Surface analysis of dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs

Journal of Proteomics

Volumn 105, Issue , 2014, Pages 232-241

  Bernal, Dolores ^a   Trelis, Maria ^a   Montaner, Sergio ^a   Cantalapiedra, Fernando ^a   Galiano, Alicia ^a   Hackenberg, Michael ^b,c   Marcilla, Antonio ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c Centro de Investigacion Biomedica   (Spain)

Author keywords

Dicrocoelium dendriticum; Exosome; Helminth; MiRNA; Proteomics; Surfome

Indexed keywords

MICROORGANISM PROTEIN; MICRORNA; PARASITE PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; HELMINTH PROTEIN; HELMINTH RNA;

ARTICLE; DICROCOELIUM; DICROCOELIUM DENDRITICUM; ECHINOSTOMA; ECHINOSTOMA CAPRONI; ELECTRON MICROSCOPY; EXOSOME; HIGH THROUGHPUT SEQUENCING; NONHUMAN; PARASITE IDENTIFICATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEOMICS; RNA PURIFICATION; SURFACE PROPERTY; ANIMAL; GENETICS; METABOLISM; PROCEDURES; PROTEIN DATABASE;

DICROCOELIUM DENDRITICUM; ECHINOSTOMA CAPRONI; VERMES;

ANIMALS; DATABASES, PROTEIN; DICROCOELIUM; EXOSOMES; HELMINTH PROTEINS; MICRORNAS; PROTEOMICS; RNA, HELMINTH;

EID: 84901833952     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.02.012     Document Type: Article

References (54)

1. Cantacessi C., Campbell B.E., Jex A.R., Young N.D., Hall R.S., Ranganathan S. Bioinformatics meets parasitology. Parasite Immunol 2011, 34:265-275.
2. Manga-Gonzalez M.Y., Gonzalez-Lanza C., Cabanas E., Campo R. Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. Parasitology 2001, 123(Suppl.):S91-S114.
3. Rojo-Vázquez F.A., Meana A., Valcárcel F., Martínez-Valladares M. Update on trematode infections in sheep. Vet Parasitol 2012, 189:15-38.
4. Otranto D., Traversa D. A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment. Vet Parasitol 2002, 107:317-335.
5. Manga-González M.Y., Ferreras M.C., Campo R., Gónzalez-Lanza C., Pérez V., García-Marín J.F. Hepatic marker enzymes, biochemical parameters and pathological effects in lambs experimentally infected with Dicrocoelium dendriticum (Digenea). Parasitol Res 2004, 93:344-355.
6. Haridy F.M., Morsy T.A., Ibrahim B.B., Abdel-Aziz A. A preliminary study on dicrocoeliasis in Egypt, with a general review. J Egypt Soc Parasitol 2003, 33:85-96.
7. Jeandron A., Rinaldi L., Abdyldaieva G., Usubalieva J., Steinmann P., Cringoli G., et al. Human infections with Dicrocoelium dendriticum in Kyrgyzstan: the tip of the iceberg?. J Parasitol 2011, 97:1170-1172.
8. Hewitson J.P., Grainger J.R., Maizels R.M. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009, 167:1-11.
9. Toledo R., Bernal M.D., Marcilla A. Proteomics of foodborne trematodes. J Proteomics 2011, 7:1485-1503.
10. Revilla-Nuín B., Manga-González M.Y., Minambres B., Gónzalez-Lanza C. Partial characterization and isolation of 130kDa antigenic protein of Dicrocoelium dendriticum adults. Vet Parasitol 2005, 134:229-240.
11. Wedrychowicz H., Ducommun D., Klockiewicz M., Pfister K. Surface and ES antigens of adult Dicrocoelium dendriticum inducing bile antibody responses in naturally infected cattle. Acta Parasitol 1996, 41:139-144.
12. Martínez-Ibeas A.M., González-Lanza C., Manga-González M.Y. Proteomic analysis of the tegument and excretory-secretory products of Dicrocoelium dendriticum (Digenea) adult worms. Exp Parasitol 2013, 133:411-420.
13. Gonzales-Santana B., Dalton J.P., Vasquez Camargo F., Parkinson M., Ndao M. The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease. PLoS Negl Trop Dis 2013, 7:e2414.
14. Martínez-Ibeas A.M., Perteguer M.J., González-Lanza C., Gárate T., Manga-González M.Y. Analysis of an expressed sequence tag library from Dicrocoelium dendriticum. Exp Parasitol 2013, 135:287-296.
15. Marcilla A., Trelis M., Cortes A., Sotillo J., Cantalapiedra F., Mínguez M.T., et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One 2012, 7:e45974.
16. Marcilla A., Sotillo J., Pérez-Garcia A., Igual-Adell R., Valero M.L., Sánchez-Pino M.M., et al. Proteomic analysis of Strongyloides stercoralis L3 larvae. Parasitology 2010, 137:1577-1583.
17. Lässer C., Eldh M., Lötvall J. Isolation and characterization of RNA-containing exosomes. J Vis Exp 2012, 59:e3037. [doi:e3037].
18. Sotillo J., Valero L., Sánchez Del Pino M.M., Fried B., Esteban J.G., Marcilla A., et al. Identification of antigenic proteins from Echinostoma caproni (Trematoda) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunol 2008, 30:271-279.
19. Garg G., Bernal D., Trelis M., Forment J., Ortiz J., Valero M.L., et al. The transcriptome of Echinostoma caproni adults: further characterization of the secretome and identification of new potential drug targets. J Proteomics 2013, 89:202-214.
20. Shilov I.V., Seymour S.L., Patel A.A., Loboda A., Tang W.H., Keating S.P., et al. The Paragon algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 2007, 6:1638-1655.
21. Hackenberg M., Rodríguez-Ezpeleta N., Aransay A.M. miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Res 2011, 39:W132-W138.
22. Kozomara A., Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42(D1):D68-D73. 10.1093/nar/gkt1181.
23. Kalra H., Simpson R.J., Ji H., Aikawa E., Altevogt P., Askenase P., et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012, 10:e1001450.
24. Xu M.J., Ai L., Fu J.H., Nisbet A.J., Liu Q.Y., Chen M.X., et al. Comparative characterization of microRNAs from the liver flukes Fasciola gigantica and F. hepatica. PLoS One 2012, 7:e53387.
25. Ferreras-Estrada M.C., Campo R., González-Lanza C., Pérez V., García-Marín J.F., Manga-González M.Y. Immunohistochemical study of the local immune response in lambs experimentally infected with Dicrocoelium dendriticum (Digenea). Parasitol Res 2007, 101:547-555.
26. Manga-González M.Y., Quiroz-Romero H., González-Lanza C., Miñambres B., Ochoa P. Strategic control of Dicrocoelium dendriticum (Digenea) egg excretion by naturally infected sheep. Vet Med 2010, 55:19-29.
27. Wilson R.A., Curwen R.S., Braschi S., Hall S.L., Coulson P.S., Ashton P.D. From genomes to vaccines via the proteome. Mem Inst Oswaldo Cruz 2004, 99:45-50.
28. Olaya-Abril A., Jimenez-Munguia I., Gómez-Gascón L., Rodríguez-Ortega M.J. Surfomics: shaving live organisms for a fast proteomic identification of surface proteins. J Proteomics 2014, 97:164-176. 10.1016/j.jprot.2013.03.035.
29. Pérez-Sánchez R., Valero M.L., Ramajo-Hernández A., Siles-Lucas M., Ramajo-Martín V., Oleaga A. A proteomic approach to the identification of tegumental proteins of male and female Schistosoma bovis worms. Mol Biochem Parasitol 2008, 161:112-123.
30. Hernández-González A., Valero M.L., Sánchez del Pino M., Oleaga A., Siles-Lucas M. Proteomic analysis of in vitro newly excysted juveniles from Fasciola hepatica. Mol Biochem Parasitol 2010, 172:121-128.
31. Santivañez S.J., Hernández-González A., Chile N., Oleaga A., Arana Y., Palma S., et al. Proteomic study of activated Taenia solium oncospheres. Mol Biochem Parasitol 2010, 171:32-39.
32. Castro-Borges W., Dowle A., Curwen R.S., Thomas-Oates J., Wilson R.A. Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Negl Trop Dis 2011, 5:e993.
33. De la Torre Escudero E., Manzano-Román R., Valero L., Oleaga A., Pérez-Sánchez R., Hernández-González A., et al. Comparative proteomic analysis of Fasciola hepatica juveniles and Schistosoma bovis schistosomula. J Proteomics 2011, 74:1534-1544.
34. Sotillo J., Valero M.L., Sánchez Del Pino M.M., Fried B., Esteban J.G., Marcilla A., et al. Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitol Res 2010, 107:691-697.
35. Ramajo-Hernández A., Oleaga A., Ramajo-Martín V., Pérez-Sánchez R. Carbohydrate profiling and protein identification of tegumental and excreted/secreted glycoproteins of adult Schistosoma bovis worms. Vet Parasitol 2007, 144:45-60.
36. Sotillo J., Trudgett A., Halferty L., Marcilla A., Esteban J.G., Toledo R. Echinostoma caproni: differential tegumental responses to growth in compatible and less compatible hosts. Exp Parasitol 2010, 125:304-309.
37. Théry C. Exosome explosion!. Scientist 2011, 25:36-40.
38. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013, 200:373-383.
39. Barteneva N.S., Maltsev N., Vorobjev I.A. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol 2013, 3:49.
40. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010, 73:1907-1920.
41. Silverman J.M., Clos J., de'Oliveira C.C., Shirvani O., Fang Y., Wang C., et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci 2010, 123:842-852.
42. Martínez-Sernández V., Mezo M., González-Warleta M., Perteguer M.J., Muino L., Guitian E., et al. The MF6p/FhHDM-1 major antigen secreted by the trematode parasite Fasciola hepatica is a heme-binding protein. J Biol Chem 2014, 289(3):1441-1456. 10.1074/jbc.M113.499517.
43. Robinson M.W., Donnelly S., Hutchinson A.T., To J., Taylor N.L., Norton R.S., et al. A family of helminth molecules that modulate innate cell responses via molecular mimicry of host antimicrobial peptides. PLoS Pathog 2011, 7:e1002042.
44. Robinson M.W., Alvarado R., To J., Hutchinson A.T., Dowdell S.N., Lund M., et al. A helminth cathelicidin-like protein suppresses antigen processing and presentation in macrophages via inhibition of lysosomal vATPase. FASEB J 2012, 26:4614-4627.
45. Valadi H., Ekstrom K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
46. Villarroya-Beltri C., Gutiérrez-Vázquez C., Sánchez-Madrid F., Mittelbrunn M. Analysis of microRNA and protein transfer by exosomes during an immune synapse. Methods Mol Biol 2013, 1024:41-51.
47. Dalton J.P., Robinson M.W., Mulcahy G., O'Neill S.M., Donnelly S. Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development. Vet Parasitol 2013, 195:272-285.
48. Simoes M.C., Lee J., Djikeng A., Cerqueira G.C., Zerlotini A., da Silva-Pereira R.A., et al. Identification of Schistosoma mansoni microRNAs. BMC Genomics 2011, 12:47. [2164-12-47].
49. Cheng G., Luo R., Hu C., Cao J., Jin Y. Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 2013, 140:1751-1761.
50. Xu M.J., Liu Q., Nisbet A.J., Cai X.Q., Yan C., Lin R.Q., et al. Identification and characterization of microRNAs in Clonorchis sinensis of human health significance. BMC Genomics 2010, 11:521. [2164-11-521].
51. Thirugnanasambantham K., Hairul-Islam V.I., Saravanan S., Subasri S., Subastri A. Computational approach for identification of Anopheles gambiae miRNA involved in modulation of host immune response. Appl Biochem Biotechnol 2013, 170:281-291.
52. Manzano-Román R., Siles-Lucas M. MicroRNAs in parasitic diseases: potential for diagnosis and targeting. Mol Biochem Parasitol 2012, 186:81-86.
53. Li H., Huang S., Guo C., Guan H., Xiong C. Cell-free seminal mRNA and microRNA exist in different forms. PLoS One 2012, 7:e34566.
54. Vickers K.C., Remaley A.T. Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol 2012, 23:91-97.