Toxoplasma gondii Recombinant antigen AMA1: Diagnostic Utility of Protein Fragments for the Detection of IgG and IgM Antibodies - Publication - MOST Wiedzy

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Toxoplasma gondii Recombinant antigen AMA1: Diagnostic Utility of Protein Fragments for the Detection of IgG and IgM Antibodies

Abstract

Toxoplasma gondii is an important zoonotic protozoan that infects a wide variety of vertebrates as intermediate hosts. For this reason, the diagnosis of this disease is very important and requires continuous improvement. One possibility is to use recombinant antigens in serological tests. Apical membrane antigen 1 (AMA1), a protein located in specific secretory organelles (micronemes) of T. gondii, is very interesting in regard to its potential diagnostic utility. In the present study, we attempted to identify a fragment of the AMA1 protein with a high sensitivity and specificity for the serological diagnosis of human toxoplasmosis. The full-length AMA1 and two different fragments (AMA1N and AMA1C) were produced using an Escherichia coli expression system. After purification by metal affinity chromatography, recombinant proteins were tested for their utility as antigens in enzyme-linked immunosorbent assays (ELISAs) for the detection of IgG and IgM anti-T. gondii antibodies in human and mouse immune sera. Our data demonstrate that the full-length AMA1 recombinant antigen (corresponding to amino acid residues 67–569 of the native protein) has a better diagnostic potential than its N- or C-terminal fragments. This recombinant protein strongly interacts with specific anti-T. gondii IgG (99.4%) and IgM (80.0%) antibodies, and may be used for developing new tools for diagnostics of toxoplasmosis.

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Details

Category:
Articles
Type:
artykuły w czasopismach
Published in:
Pathogens no. 9, pages 1 - 15,
ISSN: 2076-0817
Language:
English
Publication year:
2020
Bibliographic description:
Ferra B., Holec-Gąsior L., Gatkowska J., Dziadek B., Dzitko K.: Toxoplasma gondii Recombinant antigen AMA1: Diagnostic Utility of Protein Fragments for the Detection of IgG and IgM Antibodies// Pathogens -Vol. 9,iss. 1 (2020), s.1-15
DOI:
Digital Object Identifier (open in new tab) 10.3390/pathogens9010043
Bibliography: test
  1. Pappas, G.; Roussos, N.; Falagas, M.E. Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. J. Parasitol. 2009, 39, 1385-1394. open in new tab
  2. Torgerson, P.R.; Mastroiacovo, P. The global burden of congenital toxoplasmosis: A systematic review. Bull. World Health Organ. 2013, 91, 501-508. open in new tab
  3. Holliman, R.E. Congenital toxoplasmosis: Prevention, screening and treatment. J. Hosp. Infect. 1995, 30, 179- 190. open in new tab
  4. Schmidt, M.; Sonneville, R.; Schnell, D.; Bige, N.; Hamidfar, R.; Mongardon, N.; Castelain, V.; Razazi, K.; Marty, A.; Vincent, F.; et al. Clinical Features and Outcomes in Patients With Disseminated Toxoplasmosis Admitted to Intensive Care: A Multicenter Study. Clin. Infect. Dis. 2013, 57, 1535-1541. open in new tab
  5. Buxton, D. Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: Recent advances. Vet. Res. 1998, 29, 289-310.
  6. Holec-Gasior, L. Toxoplasma gondii recombinant antigens as tools for serodiagnosis of human toxoplasmosis: Current status of studies. Clin. Vaccine Immunol. 2013, 20, 1343-1351. open in new tab
  7. Rostami, A.; Karanis, P.; Fallahi, S. Advances in serological, imaging techniques and molecular diagnosis of Toxoplasma gondii infection. Infection 2018, 46, 303-315. open in new tab
  8. Kotresha, D.; Noordin, R. Recombinant proteins in the diagnosis of toxoplasmosis. APMIS 2010, 118, 529- 542. open in new tab
  9. Ferra, B.; Holec-Gąsior, L.; Kur, J. A new Toxoplasma gondii chimeric antigen containing fragments of SAG2, GRA1, and ROP1 proteins-Impact of immunodominant sequences size on its diagnostic usefulness. Parasitol. Res. 2015, 114, 3291-3299. open in new tab
  10. Ferra, B.; Holec-Gasior, L.; Kur, J. Serodiagnosis of Toxoplasma gondii infection in farm animals (horses, swine, and sheep) by enzyme-linked immunosorbent assay using chimeric antigens. Parasitol. Int. 2015, 64, 288-294. open in new tab
  11. Holec-Gasior, L.; Drapała, D.; Lautenbach, D.; Kur, J. Toxoplasma gondii: Usefulness of ROP1 recombinant antigen in an immunoglobulin G avidity assay for diagnosis of acute toxoplasmosis in humans. Polish J. Microbiol. 2010, 59, 307-310. open in new tab
  12. Pathogens 2020, 9, 43 14 of 15 open in new tab
  13. Holec-Gaşior, L.; Ferra, B.; Drapała, D.; Lautenbach, D.; Kur, J. A new MIC1-MAG1 recombinant chimeric antigen can be used instead of the Toxoplasma gondii lysate antigen in serodiagnosis of human toxoplasmosis. Clin. Vaccine Immunol. 2012, 19, 57-63. open in new tab
  14. Drapała, D.; Holec-Gasior, L.; Kur, J.; Ferra, B.; Hiszczyńska-Sawicka, E.; Lautenbach, D. A new human IgG avidity test, using mixtures of recombinant antigens (rROP1, rSAG2, rGRA6), for the diagnosis of difficult- to-identify phases of toxoplasmosis. Diagn. Microbiol. Infect. Dis. 2014, 79, 342-346. open in new tab
  15. Costa, J.G.; Peretti, L.E.; García, V.S.; Peverengo, L.; González, V.D.G.; Gugliotta, L.M.; Dalla Fontana, M.L.; Lagier, C.M.; Marcipar, I.S. P35 and P22 Toxoplasma gondii antigens abbreviate regions to diagnose acquired toxoplasmosis during pregnancy: Toward single-sample assays. Clin. Chem. Lab. Med. 2017, 55, 595-604. open in new tab
  16. Pietkiewicz, H.; Hiszczyńska-Sawicka, E.; Kur, J.; Petersen, E.; Nielsen, H.V.; Paul, M.; Stankiewicz, M.; Myjak, P. Usefulness of Toxoplasma gondii recombinant antigens (GRA1, GRA7 and SAG1) in an immunoglobulin G avidity test for the serodiagnosis of toxoplasmosis. Parasitol. Res. 2007, 100, 333-337. open in new tab
  17. Beghetto, E.; Buffolano, W.; Spadoni, A.; Del Pezzo, M.; Di Cristina, M.; Minenkova, O.; Petersen, E.; Felici, F.; Gargano, N. Use of an immunoglobulin G avidity assay based on recombinant antigens for diagnosis of primary Toxoplasma gondii infection during pregnancy. J. Clin. Microbiol. 2003, 41, 5414-5418. open in new tab
  18. Ferra, B.T.; Holec-Gąsior, L.; Gatkowska, J.; Dziadek, B.; Dzitko, K.; Grąźlewska, W.; Lautenbach, D. The first study on the usefulness of recombinant tetravalent chimeric proteins containing fragments of SAG2, GRA1, ROP1 and AMA1 antigens in the detection of specific anti-Toxoplasma gondii antibodies in mouse and human sera. PLoS ONE 2019, 14, e0217866. open in new tab
  19. Carruthers, V.B.; Sibley, L.D. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 1997, 73, 114-123.
  20. Joiner, K.A.; Roos, D.S. Secretory traffic in the eukaryotic parasite Toxoplasma gondii: Less is more. J. Cell Biol. 2002, 157, 557-563. open in new tab
  21. Ngô, H.M.; Hoppe, H.C.; Joiner, K.A. Differential sorting and post-secretory targeting of proteins in parasitic invasion. Trends Cell Biol. 2000, 10, 67-72. open in new tab
  22. Liu, Q.; Li, F.-C.; Zhou, C.-X.; Zhu, X.-Q. Research advances in interactions related to Toxoplasma gondii microneme proteins. Exp. Parasitol. 2017, 176, 89-98. open in new tab
  23. Poukchanski, A.; Fritz, H.M.; Tonkin, M.L.; Treeck, M.; Boulanger, M.J.; Boothroyd, J.C. Toxoplasma gondii Sporozoites Invade Host Cells Using Two Novel Paralogues of RON2 and AMA1. PLoS ONE 2013, 8, e70637. open in new tab
  24. Carruthers, V.B.; Giddings, O.K.; Sibley, L.D. Secretion of micronemal proteins is associated with toxoplasma invasion of host cells. Cell. Microbiol. 1999, 1, 225-235. open in new tab
  25. Tomley, F.M.; Soldati, D.S. Mix and match modules: Structure and function of microneme proteins in apicomplexan parasites. Trends Parasitol. 2001, 17, 81-88. open in new tab
  26. Kappe, S.; Bruderer, T.; Gantt, S.; Fujioka, H.; Nussenzweig, V.; Ménard, R. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J. Cell Biol. 1999, 147, 937-944. open in new tab
  27. Carruthers, V.B. Host cell invasion by the opportunistic pathogen Toxoplasma gondii. Acta Trop. 2002, 81, 111-122. open in new tab
  28. Huynh, M.; Rabenau, K.E.; Harper, J.M.; Beatty, W.L.; Sibley, L.D.; Carruthers, V.B. Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2-M2AP adhesive protein complex. EMBO J. 2003, 22, 2082-2090. open in new tab
  29. Jewett, T.J.; Sibley, L.D. The toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival. J. Biol. Chem. 2004, 279, 9362-9369. open in new tab
  30. Cérède, O.; Dubremetz, J.F.; Soête, M.; Deslée, D.; Vial, H.; Bout, D.; Lebrun, M. Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J. Exp. Med. 2005, 201, 453-463.
  31. Mital, J.; Meissner, M.; Soldati, D.; Ward, G.E. Conditional Expression of Toxoplasma gondii Apical Membrane Antigen-1 (TgAMA1) Demonstrates That TgAMA1 Plays a Critical Role in Host Cell Invasion. Mol. Biol. Cell 2005, 16, 4341-4349. open in new tab
  32. Sawmynaden, K.; Saouros, S.; Friedrich, N.; Marchant, J.; Simpson, P.; Bleijlevens, B.; Blackman, M.J.; Soldati-Favre, D.; Matthews, S. Structural insights into microneme protein assembly reveal a new mode of EGF domain recognition. EMBO Rep. 2008, 9, 1149-1155. open in new tab
  33. Harvey, K.L.; Yap, A.; Gilson, P.R.; Cowman, A.F.; Crabb, B.S. Insights and controversies into the role of the key apicomplexan invasion ligand, Apical Membrane Antigen 1. Int. J. Parasitol. 2014, 44, 853-857. Pathogens 2020, 9, 43 15 of 15 open in new tab
  34. Vetrivel, U.; Muralikumar, S.; Mahalakshmi, B.; Lily Therese, K.; Madhavan, H.N.; Alameen, M.; Thirumudi, I. Multilevel Precision-Based Rational Design of Chemical Inhibitors Targeting the Hydrophobic Cleft of Toxoplasma gondii Apical Membrane Antigen 1 (AMA1). Genom. Inform. 2016, 14, 53- 61. open in new tab
  35. Santos, J.M.; Ferguson, D.J.P.; Blackman, M.J.; Soldati-Favre, D. Intramembrane cleavage of AMA1 triggers Toxoplasma to switch from an invasive to a replicative mode. Science 2011, 331, 473-477. open in new tab
  36. Beghetto, E.; Spadoni, A.; Buffolano, W.; Del Pezzo, M.; Minenkova, O.; Pavoni, E.; Pucci, A.; Cortese, R.; Felici, F.; Gargano, N. Molecular dissection of the human B-cell response against Toxoplasma gondii infection by lambda display of cDNA libraries. Int. J. Parasitol. 2003, 33, 163-173. open in new tab
  37. Beghetto, E.; Nielsen, H.V.; Del Porto, P.; Buffolano, W.; Guglietta, S.; Felici, F.; Petersen, E.; Gargano, N. A Combination of Antigenic Regions of Toxoplasma gondii Microneme Proteins Induces Protective Immunity against Oral Infection with Parasite Cysts. J. Infect. Dis. 2005, 191, 637-645. open in new tab
  38. Buffolano, W.; Beghetto, E.; Del Pezzo, M.; Spadoni, A.; Di Cristina, M.; Petersen, E.; Gargano, N. Use of recombinant antigens for early postnatal diagnosis of congenital toxoplasmosis. J. Clin. Microbiol. 2005, 43, 5916-5924. open in new tab
  39. Holec, L.; Gąsior, A.; Brillowska-Dąbrowska, A.; Kur, J. Toxoplasma gondii: Enzyme-linked immunosorbent assay using different fragments of recombinant microneme protein 1 (MIC1) for detection of immunoglobulin G antibodies. Exp. Parasitol. 2008, 119, 1-6. open in new tab
  40. Montoya, J.G. Laboratory Diagnosis of Toxoplasma gondii Infection and Toxoplasmosis. J. Infect. Dis. 2002, 185, S73-S82. open in new tab
  41. Montoya, J.G.; Remington, J.S. Clinical Practice: Management of Toxoplasma gondii Infection during Pregnancy. Clin. Infect. Dis. 2008, 47, 554-566. open in new tab
  42. Robert-Gangneux, F.; Darde, M.-L. Epidemiology of and Diagnostic Strategies for Toxoplasmosis. Clin. Microbiol. Rev. 2012, 25, 264-296. open in new tab
  43. Crawford, J.; Tonkin, M.L.; Grujic, O.; Boulanger, M.J. Structural characterization of apical membrane antigen 1 (AMA1) from Toxoplasma gondii. J. Biol. Chem. 2010, 285, 15644-15652. open in new tab
  44. Krishnamurthy, S.; Deng, B.; Del Rio, R.; Buchholz, K.R.; Treeck, M.; Urban, S.; Boothroyd, J.; Lam, Y.-W.; Ward, G.E. Not a Simple Tether: Binding of Toxoplasma gondii AMA1 to RON2 during Invasion Protects AMA1 from Rhomboid-Mediated Cleavage and Leads to Dephosphorylation of Its Cytosolic Tail. MBio 2016, 7, e00754-e16. open in new tab
  45. Parussini, F.; Tang, Q.; Moin, S.M.; Mital, J.; Urban, S.; Ward, G.E. Intramembrane proteolysis of Toxoplasma apical membrane antigen 1 facilitates host-cell invasion but is dispensable for replication. Proc. Natl. Acad. Sci. USA 2012, 109, 7463-7468. open in new tab
  46. Carruthers, V.; Boothroyd, J.C. Pulling together: An integrated model of Toxoplasma cell invasion. Curr. Opin. Microbiol. 2007, 10, 83-89. open in new tab
  47. Giovannini, D.; Späth, S.; Lacroix, C.; Perazzi, A.; Bargieri, D.; Lagal, V.; Lebugle, C.; Combe, A.; Thiberge, S.; Baldacci, P.; et al. Independent Roles of Apical Membrane Antigen 1 and Rhoptry Neck Proteins during Host Cell Invasion by Apicomplexa. Cell Host Microbe 2011, 10, 591-602. open in new tab
  48. Bargieri, D.Y.; Andenmatten, N.; Lagal, V.; Thiberge, S.; Whitelaw, J.A.; Tardieux, I.; Meissner, M.; Ménard, R. Apical membrane antigen 1 mediates apicomplexan parasite attachment but is dispensable for host cell invasion. Nat. Commun. 2013, 4, 2552. © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). open in new tab
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