Comparative analysis of the secretome from a model filarial nematode (Litomosoides sigmodontis) reveals maximal diversity in gravid female parasites

Molecular and Cellular Proteomics

Volumn 13, Issue 10, 2014, Pages 2527-2544

  Armstrong, Stuart D ^a   Babayan, Simon A ^b,d   Lhermitte Vallarino, Nathaly ^c   Gray, Nick ^b   Xia, Dong ^a   Martin, Coralie ^c   Kumar, Sujai ^b,e   Taylor, David W ^b   Blaxter, Mark L ^b   Wastling, Jonathan M ^a   Makepeace, Benjamin L ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANT LARVAL TRANSCRIPT PROTEIN 1; ACTIVATION ASSOCIATED SECRETED PROTEIN 1; CALMODULIN; CATHEPSIN L LIKE PRECURSOR; EPICUTICLIN; GLUTAREDOXIN; GLUTATHIONE REDUCTASE; MSP DOMAIN CONTAINING PROTEIN; NEMATODE CUTICLE COLLAGEN N TERMINAL DOMAIN CONTAINING PROTEIN; NUCLEOREDOXIN LIKE PROTEIN 2; PROTEIN; SECRETORY PROTEIN; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; UNCLASSIFIED DRUG; VITELLOGENIN; HELMINTH PROTEIN;

ADULT; AMINO ACID SEQUENCE; ARTICLE; BIOTINYLATION; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; INTERMEDIATE FILAMENT; LITOMOSOIDES SIGMODONTIS; MERIONES UNGUICULATUS; MICROBIAL DIVERSITY; MICROFILARIA (NEMATODE LARVA); MUS MUSCULUS; NEMATODE LIFE CYCLE STAGE; NONHUMAN; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEOMICS; SIGNAL TRANSDUCTION; WOLBACHIA; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CLASSIFICATION; COMPARATIVE STUDY; DISEASE MODEL; FILARIASIS; FILARIOIDEA; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOUSE; PARASITOLOGY; PROCEDURES; SEX DIFFERENCE;

LITOMOSOIDES SIGMODONTIS;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FILARIASIS; FILARIOIDEA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; HELMINTH PROTEINS; MALE; MICE; MICE, INBRED BALB C; PROTEOMICS; SEX FACTORS;

EID: 84907958775     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.038539     Document Type: Article

References (114)

1. Mathers, C. D., Ezzati, M., and Lopez, A. D. (2007) Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl. Trop. Dis. 1, e114
2. Gardon, J., Gardon-Wendel, N., Demanga, N., Kamgno, J., Chippaux, J. P., and Boussinesq, M. (1997) Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350, 18-22
3. McCall, J. W., Genchi, C., Kramer, L. H., Guerrero, J., and Venco, L. (2008) Heartworm disease in animals and humans. Adv. Parasitol. 66, 193-285
4. Wahl, G., Achu-Kwi, M. D., Mbah, D., Dawa, O., and Renz, A. (1994) Bovine onchocercosis in north Cameroon. Vet. Parasitol. 52, 297-311
5. Osei-Atweneboana, M. Y., Eng, J. K., Boakye, D. A., Gyapong, J. O., and Prichard, R. K. (2007) Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 369, 2021-2029
6. Bourguinat, C., Keller, K., Bhan, A., Peregrine, A., Geary, T., and Prichard, R. (2011) Macrocyclic lactone resistance in Dirofilaria immitis. Vet. Parasitol. 181, 388-392
7. Morris, C. P., Evans, H., Larsen, S. E., and Mitre, E. (2013) A comprehensive, model-based review of vaccine and repeat infection trials for filariasis. Clin. Microbiol. Rev. 26, 381-421
8. Tamarozzi, F., Halliday, A., Gentil, K., Hoerauf, A., Pearlman, E., and Taylor, M. J. (2011) Onchocerciasis: the role of Wolbachia bacterial endosymbionts in parasite biology, disease pathogenesis, and treatment. Clin. Microbiol. Rev. 24, 459-468
9. Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L., and Scott, A. L. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756-1760
10. Godel, C., Kumar, S., Koutsovoulos, G., Ludin, P., Nilsson, D., Comandatore, F., Wrobel, N., Thompson, M., Schmid, C. D., Goto, S., Bringaud, F., Wolstenholme, A., Bandi, C., Epe, C., Kaminsky, R., Blaxter, M., and Maser, P. (2012) The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB J. 26, 4650-4661
11. Desjardins, C. A., Cerqueira, G. C., Goldberg, J. M., Dunning Hotopp, J. C., Haas, B. J., Zucker, J., Ribeiro, J. M., Saif, S., Levin, J. Z., Fan, L., Zeng, Q., Russ, C., Wortman, J. R., Fink, D. L., Birren, B. W., and Nutman, T. B. (2013) Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nat. Genet. 45, 495-500
12. Foster, J., Ganatra, M., Kamal, I., Ware, J., Makarova, K., Ivanova, N., Bhattacharyya, A., Kapatral, V., Kumar, S., Posfai, J., Vincze, T., Ingram, J., Moran, L., Lapidus, A., Omelchenko, M., Kyrpides, N., Ghedin, E., Wang, S., Goltsman, E., Joukov, V., Ostrovskaya, O., Tsukerman, K., Mazur, M., Comb, D., Koonin, E., and Slatko, B. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3, e121
13. Darby, A. C., Armstrong, S. D., Bah, G. S., Kaur, G., Hughes, M. A., Kay, S. M., Koldkjaer, P., Rainbow, L., Radford, A. D., Blaxter, M. L., Tanya, V. N., Trees, A. J., Cordaux, R., Wastling, J. M., and Makepeace, B. L. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res. 22, 2467-2477
14. Hewitson, J. P., Harcus, Y. M., Curwen, R. S., Dowle, A. A., Atmadja, A. K., Ashton, P. D., Wilson, A., and Maizels, R. M. (2008) The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Mol. Biochem. Parasitol. 160, 8-21
15. Bennuru, S., Meng, Z., Ribeiro, J. M., Semnani, R. T., Ghedin, E., Chan, K., Lucas, D. A., Veenstra, T. D., and Nutman, T. B. (2011) Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proc. Natl. Acad. Sci. U. S. A. 108, 9649-9654
16. Moreno, Y., and Geary, T. G. (2008) Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Negl. Trop. Dis. 2, e326
17. Bennuru, S., Semnani, R., Meng, Z., Ribeiro, J. M., Veenstra, T. D., and Nutman, T. B. (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl. Trop. Dis. 3, e410
18. Petit, G., Diagne, M., Marechal, P., Owen, D., Taylor, D., and Bain, O. (1992) Maturation of the filaria Litomosoides sigmodontis in BALB/c mice; comparative susceptibility of nine other inbred strains. Ann. Parasitol. Hum. Comp. 67, 144-150
19. Bain, O., Petit, G., and Diagne, M. (1989) [Litomosoides, parasites of rodents; taxonomic consequences]. Ann. Parasitol. Hum. Comp. 64, 268-289
20. Hoffmann, W., Petit, G., Schulz-Key, H., Taylor, D., Bain, O., and LeGoff, L. (2000) Litomosoides sigmodontis in mice: reappraisal of an old model for filarial research. Parasitol. Today 16, 387-389
21. Pfaff, A. W., Schulz-Key, H., Soboslay, P. T., Taylor, D. W., MacLennan, K., and Hoffmann, W. H. (2002) Litomosoides sigmodontis cystatin acts as an immunomodulator during experimental filariasis. Int. J. Parasitol. 32, 171-178
22. Taylor, M. D., LeGoff, L., Harris, A., Malone, E., Allen, J. E., and Maizels, R. M. (2005) Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174, 4924-4933
23. Hubner, M. P., Shi, Y., Torrero, M. N., Mueller, E., Larson, D., Soloviova, K., Gondorf, F., Hoerauf, A., Killoran, K. E., Stocker, J. T., Davies, S. J., Tarbell, K. V., and Mitre, E. (2012) Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-beta. J. Immunol. 188, 559-568
24. LeGoff, L., Martin, C., Oswald, I. P., Vuong, P. N., Petit, G., Ungeheuer, M. N., and Bain, O. (2000) Parasitology and immunology of mice vaccinated with irradiated Litomosoides sigmodontis larvae. Parasitology 120, 271-280
25. Babayan, S. A., Luo, H., Gray, N., Taylor, D. W., and Allen, J. E. (2012) Deletion of parasite immune modulatory sequences combined with immune activating signals enhances vaccine mediated protection against filarial nematodes. PLoS Negl. Trop. Dis. 6, e1968
26. Comandatore, F., Sassera, D., Montagna, M., Kumar, S., Koutsovoulos, G., Thomas, G., Repton, C., Babayan, S. A., Gray, N., Cordaux, R., Darby, A., Makepeace, B., and Blaxter, M. (2013) Phylogenomics and analysis of shared genes suggest a single transition to mutualism in Wolbachia of nematodes. Genome Biol. Evol. 5, 1668-1674
27. Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
28. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069
29. R Development Core Team. (2013) R: A Language and Environment for Statistical Computing, The R Foundation for Statistical Computing, Vienna, Austria
30. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate - A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300
31. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
32. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., and Lopez, R. (2005) InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116-W120
33. Martin, B., Chadwick, W., Yi, T., Park, S. S., Lu, D., Ni, B., Gadkaree, S., Farhang, K., Becker, K. G., and Maudsley, S. (2012) VENNTURE-a novel Venn diagram investigational tool for multiple pharmacological dataset analysis. PLoS One 7, e36911
34. Petersen, T. N., Brunak, S., von, H. G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
35. Bendtsen, J. D., Jensen, L. J., Blom, N., von, H. G., and Brunak, S. (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 17, 349-356
36. Claros, M. G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786
37. Steentoft, C., Vakhrushev, S. Y., Joshi, H. J., Kong, Y., Vester-Christensen, M. B., Schjoldager, K. T., Lavrsen, K., Dabelsteen, S., Pedersen, N. B., Marcos-Silva, L., Gupta, R., Bennett, E. P., Mandel, U., Brunak, S., Wandall, H. H., Levery, S. B., and Clausen, H. (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 32, 1478-1488
38. Duckert, P., Brunak, S., and Blom, N. (2004) Prediction of proprotein convertase cleavage sites. Protein Eng. Des. Sel. 17, 107-112
39. Jex, A. R., Liu, S., Li, B., Young, N. D., Hall, R. S., Li, Y., Yang, L., Zeng, N., Xu, X., Xiong, Z., Chen, F., Wu, X., Zhang, G., Fang, X., Kang, Y., Anderson, G. A., Harris, T. W., Campbell, B. E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E. M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P. W., Yang, H., Wang, J., Wang, J., and Gasser, R. B. (2011) Ascaris suum draft genome. Nature 479, 529-533
40. Sievers, F., and Higgins, D. G. (2014) Clustal Omega, accurate alignment of very large numbers of sequences. Methods Mol. Biol. 1079, 105-116
41. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542
42. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190
43. Lustigman, S., Brotman, B., Huima, T., Prince, A. M., and McKerrow, J. H. (1992) Molecular cloning and characterization of onchocystatin, a cysteine proteinase inhibitor of Onchocerca volvulus. J. Biol. Chem. 267, 17339-17346
44. Liebau, E., Hoppner, J., Muhlmeister, M., Burmeister, C., Luersen, K., Perbandt, M., Schmetz, C., Buttner, D., and Brattig, N. (2008) The secretory omega-class glutathione transferase OvGST3 from the human pathogenic parasite Onchocerca volvulus. FEBS J. 275, 3438-3453
45. Scott, A. L., Dinman, J., Sussman, D. J., and Ward, S. (1989) Major sperm protein and actin genes in free-living and parasitic nematodes. Parasitology 98, 471-478
46. Zahner, H., Hobom, G., and Stirm, S. (1995) The microfilarial sheath and its proteins. Parasitol. Today 11, 116-120
47. Willenbucher, J., Hofle, W., and Lucius, R. (1993) The filarial antigens Av33/Ov33-3 show striking similarities to the major pepsin inhibitor from Ascaris suum. Mol. Biochem. Parasitol. 57, 349-351
48. Harnett, W., Houston, K. M., Tate, R., Garate, T., Apfel, H., Adam, R., Haslam, S. M., Panico, M., Paxton, T., Dell, A., Morris, H., and Brzeski, H. (1999) Molecular cloning and demonstration of an aminopeptidase activity in a filarial nematode glycoprotein. Mol. Biochem. Parasitol. 104, 11-23
49. Ao, J. Q., Ling, E., Rao, X. J., and Yu, X. Q. (2008) A novel ML protein from Manduca sexta may function as a key accessory protein for lipopolysaccharide signaling. Mol. Immunol. 45, 2772-2781
50. Storch, J., and Xu, Z. (2009) Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim. Biophys. Acta 1791, 671-678
51. Erttmann, K. D., and Gallin, M. Y. (1996) Onchocerca volvulus: identification of cDNAs encoding a putative phosphatidyl-ethanolamine-binding protein and a putative partially processed mRNA precursor. Gene 174, 203-207
52. Gallin, M. Y., Tan, M., Kron, M. A., Rechnitzer, D., Greene, B. M., Newland, H. S., White, A. T., Taylor, H. R., and Unnasch, T. R. (1989) Onchocerca volvulus recombinant antigen: physical characterization and clinical correlates with serum reactivity. J. Infect. Dis. 160, 521-529
53. Dissanayake, S., Xu, M., and Piessens, W. F. (1992) A cloned antigen for serological diagnosis of Wuchereria bancrofti microfilaremia with daytime blood samples. Mol. Biochem. Parasitol. 56, 269-277
54. Hunter, S. J., Thompson, F. J., Tetley, L., and Devaney, E. (2001) Temperature is a cue for gene expression in the post-infective L3 of the parasitic nematode Brugia pahangi. Mol. Biochem. Parasitol. 112, 1-9
55. Gare, D., Boyd, J., and Connolly, B. (2004) Developmental regulation and secretion of nematode-specific cysteine-glycine domain proteins in Trichinella spiralis. Mol. Biochem. Parasitol. 134, 257-266
56. Makinen, P. L., and Makinen, K. K. (1981) Purification and properties of rat skin acid phosphatases. Int. J. Pept. Protein Res. 18, 352-369
57. Fukushige, T., Goszczynski, B., Yan, J., and McGhee, J. D. (2005) Transcriptional control and patterning of the pho-1 gene, an essential acid phosphatase expressed in the C. elegans intestine. Dev. Biol. 279, 446-461
58. Grant, R. P., Buttery, S. M., Ekman, G. C., Roberts, T. M., and Stewart, M. (2005) Structure of MFP2 and its function in enhancing MSP polymerization in Ascaris sperm amoeboid motility. J. Mol. Biol. 347, 583-595
59. Ou, X., Tang, L., McCrossan, M., Henkle-Dührsen, K., and Selkirk, M. E. (1995) Brugia malayi: localisation and differential expression of extracellular and cytoplasmic CuZn superoxide dismutases in adults and microfilariae. Exp. Parasitol. 80, 515-529
60. Ford, L., Guiliano, D. B., Oksov, Y., Debnath, A. K., Liu, J., Williams, S. A., Blaxter, M. L., and Lustigman, S. (2005) Characterization of a novel filarial serine protease inhibitor, Ov-SPI-1, from Onchocerca volvulus, with potential multifunctional roles during development of the parasite. J. Biol. Chem. 280, 40845-40856
61. Frank, G. R., Wisnewski, N., Brandt, K. S., Carter, C. R., Jennings, N. S., and Selkirk, M. E. (1999) Molecular cloning of the 22-24 kDa excretory-secretory 22U protein of Dirofilaria immitis and other filarial nematode parasites. Mol. Biochem. Parasitol. 98, 297-302
62. Gnanasekar, M., Padmavathi, B., and Ramaswamy, K. (2005) Cloning and characterization of a novel immunogenic protein 3 (NIP3) from Brugia malayi by immuno screening of a phage-display cDNA expression library. Parasitol. Res. 97, 49-58
63. Chu, D. S., Liu, H., Nix, P., Wu, T. F., Ralston, E. J., Yates, J. R., 3rd, and Meyer, B. J. (2006) Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 443, 101-105
64. Blaxter, M. (1998) Caenorhabditis elegans is a nematode. Science 282, 2041-2046
65. Beeton, C., Pennington, M. W., and Norton, R. S. (2011) Analogs of the sea anemone potassium channel blocker ShK for the treatment of autoimmune diseases. Inflamm. Allergy Drug Targets. 10, 313-321
66. Loukas, A., Hintz, M., Linder, D., Mullin, N. P., Parkinson, J., Tetteh, K. K., and Maizels, R. M. (2000) A family of secreted mucins from the parasitic nematode Toxocara canis bears diverse mucin domains but shares similar flanking six-cysteine repeat motifs. J. Biol. Chem. 275, 39600-39607
67. Yamaguchi, Y., Hasegawa, Y., Honma, T., Nagashima, Y., and Shiomi, K. (2010) Screening and cDNA cloning of Kv1 potassium channel toxins in sea anemones. Mar. Drugs 8, 2893-2905
68. Blaxter, M. L., and Robertson, W. M. (1998) The cuticle, In: Perry, R. N., and Wright, D. J. (eds), The physiology and biochemistry of free-living and plant-parasitic nematodes, pp. 25-48, CABI Publishing, Wallingford, Oxon
69. Yegutkin, G. G. (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783, 673-694
70. Peerschke, E. I., and Ghebrehiwet, B. (2007) The contribution of gC1qR/p33 in infection and inflammation. Immunobiology 212, 333-342
71. Irvine, M., Huima, T., Prince, A. M., and Lustigman, S. (1994) Identification and characterization of an Onchocerca volvulus cDNA clone encoding a highly immunogenic calponin-like protein. Mol. Biochem. Parasitol. 65, 135-146
72. Wilson, W. R., Tuan, R. S., Shepley, K. J., Freedman, D. O., Greene, B. M., Awadzi, K., and Unnasch, T. R. (1994) The Onchocerca volvulus homologue of the multifunctional polypeptide protein disulfide isomerase. Mol. Biochem. Parasitol. 68, 103-117
73. Mancuso, V. P., Parry, J. M., Storer, L., Poggioli, C., Nguyen, K. C., Hall, D. H., and Sundaram, M. V. (2012) Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans. Development 139, 979-990
74. Lu, W., Egerton, G. L., Bianco, A. E., and Williams, S. A. (1998) Thioredoxin peroxidase from Onchocerca volvulus: a major hydrogen peroxide detoxifying enzyme in filarial parasites. Mol. Biochem. Parasitol. 91, 221-235
75. Geary, J., Satti, M., Moreno, Y., Madrill, N., Whitten, D., Headley, S. A., Agnew, D., Geary, T., and Mackenzie, C. (2012) First analysis of the secretome of the canine heartworm, Dirofilaria immitis. Parasit. Vectors 5, 140
76. Babayan, S. A., Allen, J. E., and Taylor, D. W. (2012) Future prospects and challenges of vaccines against filariasis. Parasite Immunol. 34, 243-253
77. Sepsenwol, S., and Taft, S. J. (1990) In vitro induction of crawling in the amoeboid sperm of the nematode parasite, Ascaris suum. Cell Motil. Cytoskeleton 15, 99-110
78. Morgan, K. L., Estevez, A. O., Mueller, C. L., Cacho-Valadez, B., Miranda-Vizuete, A., Szewczyk, N. J., and Estevez, M. (2010) The glutaredoxin GLRX-21 functions to prevent selenium-induced oxidative stress in Caenorhabditis elegans. Toxicol. Sci. 118, 530-543
79. Hawkes, W. C., and Turek, P. J. (2001) Effects of dietary selenium on sperm motility in healthy men. J. Androl. 22, 764-772
80. Zhao, Y., Sun, W., Zhang, P., Chi, H., Zhang, M. J., Song, C. Q., Ma, X., Shang, Y., Wang, B., Hu, Y., Hao, Z., Huhmer, A. F., Meng, F., L'hernault, S. W., He, S. M., Dong, M. Q., and Miao, L. (2012) Nematode sperm maturation triggered by protease involves sperm-secreted serine protease inhibitor (Serpin). Proc. Natl. Acad. Sci. U. S. A. 109, 1542-1547
81. Johnson, M. H., Orihel, T. C., and Beaver, P. C. (1974) Dipetalonema viteae in the experimentally infected jird, Meriones unguiculatus. I. Insemination, development from egg to microfilaria, reinsemination, and longevity of mated and unmated worms. J. Parasitol. 60, 302-309
82. Funato, Y., and Miki, H. (2007) Nucleoredoxin, a novel thioredoxin family member involved in cell growth and differentiation. Antioxid. Redox. Signal. 9, 1035-1057
83. Kunchithapautham, K., Padmavathi, B., Narayanan, R. B., Kaliraj, P., and Scott, A. L. (2003) Thioredoxin from Brugia malayi: defining a 16-kilodalton class of thioredoxins from nematodes. Infect. Immun. 71, 4119-4126
84. Gems, D., and Riddle, D. L. (1996) Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature 379, 723-725
85. Kumari, S., Lillibridge, C. D., Bakeer, M., Lowrie, R. C., Jr., Jayaraman, K., and Philipp, M. T. (1994) Brugia malayi: the diagnostic potential of recombinant excretory/secretory antigens. Exp. Parasitol. 79, 489-505
86. Bi, M., Hickox, J. R., Winfrey, V. P., Olson, G. E., and Hardy, D. M. (2003) Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem. J. 375, 477-488
87. Heiman, M. G., and Shaham, S. (2009) DEX-1 and DYF-7 establish sensory dendrite length by anchoring dendritic tips during cell migration. Cell 137, 344-355
88. Matyash, V., Geier, C., Henske, A., Mukherjee, S., Hirsh, D., Thiele, C., Grant, B., Maxfield, F. R., and Kurzchalia, T. V. (2001) Distribution and transport of cholesterol in Caenorhabditis elegans. Mol. Biol. Cell 12, 1725-1736
89. Moreno, Y., Gros, P. P., Tam, M., Segura, M., Valanparambil, R., Geary, T. G., and Stevenson, M. M. (2011) Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with next-generation sequencing transcriptomic information. PLoS Negl. Trop. Dis. 5, e1370
90. Nagaraj, S. H., Gasser, R. B., and Ranganathan, S. (2008) Needles in the EST haystack: large-scale identification and analysis of excretory-secretory (ES) proteins in parasitic nematodes using expressed sequence tags (ESTs). PLoS Negl. Trop. Dis. 2, e301
91. Kang, Y., Zhao, D., Liang, H., Liu, B., Zhang, Y., Liu, Q., Wang, X., and Liu, Y. (2012) Structural study of TTR-52 reveals the mechanism by which a bridging molecule mediates apoptotic cell engulfment. Genes Dev. 26, 1339-1350
92. Jacob, J., Vanholme, B., Haegeman, A., and Gheysen, G. (2007) Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 402, 9-19
93. Saverwyns, H., Visser, A., Van, Durme, J., Power, D., Morgado, I., Kennedy, M. W., Knox, D. P., Schymkowitz, J., Rousseau, F., Gevaert, K., Vercruysse, J., Claerebout, E., and Geldhof, P. (2008) Analysis of the transthyretin-like (TTL) gene family in Ostertagia ostertagi-comparison with other strongylid nematodes and Caenorhabditis elegans. Int. J. Parasitol. 38, 1545-1556
94. Landmann, F., Foster, J. M., Slatko, B. E., and Sullivan, W. (2012) Efficient in vitro RNA interference and immunofluorescence-based phenotype analysis in a human parasitic nematode, Brugia malayi. Parasit. Vectors 5, 16
95. Wergin, W. P., and Endo, B. Y. (1976) Ultrastructure of a neurosensory organ in a root-knot nematode. J. Ultrastruct. Res. 56, 258-276
96. Madathiparambil, M. G., Kaleysa, K. N., and Raghavan, K. (2009) A diagnostically useful 200-kDa protein is secreted through the surface pores of the filarial parasite Setaria digitata. Parasitol. Res. 105, 1099-1104
97. Kolotuev, I., Apaydin, A., and Labouesse, M. (2009) Secretion of Hedgehog-related peptides and WNT during Caenorhabditis elegans development. Traffic. 10, 803-810
98. Prusse, A., Vollmer, S., and Diesfeld, H. J. (1983) Immunocytochemical and ultrastructural studies on Dipetalonema viteae (Filarioidea). J. Helminthol. 57, 127-142
99. Kozek, W. J. (2005) What is new in the Wolbachia/Dirofilaria interaction? Vet. Parasitol. 133, 127-132
100. Brattig, N. W., Bazzocchi, C., Kirschning, C. J., Reiling, N., Büttner, D. W., Ceciliani, F., Geisinger, F., Hochrein, H., Ernst, M., Wagner, H., Bandi, C., and Hoerauf, A. (2004) The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J. Immunol. 173, 437-445
101. Landmann, F., Foster, J. M., Slatko, B., and Sullivan, W. (2010) Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl. Trop. Dis. 4, e758
102. Melnikow, E., Xu, S., Liu, J., Li, L., Oksov, Y., Ghedin, E., Unnasch, T. R., and Lustigman, S. (2011) Interaction of a Wolbachia WSP-like protein with a nuclear-encoded protein of Brugia malayi. Int. J. Parasitol. 41, 1053-1061
103. Henderson, B., and Martin, A. (2011) Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect. Immun. 79, 3476-3491
104. Hansen, R. D., Trees, A. J., Bah, G. S., Hetzel, U., Martin, C., Bain, O., Tanya, V. N., and Makepeace, B. L. (2011) A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi. Proc. R. Soc. B 278, 2293-2302
105. Argueta, J. G., Shiota, S., Yamaguchi, N., Masuhiro, Y., and Hanazawa, S. (2006) Induction of Porphyromonas gingivalis GroEL signaling via binding to Toll-like receptors 2 and 4. Oral Microbiol. Immunol. 21, 245-251
106. Suba, N., Shiny, C., Taylor, M. J., and Narayanan, R. B. (2007) Brugia malayi Wolbachia HSP60 IgG antibody and isotype reactivity in different clinical groups infected or exposed to human bancroftian lymphatic filariasis. Exp. Parasitol. 116, 291-295
107. Storey, D. M., and Al-Mukhtar, A. S. (1982) Vaccination of Jirds, Meriones unguiculatus, against Litomosoides carinii and Brugia pahangi using irradiate larvae of L. carinii. Tropenmed. Parasitol. 33, 23-24
108. Babayan, S. A., Attout, T., Harris, A., Taylor, M. D., Le, Goff, L., Vuong, P. N., Renia, L., Allen, J. E., and Bain, O. (2006) Vaccination against filarial nematodes with irradiated larvae provides long-term protection against the third larval stage but not against subsequent life cycle stages. Int. J. Parasitol. 36, 903-914
109. Allen, J. E., Daub, J., Guiliano, D., McDonnell, A., Lizotte-Waniewski, M., Taylor, D. W., and Blaxter, M. (2000) Analysis of genes expressed at the infective larval stage validates utility of Litomosoides sigmodontis as a murine model for filarial vaccine development. Infect. Immun. 68, 5454-5458
110. Makepeace, B. L., Jensen, S. A., Laney, S. J., Nfon, C. K., Njongmeta, L. M., Tanya, V. N., Williams, S. A., Bianco, A. E., and Trees, A. J. (2009) Immunisation with a multivalent, subunit vaccine reduces patent infection in a natural bovine model of onchocerciasis during intense field exposure. PLoS Negl. Trop. Dis. 3, e544
111. Ziewer, S., Hubner, M. P., Dubben, B., Hoffmann, W. H., Bain, O., Martin, C., Hoerauf, A., and Specht, S. (2012) Immunization with L. sigmodontis microfilariae reduces peripheral microfilaraemia after challenge infection by inhibition of filarial embryogenesis. PLoS Negl. Trop. Dis. 6, e1558
112. Townson, S., and Bianco, A. E. (1982) Immunization of calves against the microfilariae of Onchocerca lienalis. J. Helminthol. 56, 297-303
113. Hoffmann, W. H., Pfaff, A. W., Schulz-Key, H., Soboslay, P. T., and Soboslav, P. T. (2001) Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 122, 641-649
114. Hashmi, S., Zhang, J., Oksov, Y., Ji, Q., and Lustigman, S. (2006) The Caenorhabditis elegans CPI-2a cystatin-like inhibitor has an essential regulatory role during oogenesis and fertilization. J. Biol. Chem. 281, 28415-28429