Luchini, A, Ilg, T, Granucci, F, Blackburn, CC, Ricciardi-castagnoli, P and Leishmania, Á (2005) A critical role for lipophosphoglycan in proinflammatory responses of dendritic cells to Leishmania mexicana. European Journal of Immunology 35, 476–486.Google Scholar
Akhoundi, M, Kuhls, K, Cannet, A, Votýpka, J and Marty, P (2016) A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Neglected Tropical Diseases 10, 1–40.Google Scholar
Argueta-donohué, J, Carrillo, N, Valdés-Reyes, L, Zentella, A, Aguirre-García, M, Becker, I and Gutiérrez-kobeh, L (2008) Leishmania mexicana: participation of NF-kappaB in the differential production of IL-12 in dendritic cells and monocytes induced by lipophosphoglycan (LPG). Experimental Parasitology 120, 1–9.Google Scholar
Assis, RR, Ibraim, IC, Noronha, FS, Turco, SJ and Soares, RP (2012) Glycoinositolphospholipids from Leishmania braziliensis and L. infantum: modulation of innate immune system and variations in carbohydrate structure. PLoS Neglected Tropical Diseases 6, e1543.Google Scholar
Atayde, VD, Suau, HA, Townsend, S, Hassani, K, Kamhawi, S and Olivier, M (2015) Exosome secretion by the parasitic protozoan Leishmania within the sand fly midgut. HHS Public Access 13, 957–967.Google Scholar
Australian Government (2016) Spence S. Primefact: Leishmaniasis. In Industries, DoP, editor. 1st edn. Sidney, Australia, pp. 1-3. Available at http://www.dpi.nsw.gov.au/content/biosecurity/animal/humans/leishmaniasisGoogle Scholar
Balaraman, S, Singh, VK, Tewary, P and Madhubala, R (2005) Leishmania lipophosphoglycan activates the transcription factor activating protein 1 in J774A.1 macrophages through the extracellular signal-related kinase (ERK) and p38 mitogen-activated protein kinase. Molecular and Biochemical Parasitology 139, 117–127.Google Scholar
Barratt, J, Kaufer, A, Peters, B, Craig, D, Lawrence, A, Roberts, T and Ellis, J (2017) Isolation of novel trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) provides support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae. PLoS Neglected Tropical Diseases 11, 1–26.Google Scholar
Becker, I, Salaiza, N, Aguirre, M, Delgado, J, Carrillo-Carrasco, N, Kobeh, LG, Ruiz, A, Cervantes, R, Torres, AP, Cabrera, N, González, A, Maldonado, C and Isibasi, A (2003) Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Molecular and Biochemical Parasitology 130, 65–74.Google Scholar
Belehu, A and Turk, JL (1976) Establishment of cutaneous Leishmania enriettii infection in hamsters. Infection and Immunity 13, 1235–1241.Google Scholar
Boisseau-Garsaud, AM, Cales-Quist, D, Desbois, N, Jouannelle, J, Jouannelle, A, Pratlong, F and Dedet, JP (2000) A new case of cutaneous infection by a presumed monoxenous trypanosomatid in the island of Martinique (French West Indies). Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 51–52.Google Scholar
Bryceson, AD, Bray, RS and Dumonde, DC (1974) Experimental cutaneous leishmaniasis. IV. Selective suppression of cell-mediated immunity during the response of Guinea-pigs to infection with Leishmania enriettii. Clinical Experimental Immunology 16, 189–202.Google Scholar
Bualert, L, Charungkiattikul, W, Thongsuksai, P, Mungthin, M, Siripattanapipong, S, Khositnithikul, R and Leelayoova, S (2012) Case report: autochthonous disseminated dermal and visceral leishmaniasis in an AIDS patient, Southern Thailand, caused by Leishmania siamensis. American Journal of Tropical Medicine and Hygiene 86, 821–824.Google Scholar
Campos, JH, Soares, RP, Ribeiro, K, Andrade, AC, Batista, WL and Torrecilhas, AC (2015) Extracellular vesicles: role in inflammatory responses and potential uses in vaccination in cancer and infectious diseases. Journal of Immunology Research 2015, 1–14.Google Scholar
Cantanhêde, L, da Silva Júnior, C, Ito, M, Felipin, K, Nicolete, R, Salcedo, J, Porrozzi, R, Cupolillo, E and de Ferreira, RG (2015) Further evidence of an association between the presence of Leishmania RNA virus 1 and the mucosal manifestations in tegumentary leishmaniasis patients. PLoS Neglected Tropical Diseases 15, 1–11.Google Scholar
Chow, LM, Wong, AK, Ullman, B and Wirth, DF (1993) Cloning and functional analysis of an extrachromosomally amplified multidrug resistance-like gene in Leishmania enriettii. Molecular and Biochemical Parasitology 60, 195–208.Google Scholar
Chusri, S, Thammapalo, S, Silpapojakul, K and Siriyasatien, P (2014) Animal reservoirs and potential vectors of Leishmania siamensis in southern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 45, 13–19.Google Scholar
Coelho-Finamore, JM, Freitas, VC, Assis, RR, Melo, MN, Novozhilova, N, Secundino, NF, Pimenta, PF, Turco, SJ and Soares, RP (2011) Leishmania infantum: lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. International Journal for Parasitology 41, 333–342.Google Scholar
Cotton, JA (2017) The expanding world of human leishmaniasis. Trends in Parasitology 33, 341–344.Google Scholar
de Assis, RR, Ibraim, IC, Nogueira, PM, Soares, RP and Turco, SJ (2012) Glycoconjugates in New world species of Leishmania: polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. Biochimica et Biophysica Acta 1820, 1354–1365.Google Scholar
de Guerra, JAO, das Barbosa, MGV, de Loureiro, ACSP, Coelho, CP, Rosa, GG and de Coelho, LIACR (2007) Leishmaniose tegumentar americana em crianças: aspectos epidemiológicos de casos atendidos em Manaus, Amazonas, Brasil. Cadernos de Saúde Pública 23, 2215–2223.Google Scholar
de Veer, MJ, Curtis, JM, Baldwin, TM, DiDonato, JA, Sexton, A, McConville, MJ, Handman, E and Schofield, L (2003) Myd88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and toll-like receptor 2 signaling. European Journal of Immunology 33, 2822–2831.Google Scholar
Desbois, N, Pratlong, F, Quist, D and Dedet, J-P (2014) Leishmania (Leishmania) martiniquensis n. sp. (Kinetoplastida: Trypanosomatidae), description of the parasite responsible for cutaneous leishmaniasis in Martinique Island (French West Indies). Parasite 21, 1–4.Google Scholar
Dodge, MA, Waller, RF, Chow, LMC, Zaman, MM, Cotton, LM, McConville, MJ and Wirth, DF (2004) Localization and activity of multidrug resistance protein 1 in the secretory pathway of Leishmania parasites. Molecular Microbiology 51, 1563–1575.Google Scholar
Dougall, A, Shilton, C, Low Choy, J, Alexander, B and Walton, S (2009) New reports of Australian cutaneous leishmaniasis in Northern Australian macropods. Epidemiology and Infection 137, 1516–1520.Google Scholar
Dougall, AM, Alexander, B, Holt, DC, Harris, T, Sultan, AH, Bates, PA, Rose, K and Walton, SF (2011) Evidence incriminating midges (Diptera: Ceratopogonidae) as potential vectors of Leishmania in Australia. International Journal for Parasitology 41, 571–579.Google Scholar
Ercoli, N and Fink, R (1962) Chemotherapy of experimental Leishmania enriettii infection. Experimental Biology and Medicine 27231, 445–448.Google Scholar
Espinosa, OA, Serrano, MG, Camargo, EP, Teixeira, MMG and Shaw, JJ (2016) An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology 15, 1–13.Google Scholar
Ginouvès, M, Simon, S, Bourreau, E, Lacoste, V, Ronet, C, Couppié, P and Nacher, M (2016) Prevalence and distribution of Leishmania RNA virus 1 in Leishmania parasites from French Guiana. The American Journal of Tropical Medicine and Hygiene 94, 102–106.Google Scholar
Grimaldi, G, Tesh, RB and McMahon-Pratt, D (1989) A review of the geographic distribution and epidemiology of leishmaniasis in the New World. The American Journal of Tropical Medicine and Hygiene 41, 687–725.Google Scholar
Guilbride, L, Myler, PJ and Stuart, KD (1992) Distribution and sequence divergence of LRV1 viruses among different Leishmania species. Molecular and Biochemical Parasitology 54, 101–104.Google Scholar
Hassani, K, Shio, MT, Martel, C, Faubert, D and Olivier, M (2014) Absence of metalloprotease GP63 alters the protein content of Leishmania exosomes. PLoS ONE 9, 1–14.Google Scholar
Ibraim, IC, de Assis, RR, Pessoa, NL, Campos, MA, Melo, MN, Turco, SJ and Soares, RP (2013) Two biochemically distinct lipophosphoglycans from Leishmania braziliensis and Leishmania infantum trigger different innate immune responses in murine macrophages. Parasites & Vectors 6, 1–11.Google Scholar
Ito, M, Catanhêde, L, Katsuragawa, T, Silva Junior, C, Camargo, L, de Mattos, RG and Vilallobos-Salcedo, J (2015) Correlation between presence of Leishmania RNA virus 1 and clinical characteristics of nasal mucosal. Brazilian Journal of Otorhinolaryngology 81, 533–540.Google Scholar
Ives, A, Ronet, C, Prevel, F, Ruzzante, G, Fuertes-Marraco, S, Schutz, F, Zangger, H, Revaz-Breton, M, Lye, L-F, Hickerson, SM, Beverley, SM, Acha-Orbea, H, Launois, P, Fasel, N and Masina, S (2011) Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331, 775–778.Google Scholar
Jirků, M, Yurchenko, VY, Lukeš, J and Maslov, DA (2012) New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the Trypanosomatidae. The Journal of Eukaryotic Microbiology 59, 537–547.Google Scholar
Kanjanopas, K, Siripattanapipong, S, Ninsaeng, U, Hitakarun, A, Jitkaew, S, Kaewtaphaya, P and Leelayoova, S (2013) Sergentomyia (Neophlebotomus) gemmea, a potential vector of Leishmania siamensis in southern Thailand. BMC Infectious Diseases 13, 1–4.Google Scholar
Kwakye-Nuako, G, Mosore, MT, Duplessis, C, Bates, MD, Puplampu, N, Mensah-Attipoe, I and Bates, PA (2015) First isolation of a new species of Leishmania responsible for human cutaneous leishmaniasis in Ghana and classification in the Leishmania enriettii complex. International Journal for Parasitology 45, 679–684.Google Scholar
Laban, A and Wirth, DF (1989) Transfection of Leishmania enriettii and expression of chloramphenicol acetyltransferase gene. Proceedings of the National Academy of Sciences of the USA 86, 9119–9123.Google Scholar
Laban, A, Tobin, J, Curotto de Lafaille, M and Wirth, D (1990) Stable expression of the bacterial neor gene in Leishmania enriettii. Nature 343, 572–574.Google Scholar
Lainson, R (1997) On Leishmania enriettii and other enigmatic Leishmania species of the neotropics. Memórias do Instituto Oswaldo Cruz 92, 377–387.Google Scholar
Landfear, SM and Wirth, DF (1985) Structure of mRNA encoded by tubulin genes in Leishmania enriettii. Molecular and Biochemical Parasitology 15, 61–82.Google Scholar
Landfear, SM, McMahon-Pratt, D and Wirth, DF (1983) Tandem arrangement of tubulin genes in the protozoan parasite Leishmania enriettii. Molecular and Cellular Biology 3, 1070–1076.Google Scholar
Langford, CK, Little, BM, Kavanaugh, MP and Landfear, SM (1994) Functional expression of two glucose transporter isoforms from the parasitic protozoan Leishmania enriettii. Journal of Biological Chemistry 269, 17939–17943.Google Scholar
Liautaud, B, Vignier, N, Miossec, C, Plumelle, Y, Kone, M, Delta, D, Ravel, C, Cabié, A and Desbois, N (2015) First case of visceral leishmaniasis caused by Leishmania martiniquensis. American Journal of Tropical Medicine and Hygiene 92, 317–319.Google Scholar
Lobato Paraense, W (1953) The spread of Leishmania enriettii through the body of the guinea pig. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 556–560.Google Scholar
Lobsiger, L, Muller, N, Schweizer, T, Frey, CF, Wiederkehr, D, Zumkehr, B and Gottstein, B (2010) An autochthonous case of cutaneous bovine leishmaniasis in Switzerland. Veterinary Parasitology 169, 408–414.Google Scholar
Macedo, DH, Menezes-Neto, A, Rugani, JM, Silva, SO, Melo, MN, Lye, L, Beverley, SM, Gontijo, CM and Soares, RP (2016) Typical and atypical lesions in the State of Minas Gerais, Brazil. Molecular & Biochemical Parasitology 210, 50–54.Google Scholar
Machado, MI, Milder, RV, Pacheco, RS, Silva, M, Braga, RR and Lainson, R (1994) Naturally acquired infections with Leishmania enriettii Muniz and Medina 1948 in guinea-pigs from São Paulo, Brazil. Parasitology 109, 135–138.Google Scholar
Marcilla, A, Martin-Jaular, L, Trelis, M, De Menezes-neto, A, Osuna, A, Bernal, D, Fernandez-becerra, C, Almeida, IC and Portillo, HA (2014) Extracellular vesicles in parasitic diseases. Journal of Extracellular Vesicles 1, 1–15.Google Scholar
Medina, H (2001) Estudos sobre leishmaniose: I. Primeiros casos de Leishmaniose Espontânea observados em cobáios. Brazilian Archives of Biology and Technology 1, 13–55.Google Scholar
Molyneux, DH (1974) Virus-like particles in Leishmania parasites. Nature 249, 588–589.Google Scholar
Muller, N, Welle, M, Lobsiger, L, Stoffel, MH, Boghenbor, KK, Hilbe, M and Von Bomhard, W (2009) Occurrence of Leishmania sp. in cutaneous lesions of horses in Central Europe. Veterinary Parasitology 166, 346–351.Google Scholar
Muniz, J and Medina, H (1948) Cutaneous leishmaniasis of the guinea pig, Leishmania enriettii n. sp. Hospital Rio de Janeiro, Brazil, 33, 7–25.Google Scholar
Neal, RA, van Bueren, J and Hooper, G (1988) The activity of nitrofurazone and furazolidone against Leishmania donovani, L. major and L. enriettii in vitro and in vivo. Annals of Tropical Medicine and Parasitology 82, 453–456.Google Scholar
Nogueira, PM, Ribeiro, K, Silveira, ACO, Campos, JH, Martins-Filho, OA, Bela, SR, Campos, MA, Pessoa, NL, Colli, W, Alves, MJM, Soares, RP and Torrecilhas, AC (2015) Vesicles from different Trypanosoma cruzi strains trigger differential innate and chronic immune responses. Journal of Extracellular Vesicles 4, 1–16.Google Scholar
Nogueira, PM, Assis, RR, Torrecilhas, AC, Saraiva, EM, Pessoa, NL, Campos, MA, Marialva, EF, Ríos-Velasquez, CM, Pessoa, FA, Secundino, NF, Rugani, JN, Nieves, E, Turco, SJ, Melo, MN and Soares, RP (2016) Lipophosphoglycans from Leishmania amazonensis strains display immunomodulatory properties via TLR4 and do not affect sand fly infection. PLoS Neglected Tropical Diseases 10, 1–17.Google Scholar
Ogg, MM, Carrion, R, de Botelho, ACC, Mayrink, W, Correa-Oliveira, R and Patterson, JL (2003) Short report: quantification of Leishmania virus RNA in clinical samples and its possible role in pathogenesis. The American Journal of Tropical Medicine and Hygiene 69, 309–313.Google Scholar
Paranaíba, LF, de Assis, RR, Nogueira, PM, Torrecilhas, AC, Campos, JH, de Silveira, ACO, Martins-Filho, OA, Pessoa, NL, Campos, MA, Parreiras, PM, Melo, MN, de Gontijo, NF and Soares, RPP (2015) Leishmania enriettii: biochemical characterisation of lipophosphoglycans (LPGs) and glycoinositolphospholipids (GIPLs) and infectivity to Cavia porcellus. Parasites & Vectors 8, 1–14.Google Scholar
Paranaíba, LF, Pinheiro, LJ, Torrecilhas, AC, Macedo, DH, Menezes-Neto, A, Tafuri, WL and Soares, RP (2017) Leishmania enriettii, Muniz & Medina, 1948 a highly diverse parasite is here to stay. PLoS Pathogens 13, 1–5.Google Scholar
Passero, LFD, Assis, RR, da Silva, TNF, Nogueira, PM, Macedo, DH, Pessoa, NL, Campos, MA, Laurenti, MD and Soares, RP (2015) Differential modulation of macrophage response elicited by glycoinositolphospholipids and lipophosphoglycan from Leishmania (Viannia) shawi. Parasitology International 64, 32–35.Google Scholar
Pereira, LDOR, Maretti-Mira, AC, Rodrigues, KM, Lima, RB, de Oliveira-neto, MP, Cupolillo, E, Pirmez, C and de Oliveira, MP (2013) Severity of tegumentary leishmaniasis is not exclusively associated with Leishmania RNA virus 1 infection in Brazil. Memórias do Instituto Oswaldo Cruz 108, 665–667.Google Scholar
Pereira, RMS, Luiza, K, Teixeira, D, Barreto-de-souza, V, Calegari-Silva, TC, De-Melo, LDB, Soares, DC, Bou-habib, DC, Silva, M and Saraiva, EM (2010) Novel role for the double-stranded RNA-activated protein kinase PKR: modulation of macrophage infection by the protozoan parasite Leishmania. FASEB Journal 24, 617–626.Google Scholar
Pothirat, T, Tantiworawit, A, Chaiwarith, R, Jariyapan, N, Wannasan, A, Siriyasatien, P and Bates, PA (2014) First isolation of Leishmania from Northern Thailand: case report, identification as Leishmania martiniquensis and phylogenetic position within the Leishmania enriettii complex. PLoS Neglected Tropical Diseases 8, 1–8.Google Scholar
Privé, C and Descoteaux, A (2000) A Leishmania donovani promastigotes evade the activation of mitogen-activated protein kinases p38, c-Jun N-terminal kinase, and extracellular signal-regulated kinase-1/2 during infection of naive macrophages. European Journal of Immunology 30, 2235–2244.Google Scholar
Proudfoot, L, Donnell, CAO and Liew, F (1995) Glycoinositolphospholipids of Leishmania major inhibit nitric oxide synthesis and reduce leishmanicidal activity in murine macrophages. European Journal of Immunology 25, 745–750.Google Scholar
Reuss, SM, Dunbar, MD, Calderwood Mays, MB, Owen, JL, Mallicote, MF, Archer, LL and Wellehan, JFX (2012) Autochthonous Leishmania siamensis in horse, Florida, USA. Emerging Infectious Diseases 18, 1545–1547.Google Scholar
Rezai, HR, Behbehani, AB, Gettner, S and Ardehali, S (1988) Effect of levamisole on the course of experimental leishmaniasis in guinea-pigs and mice: haematological and immunological findings. Annals of Tropical Medicine and Parasitology 82, 243–249.Google Scholar
Rocha, MN, Corrêa, CM, Melo, MN, Beverley, SM, Martins-Filho, OA, Madureira, AP and Soares, RP (2013) An alternative in vitro drug screening test using Leishmania amazonensis transfected with red fluorescent protein. Diagnostic Microbiology and Infectious Disease 75, 282–291.Google Scholar
Rose, K, Curtis, J, Baldwin, T, Mathis, A, Kumar, B, Sakthianandeswaren, A, Spurck, T, Low Choy, J and Handman, E (2004) Cutaneous leishmaniasis in red kangaroos: isolation and characterisation of the causative organisms. International Journal for Parasitology 34, 655–664.Google Scholar
Sacks, DL, Pimenta, PF, McConville, MJ, Schneider, P and Turco, SJ (1995) Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. The Journal of Experimental Medicine 181, 685–697.Google Scholar
Scheffter, SM, Ro, YT, Chung, IK and Patterson, JL (1995) The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology 212, 84–90.Google Scholar
Seblova, V, Sadlova, J, Vojtkova, B, Votypka, J, Carpenter, S, Bates, PA and Volf, P (2015) The biting midge Culicoides sonorensis (Diptera: Ceratopogonidae) is capable of developing late stage infections of Leishmania enriettii. PLoS Neglected Tropical Diseases 9, 1–15.Google Scholar
Silverman, JM, Clos, J, Horakova, E, Wang, AY, Wiesgigl, M, Kelly, I and Reiner, NE (2010) Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. The Journal of Immunology 185, 5011–5022.Google Scholar
Soares, RPP, Cardoso, TL, Barron, T, Araújo, MSS, Pimenta, PFP and Turco, SJ (2005) Leishmania braziliensis: a novel mechanism in the lipophosphoglycan regulation during metacyclogenesis. International Journal for Parasitology 35, 245–253.Google Scholar
Stack, SP, Stein, DA and Landfear, SM (1990) Structural isoforms of a membrane transport protein from Leishmania enriettii. Molecular and Cellular Biology 10, 6785–6790.Google Scholar
Stephens, NA and Hajduk, SL (2011) Endosomal localization of the serum resistance-associated protein in African trypanosomes confers human infectivity. Eukaryotic Cell 10, 1023–1033.Google Scholar
Steverding, D (2017) The history of leishmaniasis. Parasites & Vectors 10, 1–10.Google Scholar
Szempruch, AJ, Dennison, L, Kieft, R, Harrington, JM and Hajduk, SL (2016) Parasites. Nature Publishing Group 14, 669–675.Google Scholar
Tobin, JF, Laban, A and Wirth, DF (1991) Homologous recombination in Leishmania enriettii. Proceedings of the National Academy of Sciences of the USA 88, 864–868.Google Scholar
Torrecilhas, AC, Schumacher, RI, Alves, MJM and Colli, W (2012) Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes and Infection 14, 1465–1474.Google Scholar
Trocoli Torrecilhas, AC, Tonelli, RR, Pavanelli, WR, da Silva, JS, Schumacher, RI, de Souza, W and Manso Alves, MJ (2009) Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes and Infection 11, 29–39.Google Scholar
Twu, O, de Miguel, N, Lustig, G, Stevens, GC, Vashisht, AA, Wohlschlegel, JA and Johnson, PJ (2013) Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathogens 9, e1003482.Google Scholar
Villaseñor-Cardoso, M, Salaiza, N, Delgado, J, Gutiérrez-Kobeh, L, Pérez-Torres, A and Becker, I (2008) Mast cells are activated by Leishmania mexicana LPG and regulate the disease outcome depending on the genetic background of the host. Parasite Immunology 3, 425–434.Google Scholar
Vivarini, DC, de Meirelles, R, Pereira, S, Luiza, K, Teixeira, D, Calegari-silva, TC, Bellio, M, Laurenti, MD, Eduardo, C, Corbett, P, Gomes, DC, Soares, RP, Silva, M, Silveira, FT and Lopes, UG (2011) Human cutaneous leishmaniasis: interferon-dependent expression of double-stranded RNA-dependent protein kinase (PKR) via TLR2. FASEB Journal 25, 4162–4173.Google Scholar
Wong, ILK and Chow, LMC (2006) The role of Leishmania enriettii multidrug resistance protein 1 (LeMDR1) in mediating drug resistance is iron-dependent. Molecular and Biochemical Parasitology 150, 278–287.Google Scholar
Wong, ILK, Chan, K-F, Burkett, BA, Zhao, Y, Chai, Y, Sun, H, Chan, TH and Chow, LMC (2007) Flavonoid dimers as bivalent modulators for pentamidine and sodium stiboglucanate resistance in Leishmania. Antimicrobial Agents and Chemotherapy 51, 930–940.Google Scholar
Young, DG and Duncan, MA (1994) Guide to the Identification and Geographic Distribution of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae), 54th edn., Associated Publishers, American Entomological Institute, Gainesville.Google Scholar