Lipophosphoglycans from Leishmania amazonensis Strains Display Immunomodulatory Properties via TLR4 and Do Not Affect Sand Fly Infection

PLoS Neglected Tropical Diseases

Volumn 10, Issue 8, 2016, Pages

  Nogueira, Paula M ^a,b   Assis, Rafael R ^a   Torrecilhas, Ana C ^c   Saraiva, Elvira M ^d   Pessoa, Natália L ^a   Campos, Marco A ^a   Marialva, Eric F ^e   Ríos Velasquez, Cláudia M ^e   Pessoa, Felipe A ^e   Secundino, Nágila F ^a   Rugani, Jerônimo N ^a   Nieves, Elsa ^f   Turco, Salvatore J ^g   Melo, Maria N ^b   Soares, Rodrigo P ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^e INSTITUTO LEÔNIDAS E MARIA DEANE   (Brazil)

^f UNIVERSIDAD DE LOS ANDES   (Venezuela)

^g UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; I KAPPA B; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPHOSPHOGLYCAN; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCLONAL ANTIBODY; NITRITE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; CYTOKINE; GLYCOSPHINGOLIPID; MITOGEN ACTIVATED PROTEIN KINASE KINASE; TLR4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GROWTH CURVE; IMMUNOBLOTTING; IMMUNOMODULATION; INNATE IMMUNITY; LEISHMANIA AMAZONENSIS; LEISHMANIA BRAZILIENSIS; LEISHMANIA FLAVISCUTELLATA; LEISHMANIA INFANTUM; MOLECULAR TYPING; MOUSE; NONHUMAN; PARASITOSIS; PERITONEUM MACROPHAGE; PH MEASUREMENT; PHLEBOVIRUS INFECTION; SAND FLY INFECTION; SKIN LEISHMANIASIS; VISCERAL LEISHMANIASIS; WESTERN BLOTTING; ANIMAL; BRAZIL; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; GENETICS; HOST PARASITE INTERACTION; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; LEISHMANIA MEXICANA; PARASITOLOGY; PSYCHODIDAE;

ANIMALS; BRAZIL; CHO CELLS; CRICETULUS; CYTOKINES; GLYCOSPHINGOLIPIDS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, INNATE; LEISHMANIA MEXICANA; LEISHMANIASIS, CUTANEOUS; MACROPHAGES, PERITONEAL; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PSYCHODIDAE; TOLL-LIKE RECEPTOR 4;

EID: 84988026492     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004848     Document Type: Article

References (71)

1. Herwaldt BL, Leishmaniasis. Lancet. 1999;354: 1191–1199. 10513726
2. Silveira FT, Lainson R, De Castro Gomes CM, Laurenti MD, Corbett CEP, Immunopathogenic competences of Leishmania (V.) braziliensis and L. (L.) amazonensis in American cutaneous leishmaniasis. Parasite Immunol. 2009;31: 423–431. doi: 10.1111/j.1365-3024.2009.01116.x19646206
3. Carvalho BM, Rangel EF, Ready PD, Vale MM, Ecological Niche Modelling Predicts Southward Expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), Vector of Leishmania (Leishmania) amazonensis in South America, under Climate Change. PLoS ONE. 2015;10(11).
4. Grimaldi G, Tesh RB, McMahon-Pratt D, A review of the geographic distribution and epidemiology of leishmaniasis in the New World. American Journal of Tropical Medicine and Hygiene. 1989. pp. 687–725. 2701633
5. Nieves E, Pimenta PFP, Development of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). 2000;37: 134–140.
6. Lainson R, Ecological interactions in the transmission of the leishmaniases. Philos Trans R Soc Lond B Biol Sci. 1988;321: 389–404. 2907150
7. De Assis RR, Ibraim IC, Nogueira PM, Soares RP, Turco SJ, Glycoconjugates in New World species of Leishmania: Polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. Biochim Biophys Acta. Elsevier B.V.; 2012;1820: 1354–1365.
8. Pimenta PF, Saraiva EM, Rowton E, Modi GB, Garraway L a, Beverley SM, et al. Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Proc Natl Acad Sci U S A. 1994;91: 9155–9159. 8090785
9. Kamhawi S, Ramalho-Ortigao M, Van MP, Kumar S, Lawyer PG, Turco SJ, et al. A role for insect galectins in parasite survival. Cell. 2004;119: 329–341. 15543683
10. Brittingham A, Mosser D, Exploitation of the complement system by Leishmania promastigotes. Parasitol Today. 1996;12: 444–447. 15275279
11. Späth GF, Garraway L a, Turco SJ, Beverley SM, The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci U S A. 2003;100: 9536–9541. 12869694
12. Proudfoot L, Nikolaev a V, Feng GJ, Wei WQ, Ferguson M a, Brimacombe JS, et al. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc Natl Acad Sci U S A. 1996;93: 10984–10989. 8855295
13. Giorgione JR, Turco SJ, Epand RM, Transbilayer inhibition of protein kinase C by the lipophosphoglycan from Leishmania donovani. Proc Natl Acad Sci U S A. 1996;93: 11634–11639. 8876188
14. Guimarães-Costa AB, Nascimento MTC, Froment GS, Soares RPP, Morgado FN, Conceição-Silva F, et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A. 2009;106: 6748–6753. doi: 10.1073/pnas.090022610619346483
15. de Carvalho Vivarini a., Pereira RDMS, Dias Teixeira KL, Calegari-Silva TC, Bellio M, Laurenti MD, et al. Human cutaneous leishmaniasis: interferon-dependent expression of double-stranded RNA-dependent protein kinase (PKR) via TLR2. FASEB J. 2011;25: 4162–4173. doi: 10.1096/fj.11-18516521846836
16. Tavares NM, Araújo-Santos T, Afonso L, Nogueira PM, Lopes UG, Soares RP, et al. Understanding the Mechanisms Controlling Leishmania amazonensis Infection In Vitro: The Role of LTB4 Derived From Human Neutrophils. J Infect Dis. 2014;210: 1–11.
17. McConville MJ, Turco SJ, Ferguson M a, Sacks DL, Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 1992;11: 3593–3600. 1396559
18. McConville MJ, Schnur LF, Jaffe C, Schneider P, Structure of Leishmania lipophosphoglycan: inter- and intra-specific polymorphism in Old World species. Biochem J. 1995;310: 807–818. 7575413
19. Sacks DL, Pimenta PF, McConville MJ, Schneider P, Turco SJ, Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J Exp Med. 1995;181: 685–697. 7836922
20. Mahoney AB, Sacks DL, Saraiva E, Modi G, Turco SJ, Intra-species and stage-specific polymorphisms in lipophosphoglycan structure control Leishmania donovani—Sand fly interactions. Biochemistry. 1999;38: 9813–9823. 10433687
21. Soares RPP, Macedo ME, Ropert C, Gontijo NF, Almeida IC, Gazzinelli RT, et al. Leishmania chagasi: Lipophosphoglycan characterization and binding to the midgut of the sand fly vector Lutzomyia longipalpis. Mol Biochem Parasitol. 2002;121: 213–224. 12034455
22. Soares RPP, Barron T, McCoy-Simandle K, Svobodova M, Warburg A, Turco SJ, Leishmania tropica: Intraspecific polymorphisms in lipophosphoglycan correlate with transmission by different Phlebotomus species. Exp Parasitol. 2004;107: 105–114. 15208044
23. Soares RPP, Cardoso TL, Barron T, Araújo MSS, Pimenta PFP, Turco SJ, Leishmania braziliensis: A novel mechanism in the lipophosphoglycan regulation during metacyclogenesis. Int J Parasitol. 2005;35: 245–253. 15722076
24. Coelho-Finamore JM, Freitas VC, Assis RR, Melo MN, Novozhilova N, Secundino NF, et al. Leishmania infantum: Lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. Int J Parasitol. Australian Society for Parasitology Inc.; 2011;41: 333–342.
25. Paranaíba L, de Assis R, Nogueira P, Torrecilhas A, Campos J, Silveira A, et al. Leishmania enriettii: biochemical characterisation of lipophosphoglycans (LPGs) and glycoinositolphospholipids (GIPLs) and infectivity to Cavia porcellus. Parasit Vectors. 2015;8: 31. doi: 10.1186/s13071-015-0633-825595203
26. Passero LFD, Assis RR, da Silva TNF, Nogueira PM, Macedo DH, Pessoa NL, et al. Differential modulation of macrophage response elicited by glycoinositolphospholipids and lipophosphoglycan from Leishmania (Viannia) shawi. Parasitol Int. Elsevier Ireland Ltd; 2015;64: 32–35.
27. Turco SJ, Descoteaux A, The Lipophosphoglycan of Leishmania Parasites. 1992; 65–94.
28. Becker I, Salaiza N, Aguirre M, Delgado J, Carrillo-Carrasco N, Kobeh LG, et al. Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol Biochem Parasitol. 2003;130: 65–74. 12946842
29. de Veer MJ, Curtis JM, Baldwin TM, DiDonato J a., Sexton A, McConville MJ, et al. MyD88 is essential for clearance of Leishmania major: Possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur J Immunol. 2003;33: 2822–2831. 14515266
30. Ibraim IC, de Assis RR, Pessoa NL, Campos MA, Melo MN, Turco SJ, et al. Two biochemically distinct lipophosphoglycans from Leishmania braziliensis and Leishmania infantum trigger different innate immune responses in murine macrophages. Parasit Vectors. 2013;6: 54. doi: 10.1186/1756-3305-6-5423497381
31. Garcia L, Kindt A, Bermudez H, Llanos-Cuentas A, De Doncker S, Arevalo J, et al. Culture-Independent Species Typing of Neotropical Leishmania for Clinical Validation of a PCR-Based Assay Targeting Heat Shock Protein 70 Genes. J Clin Microbiol. 2004;42: 2294–2297. 15131217
32. Orlandi PA, Turco SJ, Structure of the lipid moiety of the Leishmania donovani lipophosphoglycan. J Biol Chem. 1987;262: 10384–10391. 3611065
33. Dubois M, Gilles KA, Hamilton JKJ, Rebers PA, Smith F, Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28: 350–356.
34. Tolson DL, Turco SJ, Beecroft RP, Pearson TW, The immunochemical structure and surface arrangement of Leishmania donovani lipophosphoglycan determined using monoclonal antibodies. Mol Biochem Parasitol. 1989;35: 109–118. 2475775
35. Kelleher M, Curtis JM, Sacks DL, Handman E, Bacic A, Epitope mapping of monoclonal antibodies directed against lipophosphoglycan of Leishmania major promastigotes. Mol Biochem Parasitol. 1994;66: 187–200. 7808469
36. Kolodziej H, Radtke O a., Kiderlen AF, Stimulus (polyphenol, IFN-y, LPS)-dependent nitric oxide production and antileishmanial effects in RAW 264.7 macrophages. Phytochemistry. Elsevier Ltd; 2008;69: 3103–3110.
37. Shapiro SS. JSTOR: Biometrika, Vol. 52, No. 3/4 (Dec., 1965), pp. 591–611. Biometrika. 1965;
38. Desjeux P, Leishmaniasis: Current situation and new perspectives. Comp Immunol Microbiol Infect Dis. 2004;27: 305–318. 15225981
39. Silveira FT, Lainson R, Corbett CEP, Further observations on clinical, histopathological, and immunological features of borderline disseminated cutaneous leishmaniasis caused by Leishmania (Leishmania) amazonensis. Mem Inst Oswaldo Cruz. 2005;100: 525–534. 16184231
40. Sacks D, Kamhawi S. Molecular Aspects of Parasite-Vector and Vector-Host Interacions in Leishmaniasis. 2001;
41. Assis RR, Ibraim IC, Noronha FS, Turco SJ, Soares RP, Glycoinositolphospholipids from Leishmania braziliensis and Leishmania infantum: Modulation of innate immune system and variations in carbohydrate structure. PLoS Negl Trop Dis. 2012;6: 1–11.
42. Rojas-Bernabé A, Garcia-Hernández O, Maldonado-Bernal C, Delegado-Dominguez J, Ortega E, Gutiérrez-Kobeh L, et al. Leishmania mexicana lipophosphoglycan activates ERK and p38 MAP kinase and induces production of proinflammatory cytokines in human macrophages through TLR2 and TLR4. Parasitology. 2014;141: 788–800. doi: 10.1017/S003118201300218724512642
43. Ilg T, Etgess R, Overath P, Mcconvilleq MJ, Thomas-oatest J, Thomasll J, et al. Structure of Leishmania mexicana Lipophosphoglycan. 1992;
44. Argueta-Donohué J, Carrillo N, Valdés-Reyes L, Zentella A, Aguirre-García M, Becker I, et al. Leishmania mexicana: Participation of NF-κB in the differential production of IL-12 in dendritic cells and monocytes induced by lipophosphoglycan (LPG). Exp Parasitol. 2008;120: 1–9. doi: 10.1016/j.exppara.2008.04.00218508052
45. Holzmuller P, Bras-Gonçalves R, Lemesre J-L, Phenotypical characteristics, biochemical pathways, molecular targets and putative role of nitric oxide-mediated programmed cell death in Leishmania. Parasitology. 2006;132Suppl: S19–S32. 17018162
46. Mosser DM, Edwards JP, Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8: 958–969. doi: 10.1038/nri244819029990
47. Cameron P, McGachy A, Anderson M, Paul A, Coombs GH, Mottram JC, et al. Inhibition of lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: the role of cysteine peptidases and the NF-kappaB signaling pathway. J Immunol. 2004;173: 3297–3304. 15322192
48. Calegari-Silva TC, Pereira RMS, De-Melo LDB, Saraiva EM, Soares DC, Bellio M, et al. NF-κB-mediated repression of iNOS expression in Leishmania amazonensis macrophage infection. Immunol Lett. 2009;127: 19–26. doi: 10.1016/j.imlet.2009.08.00919712696
49. Yang Z, Mosser DM, Zhang X, Activation of the MAPK, ERK, following Leishmania amazonensis infection of macrophages. J Immunol. 2007;178: 1077–1085. 17202371
50. Martiny A, Meyer-Fernandes JR, De Souza W, Vannier-Santos MA, Altered tyrosine phosphorylation of ERK1 MAP kinase and other macrophage molecules caused by Leishmania amastigotes. Mol Biochem Parasitol. 1999;102: 1–12. 10477171
51. Calegari-silva TC, Vivarini C, Miqueline M, Dos Santos GRRM, Teixeira KL, Saliba AM, et al. The human parasite Leishmania amazonensis downregulates iNOS expression via NF- k B p50 / p50 homodimer: role of the PI3K / Akt pathway. Open Biol. 2015;5.
52. Srivastava A, Singh N, Mishra M, Kumar V, Gour JK, Bajpai S, et al. Identification of TLR inducing Th1-responsive Leishmania donovani amastigote-specific antigens. Mol Cell Biochem. 2012;359: 359–368. doi: 10.1007/s11010-011-1029-521858498
53. Sarkar A, Aga E, Bussmeyer U, Bhattacharyya A, Möller S, Hellberg L, et al. Infection of neutrophil granulocytes with Leishmania major activates ERK 1/2 and modulates multiple apoptotic pathways to inhibit apoptosis. Med Microbiol Immunol. 2013;202: 25–35. doi: 10.1007/s00430-012-0246-122661217
54. Pimenta PF, Turco SJ, McConville MJ, Lawyer PG, Perkins P V, Sacks DL, Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Science. 1992;256: 1812–1815. 1615326
55. Soares RP, Margonari C, Secundino NC, MacÊdo ME, Da Costa SM, Rangel EF, et al. Differential midgut attachment of Leishmania (Viannia) braziliensis in the sand flies Lutzomyia (Nyssomyia) whitmani and Lutzomyia (Nyssomyia) intermedia. J Biomed Biotechnol. 2010;2010. doi: 10.1155/2010/439174
56. Wilson R, Bates MD, Dostalova A, Jecna L, Dillon RJ, Volf P, et al. Stage-Specific Adhesion of Leishmania Promastigotes to Sand Fly Midguts Assessed Using an Improved Comparative Binding Assay. PLoS Negl Trop Dis. 2010;4: e816. doi: 10.1371/journal.pntd.000081620838647
57. Kamhawi S, Phlebotomine sand flies and Leishmania parasites: friends or foes?Trends Parasitol. 2006;22: 439–445. 16843727
58. Volf P, Myskova J, Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol. 2007;23: 91–92. 17207663
59. Svárovská A, Ant TH, Seblová V, Jecná L, Beverley SM, Volf P, Leishmania major glycosylation mutants require phosphoglycans (lpg2 -) but not lipophosphoglycan (lpg1-) for survival in permissive sand fly vectors. PLoS Negl Trop Dis. 2010;4: 1–7.
60. Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL, The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology. 2000;121 (Pt 1: 25–33. 11085222)
61. Chajbullinova A, Votypka J, Sadlova J, Kvapilova K, Seblova V, Kreisinger J, et al. The development of Leishmania turanica in sand flies and competition with L. major. Parasit Vectors. Parasites & Vectors; 2012;5: 219. doi: 10.1186/1756-3305-5-21923031344
62. Volf P, Nogueira PM, Myskova J, Turco SJ, Soares RP, Structural comparison of lipophosphoglycan from Leishmania turanica and L. major, two species transmitted by Phlebotomus papatasi. Parasitol Int. Elsevier Ireland Ltd; 2014;63: 683–686.
63. Jecna L, Dostalova A, Wilson R, Seblova V, Chang K-P, Bates P a, et al. The role of surface glycoconjugates in Leishmania midgut attachment examined by competitive binding assays and experimental development in sand flies. Parasitology. 2013;140: 1026–32. doi: 10.1017/S003118201300035823611086
64. Di-Blasi T, Lobo AR, Nascimento LM, Córdova-Rojas JL, Pestana K, Marín-Villa M, et al. The Flagellar Protein FLAG1/SMP1 is a Candidate for Leishmania–Sand Fly Interaction. Vector-Borne Zoonotic Dis. 2015;15: 202–209. doi: 10.1089/vbz.2014.173625793476
65. Sacks DL, Leishmania-sand fly interactions controlling species-specific vector competence. Cell Microbiol. 2001;3: 189–196. 11298643
66. Dostálová A, Volf P, Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5: 276. doi: 10.1186/1756-3305-5-27623206339
67. Soares RP, Turco SJ, Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae): a review. An Acad Bras Cienc. 2003;75: 301–330. 12947480
68. Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Filho SPB, et al. Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasit Vectors. Parasites & Vectors; 2016;9: 159. doi: 10.1186/s13071-016-1444-226988559
69. Butcher BA, Turco SJ, Hilty BA, Pimenta PF, Panunzio M, Sacks DL, Deficiency in b1, 3-Galactosyltransferase of a Leishmania major Lipophosphoglycan Mutant Adversely Influences the Leishmania -Sand Fly Interaction. 1996;271: 20573–20579.
70. Dillon RJ, Lane RP, Detection of Leishmania lipophosphoglycan binding proteins in the gut of the sandfly vector. 1999; 27–32.
71. Myskova J, Svobodova M, Beverley SM, Volf P, A lipophosphoglycan-independent development of Leishmania in permissive sand flies. Microbes Infect. 2007;9: 317–324. 17307009