Serodiagnosis and therapeutic monitoring of New-World tegumentary leishmaniasis using synthetic type-2 glycoinositolphospholipid-based neoglycoproteins

References

• Goto H, Lindoso JA. Current diagnosis and treatment of cutaneous and mucocutaneous leishmaniasis. Expert Rev Anti Infect Ther. 2010;8(4):419–433.
   PubMed Web of Science ®Google Scholar
• Ramírez JL, Guevara P. Persistent infections by Leishmania (Viannia) braziliensis. Mem Inst Oswaldo Cruz. 1997;92(3):333–338.
   PubMed Web of Science ®Google Scholar
• Amato VS, Tuon FF, Bacha HA, et al. Mucosal leishmaniasis. Current scenario and prospects for treatment. Acta Trop. 2008;105:1–9.
   PubMed Web of Science ®Google Scholar
• Gaze ST, Dutra WO, Lessa M, et al. Mucosal leishmaniasis patients display an activated inflammatory T-cell phenotype associated with a nonbalanced monocyte population. Scand J Immunol. 2006;63(1):70–78.
   PubMed Web of Science ®Google Scholar
• Scorza B, Carvalho E, Wilson M. Cutaneous manifestations of human and murine leishmaniasis. Int J Mol Sci. 2017;18(6):1296–1296.
   PubMed Web of Science ®Google Scholar
• Hashiguchi Y, Gomez EL, Kato H, et al. Diffuse and disseminated cutaneous leishmaniasis: clinical cases experienced in Ecuador and a brief review. Trop Med Health. 2016 Mar 14;44:2. doi:10.1186/s41182-016-0002-0. PMID: 27398061; PMCID: PMC4934146.
   PubMedGoogle Scholar
• Turetz ML, Machado PR, Ko AI, et al. Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis. 2002;186(12):1829–1834.
   PubMed Web of Science ®Google Scholar
• Machado PRL, Rosa MEA, Guimarães LH, et al. Treatment of disseminated leishmaniasis with liposomal amphotericin B. Clin Infect Dis. 2015;61(6):945–949.
   PubMed Web of Science ®Google Scholar
• Neves LO, Talhari AC, Gadelha EPN, et al. Estudo clínico randomizado comparando antimoniato de meglumina, pentamidina e anfotericina B para o tratamento da leishmaniose cutânea ocasionada por Leishmania guyanensis. An Bras Dermatol. 2011;86(6):1092–1101.
   PubMed Web of Science ®Google Scholar
• Zulfiqar B, Shelper TB, Avery VM. Leishmaniasis drug discovery: recent progress and challenges in assay development. Drug Discov Today. 2017;22:1516–1531.
   PubMed Web of Science ®Google Scholar
• Gomes CM, de Morais OO, Roselino AM, et al. Complementary exams in the diagnosis of American tegumentary leishmaniasis. An Bras Dermatol. 2014;89(5):701–709.
   PubMed Web of Science ®Google Scholar
• Pessoa-e-Silva R, Trajano-Silva LAM, Souza MA, et al. Epidemiological, clinical and laboratorial diagnosis of trypanosomiasis. In: Cavalcanti MP, Pereira VRA, Dessein AJJ, editors. Tropical Diseases: An Overview of Major Diseases Occurring in the Americas: Bentham Science Publishers; 2017. p. 1-50.
   Google Scholar
• Maia Z, Lírio M, Mistro S, et al. Comparative study of rK39 Leishmania antigen for serodiagnosis of visceral leishmaniasis: systematic review with meta-analysis. PLoS Negl Trop Dis. 2012 Jan;6(1):e1484. doi:10.1371/journal.pntd.0001484. Epub 2012 Jan 31. PMID: 22303488; PMCID: PMC3269412.
   PubMed Web of Science ®Google Scholar
• Sánchez-Ovejero C, Benito-Lopez F, Díez P, et al. Sensing parasites: Proteomic and advanced bio-detection alternatives. J Proteomics. 2016;136:145–156.
   PubMed Web of Science ®Google Scholar
• Zanetti ADS, Sato CM, Longhi FG, et al. Diagnostic accuracy of Enzyme-Linked Immunosorbent Assays to detect anti-Leishmania antibodies in patients with American Tegumentary Leishmaniasis: a systematic review. Rev Inst Med Trop Sao Paulo. 2019 Aug 19;61:e42. doi:10.1590/S1678-9946201961042. PMID: 31432991; PMCID: PMC6710007.
   PubMed Web of Science ®Google Scholar
• McConville MJ, Homans SW, Thomas-Oates JE, et al. Structures of the glycoinositolphospholipids from Leishmania major. A family of novel galactofuranose-containing glycolipids. J Biol Chem. 1990;265(13):7385–7394.
   PubMed Web of Science ®Google Scholar
• Naderer T, Vince JE, McConville MJ. Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Curr Mol Med. 2004 Sep;4(6):649–665.
   PubMed Web of Science ®Google Scholar
• de Assis RR, Ibraim IC, Nogueira PM, et al. Glycoconjugates in New World species of Leishmania: polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. Biochim Biophys Acta. 2012 Sep;1820(9):1354–1365.
   PubMed Web of Science ®Google Scholar
• Avila JL, Rojas M. A galactosyl(alpha 1-3)mannose epitope on phospholipids of Leishmania mexicana and L. braziliensis is recognized by trypanosomatid-infected human sera. J Clin Microbiol. 1990 Jul;28(7):1530–1537.
   PubMed Web of Science ®Google Scholar
• Avila JL, Rojas M, Garcia L. Persistence of elevated levels of galactosyl-alpha(1-3)galactose antibodies in sera from patients cured of visceral leishmaniasis. J Clin Microbiol. 1988 Sep;26(9):1842–1847.
   PubMed Web of Science ®Google Scholar
• de Souza LMB, Thomaz Soccol V, Petterle RR, et al. Analysis of Leishmania mimetic neoglycoproteins for the cutaneous leishmaniasis diagnosis. Parasitology. 2018;145(14):1938–1948.
   PubMed Web of Science ®Google Scholar
• Al-Salem WS, Ferreira DM, Dyer NA, et al. Detection of high levels of anti-α-galactosyl antibodies in sera of patients with Old World cutaneous leishmaniasis: A possible tool for diagnosis and biomarker for cure in an elimination setting. Parasitology. 2014;141(14):1898–1903.
   PubMed Web of Science ®Google Scholar
• Avila JL, Rojas M, Galili U. Immunogenic Gal alpha 1----3Gal carbohydrate epitopes are present on pathogenic American Trypanosoma and Leishmania. J Immunol. 1989 Apr 15;142(8):2828–2834.
   PubMed Web of Science ®Google Scholar
• Montoya AL, Austin VM, Portillo S, et al. Reversed Immunoglycomics Identifies alpha-Galactosyl-Bearing Glycotopes Specific for Leishmania major Infection. JACS Au. 2021 Aug;1(8):1275–1287.
   PubMedGoogle Scholar
• Almeida IC, Covas DT, Soussumi LM, et al. A highly sensitive and specific chemiluminescent enzyme-linked immunosorbent assay for diagnosis of active Trypanosoma cruzi infection. Transfusion. 1997 Aug;37(8):850–857.
   PubMed Web of Science ®Google Scholar
• Almeida IC, Ferguson MA, Schenkman S, et al. Lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem J. 1994 Dec 15;304(Pt 3):793–802.
   PubMedGoogle Scholar
• Almeida IC, Krautz GM, Krettli AU, et al. Glycoconjugates of Trypanosoma cruzi: A 74 kD antigen of trypomastigotes specifically reacts with lytic anti-α-galactosyl antibodies from patients with chronic Chagas disease. J Clin Lab Anal. 1993;7(6):307–316.
   PubMed Web of Science ®Google Scholar
• Almeida IC, Milani SR, Gorin PA, et al. Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. J Immunol. 1991;146(7):2394–2400.
   PubMed Web of Science ®Google Scholar
• Milani SR, Travassos LR. Anti-alpha-galactosyl antibodies in chagasic patients. Possible biological significance. Braz J Med Biol Res. 1988;21(6):1275–1286.
   PubMed Web of Science ®Google Scholar
• Galili U. Anti-Gal Interaction with Trypanosoma, Leishmania, and Plasmodium Parasites. In: Galili U, editor. The Natural Anti-Gal Antibody as Foe Turned Friend in Medicine. London, San Diego, Cambridge, Oxford: Academic Press, Elsevier; 2018. p. 57–71.
   Google Scholar
• Subramaniam, KS., Austin V, Schocker NS, et al. Anti-α-Gal antibodies detected by novel neoglycoproteins as a diagnostic tool for Old World cutaneous leishmaniasis caused by Leishmania major. Parasitology. 2018;145(13):1758–1764. doi:10.1017/S0031182018000860. PMID: 29898796.
   PubMed Web of Science ®Google Scholar
• Montoya AL, Gil ER, Heydemann EL, et al. Specific Recognition of β-Galactofuranose-Containing Glycans of Synthetic Neoglycoproteins by Sera of Chronic Chagas Disease Patients. Molecules. 2022 Jan 9;27(2):411.
   PubMed Web of Science ®Google Scholar
• Aronson N, Herwaldt BL, Libman M, et al. Diagnosis and Treatment of Leishmaniasis: Clinical Practice Guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Clin Infect Dis. 2016 Dec 15;63(12):e202–e264.
   PubMed Web of Science ®Google Scholar
• Machado GU, Prates FV, Machado PRL. Disseminated leishmaniasis: clinical, pathogenic, and therapeutic aspects. An Bras Dermatol. 2019;94(1):9–16.
   PubMed Web of Science ®Google Scholar
• Weirather JL, Jeronimo SM, Gautam S, et al. Serial quantitative PCR assay for detection, species discrimination, and quantification of Leishmania spp. in human samples. J Clin Microbiol. 2011 Nov;49(11):3892–3904.
   PubMed Web of Science ®Google Scholar
• Muniz AC, Bacellar O, Lago EL, et al. Immunologic Markers of Protection in Leishmania (Viannia) braziliensis Infection: A 5-Year Cohort Study. J Infect Dis. 2016 Aug 15;214(4):570–576.
   PubMed Web of Science ®Google Scholar
• Reed SG, Badaro R, Masur H, et al. Selection of a skin test antigen for American visceral leishmaniasis. Am J Trop Med Hyg. 1986 Jan;35(1):79–85.
   PubMed Web of Science ®Google Scholar
• Ministério da Saúde [Brazilian Ministry of Health]. Manual de Vigilância da Leishmaniose Tegumentar Americana [Manual for Surveillance of cutaneous leishmaniasis]. Brasilia, Brazil: Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis; 2017. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/manual_vigilancia_leishmaniose_tegumentar.pdf.
   Google Scholar
• Pinart M, Rueda JR, Romero GA, et al. Interventions for American cutaneous and mucocutaneous leishmaniasis. Cochrane Database Syst Rev. 2020 Aug 27;8(8):CD004834. doi:10.1002/14651858.CD004834.pub3. PMID: 32853410; PMCID: PMC8094931.
   PubMedGoogle Scholar
• McConville MJ, Ferguson MA. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem J. 1993 Sep 1;294(Pt 2):305–324.
   PubMedGoogle Scholar
• Frey A, Di Canzio J, Zurakowski D. A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods. 1998 Dec 1;221(1-2):35–41.
   PubMed Web of Science ®Google Scholar
• Jirmanus L, Glesby MJ, Guimaraes LH, et al. Epidemiological and clinical changes in American tegumentary leishmaniasis in an area of Leishmania (Viannia) braziliensis transmission over a 20-year period. Am J Trop Med Hyg. 2012 Mar;86(3):426–433.
   PubMed Web of Science ®Google Scholar
• de Lederkremer RM, Colli W. Galactofuranose-containing glycoconjugates in trypanosomatids. Glycobiology. 1995 Sep;5(6):547–552.
   PubMed Web of Science ®Google Scholar
• Travassos LR, Almeida IC. Carbohydrate immunity in American trypanosomiasis. Springer Semin Immunopathol. 1993;15(2-3):183–204.
   PubMed Web of Science ®Google Scholar
• Golgher DB, Colli W, Souto-Padron T, et al. Galactofuranose-containing glycoconjugates of epimastigote and trypomastigote forms of Trypanosoma cruzi. Mol Biochem Parasitol. 1993 Aug;60(2):249–264.
   PubMed Web of Science ®Google Scholar
• Suzuki E, Tanaka AK, Toledo MS, et al. Role of beta-D-galactofuranose in Leishmania major macrophage invasion. Infect Immun. 2002 Dec;70(12):6592–6596.
   PubMed Web of Science ®Google Scholar
• Schnaidman BB, Yoshida N, Gorin PA, et al. Cross-reactive polysaccharides from Trypanosoma cruzi and fungi (especially Dactylium dendroides). J Protozool. 1986 May;33(2):186–191.
   PubMedGoogle Scholar
• Follador I, Araujo C, Bacellar O, et al. Epidemiologic and immunologic findings for the subclinical form of Leishmania braziliensis infection. Clin Infect Dis. 2002 Jun 1;34(11):E54–E58.
   PubMed Web of Science ®Google Scholar
• Greiner M, Pfeiffer D, Smith RD. Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev Vet Med. 2000 May 30;45(1-2):23–41.
   PubMed Web of Science ®Google Scholar
• Fagundes-Silva GA, Vieira-Goncalves R, Nepomuceno MP, et al. Decrease in anti-Leishmania IgG3 and IgG1 after cutaneous leishmaniasis lesion healing is correlated with the time of clinical cure. Parasite Immunol. 2012 Oct;34(10):486–491.
   PubMed Web of Science ®Google Scholar
• de Lima CMF, Magalhães AS, Costa R, et al. High anti-leishmania IgG antibody levels are associated with severity of mucosal leishmaniasis. Front Cell Infect Microbiol. 2021 Apr 9;11:652956. doi:10.3389/fcimb.2021.652956. PMID: 33898330; PMCID: PMC8063102.
   PubMed Web of Science ®Google Scholar
• Ribeiro-de-Jesus A, Almeida RP, Lessa H, et al. Cytokine profile and pathology in human leishmaniasis. Braz J Med Biol Res. 1998 Jan;31(1):143–148.
   PubMed Web of Science ®Google Scholar
• Avila JL, Rojas M, Acosta A. Glycoinositol phospholipids from American Leishmania and Trypanosoma spp: partial characterization of the glycan cores and the human humoral immune response to them. J Clin Microbiol. 1991 Oct;29(10):2305–2312.
   PubMed Web of Science ®Google Scholar
• Assis RR, Ibraim IC, Noronha FS, et al. Glycoinositolphospholipids from Leishmania braziliensis and L. infantum: modulation of innate immune system and variations in carbohydrate structure. PLoS Negl Trop Dis. 2012;6(2):e1543. doi:10.1371/journal.pntd.0001543. Epub 2012 Feb 28. PMID: 22389743; PMCID: PMC3289616.
   PubMed Web of Science ®Google Scholar
• Cabezas Y, Legentil L, Robert-Gangneux F, et al. Leishmania cell wall as a potent target for antiparasitic drugs. A focus on the glycoconjugates. Org Biomol Chem. 2015 Aug;13(31):8393–8404.
   PubMed Web of Science ®Google Scholar
• Mendonca VJ, de Oliveira J, Rimoldi A, et al. Triatominae survey (Hemiptera: Reduviidae: Triatominae) in the south-central region of the state of Bahia, Brazil between 2008 and 2013. Am J Trop Med Hyg. 2015 May;92(5):1076–1080.
   PubMed Web of Science ®Google Scholar
• Ribeiro G, Jr., Dos Santos CGS, Lanza F, et al. Wide distribution of Trypanosoma cruzi-infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019 Dec 26;12(1):604. doi:10.1186/s13071-019-3849-1. PMID: 31878960; PMCID: PMC6933904.
   PubMed Web of Science ®Google Scholar
• Singh S, Kumari V, Singh N. Predicting kala-azar disease manifestations in asymptomatic patients with latent Leishmania donovani infection by detection of antibody against recombinant K39 antigen. Clin Diag Lab Immunol. 2002 May;9(3):568–572.
   PubMedGoogle Scholar
• Pinazo MJ, Posada Ede J, Izquierdo L, et al. Altered hypercoagulability factors in patients with chronic Chagas disease: potential biomarkers of therapeutic response. PLoS Negl Trop Dis. 2016 Jan 4;10(1):e0004269. doi:10.1371/journal.pntd.0004269. PMID: 26727000; PMCID: PMC4700971.
   PubMed Web of Science ®Google Scholar
• Torrico F, Gascon J, Ortiz L, et al. Treatment of adult chronic indeterminate Chagas disease with benznidazole and three E1224 dosing regimens: a proof-of-concept, randomised, placebo-controlled trial. Lancet Infect Dis. 2018 Apr;18(4):419–430.
   PubMed Web of Science ®Google Scholar