Advertisement

Parasitology Research

, Volume 113, Issue 5, pp 1955–1969 | Cite as

Analysis of the expression of cytoskeletal proteins of Taenia crassiceps ORF strain cysticerci (Cestoda)

  • Olivia Reynoso-Ducoing
  • Laura Valverde-Islas
  • Cristina Paredes-Salomon
  • América Pérez-Reyes
  • Abraham Landa
  • Lilia Robert
  • Guillermo Mendoza
  • Javier R. AmbrosioEmail author
Original Paper

Abstract

The Taenia crassiceps ORF strain is used to generate a murine model of cysticercosis, which is used for diagnosis, evaluation of drugs, and vaccination. This particular strain only exists as cysticerci, is easily maintained under in vivo and in vitro conditions, and offers an excellent model for studying the cytoskeletons of cestodes. In this study, several experimental approaches were used to determine the tissue expression of its cytoskeletal proteins. The techniques used were microscopy (video, confocal, and transmission electron), one-dimensional (1D) and two-dimensional (2D) electrophoresis, immunochemistry, and mass spectrometry. The tissue expression of actin, tubulin, and paramyosin was assessed using microscopy, and their protein isoforms were determined with 1D and 2D electrophoresis and immunochemistry. Nineteen spots were excised from a proteomic gel and identified by liquid chromatography–tandem mass spectrometry and immunochemistry. The proteins identified were classic cytoskeletal proteins, metabolic enzymes, and proteins with diverse biological functions, but mainly involved in detoxification activities. Research suggests that most noncytoskeletal proteins interact with actin or tubulin, and the results of the present study suggest that the proteins identified may be involved in supporting the dynamics and plasticity of the cytoskeleton of T. crassiceps cysticerci. These results contribute to our knowledge of the cellular biology and physiology of cestodes.

Keywords

Taenia crassiceps Cysticerci Cytoskeleton Proteomics Immunohistochemistry Protein isoforms 

Notes

Acknowledgments

This work was supported by grants (IN201003, IN216107, IN201510, IX200610, and IN216213) from Dirección General de Apoyo al Personal Académico, Universidad Nacional Autónoma de México. Laser scanning confocal microscopy expertise was supported by Biólogo Gabriel Ortiz from the Instituto de Fisiología Celular, Universidad Nacional Autónoma de México and Cirujano Dentista María José Gómora Herrera from the Embryology Department, Facultad de Medicina. Laura Valverde-Islas is a PhD student of the Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México. We thank M.L.I. Rafael Ibarra for his encouragement and guidance.

Supplementary material

Online Resource 1

Cysticerci of T. crassiceps ORF strain Parasites were recovered from experimentally infected mice after infection for 3 months, washed in PBS to eliminate any host residue, and observed under a dissection microscope at ×3 magnification. After stimulation with light, the tapeworms showed intense movement of the bladder wall and intense motility. The cysticerci are full of vesicular fluid. The parasites have an elliptical form with two poles. One pole corresponds to the budding region (in the movie at the left) and the other corresponds to the pore (at the right) that is seen in Fig. 1b after the cytoskeleton of the cysticerci was fluorescently stained. (MPG 1,792 kb)

Online Resource 2

Flame cells of T. crassiceps ORF strain cysticerci Tissues of live cysticerci were observed with a laser scanning confocal microscope (Olympus FV1000, UPLSAPO; ×60 magnification; NA: 1.35) and the movement of the ciliary tufts of several flame cells was observed with the Fluoview FV1000 software. The ciliary tufts are those stained fluorescent green for α-tubulin in Figs. 1f and 2. (MPG 1,290 kb)

References

  1. Aguilar-Díaz H, Bobes RJ, Carrero JC, Camacho-Carranza R, Cervantes C, Cevallos MA, Dávila G, Rodríguez-Dorantes M, Escobedo G, Fernández JL, Fragoso G, Gaytán P, Garciarubio A, González VM, González L, José MV, Jiménez L, Laclette JP, Landa A, Larralde C, Morales-Montor J, Morett E, Ostoa-Saloma P, Sciutto E, Santamaría RI, Soberón X, de la Torre P, Valdés V, Yánez J (2006) The genome project of Taenia solium. Parasitol Int 55(Suppl):S127–130PubMedCrossRefGoogle Scholar
  2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. Garland Science, New YorkGoogle Scholar
  3. Almeida CR, Stoco PH, Wagner G, Sincero TC, Rotava G, Bayer Santos E, Rodrigues JB, Sperandio MM, Maia AA, Ojopi EP, Zaha A, Ferreira HB, Tyler KM, Dávila AM, Grisard EC, Dias-Neto E (2009) Transcriptome analysis of Taenia solium cysticerci using Open Reading Frame ESTs (ORESTES). Parasit Vectors 31 2(1):35CrossRefGoogle Scholar
  4. Ambrosio J, Landa A, Merchant M, Laclette J (1994) Protein uptake by cysticerci of Taenia crassiceps. Arch Med Res 25(3):325–330PubMedGoogle Scholar
  5. Ambrosio J, Cruz-Rivera M, Allan J, Morán E, Ersfeld K, Flisser A (1997) Identification and partial characterization of a myosin-like protein from cysticerci and adults of Taenia solium using a monoclonal antibody. Parasitology 114(6):545–553PubMedGoogle Scholar
  6. Ambrosio J, Reynoso-Ducoing O, Hernández-Sanchez H, Correa-Piña D, González-Malerva L, Cruz-Rivera M, Flisser A (2003) Actin expression in Taenia solium cysticerci (Cestoda): tisular distribution and detection of isoforms. Cell Biol Int 27(9):727–733PubMedCrossRefGoogle Scholar
  7. Ambrosio JR, Zepeda-Rodriguez A, Ferrer A, Reynoso-Ducoing O, Fortoul TI (2011) Scanning electron microscopy observations of the cross-section of a Taenia solium adult tapeworm. Int J Morphol 29(1):127–132CrossRefGoogle Scholar
  8. Ardizzi JP, Epstein HF (1987) Immunochemical localization of myosin heavy chain isoforms and paramyosin in developmentally and structurally diverse muscle cell types of the nematode Caenorhabditis elegans. J Cell Biol 105(6 Pt 1):2763–2770PubMedCrossRefGoogle Scholar
  9. Aziz A, Zhang W, Li J, Loukas A, McManus DP, Mulvenna J (2011) Proteomic characterisation of Echinococcus granulosus hydatid cyst fluid from sheep, cattle and humans. J Proteomics 24 74(9):1560–1572CrossRefGoogle Scholar
  10. Carafoli E (2004) Calcium signaling: a historical account. Biol Res 37(4):497–505PubMedCrossRefGoogle Scholar
  11. Cassimeris L, Silva VC, Miller E, Ton Q, Molnar C, Fong J (2012) Fueled by microtubules: does tubulin dimer/polymer partitioning regulate intracellular metabolism? Cytoskeleton 69(3):133–143PubMedCrossRefGoogle Scholar
  12. Cevallos AM, Segura-Kato YX, Merchant-Larios H, Manning-Cela R, Alberto Hernández-Osorio L, Márquez-Dueñas C, Ambrosio JR, Reynoso-Ducoing O, Hernández R (2011) Trypanosoma cruzi: multiple actin isovariants are observed along different developmental stages. Exp Parasitol 127(1):249–259PubMedCrossRefGoogle Scholar
  13. Chiumiento L, Bruschi F (2009) Enzymatic antioxidant systems in helminth parasites. Parasitol Res 105(3):593–603PubMedCrossRefGoogle Scholar
  14. Creighton TE (1997) Protein structure: a practical approach. IRL Press at Oxford University Press, Oxford ; New YorkGoogle Scholar
  15. Cruz-Rivera M, Reyes-Torres A, Reynoso-Ducoing O, Flisser A, Ambrosio J (2006) Comparison of biochemical and immunochemical properties of myosin II in taeniid parasites. Cell Biol Int 30(7):598–602PubMedCrossRefGoogle Scholar
  16. Cui SJ, Xu LL, Zhang T, Xu M, Yao J, Fang CY, Feng Z, Yang PY, Hu W, Liu F (2013) Proteomic characterization of larval and adult developmental stages in Echinococcus granulosus reveals novel insight into host-parasite interactions. J Proteomics 84:158–175PubMedCrossRefGoogle Scholar
  17. de la Torre-Escudero E, Manzano-Román R, Siles-Lucas M, Pérez-Sánchez R, Moyano JC, Barrera I, Oleaga A (2012) Molecular and functional characterization of a Schistosoma bovis annexin: fibrinolytic and anticoagulant activity. Vet Parasitol 184(1):25–36PubMedCrossRefGoogle Scholar
  18. Diaz-Masmela Y, Fragoso G, Ambrosio JR, Mendoza-Hernández G, Rosas G, Estrada K, Carrero JC, Sciutto E, Laclette JP, Bobes R (2013) Immunodiagnosis of porcine cysticercosis: identification of candidate antigens trough immunoproteomics. Vet J 198(3):656–660PubMedCrossRefGoogle Scholar
  19. Dziewulska-Szwajkowska D, Ogorzałek A (2005) F-actin, beta-tubulin, aldolase, and fructose-1,6-bisphosphatase in heteropteran ovarioles–I. Immunocytochemical investigations of whole-mounted ovarioles. Cell Tissue Res 321(2):311–321PubMedCrossRefGoogle Scholar
  20. Gao YJ, Yan HL, Ding FX, Lu YM, Sun SH (2007) Annexin B1 at the host-parasite interface of the Taenia solium cysticercus: secreted and associated with inflammatory reaction. Acta Trop 101(3):192–199PubMedCrossRefGoogle Scholar
  21. Garcia E, Ordoñez G, Sotelo J (1995) Antigens from Taenia crassiceps cysticerci used in complement fixation, enzyme-linked immunosorbent assay, and western blot (immunoblot) for diagnosis of neurocysticercosis. J Clin Microbiol 33(12):3324–3325PubMedCentralPubMedGoogle Scholar
  22. Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6(6):449–461PubMedCrossRefGoogle Scholar
  23. Goding J (1986) Monoclonal antibodies: principles and practice: production and application of monoclonal antibodies in cell biology, biochemistry, and immunology. Academic, LondonGoogle Scholar
  24. Gonzalez-Malerva L, Cruz-Rivera M, Reynoso-Ducoing O, Retamal C, Flisser A, Ambrosio JR (2004) Muscular myosin isoforms of Taenia solium (Cestoda). Cell Biol Int 28(12):885–894PubMedCrossRefGoogle Scholar
  25. Harlow E, Lane D (1999) Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor N.YGoogle Scholar
  26. Hasan MR, Koikawa S, Kotani S, Miyamoto S, Nakagawa H (2006) Ferritin forms dynamic oligomers to associate with microtubules in vivo: implication for the role of microtubules in iron metabolism. Exp Cell Res 312(11):1950–1960PubMedCrossRefGoogle Scholar
  27. Ibarra-Coronado EG, Escobedo G, Nava K, Hernández-Bello R, García-Varela M, Ambrosio JR, Reynoso-Ducoing O, Fonseca-Liñán R, Ortega-Pierres G, Pavón L, Hernández ME, Morales-Montor J (2011) A helminth cestode parasite express an estrogen-binding protein resembling classic nuclear estrogen receptor. Steroids 76(10–11):1149–1159PubMedCrossRefGoogle Scholar
  28. Illescas O, Carrero JC, Bobes RJ, Flisser A, Rosas G, Laclette JP (2012) Molecular characterization, functional expression, tissue localization and protective potential of a Taenia solium fatty acid-binding protein. Mol Biochem Parasitol 186(2):117–125PubMedCrossRefGoogle Scholar
  29. Infante AA, Infante D, Chan MC, How PC, Kutschera W, Linhartová I, Müllner EW, Wiche G, Propst F (2007) Ferritin associates with marginal band microtubules. Exp Cell Res 313(8):1602–1614PubMedCrossRefGoogle Scholar
  30. Ingber DE (2008) Tensegrity and mechanotransduction. J Bodyw Mov Ther 12(3):198–200PubMedCentralPubMedCrossRefGoogle Scholar
  31. Janke C, Bulinski JC (2011) Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat Rev Mol Cell Biol 12(12):773–786PubMedCrossRefGoogle Scholar
  32. Jiménez L, Fernández-Velasco DA, Willms K, Landa A (2003) A comparative study of biochemical and immunological properties of triosephosphate isomerase from Taenia solium and Sus scrofa. J Parasitol 89(2):209–214PubMedCrossRefGoogle Scholar
  33. Keller A, Peltzer J, Carpentier G, Horváth I, Oláh J, Duchesnay A, Orosz F, Ovádi J (2007) Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim Biophys Acta 1770(6):919–926PubMedCrossRefGoogle Scholar
  34. Kishi Y, Sugo T, Mahadeo D, Cotter D, Sameshima M (2001) S-Adenosyl-l-homocysteine hydrolase is sequestered into actin rods in Dictyostelium discoideum spores. FEBS Lett 508(3):433–437PubMedCrossRefGoogle Scholar
  35. Koziol U, Krohne G, Brehm K (2013) Anatomy and development of the larval nervous system in Echinococcus multilocularis. Frontiers in zoology 10(1):24PubMedCentralPubMedCrossRefGoogle Scholar
  36. Laclette JP, Landa A, Arcos L, Willms K, Davis AE, Shoemaker CB (1991) Paramyosin is the Schistosoma mansoni (Trematoda) homologue of antigen B from Taenia solium (Cestoda). Mol Biochem Parasitol 44(2):287–295PubMedCrossRefGoogle Scholar
  37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685PubMedCrossRefGoogle Scholar
  38. Márquez-Navarro A, Pérez-Reyes A, Zepeda-Rodríguez A, Reynoso-Ducoing O, Hernández-Campos A, Hernández-Luis F, Castillo R, Yépez-Mulia L, Ambrosio JR (2013) RCB20, an experimental benzimidazole derivative, affects tubulin expression and induces gross anatomical changes in Taenia crassiceps cysticerci. Parasitol Res 112(6):2215–26PubMedCrossRefGoogle Scholar
  39. Matadamas-Martínez F, Nogueda-Torres B, Hernández-Campos A, Hernández-Luis F, Castillo R, Mendoza G, Ambrosio JR, Andrés-Antonio G, Yépez-Mulia L (2013) Analysis of the effect of a 2-(trifluoromethyl)-1H-benzimidazole derivative on Trichinella spiralis muscle larvae. Vet Parasitol 194(2–4):193–197PubMedCrossRefGoogle Scholar
  40. Maule AG, Marks NJ (2006) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. CABI, Wallingford, UK, Cambridge, USAGoogle Scholar
  41. Molina-López J, Jiménez L, Ochoa-Sánchez A, Landa A (2006) Molecular cloning and characterization of a 2-Cys peroxiredoxin from Taenia solium. J Parasitol 92(4):796–802PubMedCrossRefGoogle Scholar
  42. Moxon JV, LaCourse EJ, Wright HA, Perally S, Prescott MC, Gillard JL, Barrett J, Hamilton JV, Brophy PM (2010) Proteomic analysis of embryonic Fasciola hepatica: characterization and antigenic potential of a developmentally regulated heat shock protein. Vet Parasitol 169(1–2):62–75PubMedCrossRefGoogle Scholar
  43. Ochoa-Sánchez A, Jiménez L, Landa A (2011) The hamster model for identification of specific antigens of Taenia solium tapeworms. J Biomed Biotechnol 2011:504959PubMedCentralPubMedCrossRefGoogle Scholar
  44. Oliver JM, Albertini DF, Berlin RD (1976) Effects of glutathione-oxidizing agents on microtubule assembly and microtubule-dependent surface properties of human neutrophils. J Cell Biol 71(3):921–932PubMedCrossRefGoogle Scholar
  45. Palomares F, Palencia G, Pérez R, González-Esquivel D, Castro N, Cook HJ (2004) In vitro effects of albendazole sulfoxide and praziquantel against Taenia solium and Taenia crassiceps cysts. Antimicrob Agents Chemother 48(6):2302–2304PubMedCentralPubMedCrossRefGoogle Scholar
  46. Palomares F, Palencia G, Ambrosio J, Ortiz A, Jung-Cook H (2006) Evaluation of the efficacy of albendazole sulphoxide and praziquantel in combination on Taenia crassiceps cysts: in vitro studies. J Antimicrob Chemother 57(3):482–488PubMedCrossRefGoogle Scholar
  47. Palomares-Alonso F, Piliado JC, Palencia G, Ortiz-Plata A, Jung-Cook H (2007) Efficacy of nitazoxanide, tizoxanide and tizoxanide/albendazole sulphoxide combination against Taenia crassiceps cysts. J Antimicrob Chemother 59(2):212–218PubMedCrossRefGoogle Scholar
  48. Peralta RH, Espíndola NM, Pardini AX, Iha AH, Moura H, Barr JR, Vaz AJ, Peralta JM (2010) Taenia crassiceps cysticerci: characterization of the 14-kDa glycoprotein with homologies to antigens from Taenia solium cysticerci. Exp Parasitol 124(3):295–300PubMedCrossRefGoogle Scholar
  49. Roberts LS, Schmidt GD, Janovy J (2009) Foundations of parasitology. McGraw-Hill Higher Education, BostonGoogle Scholar
  50. Sato H, Kamiya H (2000) Immunofluorescent localization of intermediate filaments (IFs) in helminths using anti-mammalian IFs monoclonal antibody. J Parasitol 86(4):711–715PubMedCrossRefGoogle Scholar
  51. Schmidt J, Bodor O, Gohr L, Kunz W (1996) Paramyosin isoforms of Schistosoma mansoni are phosphorylated and localized in a large variety of muscle types. Parasitology 112(Pt 5):459–467PubMedCrossRefGoogle Scholar
  52. Sciutto E, Fragoso G, Larralde C (2011) Taenia crassiceps as a model for Taenia solium and the S3Pvac vaccine. Parasite Immunol 33(1):79–80PubMedCrossRefGoogle Scholar
  53. Shelanski ML, Gaskin F, Cantor CR (1973) Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci U S A 70(3):765–768PubMedCentralPubMedCrossRefGoogle Scholar
  54. Shu S, Mahadeo DC, Liu X, Liu W, Parent CA, Korn ED (2006) S-adenosylhomocysteine hydrolase is localized at the front of chemotaxing cells, suggesting a role for transmethylation during migration. Proc Natl Acad Sci U S A 103(52):19788–19793PubMedCentralPubMedCrossRefGoogle Scholar
  55. Smyth JD (1969) The physiology of cestodes. University reviews in biology. W. H, Freeman, San FranciscoGoogle Scholar
  56. Suzuki LA, Arruda GC, Quagliato EM, Rossi QL (2007) Evaluation of Taenia solium and Taenia crassiceps cysticercal antigens for immunodiagnosis of neurocysticercosis using ELISA on cerebrospinal fluid samples. Rev Soc Bras Med Trop 40(2):152–155PubMedGoogle Scholar
  57. Szent-Györgyi AG, Cohen C, Kendrick-Jones J (1971) Paramyosin and the filaments of molluscan “catch” muscles. II. Native filaments: isolation and characterization. J Mol Biol 56(2):239–258PubMedCrossRefGoogle Scholar
  58. Terman JR, Kashina A (2012) Post-translational modification and regulation of actin. Curr Opin Cell Biol 25(1):30–38PubMedCentralPubMedGoogle Scholar
  59. Toledo A, Larralde C, Fragoso G, Gevorkian G, Manoutcharian K, Hernández M, Acero G, Rosas G, López-Casillas F, Garfias CK, Vázquez R, Terrazas I, Sciutto E (1999) Towards a Taenia solium cysticercosis vaccine: an epitope shared by Taenia crassiceps and Taenia solium protects mice against experimental cysticercosis. Infect Immun 67(5):2522–2530PubMedCentralPubMedGoogle Scholar
  60. Trejo-Chávez H, García-Vilchis D, Reynoso-Ducoing O, Ambrosio JR (2011) In vitro evaluation of the effects of cysticidal drugs in the Taenia crassiceps cysticerci ORF strain using the fluorescent Cell Tracker CMFDA. Exp Parasitol 127(1):294–299PubMedCrossRefGoogle Scholar
  61. Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, Aslett M, Beasley H, Bennett HM, Cai J, Camicia F, Clark R, Cucher M, De Silva N, Day TA, Deplazes P, Estrada K, Fernández C, Holland PW, Hou J, Hu S, Huckvale T, Hung SS, Kamenetzky L, Keane JA, Kiss F, Koziol U, Lambert O, Liu K, Luo X, Luo Y, Macchiaroli N, Nichol S, Paps J, Parkinson J, Pouchkina Stantcheva N, Riddiford N, Rosenzvit M, Salinas G, Wasmuth JD, Zamanian M, Zheng Y, Sánchez Flores A, Cevallos MA, Morett E, González V, Portillo T, Ochoa-Leyva A, José MV, Landa A, Jiménez L, Valdés V, Carrero JC, Larralde C, Morales Montor J, Limón Lason J, Soberón X, Laclette JP, Cai X, Olson PD, Brehm K, Berriman M, Consortium TTG (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496(7443):57–63PubMedCentralPubMedCrossRefGoogle Scholar
  62. Vaca-Paniagua F, Parra-Unda R, Landa A (2009) Characterization of one typical 2-Cys peroxiredoxin gene of Taenia solium and Taenia crassiceps. Parasitol Res 105(3):781–787PubMedCrossRefGoogle Scholar
  63. Valverde-Islas LE, Arrangoiz E, Vega E, Robert L, Villanueva R, Reynoso-Ducoing O, Willms K, Zepeda-Rodríguez A, Fortoul TI, Ambrosio JR (2011) Visualization and 3D reconstruction of flame cells of Taenia solium (Cestoda). PLoS ONE 6(3):e14754PubMedCentralPubMedCrossRefGoogle Scholar
  64. Vargas-Parada L, Laclette JP (2003) Gene structure of Taenia solium paramyosin. Parasitol Res 89(5):375–378PubMedGoogle Scholar
  65. Virginio VG, Monteiro KM, Drumond F, de Carvalho MO, Vargas DM, Zaha A, Ferreira HB (2012) Excretory/secretory products from in vitro-cultured Echinococcus granulosus protoscoleces. Mol Biochem Parasitol 183(1):15–22PubMedCrossRefGoogle Scholar
  66. Voge M (1963) Observations on the structure of cysticerci of Taenia solium and Taenia saginata (Cestoda:Taeniidae). J Parasitol 49:85–90PubMedCrossRefGoogle Scholar
  67. Willms K, Zurabian R (2010) Taenia crassiceps: in vivo and in vitro models. Parasitology 137(3):335–346PubMedCrossRefGoogle Scholar
  68. Wu L, Diao Z, Deng X, Gao J, Zhou Z, Liu Y, Wang Y (2005) DNA vaccine against Taenia solium cysticercosis expressed as a modified hepatitis B virus core particle containing three epitopes shared by Taenia crassiceps and Taenia solium. J Nanosci Nanotechnol 5(8):1204–1210PubMedCrossRefGoogle Scholar
  69. Xi JH, Bai F, McGaha R, Andley UP (2006) Alpha-crystallin expression affects microtubule assembly and prevents their aggregation. FASEB J 20(7):846–857PubMedCrossRefGoogle Scholar
  70. Yang D, Fu Y, Wu X, Xie Y, Nie H, Chen L, Nong X, Gu X, Wang S, Peng X, Yan N, Zhang R, Zheng W, Yang G (2012) Annotation of the transcriptome from Taenia pisiformis and its comparative analysis with three Taeniidae species. PLoS One 7(4):e32283PubMedCentralPubMedCrossRefGoogle Scholar
  71. Yong WK, Heath DD, Van Knapen F (1984) Comparison of cestode antigens in an enzyme-linked immunosorbent assay for the diagnosis of Echinococcus granulosus, Taenia hydatigena and T ovis infections in sheep. Res Vet Sci 36(1):24–31PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Olivia Reynoso-Ducoing
    • 1
  • Laura Valverde-Islas
    • 1
  • Cristina Paredes-Salomon
    • 1
  • América Pérez-Reyes
    • 1
  • Abraham Landa
    • 1
  • Lilia Robert
    • 1
  • Guillermo Mendoza
    • 2
  • Javier R. Ambrosio
    • 1
    Email author
  1. 1.Facultad de Medicina, Departamento de Microbiología y ParasitologíaUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  2. 2.Facultad de Medicina, Departamento de BioquímicaUniversidad Nacional Autónoma de MéxicoMéxicoMéxico

Personalised recommendations