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Journal of Immunology Research
Volume 2018, Article ID 8964085, 14 pages
https://doi.org/10.1155/2018/8964085
Research Article

Recombinant Enolase of Trypanosoma cruzi as a Novel Vaccine Candidate against Chagas Disease in a Mouse Model of Acute Infection

1Departamento de Biología Molecular, Juan Badiano No. 1, Col. Sección XVI, Delegación Tlalpan, Instituto Nacional de Cardiología “Ignacio Chávez”, 14080 Mexico City, Mexico
2Departamento de Biología Celular, Avenida Instituto Politecnico Nacional No. 2508, Col. San Pedro Zacatenco, Centro de Investigación y de Estudios Avanzados del Instituto Politecnico Nacional, 07360 Mexico City, Mexico
3Departamento de Anatomía Patológica, Juan Badiano No. 1, Col. Sección XVI, Delegación Tlalpan, Instituto Nacional de Cardiología “Ignacio Chávez”, 14080 Mexico City, Mexico
4Departamento de Infectómica y Patogénesis Molecular, Avenida Instituto Politecnico Nacional No. 2508, Col. San Pedro Zacatenco, Centro de Investigación y de Estudios Avanzados del Instituto Politecnico Nacional, 07360 Mexico City, Mexico

Correspondence should be addressed to Alejandro Carabarin-Lima; moc.liamtoh@57_iloce

Received 7 February 2018; Accepted 3 April 2018; Published 7 May 2018

Academic Editor: Giuseppe A. Sautto

Copyright © 2018 Minerva Arce-Fonseca et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, “World Health Organization,” 2017, March 2018, http://www.who.int/chagas/en/. View at Google Scholar
  2. J. A. Perez-Molina and I. Molina, “Chagas disease,” Lancet, vol. 391, no. 10115, pp. 82–94, 2018. View at Publisher · View at Google Scholar · View at Scopus
  3. World Health Organization, Chagas Disease (American Trypanosomiasis), World Health Organization, Geneva, 2015, March 2018, http://www.who.int/mediacentre/factsheets/fs340/en/.
  4. C. Bern, S. Kjos, M. J. Yabsley, and S. P. Montgomery, “Trypanosoma cruzi and Chagas’ disease in the United States,” Clinical Microbiology Reviews, vol. 24, no. 4, pp. 655–681, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Jackson, L. Gétaz, H. Wolff et al., “Prevalence, clinical staging and risk for blood-borne transmission of Chagas disease among Latin American migrants in Geneva, Switzerland,” PLoS Neglected Tropical Diseases, vol. 4, no. 2, article e592, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. F. X. Lescure, A. Canestri, H. Melliez et al., “Chagas disease, France,” Emerging Infectious Diseases, vol. 14, no. 4, pp. 644–646, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Muñoz, O. Coll, T. Juncosa et al., “Prevalence and vertical transmission of Trypanosoma cruzi infection among pregnant Latin American women attending 2 maternity clinics in Barcelona, Spain,” Clinical Infectious Diseases, vol. 48, no. 12, pp. 1736–1740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. G. A. Schmunis, “Epidemiology of Chagas disease in non endemic countries: the role of international migration,” Memórias do Instituto Oswaldo Cruz, vol. 102, Supplement 1, pp. 75–86, 2007. View at Publisher · View at Google Scholar
  9. A. Carabarin-Lima, M. C. González-Vázquez, O. Rodríguez-Morales et al., “Chagas disease (American trypanosomiasis) in Mexico: an update,” Acta Tropica, vol. 127, no. 2, pp. 126–135, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. F. J. Carod-Artal and J. Gascon, “Chagas disease and stroke,” Lancet Neurology, vol. 9, no. 5, pp. 533–542, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. L. M. G. Bahia‐Oliveira, J. A. S. Gomes, J. R. Cançado et al., “Immunological and clinical evaluation of chagasic patients subjected to chemotherapy during the acute phase of Trypanosoma cruzi infection 14-30 years ago,” The Journal of Infectious Diseases, vol. 182, no. 2, pp. 634–638, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. J. R. Cancado, “Criteria of Chagas disease cure,” Memórias do Instituto Oswaldo Cruz, vol. 94, Supplement 1, pp. 331–335, 1999. View at Publisher · View at Google Scholar
  13. S. I. Cazorla, P. D. Becker, F. M. Frank et al., “Oral vaccination with Salmonella enterica as a cruzipain-DNA delivery system confers protective immunity against Trypanosoma cruzi,” Infection and Immunity, vol. 76, no. 1, pp. 324–333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. F. M. Frank, S. I. Cazorla, M. J. Sartori, and R. S. Corral, “Elicitation of specific, Th1-biased immune response precludes skeletal muscle damage in cruzipain-vaccinated mice,” Experimental and Molecular Pathology, vol. 84, no. 1, pp. 64–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Costa, G. Franchin, V. L. Pereira-Chioccola, M. Ribeirao, S. Schenkman, and M. M. Rodrigues, “Immunization with a plasmid DNA containing the gene of trans-sialidase reduces Trypanosoma cruzi infection in mice,” Vaccine, vol. 16, no. 8, pp. 768–774, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. D. F. Hoft, C. S. Eickhoff, O. K. Giddings, J. R. C. Vasconcelos, and M. M. Rodrigues, “Trans-sialidase recombinant protein mixed with CpG motif-containing oligodeoxynucleotide induces protective mucosal and systemic Trypanosoma cruzi immunity involving CD8+ CTL and B cell-mediated cross-priming,” Journal of Immunology, vol. 179, no. 10, pp. 6889–6900, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. E. L. V. Silveira, C. Claser, F. A. B. Haolla, L. G. Zanella, and M. M. Rodrigues, “Novel protective antigens expressed by Trypanosoma cruzi amastigotes provide immunity to mice highly susceptible to Chagas’ disease,” Clinical and Vaccine Immunology, vol. 15, no. 8, pp. 1292–1300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. B. H. Fralish and R. L. Tarleton, “Genetic immunization with LYT1 or a pool of trans-sialidase genes protects mice from lethal Trypanosoma cruzi infection,” Vaccine, vol. 21, no. 21-22, pp. 3070–3080, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. K. A. Luhrs, D. L. Fouts, and J. E. Manning, “Immunization with recombinant paraflagellar rod protein induces protective immunity against Trypanosoma cruzi infection,” Vaccine, vol. 21, no. 21-22, pp. 3058–3069, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Pal-Bhowmick, M. Mehta, I. Coppens, S. Sharma, and G. K. Jarori, “Protective properties and surface localization of Plasmodium falciparum enolase,” Infection and Immunity, vol. 75, no. 11, pp. 5500–5508, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. W. Q. Li, X. C. Hu, X. Zhang et al., “Immunisation with the glycolytic enzyme enolase confers effective protection against Candida albicans infection in mice,” Vaccine, vol. 29, no. 33, pp. 5526–5533, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Chen, Z. G. Yuan, M. J. Xu et al., “Ascaris suum enolase is a potential vaccine candidate against ascariasis,” Vaccine, vol. 30, no. 23, pp. 3478–3482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. V. Pancholi, “Multifunctional alpha-enolase: its role in diseases,” Cellular and Molecular Life Sciences, vol. 58, no. 7, pp. 902–920, 2001. View at Publisher · View at Google Scholar
  24. S. Bergmann, M. Rohde, G. S. Chhatwal, and S. Hammerschmidt, “alpha-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface,” Molecular Microbiology, vol. 40, no. 6, pp. 1273–1287, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Pancholi and V. A. Fischetti, “alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci,” Journal of Biological Chemistry, vol. 273, no. 23, pp. 14503–14515, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. D. J. P. Ferguson, S. F. Parmley, and S. Tomavo, “Evidence for nuclear localisation of two stage-specific isoenzymes of enolase in Toxoplasma gondii correlates with active parasite replication,” International Journal for Parasitology, vol. 32, no. 11, pp. 1399–1410, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Labbe, M. Peroval, C. Bourdieu, F. Girard-Misguich, and P. Pery, “Eimeria tenella enolase and pyruvate kinase: a likely role in glycolysis and in others functions,” International Journal for Parasitology, vol. 36, no. 14, pp. 1443–1452, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Mouveaux, G. Oria, E. Werkmeister et al., “Nuclear glycolytic enzyme enolase of Toxoplasma gondii functions as a transcriptional regulator,” PLoS One, vol. 9, no. 8, article e105820, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Lee, Y. Guo, M. Ohta, L. Xiong, B. Stevenson, and J. K. Zhu, “LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase,” EMBO Journal, vol. 21, no. 11, pp. 2692–2702, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Feo, D. Arcuri, E. Piddini, R. Passantino, and A. Giallongo, “ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: relationship with Myc promoter-binding protein 1 (MBP-1),” FEBS Letters, vol. 473, no. 1, pp. 47–52, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Subramanian and D. M. Miller, “Structural analysis of alpha-enolase. Mapping the functional domains involved in down-regulation of the c-myc protooncogene,” The Journal of Biological Chemistry, vol. 275, no. 8, pp. 5958–5965, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. J. C. Wilkins, K. A. Homer, and D. Beighton, “Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions,” Applied and Environmental Microbiology, vol. 68, no. 5, pp. 2382–2390, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. B. L. Decker and W. T. Wickner, “Enolase activates homotypic vacuole fusion and protein transport to the vacuole in yeast,” The Journal of Biological Chemistry, vol. 281, no. 20, pp. 14523–14528, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Brandina, J. Graham, C. Lemaitre-Guillier et al., “Enolase takes part in a macromolecular complex associated to mitochondria in yeast,” Biochimica et Biophysica Acta (BBA) - Bioenergetics, vol. 1757, no. 9-10, pp. 1217–1228, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Entelis, I. Brandina, P. Kamenski, I. A. Krasheninnikov, R. P. Martin, and I. Tarassov, “A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae,” Genes and Development, vol. 20, no. 12, pp. 1609–1620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Carabarín-Lima, O. Rodríguez-Morales, M. C. González-Vázquez et al., “In silico approach for the identification of immunological properties of enolase from Trypanosoma cruzi and its possible usefulness as vaccine in Chagas disease,” Parasitology Research, vol. 113, no. 3, pp. 1029–1039, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. W. H. Lee, H. I. Choi, S. W. Hong, K. S. Kim, Y. S. Gho, and S. G. Jeon, “Vaccination with Klebsiella pneumoniae-derived extracellular vesicles protects against bacteria-induced lethality via both humoral and cellular immunity,” Experimental and Molecular Medicine, vol. 47, no. 9, article e183, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. K. A. Pasquevich, S. M. Estein, C. G. Samartino et al., “Immunization with recombinant Brucella species outer membrane protein Omp16 or Omp19 in adjuvant induces specific CD4+ and CD8+ T cells as well as systemic and oral protection against Brucella abortus infection,” Infection and Immunity, vol. 77, no. 1, pp. 436–445, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. C. N. Pollak, M. M. Wanke, S. M. Estein et al., “Immunization with Brucella VirB proteins reduces organ colonization in mice through a Th1-type immune response and elicits a similar immune response in dogs,” Clinical and Vaccine Immunology, vol. 22, no. 3, pp. 274–281, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Serna, J. A. Lara, S. P. Rodrigues, A. F. Marques, I. C. Almeida, and R. A. Maldonado, “A synthetic peptide from Trypanosoma cruzi mucin-like associated surface protein as candidate for a vaccine against Chagas disease,” Vaccine, vol. 32, no. 28, pp. 3525–3532, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Shimizu, H. Takagi, T. Nakayama et al., “Intraperitoneal immunization with oligomannose-coated liposome-entrapped soluble leishmanial antigen induces antigen-specific T-helper type immune response in BALB/c mice through uptake by peritoneal macrophages,” Parasite Immunology, vol. 29, no. 5, pp. 229–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Arce-Fonseca, A. Ramos-Ligonio, A. Lopez-Monteon, B. Salgado-Jimenez, P. Talamas-Rohana, and J. L. Rosales-Encina, “A DNA vaccine encoding for TcSSP4 induces protection against acute and chronic infection in experimental Chagas disease,” International Journal of Biological Sciences, vol. 7, no. 9, pp. 1230–1238, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Guide for the Care and Use of Laboratory Animals, National Academies Press (US), Washington (DC), 8th edition, 2011.
  44. P. Hotez, E. Ottesen, A. Fenwick, and D. Molyneux, “The neglected tropical diseases: the ancient afflictions of stigma and poverty and the prospects for their control and elimination,” Advances in Experimental Medicine and Biology, vol. 582, pp. 23–33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Bern, “Antitrypanosomal therapy for chronic Chagas’ disease,” The New England Journal of Medicine, vol. 364, no. 26, pp. 2527–2534, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. J. J. Donnelly, B. Wahren, and M. A. Liu, “DNA vaccines: progress and challenges,” Journal of Immunology, vol. 175, no. 2, pp. 633–639, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Garg and R. L. Tarleton, “Genetic immunization elicits antigen-specific protective immune responses and decreases disease severity in Trypanosoma cruzi infection,” Infection and Immunity, vol. 70, no. 10, pp. 5547–5555, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Carabarin-Lima, M. C. González-Vázquez, B.-P. Lidia, P.-T. Rohana, and R.-E. J. Luis, “Immunization with the recombinant surface protein rTcSP2 alone or fused to the CHP or ATPase domain of TcHSP70 induces protection against acute Trypanosoma cruzi infection,” Journal of Vaccines & Vaccination, vol. 1, no. 3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. R. A. Wrightsman and J. E. Manning, “Paraflagellar rod proteins administered with alum and IL-12 or recombinant adenovirus expressing IL-12 generates antigen-specific responses and protective immunity in mice against Trypanosoma cruzi,” Vaccine, vol. 18, no. 14, pp. 1419–1427, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. W. Gan, G. Zhao, H. Xu et al., “Reverse vaccinology approach identify an Echinococcus granulosus tegumental membrane protein enolase as vaccine candidate,” Parasitology Research, vol. 106, no. 4, pp. 873–882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. V. Mundodi, A. S. Kucknoor, and J. F. Alderete, “Immunogenic and plasminogen-binding surface-associated α-enolase of Trichomonas vaginalis,” Infection and Immunity, vol. 76, no. 2, pp. 523–531, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Olver and M. Vidal, “Proteomic analysis of secreted exosomes,” Subcellular Biochemistry, vol. 43, pp. 99–131, 2007. View at Publisher · View at Google Scholar
  53. Y. Feng, X. Pan, W. Sun et al., “Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface,” The Journal of Infectious Diseases, vol. 200, no. 10, pp. 1583–1592, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Sha, T. E. Erova, R. A. Alyea et al., “Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila,” Journal of Bacteriology, vol. 191, no. 9, pp. 3095–3107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Zhang, B. Chen, X. Mu et al., “Identification and characterization of a novel protective antigen, enolase of Streptococcus suis serotype 2,” Vaccine, vol. 27, no. 9, pp. 1348–1353, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. D. F. Hoft and C. S. Eickhoff, “Type 1 immunity provides optimal protection against both mucosal and systemic Trypanosoma cruzi challenges,” Infection and Immunity, vol. 70, no. 12, pp. 6715–6725, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. C. N. Paiva, M. T. L. Castelo-Branco, J. Lannes-Vieira, and C. R. Gattass, “Trypanosoma cruzi: protective response of vaccinated mice is mediated by CD8+ cells, prevents signs of polyclonal T lymphocyte activation, and allows restoration of a resting immune state after challenge,” Experimental Parasitology, vol. 91, no. 1, pp. 7–19, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. R. T. Gazzinelli, I. P. Oswald, S. Hieny, S. L. James, and A. Sher, “The microbicidal activity of interferon-γ-treated macrophages againstTrypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-β,” European Journal of Immunology, vol. 22, no. 10, pp. 2501–2506, 1992. View at Publisher · View at Google Scholar · View at Scopus
  59. A. M. Abdelnoor, “Plasmid DNA vaccines,” Current Drug Targets - Immune, Endocrine & Metabolic Disorders, vol. 1, no. 1, pp. 79–92, 2001. View at Publisher · View at Google Scholar
  60. G. Trinchieri, “Interleukin-10 production by effector T cells: Th1 cells show self control,” Journal of Experimental Medicine, vol. 204, no. 2, pp. 239–243, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. J. L. Mege, S. Meghari, A. Honstettre, C. Capo, and D. Raoult, “The two faces of interleukin 10 in human infectious diseases,” The Lancet Infectious Diseases, vol. 6, no. 9, pp. 557–569, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. Z. A. Andrade, S. G. Andrade, R. Correa, M. Sadigursky, and V. J. Ferrans, “Myocardial changes in acute Trypanosoma cruzi infection. Ultrastructural evidence of immune damage and the role of microangiopathy,” American Journal of Pathology, vol. 144, no. 6, pp. 1403–1411, 1994. View at Google Scholar
  63. J. A. Marin-Neto, E. Cunha-Neto, B. C. Maciel, and M. V. Simoes, “Pathogenesis of chronic Chagas heart disease,” Circulation, vol. 115, no. 9, pp. 1109–1123, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Zapataestrella, C. Hummelnewell, G. Sanchezburgos et al., “Control of Trypanosoma cruzi infection and changes in T-cell populations induced by a therapeutic DNA vaccine in mice,” Immunology Letters, vol. 103, no. 2, pp. 186–191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Tekiel, C. D. Alba-Soto, S. M. Gonzalez Cappa, M. Postan, and D. O. Sanchez, “Identification of novel vaccine candidates for Chagas’ disease by immunization with sequential fractions of a trypomastigote cDNA expression library,” Vaccine, vol. 27, no. 9, pp. 1323–1332, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Arce-Fonseca, M. A. Ballinas-Verdugo, E. R. A. Zenteno et al., “Specific humoral and cellular immunity induced by Trypanosoma cruzi DNA immunization in a canine model,” Veterinary Research, vol. 44, no. 1, p. 15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Esgleas, M. de la Cruz Dominguez-Punaro, Y. Li, J Ã.©e. Harel, J. Daniel Dubreuil, and M. Gottschalk, “Immunization with SsEno fails to protect mice against challenge with Streptococcus suis serotype 2,” FEMS Microbiology Letters, vol. 294, no. 1, pp. 82–88, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. A. O'Garra and P. Vieira, “TH1 cells control themselves by producing interleukin-10,” Nature Reviews Immunology, vol. 7, no. 6, pp. 425–428, 2007. View at Publisher · View at Google Scholar · View at Scopus