Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with Next-Generation sequencing transcriptomic information

PLoS Neglected Tropical Diseases

Volumn 5, Issue 10, 2011, Pages

  Moreno, Yovany ^a   Gros, Pierre Paul ^b   Tam, Mifong ^b   Segura, Mariela ^b   Valanparambil, Rajesh ^b   Geary, Timothy G ^a   Stevenson, Mary M ^b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CYSTEINE PROTEINASE INHIBITOR; FATTY ACID BINDING PROTEIN; GALECTIN; GLOBIN; GLUTATHIONE TRANSFERASE; HELMINTH PROTEIN; LECTIN; MACROPHAGE MIGRATION INHIBITION FACTOR; PEROXIREDOXIN; RETINOL; VITELLOGENIN; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; FEMALE; FUNCTIONAL PROTEOMICS; HELIGMOSOMOIDES POLYGYRUS; HOST PARASITE INTERACTION; IMMUNOMODULATION; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARASITE SURVIVAL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN FUNCTION; RNA SEQUENCE; TRANSCRIPTOMICS; TRICHOSTRONGYLOSIS; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; NEMATOSPIROIDES DUBIUS; TANDEM MASS SPECTROMETRY;

ANIMALS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GENE EXPRESSION PROFILING; HELMINTH PROTEINS; MALE; MICE; MICE, INBRED BALB C; NEMATOSPIROIDES DUBIUS; PROTEOME; SEQUENCE ANALYSIS, DNA; TANDEM MASS SPECTROMETRY;

EID: 80055099099     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001370     Document Type: Article

References (89)

1. Eziefula AC, Brown M, (2008) Intestinal nematodes: Disease burden, deworming and the potential importance of co-infection. Curr Opin Infect Dis 21: 516-522.
2. Behnke JM, Barnard CJ, Wakelin D, (1992) Understanding chronic nematode infections: Evolutionary considerations, current hypotheses and the way forward. Int J Parasitol 22: 861-907.
3. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, et al. (2004) Helminth parasites - masters of regulation. Immunol Rev 201: 89-116.
4. Nacher M, (2008) Worms and malaria: blind men feeling the elephant? Parasitology 135: 861-868.
5. Liu Q, Sundar K, Mishra PK, Mousavi G, Liu Z, et al. (2009) Helminth infection can reduce insulitis and Type 1 diabetes through CD25- and IL-10-independent mechanisms. Infect Immun 77: 5347-5358.
6. Behnke JM, Menge DM, Noyes H, (2009) Heligmosomoides bakeri: a model for exploring the biology and genetics of resistance to chronic gastrointestinal nematode infections. Parasitology 136: 1565-1580.
7. Finney CAM, Taylor MD, Wilson MS, Maizels RM, (2007) Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 37: 1874-1886.
8. Weng M, Huntley D, Huang I-F, Foye-Jackson O, Wang L, et al. (2007) Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J Immunol 179: 4721-4731.
9. Segura M, Su Z, Piccirillo C, Stevenson MM, (2007) Impairment of dendritic cell function by excretory-secretory products: A potential mechanism for nematode-induced immunosuppression. Eur J Immunol 37: 1887-1904.
10. Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y, et al. (2010) Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J Exp Med 207: 2331-2341.
11. Wilson MS, Taylor MD, Balic A, Finney CAM, Lamb JR, et al. (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202: 1199-1212.
12. Rzepecka J, Donskow-Schmelter K, Doligalska M, (2007) Heligmosomoides polygyrus infection down-regulates eotaxin concentration and CCR3 expression on lung eosinophils in murine allergic pulmonary inflammation. Parasite Immunol 29: 405-413.
13. Hewitson JP, Harcus YM, Curwen RS, Dowle AA, Atmadja AK, et al. (2008) The secretome of the filarial parasite, Brugia malayi: Proteomic profile of adult excretory-secretory products. Mol Biochem Parasitol 160: 8-21.
14. Nesvizhskii AI, (2007) Protein identification by tandem mass spectrometry and sequence database searching. In: Matthiesen R, editors. Mass Spectrometry Data Analysis in Proteomics Humana Press pp. 87-119.
15. Quirino BF, Candido ES, Campos PF, Franco OL, Krüger RH, (2010) Proteomic approaches to study plant-pathogen interactions. Phytochemistry 71: 351-362.
16. Carpentier SC, Panis B, Vertommen A, Swennen R, Sergeant K, et al. (2008) Proteome analysis of non-model plants: A challenging but powerful approach. Mass Spectrom Rev 27: 354-377.
17. Barrett J, Brophy PM, Hamilton JV, (2005) Analysing proteomic data. Int J Parasitol 35: 543-553.
18. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
19. Su Z, Segura M, Morgan K, Loredo-Osti JC, Stevenson MM, (2005) Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect Immun 73: 3531-3539.
20. Moreno Y, Geary TG, (2008) Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Negl Trop Dis 2: e326.
21. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
22. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.
23. Zerbino DR, Birney E, (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
24. Elsworth B, Wasmuth J, Blaxter M, NEMBASE4: The nematode transcriptome resource. Int J Parasitol In Press, Uncorrected Proof.
25. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
26. Bluthgen N, Brand K, Cajavec B, Swat M, Herzel H, et al. (2005) Biological profiling of gene groups utilizing Gene Ontology. Genome informatics series: proceedings of the Workshop on Genome Informatics Workshop on Genome Informatics 16: 106-115.
27. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-D215.
28. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, et al. (2005) InterProScan: Protein domains identifier. Nucleic Acids Res 33: W116-W120.
29. Al-Shahrour F, Díaz-Uriarte R, Dopazo J, (2004) FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20: 578-580.
30. Medina I, Carbonell J, Pulido L, Madeira SC, Goetz S, et al. (2010) Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res 38: W210-W213.
31. Hoehenwarter W, Wienkoop S, (2010) Spectral counting robust on high mass accuracy mass spectrometers. Rapid Commun Mass Spectrom 24: 3609-3614.
32. Hewitson JP, Grainger JR, Maizels RM, (2009) Helminth immunoregulation: The role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 167: 1-11.
33. Ranganathan S, Garg G, (2009) Secretome: clues into pathogen infection and clinical applications. Genome Med 1: 113.
34. Cantacessi C, Mitreva M, Campbell BE, Hall RS, Young ND, et al. (2010) First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infect Genet Evol 10: 1199-1207.
35. Cantacessi C, Mitreva M, Jex AR, Young ND, Campbell BE, et al. (2010) Massively parallel sequencing and analysis of the Necator americanus transcriptome. PLoS Negl Trop Dis 4: e684.
36. Wang Z, Abubucker S, Martin J, Wilson R, Hawdon J, et al. (2010) Characterizing Ancylostoma caninum transcriptome and exploring nematode parasitic adaptation. BMC Genomics 11: 307.
37. Renuse S, Chaerkady R, Pandey A, (2011) Proteogenomics. Proteomics 11: 620-630.
38. Kumar S, Blaxter M, (2010) Comparing de novo assemblers for 454 transcriptome data. BMC Genomics 11: 571.
39. Hoogewijs D, De Henau S, Dewilde S, Moens L, Couvreur M, et al. (2008) The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification. BMC Evol Biol 8: 279.
40. Blaxter ML, (1993) Nemoglobins: Divergent nematode globins. Parasitology Today 9: 353-360.
41. Bansemir AD, Sukhdeo MVK, (1996) Villus length influences habitat selection by Heligmosomoides polygyrus. Parasitology 113: 311-316.
42. Huang S, Huang J, Kloek AP, Goldberg DE, Friedman JM, (1996) Hydrogen B bonding of tyrosine B10 to heme-bound oxygen in Ascaris hemoglobin. J Biol Chem 271: 958-962.
43. Rao AU, Carta LK, Lesuisse E, Hamza I, (2005) Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci U S A 102: 4270-4275.
44. Kennedy MW, (2001) Structurally novel lipid-binding proteins Wallingford CABI Publishing pp. 309-330.
45. Kennedy MW, (2000) The polyprotein lipid binding proteins of nematodes. Biochimica et Biophysica Acta (BBA)- Protein Structure and Molecular Enzymology 1476: 149-164.
46. McDermott L, Cooper A, Kennedy MW, (1999) Novel classes of fatty acid and retinol binding protein from nematodes. Mol Cell Biochem 192: 69-75.
47. Kennedy MW, Garside LH, Goodrick LE, McDermott L, Brass A, et al. (1997) The Ov20 protein of the parasitic nematode Onchocerca volvulus. J Biol Chem 272: 29442-29448.
48. Koski KG, Scott ME, (2001) Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annu Rev Nutr 21: 297-321.
49. Stephensen CB, (2001) Vitamin A, infection, and immune function. Annu Rev Nutr 21: 167-192.
50. Mora JR, Iwata M, von Andrian UH, (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8: 685-698.
51. Vercauteren I, Geldhof P, Peelaers I, Claerebout E, Berx G, et al. (2003) Identification of excretory-secretory products of larval and adult Ostertagia ostertagi by immunoscreening of cDNA libraries. Mol Biochem Parasitol 126: 201-208.
52. Mulvenna J, Hamilton B, Nagaraj SH, Smyth D, Loukas A, et al. (2009) Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Mol Cell Proteomics 8: 109-121.
53. Hall DH, Winfrey VP, Blaeuer G, Hoffman LH, Furuta T, et al. (1999) Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: Relations between the germ line and soma. Dev Biol 212: 101-123.
54. Grant B, Hirsh D, (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
55. Lee KM, Lee KY, Choi HW, Cho MY, Kwon TH, et al. (2000) Activated phenoloxidase from Tenebrio molitor larvae enhances the synthesis of melanin by using a vitellogenin-like protein in the presence of dopamine. Eur J Biochem 267: 3695-3703.
56. Smolenaars MMW, Madsen O, Rodenburg KW, Van der Horst DJ, (2007) Molecular diversity and evolution of the large lipid transfer protein superfamily. J Lipid Res 48: 489-502.
57. Rono MK, Whitten MMA, Oulad-Abdelghani M, Levashina EA, Marois E, (2010) The major yolk protein vitellogenin interferes with the anti-Plasmodium response in the malaria mosquito Anopheles gambiae. PLoS Biol 8: e1000434.
58. McKerrow JH, Caffrey C, Kelly B, Loke Pn, Sajid M, (2006) Proteases in parasitic diseases. Annu Rev Pathol 1: 497-536.
59. Lawrence CE, Pritchard DI, (1993) Differential secretion of acetylcholinesterase and proteases during the development of Heligmosomoides polygyrus. Int J Parasitol 23: 309-314.
60. Williamson AL, Lecchi P, Turk BE, Choe Y, Hotez PJ, et al. (2004) A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms. J Biol Chem 279: 35950-35957.
61. Gounaris K, Selkirk ME, (2005) Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends Parasitol 21: 17-21.
62. Gounaris K, (2002) Nucleotidase cascades are catalyzed by secreted proteins of the parasitic nematode Trichinella spiralis. Infect Immun 70: 4917-4924.
63. Yatsuda AP, Krijgsveld J, Cornelissen AWCA, Heck AJR, 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.
64. Craig H, Wastling JM, Knox DP, (2006) A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 132: 535-543.
65. Cantacessi C, Campbell BE, Visser A, Geldhof P, Nolan MJ, et al. (2009) A portrait of the "SCP/TAPS" proteins of eukaryotes - Developing a framework for fundamental research and biotechnological outcomes. Biotechnology Advances 27: 376-388.
66. Chalmers I, McArdle A, Coulson R, Wagner M, Schmid R, et al. (2008) Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC Genomics 9: 89.
67. Hawdon JM, Jones BF, Hoffman DR, Hotez PJ, (1996) Cloning and characterization of Ancylostoma-secreted protein. J Biol Chem 271: 6672-6678.
68. Bower MA, Constant SL, Mendez S, (2008) Necator americanus: The Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro. Exp Parasitol 118: 569-575.
69. Tawe W, Pearlman E, Unnasch TR, Lustigman S, (2000) Angiogenic activity of Onchocerca volvulus recombinant proteins similar to vespid venom antigen 5. Mol Biochem Parasitol 109: 91-99.
70. Pancholi V, (2001) Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci 58: 902-920.
71. Sirover MA, (1999) New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochimica et Biophysica Acta (BBA)- Protein Structure and Molecular Enzymology 1432: 159-184.
72. Pereira LA, Báo SN, Barbosa MS, Da Silva JLM, Felipe MSS, et al. (2007) Analysis of the Paracoccidioides brasiliensis triosephosphate isomerase suggests the potential for adhesin function. FEMS Yeast Res 7: 1381-1388.
73. Veiga-Malta I, Duarte M, Dinis M, Tavares D, Videira A, et al. (2004) Enolase from Streptococcus sobrinus is an immunosuppressive protein. Cell Microbiol 6: 79-88.
74. Vermeire JJ, Cho Y, Lolis E, Bucala R, Cappello M, (2008) Orthologs of macrophage migration inhibitory factor from parasitic nematodes. Trends Parasitol 24: 355-363.
75. Prieto-Lafuente L, Gregory WF, Allen JE, Maizels RM, (2009) MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages. J Leukoc Biol 85: 844-854.
76. Dainichi T, Maekawa Y, Ishii K, Zhang T, Nashed BF, et al. (2001) Nippocystatin, a cysteine protease inhibitor from Nippostrongylus brasiliensis, inhibits antigen processing and modulates antigen-specific immune response. Infect Immun 69: 7380-7386.
77. Manoury B, Gregory WF, Maizels RM, Watts C, (2001) Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol 11: 447-451.
78. Schönemeyer A, Lucius R, Sonnenburg B, Brattig N, Sabat R, et al. (2001) Modulation of human T cell responses and macrophage functions by onchocystatin, a secreted protein of the filarial nematode Onchocerca volvulus. J Immunol 167: 3207-3215.
79. Harcus Y, Nicoll G, Murray J, Filbey K, Gomez-Escobar N, et al. (2009) C-type lectins from the nematode parasites Heligmosomoides polygyrus and Nippostrongylus brasiliensis. Parasitol Int 58: 461-470.
80. Garin MI, Chu C-C, Golshayan D, Cernuda-Morollon E, Wait R, et al. (2007) Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells. Blood 109: 2058-2065.
81. Toscano MA, Commodaro AG, Ilarregui JM, Bianco GA, Liberman A, et al. (2006) Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J Immunol 176: 6323-6332.
82. Ilarregui JM, Croci DO, Bianco GA, Toscano MA, Salatino M, et al. (2009) Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol 10: 981-991.
83. Loukas A, Maizels RM, (2000) Helminth C-type lectins and host-parasite interactions. Parasitology Today 16: 333-339.
84. Turner DG, Wildblood LA, Inglis NF, Jones DG, (2008) Characterization of a galectin-like activity from the parasitic nematode, Haemonchus contortus, which modulates ovine eosinophil migration in vitro. Vet Immunol Immunopathol 122: 138-145.
85. Henkle-Dührsen K, Kampkötter A, (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114: 129-142.
86. Selkirk ME, Smith VP, Thomas GR, Gounaris K, (1998) Resistance of filarial nematode parasites to oxidative stress. Int J Parasitol 28: 1315-1332.
87. Robinson MW, Hutchinson AT, Dalton JP, Donnelly S, (2010) Peroxiredoxin: a central player in immune modulation. Parasite Immunol 32: 305-313.
88. Perally Sr, LaCourse EJ, Campbell AM, Brophy PM, (2008) Heme transport and detoxification in nematodes: Subproteomics evidence of differential role of glutathione transferases. J Proteome Res 7: 4557-4565.
89. Zhan B, Liu S, Perally S, Xue J, Fujiwara R, et al. (2005) Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect Immun 73: 6903-6911.