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Identification of somatic proteins in Haemonchus contortus infective larvae (L3) and adults Cover

Identification of somatic proteins in Haemonchus contortus infective larvae (L3) and adults

Open Access
|Sep 2022

References

  1. Aguerre, S., Jacquiet, P., Brodier, H., Bournazel, J.P., Grisez, C., Prévot, F., Michot, L., Fidelle, F., Astruc, J.M., Moreno, C.R. (2018): Resistance to gastrointestinal nematodes in dairy sheep: Genetic variability and relevance of artificial infection of nucleus rams to select for resistant ewes on farms. Vet Parasitol, 256: 16–23. DOI: 10.1016/j.vetpar.2018.04.004
  2. Alunda, R.J.M., Cuquerella, A.M., Mohamed, F.E. (2014): Proteína recombinante de Haemonchus contortus y su aplicación para la producción de una vacuna frente a la hemoncosis [Recombinant protein of Haemonchus contortus and use thereof for the production of a vaccine against haemonchosis]. Oficina Española Depatentes y Marcas N° 201200865 (In Spanish)
  3. Arike, L., Peil, L. (2014): Spectral counting label-free proteomics. In: Martins-de-Souza, D. (Ed) Shotgun Proteomics. Methods in Molecular Biology Methods and Protocols). Volume 1156. Humana Press, New York, NY, pp. 213–222. DOI:10.1007/978-1-4939-0685-7_14
  4. Arsenopoulos, K.V., Fthenakis, G.C., Katsarou, E.I., Papadopoulos, E. (2021): Haemonchosis: A challenging parasitic infection of sheep and goats. Animals, 11(2): 363. DOI: 10.3390/ani11020363Bassetto, C.C., Almeida, F.A., Newlands, G.F.J., Smith, W.D., Castilhos, A.M., Fernandes, S., Siqueira, E.R., Amarante, A.F.T. (2018): Trials with the Haemonchus vaccine, Barbervax®, in ewes and lambs in a tropical environment: Nutrient supplementation improves protection in periparturient ewes. Vet Parasitol, 264: 52–57. DOI: 10.1016/j.vetpar.2018.11.006
  5. Bordoloi, G., Jas, R., Ghosh, J.D. (2012): Changes in the haema-to-biochemical pattern due to experimentally induced haemonchosis in Sahabadi sheep. J Parasit Dis, 36: 101–105. DOI: 10.1007/s12639-011-0079-7
  6. Corticelli, B., Lai, M. (1963): Studies on the technique of culture of infective larvae of gastrointestinal strongyles of cattle. Acta Med Vet (Napoli), 9: 347–357
  7. Cox, G.N., Pratt, D., Hageman, R., Boisvenue, R.J. (1990): Molecular cloning and primary sequence of a cysteine protease expressed by Haemonchus contortus adult worms Mol Biochem Parasitol, 41: 25–34. DOI: 10.1016/0166-6851(90)90093-2
  8. Cringoli, G., Rinaldi, L., Veneziano, V., Capelli, G., Scala, A. (2004): The influence of flotation solution, sample dilution and the choice of McMaster slide area (volume) on the reliability of the McMaster technique in estimating the faecal egg counts of gastrointestinal strongyles and Dicrocoelium dendriticum in sheep. Vet Parasitol, 123: 121–131. DOI: 10.1016/j.vetpar.2004.05.021
  9. Cruz-Tamayo, A., Garduño, R., Torres-Hernández, G., Becerril Pérez, C.M., Hernández-Mendo, O., Ramírez-Bribiesca, J.E., López-Arellano, M., Vargas-Magaña, J., Ojeda-Robertos, N. (2020): Comparison of two phenotypical methods to segregate resistant and susceptible lambs to parasitic nematodes Austral J Vet Sci, 52 (1): 9–18. DOI: 10.4067/S0719-81322020000100103
  10. De Albuquerque, A.C.A., Bassetto, C.C., De Almeida, F.A. Amarante, A.F.T. (2017): Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Vet Parasitol, 246: 112–117. DOI: 10.1016/j.vetpar.2017.09.010
  11. Dufour, S., Mège, R.M., Thiery, J.P. (2013): α-catenin, vinculin, and F-actin in strengthening E-cadherin cell-cell adhesions and mechanosensing. Cell Adh Migr, 7 (4): 345–350. DOI: 10.4161/cam.25139
  12. El-Mezgueldi, M. (1996): Calponin. Int J Biochem Cell Biol, 28: 1185–1189. DOI: 10.1016/S1357-2725(96)00085-4
  13. Eng, J.K., McCormack, A.L., Yates, J.R. (1994): An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom, 5: 976–989. DOI: 10.1016/1044-0305(94)80016-2
  14. Estrada-Reyes, Z.M., Tsukahara, Y., Amadeu, R.R., Goetsch, A.L., Gipson, T.A., Sahlu, T., Puchala, R., Wang, Z., Hart, S.P., Mateescu, R.G. (2019): Signatures of selection for resistance to Haemonchus contortus in sheep and goats. BMC Genomics, 20: 735. DOI: 10.1186/s12864-019-6150-y
  15. Gadahi, J.A., Wang, S., Bo, G., Ehsan, M., Yan, R., Song, X., Xu, L., Li, X. (2016): Proteomic analysis of the excretory and secretory proteins of Haemonchus contortus (HcESP) binding to goat PB-MCs in vivo revealed stage-specific binding profiles. PloS One, 11: e0159796 – e0159796. DOI: 10.1371/journal.pone.0159796
  16. García-Coiradas, L., Angulo-Cubillán, F., Valladares, B., Martínez, E., De La Fuente, C., Alunda, J.M., Cuquerella, M. (2010): Immunization against lamb haemonchosis with a recombinant somatic antigen of Haemonchus contortus (rHcp26/23). Vet Med Int, Article ID 852146, 8 pages. DOI: 10.4061/2010/852146
  17. González-Sánchez, M. E, Cuquerella, M, Alunda, J.M. (2018): Vaccination of lambs against Haemonchus contortus with the recombinant rHc23. Effect of adjuvant and antigen dose. PLoS ONE, 13(3): e0193118. DOI: 10.1371/journal.pone.0193118
  18. González-Sánchez, M.E., Ndombasi-Bokuy, M., Cuquerella, M., Alunda, J.M. (2019): Immunization with recombinant rHc23 partially protects lambs against trickle infections by Haemonchus contortus BMC Vet Res, 15(1): 333. DOI: 10.1186/s12917-019-2084-5
  19. Guo, X., Zhang, H., Zheng, X., Zhou, Q., Yang, Y., Chen, X., Du, A. (2016): Structural and functional characterization of a novel gene, Hc-daf-22, from the strongylid nematode Haemonchus contortus Parasit Vectors, 9: 422. DOI: 10.1186/s13071-016-1704-1
  20. Harder, A. (2016): The Biochemistry of Haemonchus contortus and other parasitic nematodes. Adv Parasitol, 93: 69–94. DOI: 10.1016/bs.apar.2016.02.010
  21. Javare, G.A.K. (2017): Immunodiagnosis of Haemonchus contortus infection in sheep by counter immuno-electrophoresis using somatic antigen. J Parasit Dis, 41(2): 352–355. DOI: 10.1007/s12639-016-0801-6
  22. Karanu, F., McGuire, T., Davis, W.C., Beser, T., Jasmer, D. (1997): CD4+ T lymphocytes contribute to protective immunity induced in sheep and goats by Haemonchus contortus gut antigens. Parasite Immunol, 19: 435–445. DOI: 10.1046/j.1365-3024.1997.d01-149.x
  23. Kebeta, M.M., Hine, B.C., Walkden-Brown, S.W., Kahn, L.P., Doyle, E.K. (2021): Protective efficacy of Barbervax® in Merino weaner sheep trickle infected with five doses of Haemonchus contortus infective larvae. Vet Parasitol, 292: 109386. DOI: 10.1016/j.vet-par.2021.109386
  24. Kotze, A. (2003): Catalase induction protects Haemonchus contortus against hydrogen peroxide in vitro Int J Parasitol, 33: 393–400. DOI: 10.1016/s0020-7519(03)00012-2
  25. Kotze, A.C., Mcclure, S.J. (2001): Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro Int J Parasitol, 31: 1563–1571. DOI: 10.1016/S0020-7519(01)00303-4
  26. Laing, R., Kikuchi, T., Martinelli, A., Tsai, I.J., Beech, R.N., Redman, E., Holroyd, N., Bartley, D.J., Beasley, H., Britton, C., Curran, D., Devaney, E., Gilabert, A., Hunt, M., Jackson, F., Johnston, S.L., Kryukov, I., Li, K., Morrison, A.A., Reid, A.J., Sargison, N., Saunders, G.I., Wasmuth, J.D., Wolstenholme, A., Berriman, M., Gilleard, J.S., Cotton, J.A. (2013): The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol, 14: R88. DOI: 10.1186/gb-2013-14-8-r88Lang, T., Lee, J.P.W., Elgas, K., Pinar, A.A., Tate, M.D., Aitken, E.H., Fan, H., Creed, S.J., Deen, N.S., Traore, D.A.K., Mueller, I., Stanisic, D., Baiwog, F.S., Skene, C., Wilce, M.C.J., Mansell, A., Morand, E.F., Harris, J. (2018): Macrophage migration inhibitory factor is required for NLRP3 inflammasome activation. Nat Commun, 9: 2223. DOI: 10.1038/s41467-018-04581-2
  27. Lu, M., Tian, X., Yang, Z., Wang, W., Tian, A.-L., Li, C., Yan, R., Xu, L., Song, X., Li, X. (2020): Proteomic analysis revealed T cell hyporesponsiveness induced by Haemonchus contortus excretory and secretory proteins. Vet Res, 51: 65. DOI: 10.1186/s13567-020-00790-0
  28. Naqvi, M.A., Aimulajiang, K., Memon, M.A., Hasan, M.W., Naqvi, S. Z., Lakho, S. A., Chu, W., Xu, L., Song, X., Li, X., And Yan, R. (2020b). Recombinant cold shock domain containing protein is a potential antigen to detect specific antibody during early and late infections of Haemonchus contortus in goat. BMC Vet Res, 16(1): 36. DOI: 10.1186/s12917-020-2261-6
  29. Naqvi, M.A., Memon, M.A., Jamil, T., Naqvi, S.Z., Aimulajiang, K., Gadahi, J.A., Xu, L., Song, X., Li, X., Yan, R. (2020): Galectin domain containing protein from Haemonchus contortus modulates the immune functions of goat PBMCs and regulates CD4+ T-Helper cells in vitro Biomolecules., 10: 116. DOI: 10.3390/biom10010116
  30. Nisbet, A.J., Meeusen, E.N., González, J.F., Piedrafita, D.M. (2016): Chapter Eight - Immunity to Haemonchus contortus and vaccine development. In: Gaser, R.B., von Samson-Himelstjerna, G. (Eds) Haemonchus contortus and Haemonchosis – Past, Present and Future Trends, (Academic Press). Adv Parasitol, 93: 353–396. DOI: 10.1016/bs.apar.2016.02.011
  31. Niu, L., Zhang, H., Wu, Z., Wang, Y., Liu, H., Wu, X., Wang, W. (2018): Modified TCA/acetone precipitation of plant proteins for proteomic analysis. PLoS One, 13: e0202238 – e0202238. DOI: 10.1371/journal.pone.0202238
  32. Palomo-Couoh, J.G., Aguilar-Caballero, A.J., Torres-Acosta, J.F.J., González-Garduño, R. (2017): Comparing the phenotypic susceptibility of Pelibuey and Katahdin female lambs against natural gastrointestinal nematode infections under hot humid tropical conditions. Parasitol Res, 116: 1627–1636. DOI: 10.1007/s00436-017-5437-7
  33. Palomo-Couoh, J.G., Aguilar-Caballero, A.J., Torres-Acosta, J.F.J. Magaña-Monforte, J.G. (2016): Evaluation of different models to segregate Pelibuey and Katahdin ewes into resistant or susceptible to gastrointestinal nematodes. Trop Anim Health Prod, 48: 1517–1524. DOI: 10.1007/s11250-016-1122-6
  34. Pandey, V.S., Sivaraj, S. (1994): Anthelmintic resistance in Haemonchus contortus from sheep in Malaysia. Vet Parasitol, 53 (1-2): 67–74. DOI: 10.1016/0304-4017(94)90018-3
  35. Peterson, G.L. (1977): A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem, 83: 346–356. DOI: 10.1016/0003-2697(77)90043-4
  36. Rohrbough, J.G., Breci, L., Merchant, N., Miller, S., Haynes, P.A. (2006): Verification of single-peptide protein identifications by the application of complementary database search algorithms. J Bio-mol Tech, 17: 327–332
  37. Sakthivel, D., Swan, J., Preston, S., Shakif-Azam, M.D., Faou, P., Jiao, Y., Downs, R., Rajapa ksha, H., Gasser, R., Piedrafita., Beddoe, T. (2018): Proteomic identification of galectin-11 and 14 ligands from Haemonchus contortus PeerJ, 6: e4510 – e4510. DOI: 10.7717/peerj.4510
  38. Scarff, C.A., Thompson, R.F., Newlands, G.F.J., Jamson, A.H., Kennaway, C., Da Silva, V.J., Rabelo, E.M., Song, C.-F., Trinick, J., Smith, W.D., Muench, S.P. (2020): Structure of the protective nematode protease complex H-gal-GP and its conservation across roundworm parasites. PLoS Pathog, 16: e1008465 – e1008465. DOI: 10.1371/journal.ppat.1008465
  39. Tian, X., Lu, M., Jia, C., Bu, Y., Aimulajiang, K., Zhang, Y., Li, C., Yan, R., Xu, L., Song, X., Li, X. (2020): Haemonchus contortus transthyretin domain-containing protein (HcTTR): A promising vaccine candidate against Haemonchus contortus infection Vet Parasitol, 279: 109045. DOI: 10.1016/j.vetpar.2020.109045
  40. Van Wyk, J.A., Mayhew, E. (2013): Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: A practical lab guide. Onderstepoort J Vet Res, 8: 1–14. DOI: 10.4102/ojvr.v80i1.539
  41. Wang, Q., Michalak, M. (2020): Calsequestrin. Structure, function, and evolution. Cell Calcium, 90: 102242. DOI: 10.1016/j.ceca.2020.102242
  42. Wang, T., Ma, G., Ang, C.-S., Korhonen, P.K., Koehler, A. V, Young, N.D., Nie, S., Williamson, N.A., Gasser, R.B. (2019a): High throughput LC-MS/MS-based proteomic analysis of excretory-secretory products from short-term in vitro culture of Haemonchus contortus. J Proteomics, 204: 103375. DOI: 10.1016/j.jprot.2019.05.003
  43. Wang, T., Ma, G., Ang, C.-S., Korhonen, P.K., Xu, R., Nie, S., Koehler, A. V., Simpson, R.J., Greening, D.W., Reid, G.E., Williamson, N.A., Gasser, R.B. (2019b). Somatic proteome of Haemonchus contortus Int J Parasitol, 49: 311–320. DOI: 10.1016/j.ijpa-ra.2018.12.003
  44. Wang, T., Nie, S., Ma, G., Korhonen, P.K., Koehler, A. V, Ang, C.-S., Reid, G.E., Williamson, N.A., Gasser, R.B. (2018): The developmental lipidome of Haemonchus contortus. Int J Parasitol, 48: 887–895. DOI: 10.1016/j.ijpara.2018.06.002
  45. Xie, K., Zhang, P., Na, H., Liu, Y., Zhang, H., Liu, P. (2019). MDT-28/PLIN-1 mediates lipid droplet-microtubule interaction via DLC-1 in Caenorhabditis elegans Sci Rep, 9: 14902. DOI: 10.1038/s41598-019-51399-z
  46. Yang, Y., Zhang, G., Wu, J., Chen, X., Tong, D., Yang, Y., Shi, H., Yao, C., Zhuang, L., Wang, J., Du, A. (2020): Recombinant HcGAP-DH protein expressed on probiotic Bacillus subtilis spores protects sheep from Haemonchus contortus infection by inducing both humoral and cellmediated responses. mSystems, 5(3): e00239-20. DOI: 10.1128/mSystems.00239-20
  47. Yanming, S., Ruofeng, Y., Muleke, C.I., Guangwei, Z., Lixin, X., Xiangrui, L. (2007): Vaccination of goats with recombinant galectin antigen induces partial protection against Haemonchus contortus infection. Parasite Immunol, 29: 319–326. DOI: 10.1111/j.1365-3024.2007.00949.x
  48. Yan, R., Wang, J., Xu, L., Song, X., Li, X. (2014): DNA vaccine encoding Haemonchus contortus actin induces partial protection in goats. Acta Parasitol, 59 (4): 698–709. DOI: 10.2478/s11686-014-0298-z
  49. Yatsuda, A., Krijgsveld, J., Cornelissen, A., Heck, A., De Vries, E. (2003): Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J Biol Chem, 278: 16941–16951. DOI: 10.1074/jbc.M212453200
  50. Yi, D., Xu, L., Yan, R., Li, X. (2010): Haemonchus contortus: Cloning and characterization of serpin. Exp Parasitol, 125: 363–370. DOI: 10.1016/j.exppara.2010.03.002
  51. Zaragoza-Vera, C.V., Aguilar-Caballero, A.J., González-Garduño, R., Arjona-Jiménez, G., Zaragoza-Vera, M., Torres-Acosta, J.F.J., Medina-Reynés, J.U., Berumen-Alatorre, A.C. (2019): Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico. Parasitol Res, 118: 567–573. DOI:10.1007/s00436-018-06201-w
  52. Supplementary Table S1. The full list of somatic proteins found in L3 and adults of Haemonchus contortus is available online at https://doi.org/10.2478/helm-2022-0017
DOI: https://doi.org/10.2478/helm-2022-0017 | Journal eISSN: 1336-9083 | Journal ISSN: 0440-6605
Language: English
Page range: 143 - 151
Submitted on: Dec 1, 2021
Accepted on: May 5, 2022
Published on: Sep 3, 2022
Published by: Slovak Academy of Sciences
In partnership with: Paradigm Publishing Services
Publication frequency: 4 times per year

© 2022 M. Zaragoza-Vera, R. González-Garduño, L. Brito-Argáez, A. J. Aguilar-Caballero, C. V. Zaragoza-Vera, G. Arjona-Jiménez, V. M. Loyola-Vargas, V. Aguilar-Hernández, O. M. Torres-Chable, published by Slovak Academy of Sciences
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