Hookworms are intestinal parasitic nematodes that chronically infect ~500 million people, with reinfection common even after clearance by drugs. How infecting hookworms successfully overcome host protective mechanisms is unclear, but it may involve hookworm proteins that digest host tissues, or counteract the host's immune system, or both. To find such proteins in the zoonotic hookworm Ancylostoma ceylanicum, we identified hookworm genes encoding excreted-secreted (ES) proteins, hookworm genes preferentially expressed in the hookworm intestine, and hookworm genes whose transcription is stimulated by the host immune system. We collected ES proteins from adult hookworms harvested from hamsters; mass spectrometry identified 565 A. ceylanicum genes encoding ES proteins. We also used RNA-seq to identify A. ceylanicum genes expressed both in young adults (12 days post-infection) and in intestinal and non-intestinal tissues dissected from mature adults (19 days post-infection), with hamster hosts that either had normal immune systems or were immunosuppressed by dexamethasone. In adult A. ceylanicum, we observed 1,670 and 1,196 genes with intestine- and non-intestine-biased expression, respectively. Comparing hookworm gene activity in normal versus immunosuppressed hosts, we observed almost no changes of gene activity in 12-day young adults or non-intestinal 19-day adult tissues. However, in intestinal 19-day adult tissues, we observed 1,951 positively immunoregulated genes (upregulated at least two-fold in normal hosts versus immunosuppressed hosts), and 137 genes that were negatively immunoregulated. Thus, immunoregulation was observed primarily in mature adult hookworm intestine directly exposed to host blood; it may include hookworm genes activated in response to the host immune system in order to neutralize the host immune system. We observed 153 ES genes showing positive immunoregulation in 19-day adult intestine; of these genes, 69 had ES gene homologs in the closely related hookworm Ancylostoma caninum, 24 in the human hookworm Necator americanus, and 24 in the more distantly related strongylid parasite Haemonchus contortus. Such a mixture of rapidly evolving and conserved genes could comprise virulence factors enabling infection, provide new targets for drugs or vaccines against hookworm, and aid in developing therapies for autoimmune diseases.

Current address Cellular and Molecular Biology Graduate Program University of Wisconsin 413 Bock Labs 1525 Linden Drive Madison WI 53706 USA

Current address Leveragen Inc 17 Briden Street Worcester MA 01605 USA

Department of Biochemistry University of Wisconsin Madison Madison WI 53706 USA

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 267 2 611 37 Brno Czech Republic

Department of Molecular Biology and Genetics Cornell University Ithaca NY 14853 USA

Division of Biology and Biological Engineering California Institute of Technology Pasadena CA 91125 USA

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

ioGenetics LLC 301 South Bedford Street Ste 1 Madison WI 53703 USA

Program in Molecular Medicine University of Massachusetts Chan Medical School Worcester MA 01605 USA

Zobrazit více v PubMed

Abuzeid A. M. I., Zhou X., Huang Y. and Li G., 2020. Twenty-five-year research progress in hookworm excretory/secretory products. Parasites & vectors 13: 136. PubMed PMC

Anderson R. C., 1984. The origins of zooparasitic nematodes. Canadian Journal of Zoology 62: 317–328.

Anisimov A. P., and Tokmakova N. P., 1974. Proliferation and growth of intestinal epithelium in Ascaris suum (Nematoda) during postnatal ontogeny. I. Mitotic activity in the intestinal epithelium. Sov J Dev Biol 4: 341–348. PubMed

Anisimov A. P., and Usheva L. N., 1974. Proliferation and growth of intestinal epithelium in Ascaris suum (Nematoda) during postnatal ontogeny. II. Increase in the number and size of cells as a growth factor. Sov J Dev Biol 4: 379–383. PubMed

Ashburner M., Ball C. A., Blake J. A., Botstein D., Butler H. et al., 2000. Gene ontology: tool for the unification of biology. Nature Genetics 25: 25–29. PubMed PMC

Bailey T. L., Boden M., Buske F. A., Frith M., Grant C. E. et al., 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37: W202–208. PubMed PMC

Balmer E. A., and Faso C., 2021. The road less traveled? Unconventional protein secretion at parasite-host interfaces. Front Cell Dev Biol 9: 662711. PubMed PMC

Bansemir A. D., and Sukhdeo M. V., 1994. The food resource of adult Heligmosomoides polygyrus in the small intestine. The Journal of parasitology 80: 24–28. PubMed

Bansemir A. D., and Sukhdeo M. V., 2001. Intestinal distribution of worms and host ingesta in Nippostrongylus brasiliensis. J Parasitol 87: 1470–1472. PubMed

Banyai L., and Patthy L., 1998. Amoebapore homologs of Caenorhabditis elegans. Biochim Biophys Acta 1429: 259–264. PubMed

Barnett D. W., Garrison E. K., Quinlan A. R., Stromberg M. P. and Marth G. T., 2011. BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27: 1691–1692. PubMed PMC

Beaver P. C., 1988. Light, long-lasting Necator infection in a volunteer. The American journal of tropical medicine and hygiene 39: 369–372. PubMed

Behnke J., and Harris P. D., 2010. Heligmosomoides bakeri: a new name for an old worm? Trends Parasitol 26: 524–529. PubMed

Bell A. D., Chou H. T., Valencia F. and Paaby A. B., 2023. Beyond the reference: gene expression variation and transcriptional response to RNA interference in Caenorhabditis elegans. G3 (Bethesda) 13. PubMed PMC

Berkachy R., Smyth D. J., Schnoeller C., Harcus Y., Maizels R. M. et al., 2021. Characterisation of the secreted apyrase family of Heligmosomoides polygyrus. Int J Parasitol 51: 39–48. PubMed

Bernot J. P., Rudy G., Erickson P. T., Ratnappan R., Haile M. et al., 2020. Transcriptomic analysis of hookworm Ancylostoma ceylanicum life cycle stages reveals changes in G-protein coupled receptor diversity associated with the onset of parasitism. Int J Parasitol 50: 603–610. PubMed PMC

Bethony J., Brooker S., Albonico M., Geiger S. M., Loukas A. et al., 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–1532. PubMed

Bethony J., Loukas A., Smout M., Brooker S., Mendez S. et al., 2005. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB Journal 19: 1743–1745. PubMed

Bouchery T., Moyat M., Sotillo J., Silverstein S., Volpe B. et al., 2020. Hookworms evade host immunity by secreting a deoxyribonuclease to degrade neutrophil extracellular traps. Cell Host Microbe 27: 277–289 e276. PubMed

Brophy P. M., Patterson L. H. and Pritchard D. L., 1995. Secretory nematode SOD--offensive or defensive? Int J Parasitol 25: 865–866. PubMed

Brůna T., Hoff K. J., Lomsadze A., Stanke M. and Borodovsky M., 2021. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR genomics and bioinformatics 3: lqaa108. PubMed PMC

Buchfink B., Reuter K. and Drost H. G., 2021. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods 18: 366–368. PubMed PMC

Buck A. H., Coakley G., Simbari F., McSorley H. J., Quintana J. F. et al., 2014. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun 5: 5488. PubMed PMC

Caffrey C. R., Goupil L., Rebello K. M., Dalton J. P. and Smith D., 2018. Cysteine proteases as digestive enzymes in parasitic helminths. PLoS Negl Trop Dis 12: e0005840. PubMed PMC

Cantacessi C., Campbell B. E., Visser A., Geldhof P., Nolan M. J. et al., 2009. A portrait of the “SCP/TAPS” proteins of eukaryotes--developing a framework for fundamental research and biotechnological outcomes. Biotechnol Adv 27: 376–388. PubMed

Carbon S., Douglass E., Good B., Unni D., Harris N. et al., 2021. The Gene Ontology resource: enriching a GOld mine. Nucleic acids research 49: D325–D334. PubMed PMC

Chen L. Q., Cheung L. S., Feng L., Tanner W. and Frommer W. B., 2015. Transport of sugars. Annu Rev Biochem 84: 865–894. PubMed

Chen N., Yuan Z. G., Xu M. J., Zhou D. H., Zhang X. X. et al., 2012. Ascaris suum enolase is a potential vaccine candidate against ascariasis. Vaccine 30: 3478–3482. PubMed

Chen S., Zhou Y., Chen Y. and Gu J., 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34: i884–i890. PubMed PMC

Chhabra S., Chang S. C., Nguyen H. M., Huq R., Tanner M. R. et al., 2014. Kv1.3 channel-blocking immunomodulatory peptides from parasitic worms: implications for autoimmune diseases. FASEB J. PubMed PMC

Cho Y., Jones B. F., Vermeire J. J., Leng L., DiFedele L. et al., 2007. Structural and functional characterization of a secreted hookworm Macrophage Migration Inhibitory Factor (MIF) that interacts with the human MIF receptor CD74. Journal of Biological Chemistry 282: 23447–23456. PubMed PMC

Chu D., Bungiro R. D., Ibanez M., Harrison L. M., Campodonico E. et al., 2004. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infection and Immunity 72: 2214–2221. PubMed PMC

Clark W. C., 1994. Origins of the parasitic habit in the nematoda. Int J Parasitol 24: 1117–1129. PubMed

Coakley G., McCaskill J. L., Borger J. G., Simbari F., Robertson E. et al., 2017. Extracellular vesicles from a helminth parasite suppress macrophage activation and constitute an effective vaccine for protective immunity. Cell reports 19: 1545–1557. PubMed PMC

Coghlan A., Tyagi R., Cotton J. A., Holroyd N., Rosa B. A. et al., 2019. Comparative genomics of the major parasitic worms. Nature genetics 51: 163–174. PubMed PMC

Cohen J., 2016. Unfilled vials. Science 351: 16–19. PubMed

Cole R., Holroyd N., Tracey A., Berriman M. and Viney M., 2023. The parasitic nematode Strongyloides ratti exists predominantly as populations of long-lived asexual lineages. Nat Commun 14: 6427. PubMed PMC

Colella V., Bradbury R. and Traub R., 2021. Ancylostoma ceylanicum. Trends Parasitol 37: 844–845. PubMed

Costa A. F., Gasser R. B., Dias S. R. and Rabelo E. M., 2009. Male-enriched transcription of genes encoding ASPs and Kunitz-type protease inhibitors in Ancylostoma species. Molecular and Cellular Probes 23: 298–303. PubMed

Crusoe M. R., Alameldin H. F., Awad S., Boucher E., Caldwell A. et al., 2015. The khmer software package: enabling efficient nucleotide sequence analysis. F1000Research 4: 900. PubMed PMC

Dainat J., 2023. AGAT: Another Gff Analysis Toolkit to handle annotations in any GTF/GFF format, pp., Zenodo.

Danecek P., Bonfield J. K., Liddle J., Marshall J., Ohan V. et al., 2021. Twelve years of SAMtools and BCFtools. Gigascience 10. PubMed PMC

Davis P., Zarowiecki M., Arnaboldi V., Becerra A., Cain S. et al., 2022. WormBase in 2022-data, processes, and tools for analyzing Caenorhabditis elegans. Genetics 220. PubMed PMC

Degner J. F., Marioni J. C., Pai A. A., Pickrell J. K., Nkadori E. et al., 2009. Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25: 3207–3212. PubMed PMC

Del Valle A., Jones B. F., Harrison L. M., Chadderdon R. C. and Cappello M., 2003. Isolation and molecular cloning of a secreted hookworm platelet inhibitor from adult Ancylostoma caninum. Molecular and Biochemical Parasitology 129: 167–177. PubMed

Dimou E., and Nickel W., 2018. Unconventional mechanisms of eukaryotic protein secretion. Curr Biol 28: R406–R410. PubMed

Diop A., Santorelli D., Malagrino F., Nardella C., Pennacchietti V. et al., 2022. SH2 domains: folding, binding and therapeutical approaches. Int J Mol Sci 23. PubMed PMC

Doyle S. R., Tracey A., Laing R., Holroyd N., Bartley D. et al., 2020. Genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm. Communications biology 3: 656. PubMed PMC

Drew D., North R. A., Nagarathinam K. and Tanabe M., 2021. Structures and general transport mechanisms by the major facilitator superfamily (MFS). Chem Rev 121: 5289–5335. PubMed PMC

Durette-Desset M. C., Beveridge I. and Spratt D. M., 1994. The origins and evolutionary expansion of the strongylida (Nematoda). International Journal for Parasitology 24: 1139–1165. PubMed

Ebert D., and Fields P. D., 2020. Host-parasite co-evolution and its genomic signature. Nat Rev Genet 21: 754–768. PubMed

Eddy S. R., 2009. A new generation of homology search tools based on probabilistic inference. Genome Inform 23: 205–211. PubMed

Emms D. M., and Kelly S., 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome biology 20: 238. PubMed PMC

Fairfax K. C., Vermeire J. J., Harrison L. M., Bungiro R. D., Grant W. et al., 2009. Characterisation of a fatty acid and retinol binding protein orthologue from the hookworm Ancylostoma ceylanicum. International Journal for Parasitology 39: 1561–1571. PubMed PMC

Ferguson A. A., Inclan-Rico J. M., Lu D., Bobardt S. D., Hung L. et al., 2023. Hookworms dynamically respond to loss of Type 2 immune pressure. PLoS Pathog 19: e1011797. PubMed PMC

Ferguson A. A., Rossi H. L. and Herbert D. R., 2024. The secretome of adult murine hookworms is shaped by host expression of STAT6. Parasite Immunol 46: e13056. PubMed PMC

Finn R. D., Coggill P., Eberhardt R. Y., Eddy S. R., Mistry J. et al., 2016. The Pfam protein families database: towards a more sustainable future. Nucleic acids research 44: D279–285. PubMed PMC

Fujiwara R. T., Zhan B., Mendez S., Loukas A., Bueno L. L. et al., 2007. Reduction of worm fecundity and canine host blood loss mediates protection against hookworm infection elicited by vaccination with recombinant Ac-16. Clin Vaccine Immunol 14: 281–287. PubMed PMC

Garside P., and Behnke J. M., 1989. Ancylostoma ceylanicum in the hamster: observations on the host-parasite relationship during primary infection. Parasitology 98 Pt 2: 283–289. PubMed

Gems D., 2000. Longevity and ageing in parasitic and free-living nematodes. Biogerontology 1: 289–307. PubMed

Gibbs G. M., Roelants K. and O’Bryan M. K., 2008. The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins--roles in reproduction, cancer, and immune defense. Endocrine Reviews 29: 865–897. PubMed

Gillis-Germitsch N., Kockmann T., Asmis L. M., Tritten L. and Schnyder M., 2021. The Angiostrongylus vasorum excretory/secretory and surface proteome contains putative modulators of the host coagulation. Front Cell Infect Microbiol 11: 753320. PubMed PMC

Gounaris K., and Selkirk M. E., 2005. Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends Parasitol 21: 17–21. PubMed

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. PubMed

Gruning B., Dale R., Sjodin A., Chapman B. A., Rowe J. et al., 2018. Bioconda: sustainable and comprehensive software distribution for the life sciences. Nature methods 15: 475–476. PubMed PMC

Gu Z., 2022. Complex heatmap visualization. iMeta 1: e43. PubMed PMC

Guigó R., 2023. Genome annotation: From human genetics to biodiversity genomics. Cell Genom 3: 100375. PubMed PMC

Guiguet A., Dubreuil G., Harris M. O., Appel H. M., Schultz J. C. et al., 2016. Shared weapons of blood- and plantfeeding insects: Surprising commonalities for manipulating hosts. J Insect Physiol 84: 4–21. PubMed

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. PubMed PMC

Harnett M. M., Melendez A. J. and Harnett W., 2010. The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease. Clin Exp Immunol 159: 256–267. PubMed PMC

Hart A. J., Ginzburg S., Xu M. S., Fisher C. R., Rahmatpour N. et al., 2020. EnTAP: Bringing faster and smarter functional annotation to non-model eukaryotic transcriptomes. Mol Ecol Resour 20: 591–604. PubMed

Hartmann S., and Lucius R., 2003. Modulation of host immune responses by nematode cystatins. International Journal for Parasitology 33: 1291–1302. PubMed

Hatje K., Muhlhausen S., Simm D. and Kollmar M., 2019. The protein-coding human genome: annotating high-hanging fruits. Bioessays 41: e1900066. PubMed

Hawdon J. M., Jones B. F., Hoffman D. R. and Hotez P. J., 1996. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. Journal of Biological Chemistry 271: 6672–6678. PubMed

He L., Abuzeid A. M. I., Zhuang T., Zhao Q., Zhu S. et al., 2021. Expression and biological functions of Ancylostoma ceylanicum saposin-like protein. Parasitol Res 120: 3805–3813. PubMed

Heger P., Kroiher M., Ndifon N. and Schierenberg E., 2010. Conservation of MAP kinase activity and MSP genes in parthenogenetic nematodes. BMC developmental biology 10: 51. PubMed PMC

Hernandez-Plaza A., Szklarczyk D., Botas J., Cantalapiedra C. P., Giner-Lamia J. et al., 2023. eggNOG 6.0: enabling comparative genomics across 12 535 organisms. Nucleic Acids Res 51: D389–D394. PubMed PMC

Hewitson J. P., Harcus Y., Murray J., van Agtmaal M., Filbey K. J. et al., 2011. Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins. Journal of proteomics 74: 1573–1594. PubMed PMC

Hewitson J. P., Ivens A. C., Harcus Y., Filbey K. J., McSorley H. J. et al., 2013. Secretion of protective antigens by tissue-stage nematode larvae revealed by proteomic analysis and vaccination-induced sterile immunity. PLoS Pathogens 9: e1003492. PubMed PMC

Hoagland K. E., and Schad G. A., 1978. Necator americanus and Ancylostoma duodenale: life history parameters and epidemiological implications of two sympatric hookworms of humans. Experimental Parasitology 44: 36–49. PubMed

Hoeckendorf A., and Leippe M., 2012. SPP-3, a saposin-like protein of Caenorhabditis elegans, displays antimicrobial and pore-forming activity and is located in the intestine and in one head neuron. Dev Comp Immunol 38: 181–186. PubMed

Hoeckendorf A., Stanisak M. and Leippe M., 2012. The saposin-like protein SPP-12 is an antimicrobial polypeptide in the pharyngeal neurons of Caenorhabditis elegans and participates in defence against a natural bacterial pathogen. Biochem J 445: 205–212. PubMed

Hong M., Zhou X., Zeng C., Xu D., Xu T. et al., 2024. Nucleolar stress induces nucleolar stress body formation via the NOSR-1/NUMR-1 axis in Caenorhabditis elegans. Nat Commun 15: 7256. PubMed PMC

Hotez P. J., Narasimhan S., Haggerty J., Milstone L., Bhopale V. et al., 1992. Hyaluronidase from infective Ancylostoma hookworm larvae and its possible function as a virulence factor in tissue invasion and in cutaneous larva migrans. Infect Immun 60: 1018–1023. PubMed PMC

Howe K. L., Bolt B. J., Shafie M., Kersey P. and Berriman M., 2017. WormBase ParaSite - a comprehensive resource for helminth genomics. Molecular and biochemical parasitology 215: 2–10. PubMed PMC

Hu Y., Zhan B., Keegan B., Yiu Y. Y., Miller M. M. et al., 2012. Mechanistic and single-dose in vivo therapeutic studies of Cry5B anthelmintic action against hookworms. PLoS Negl Trop Dis 6: e1900. PubMed PMC

Huang Y., Abuzeid A. M. I., Liu Y., He L., Zhao Q. et al., 2020. Identification and localization of hookworm platelet inhibitor in Ancylostoma ceylanicum. Infect Genet Evol 77: 104102. PubMed

Hunt V. L., Tsai I. J., Selkirk M. E. and Viney M., 2017. The genome of Strongyloides spp. gives insights into protein families with a putative role in nematode parasitism. Parasitology 144: 343–358. PubMed

Irvine A., Huws S. A., Atkinson L. E. and Mousley A., 2023. Exploring the antimicrobial peptidome of nematodes through phylum-spanning in silico analyses highlights novel opportunities for pathogen control. PLoS Negl Trop Dis 17: e0011618. PubMed PMC

Jenkins R. E., Taylor M. J., Gilvary N. and Bianco A. E., 1996. Characterization of a secreted antigen of Onchocerca volvulus with host-protective potential. Parasite Immunol 18: 29–42. PubMed

Jex A. R., Nejsum P., Schwarz E. M., Hu L., Young N. D. et al., 2014. Genome and transcriptome of the porcine whipworm Trichuris suis. Nature genetics 46: 701–706. PubMed PMC

Jia T. W., Melville S., Utzinger J., King C. H. and Zhou X. N., 2012. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS neglected tropical diseases 6: e1621. PubMed PMC

Jung S., Sonnichsen F. D., Hung C. W., Tholey A., Boidin-Wichlacz C. et al., 2012. Macin family of antimicrobial proteins combines antimicrobial and nerve repair activities. J Biol Chem 287: 14246–14258. PubMed PMC

Käll L., Krogh A. and Sonnhammer E. L., 2004. A combined transmembrane topology and signal peptide prediction method. Journal of Molecular Biology 338: 1027–1036. PubMed

Kanehisa M., Furumichi M., Sato Y., Kawashima M. and Ishiguro-Watanabe M., 2023. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res 51: D587–D592. PubMed PMC

Katz K., Shutov O., Lapoint R., Kimelman M., Brister J. R. et al., 2022. The Sequence Read Archive: a decade more of explosive growth. Nucleic Acids Res 50: D387–D390. PubMed PMC

Keiser J., and Utzinger J., 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA : the journal of the American Medical Association 299: 1937–1948. PubMed

Klotz C., Ziegler T., Figueiredo A. S., Rausch S., Hepworth M. R. et al., 2011. A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS pathogens 7: e1001248. PubMed PMC

Knox D., 2012. Proteases as vaccines against gastrointestinal nematode parasites of sheep and cattle, pp. 399–420 in Parasitic Helminths: Targets, Screens, Drugs, and Vaccines, edited by Caffrey C. R.. Wiley-VCH Verlag & Co. KGaA., Weinheim, Germany.

Knox D. P., 2007. Proteinase inhibitors and helminth parasite infection. Parasite Immunol 29: 57–71. PubMed

Knox D. P., and Jones D. G., 1992. A comparison of superoxide dismutase (SOD, EC:1.15.1.1) distribution in gastro-intestinal nematodes. Int J Parasitol 22: 209–214. PubMed

Kokot T., and Kohn M., 2022. Emerging insights into serine/threonine-specific phosphoprotein phosphatase function and selectivity. J Cell Sci 135. PubMed

Kvist S., Manzano-Marin A., de Carle D., Trontelj P. and Siddall M. E., 2020. Draft genome of the European medicinal leech Hirudo medicinalis (Annelida, Clitellata, Hirudiniformes) with emphasis on anticoagulants. Sci Rep 10: 9885. PubMed PMC

Laing R., Kikuchi T., Martinelli A., Tsai I. J., Beech R. N. et al., 2013. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome biology 14: R88. PubMed PMC

Lee R. Y. N., Howe K. L., Harris T. W., Arnaboldi V., Cain S. et al., 2017. WormBase 2017: molting into a new stage. Nucleic acids research 46: D869–D874. PubMed PMC

Li W., and Godzik A., 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659. PubMed

Lightowlers M. W., and Rickard M. D., 1988. Excretory-secretory products of helminth parasites: effects on host immune responses. Parasitology 96 Suppl: S123–166. PubMed

Lo S. K., Rahman A., Xu N., Zhou M. Y., Nagpala P. et al., 1999. Neutrophil inhibitory factor abrogates neutrophil adhesion by blockade of CD11a and CD11b beta(2) integrins. Mol Pharmacol 56: 926–932. PubMed

Loeb L., and Smith A. J., 1904. The presence of a substance inhibiting the coagulation of the blood in Anchylostoma. Proceedings of the Pathological Society of Philadelphia 7: 173–178.

Logan J., Pearson M. S., Manda S. S., Choi Y. J., Field M. et al., 2020. Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms. PLoS neglected tropical diseases 14: e0008237. PubMed PMC

Lomsadze A., Burns P. D. and Borodovsky M., 2014. Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Res 42: e119. PubMed PMC

Loukas A., Doedens A., Hintz M. and Maizels R. M., 2000. Identification of a new C-type lectin, TES-70, secreted by infective larvae of Toxocara canis, which binds to host ligands. Parasitology 121 Pt 5: 545–554. PubMed

Loukas A., Hotez P. J., Diemert D., Yazdanbakhsh M., McCarthy J. S. et al., 2016. Hookworm infection. Nature reviews. Disease primers 2: 16088. PubMed

Lupas A., 1996. Prediction and analysis of coiled-coil structures. Methods in Enzymology 266: 513–525. PubMed

Maizels R. M., 2020. Regulation of immunity and allergy by helminth parasites. Allergy 75: 524–534. PubMed

Maizels R. M., Hewitson J. P. and Gause W. C., 2011. Heligmosomoides polygyrus: one species still. Trends in parasitology 27: 100–101. PubMed

Maizels R. M., Smits H. H. and McSorley H. J., 2018. Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity 49: 801–818. PubMed PMC

Manoury B., Gregory W. F., Maizels R. M. and Watts C., 2001. Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Current biology : CB 11: 447–451. PubMed

Maruszewska-Cheruiyot M., Szewczak L., Krawczak-Wojcik K., Kierasinska M., Stear M. et al., 2023. The impact of intestinal inflammation on nematode’s excretory-secretory proteome. Int J Mol Sci 24. PubMed PMC

Matouskova P., Vokral I., Lamka J. and Skalova L., 2016. The role of xenobiotic-metabolizing enzymes in anthelmintic deactivation and resistance in helminths. Trends Parasitol 32: 481–491. PubMed

McCarthy J. S., Wieseman M., Tropea J., Kaslow D., Abraham D. et al., 2002. Onchocerca volvulus glycolytic enzyme fructose-1,6-bisphosphate aldolase as a target for a protective immune response in humans. Infect Immun 70: 851–858. PubMed PMC

McNeilly T. N., Frew D., Burgess S. T. G., Wright H., Bartley D. J. et al., 2017. Niche-specific gene expression in a parasitic nematode; increased expression of immunomodulators in Teladorsagia circumcincta larvae derived from host mucosa. Sci Rep 7: 7214. PubMed PMC

Mistry J., Chuguransky S., Williams L., Qureshi M., Salazar G. A. et al., 2021. Pfam: The protein families database in 2021. Nucleic Acids Res 49: D412–D419. PubMed PMC

Morante T., Shepherd C., Constantinoiu C., Loukas A. and Sotillo J., 2017. Revisiting the Ancylostoma caninum secretome provides new information on hookworm-host interactions. Proteomics 17. PubMed

Moreno Y., Gros P. P., Tam M., Segura M., Valanparambil R. et al., 2011. Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with next-generation sequencing transcriptomic information. PLoS Negl Trop Dis 5: e1370. PubMed PMC

Moyle M., Foster D. L., McGrath D. E., Brown S. M., Laroche Y. et al., 1994. A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. The Journal of biological chemistry 269: 10008–10015. PubMed

Neph S., Kuehn M. S., Reynolds A. P., Haugen E., Thurman R. E. et al., 2012. BEDOPS: high-performance genomic feature operations. Bioinformatics 28: 1919–1920. PubMed PMC

Nisbet A. J., McNeilly T. N., Price D. R. G., Oliver E. M., Bartley Y. et al., 2019. The rational simplification of a recombinant cocktail vaccine to control the parasitic nematode Teladorsagia circumcincta. Int J Parasitol 49: 257–265. PubMed PMC

Noble W. S., 2009. How does multiple testing correction work? Nature Biotechnology 27: 1135–1137. PubMed PMC

Noon J. B., Schwarz E. M., Ostroff G. R. and Aroian R. V., 2019. A highly expressed intestinal cysteine protease of Ancylostoma ceylanicum protects vaccinated hamsters from hookworm infection. PLoS neglected tropical diseases 13: e0007345. PubMed PMC

O’Leary N. A., Wright M. W., Brister J. R., Ciufo S., Haddad D. et al., 2016. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44: D733–745. PubMed PMC

Oliveira P. L., and Genta F. A., 2021. Blood digestion in triatomine insects in Triatominae - The Biology of Chagas Disease Vectors, edited by Guarneri A. and Lorenzo M.. Springer, Cham.

Orr A. R., Quagraine J. E., Suwondo P., George S., Harrison L. M. et al., 2019. Genetic markers of benzimidazole resistance among human hookworms (Necator americanus) in Kintampo North Municipality, Ghana. The American journal of tropical medicine and hygiene 100: 351–356. PubMed PMC

Ow M. C., Nishiguchi M. A., Dar A. R., Butcher R. A. and Hall S. E., 2024. RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans. Front Mol Biosci 11: 1396587. PubMed PMC

Pala Z. R., Alves E. S. T. L., Minai M., Crews B., Patino-Martinez E. et al., 2023. Anopheles salivary apyrase regulates blood meal hemostasis and drives malaria parasite transmission. bioRxiv. PubMed PMC

Parks S. C., Nguyen S., Nasrolahi S., Bhat C., Juncaj D. et al., 2021. Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways. PLoS Pathog 17: e1010027. PubMed PMC

Parks S. C., Okakpu O. K., Azizpor P., Nguyen S., Martinez-Beltran S. et al., 2023. Parasitic nematode secreted phospholipase A(2) suppresses cellular and humoral immunity by targeting hemocytes in Drosophila melanogaster. Front Immunol 14: 1122451. PubMed PMC

Patro R., Duggal G., Love M. I., Irizarry R. A. and Kingsford C., 2017. Salmon provides fast and bias-aware quantification of transcript expression. Nature methods 14: 417–419. PubMed PMC

Paysan-Lafosse T., Blum M., Chuguransky S., Grego T., Pinto B. L. et al., 2023. InterPro in 2022. Nucleic Acids Res 51: D418–D427. PubMed PMC

Pearson M. S., Tribolet L., Cantacessi C., Periago M. V., Valero M. A. et al., 2012. Molecular mechanisms of hookworm disease: stealth, virulence, and vaccines. Journal of Allergy and Clinical Immunology 130: 13–21. PubMed

Perez-Riverol Y., Bai J., Bandla C., Garcia-Seisdedos D., Hewapathirana S. et al., 2022. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res 50: D543–D552. PubMed PMC

Pertea G., Huang X., Liang F., Antonescu V., Sultana R. et al., 2003. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19: 651–652. PubMed

Pertea G., and Pertea M., 2020. GFF utilities: GffRead and GffCompare. F1000Res 9. PubMed PMC

Pollo S. M. J., Liu H., Coria A. L., Rosin N., Labit E. et al., 2024. A single-cell transcriptomics atlas for the parasitic nematode Heligmosomoides bakeri: Extrapolating model organism information to non-model systems. bioRxiv.

Price D. R. G., Nisbet A. J., Frew D., Bartley Y., Oliver E. M. et al., 2019. Characterisation of a niche-specific excretory-secretory peroxiredoxin from the parasitic nematode Teladorsagia circumcincta. Parasit Vectors 12: 339. PubMed PMC

Price D. R. G., Steele P., Frew D., McLean K., Androscuk D. et al., 2024. Characterisation of protective vaccine antigens from the thiol-containing components of excretory/secretory material of Ostertagia ostertagi. Vet Parasitol 328: 110154. PubMed

Pritchard D. I., 1986. Antigens of gastrointestinal nematodes. Trans R Soc Trop Med Hyg 80: 728–734. PubMed

Pullan R. L., Smith J. L., Jasrasaria R. and Brooker S. J., 2014. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & vectors 7: 37. PubMed PMC

Quinlan A. R., and Hall I. M., 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842. PubMed PMC

Ranjit N., Zhan B., Hamilton B., Stenzel D., Lowther J. et al., 2009. Proteolytic degradation of hemoglobin in the intestine of the human hookworm Necator americanus. Journal of Infectious Diseases 199: 904–912. PubMed

Ray D. K., Bhopale K. K. and Shrivastava V. B., 1972. Migration and growth of Ancylostoma ceylanicum in golden hamsters Mesocricetus auratus. Journal of Helminthology 46: 357–362. PubMed

Raza A., Williams A. R. and Abeer M. M., 2023. Importance of ABC transporters in the survival of parasitic nematodes and the prospect for the development of novel control strategies. Pathogens 12. PubMed PMC

Rezansoff A. M., Laing R., Martinelli A., Stasiuk S., Redman E. et al., 2019. The confounding effects of high genetic diversity on the determination and interpretation of differential gene expression analysis in the parasitic nematode Haemonchus contortus. International journal for parasitology 49: 847–858. PubMed

Robinson M. D., McCarthy D. J. and Smyth G. K., 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. PubMed PMC

Rödelsperger C., Ebbing A., Sharma D. R., Okumura M., Sommer R. J. et al., 2021. Spatial transcriptomics of nematodes identifies sperm cells as a source of genomic novelty and rapid evolution. Mol Biol Evol 38: 229–243. PubMed PMC

Roeder T., Stanisak M., Gelhaus C., Bruchhaus I., Grotzinger J. et al., 2010. Caenopores are antimicrobial peptides in the nematode Caenorhabditis elegans instrumental in nutrition and immunity. Dev Comp Immunol 34: 203–209. PubMed

Romeo Y., and Lemaitre B., 2008. Drosophila immunity: methods for monitoring the activity of Toll and Imd signaling pathways. Methods in Molecular Biology 415: 379–394. PubMed

Ryan S. M., Ruscher R., Johnston W. A., Pickering D. A., Kennedy M. W. et al., 2022. Novel antiinflammatory biologics shaped by parasite-host coevolution. Proc Natl Acad Sci U S A 119: e2202795119. PubMed PMC

Scanlan J. L., Battlay P. and Robin C., 2022. Ecdysteroid kinase-like (EcKL) paralogs confer developmental tolerance to caffeine in Drosophila melanogaster. Curr Res Insect Sci 2: 100030. PubMed PMC

Schmitz C., Kinge P. and Hutter H., 2007. Axon guidance genes identified in a large-scale RNAi screen using the RNAi-hypersensitive Caenorhabditis elegans strain nre-1(hd20) lin-15b(hd126). Proceedings of the National Academy of Sciences of the United States of America 104: 834–839. PubMed PMC

Schurch N. J., Schofield P., Gierlinski M., Cole C., Sherstnev A. et al., 2016. How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA 22: 839–851. PubMed PMC

Schwarz E. M., Hu Y., Antoshechkin I., Miller M. M., Sternberg P. W. et al., 2015. The genome and transcriptome of the zoonotic hookworm Ancylostoma ceylanicum identify infection-specific gene families. Nature genetics 47: 416–422. PubMed PMC

Schwarz E. M., Kato M. and Sternberg P. W., 2012. Functional transcriptomics of a migrating cell in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 109: 16246–16251. PubMed PMC

Shinoda K., Choe A., Hirahara K., Kiuchi M., Kokubo K. et al., 2022. Nematode ascarosides attenuate mammalian type 2 inflammatory responses. Proc Natl Acad Sci U S A 119. PubMed PMC

Shumate A., and Salzberg S. L., 2020. Liftoff: accurate mapping of gene annotations. Bioinformatics 37: 1639–1643. PubMed PMC

Smallwood T. B., Navarro S., Cristofori-Armstrong B., Watkins T. S., Tungatt K. et al., 2021. Synthetic hookworm-derived peptides are potent modulators of primary human immune cell function that protect against experimental colitis in vivo. J Biol Chem 297: 100834. PubMed PMC

Smith H. E., 2014. Nematode sperm motility. WormBook: 1–15. PubMed PMC

Sotillo J., Sanchez-Flores A., Cantacessi C., Harcus Y., Pickering D. et al., 2014. Secreted proteomes of different developmental stages of the gastrointestinal nematode Nippostrongylus brasiliensis. Mol Cell Proteomics 13: 2736–2751. PubMed PMC

Sparkes A., De Baetselier P., Roelants K., De Trez C., Magez S. et al., 2017. The non-mammalian MIF superfamily. Immunobiology 222: 473–482. PubMed PMC

Srinivasan J., Dillman A. R., Macchietto M. G., Heikkinen L., Lakso M. et al., 2013. The draft genome and transcriptome of Panagrellus redivivus are shaped by the harsh demands of a free-living lifestyle. Genetics. PubMed PMC

Srivastava A., Malik L., Sarkar H., Zakeri M., Almodaresi F. et al., 2020. Alignment and mapping methodology influence transcript abundance estimation. Genome Biol 21: 239. PubMed PMC

Srivastava A., Zakeri M., Sarkar H., Soneson C., Kingsford C. et al., 2021. Accounting for fragments of unexpected origin improves transcript quantification in RNA-seq simulations focused on increased realism. bioRxiv.

Stanke M., Diekhans M., Baertsch R. and Haussler D., 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637–644. PubMed

Stassens P., Bergum P. W., Gansemans Y., Jespers L., Laroche Y. et al., 1996. Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proceedings of the National Academy of Sciences of the United States of America 93: 2149–2154. PubMed PMC

Stevens L., Martinez-Ugalde I., King E., Wagah M., Absolon D. et al., 2023. Ancient diversity in host-parasite interaction genes in a model parasitic nematode. Nat Commun 14: 7776. PubMed PMC

Stirewalt M. A., 1963. Chemical biology of secretions of larval helminths. Ann N Y Acad Sci 113: 36–53. PubMed

Stracke K., Jex A. R. and Traub R. J., 2020. Zoonotic ancylostomiasis: an update of a continually neglected zoonosis. The American journal of tropical medicine and hygiene 103: 64–68. PubMed PMC

Tang Y. T., Gao X., Rosa B. A., Abubucker S., Hallsworth-Pepin K. et al., 2014. Genome of the human hookworm Necator americanus. Nature Genetics 46: 261–269. PubMed PMC

Taylor S. S., and Kornev A. P., 2011. Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem Sci 36: 65–77. PubMed PMC

Tellier A., Moreno-Gamez S. and Stephan W., 2014. Speed of adaptation and genomic footprints of host-parasite coevolution under arms race and trench warfare dynamics. Evolution 68: 2211–2224. PubMed

Thomas J. H., and Robertson H. M., 2008. The Caenorhabditis chemoreceptor gene families. BMC biology 6: 42. PubMed PMC

Tian X., Lu M., Jia C., Bu Y., Aimulajiang K. et al., 2020. Haemonchus contortus transthyretin domain - containing protein (HcTTR): A promising vaccine candidate against Haemonchus contortus infection. Vet Parasitol 279: 109045. PubMed

Tian X., Lu M., Wang W., Jia C., Muhammad E. et al., 2019. HcTTR: a novel antagonist against goat interleukin 4 derived from the excretory and secretory products of Haemonchus contortus. Vet Res 50: 42. PubMed PMC

Traub R. J., 2013. Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. International Journal for Parasitology 43: 1009–1015. PubMed

Tribolet L., Cantacessi C., Pickering D. A., Navarro S., Doolan D. L. et al., 2015. Probing of a human proteome microarray with a recombinant pathogen protein reveals a novel mechanism by which hookworms suppress B-cell receptor signaling. The Journal of infectious diseases 211: 416–425. PubMed

Tritten L., Ballesteros C., Beech R., Geary T. G. and Moreno Y., 2021. Mining nematode protein secretomes to explain lifestyle and host specificity. PLoS Negl Trop Dis 15: e0009828. PubMed PMC

Tritten L., Nwosu U., Vargas M. and Keiser J., 2012. In vitro and in vivo efficacy of tribendimidine and its metabolites alone and in combination against the hookworms Heligmosomoides bakeri and Ancylostoma ceylanicum. Acta Tropica 122: 101–107. PubMed

Tvermoes B. E., Boyd W. A. and Freedman J. H., 2010. Molecular characterization of numr-1 and numr-2: genes that increase both resistance to metal-induced stress and lifespan in Caenorhabditis elegans. J Cell Sci 123: 2124–2134. PubMed PMC

UniProt C., 2023. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res 51: D523–D531. PubMed PMC

Uzoechi S. C., Rosa B. A., Singh K. S., Choi Y. J., Bracken B. K. et al., 2023. Excretory/secretory proteome of females and males of the hookworm Ancylostoma ceylanicum. Pathogens 12. PubMed PMC

van Megen H., van den Elsen S., Holterman M., Karssen G., Mooyman P. et al., 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11: 927–950.

Venkatesan A., Jimenez Castro P. D., Morosetti A., Horvath H., Chen R. et al., 2023. Molecular evidence of widespread benzimidazole drug resistance in Ancylostoma caninum from domestic dogs throughout the USA and discovery of a novel beta-tubulin benzimidazole resistance mutation. PLoS Pathog 19: e1011146. PubMed PMC

Vlaminck J., Cools P., Albonico M., Ame S., Ayana M. et al., 2019. Therapeutic efficacy of albendazole against soil-transmitted helminthiasis in children measured by five diagnostic methods. PLoS Negl Trop Dis 13: e0007471. PubMed PMC

Walker M., Cools P., Albonico M., Ame S. M., Ayana M. et al., 2021. Individual responses to a single oral dose of albendazole indicate reduced efficacy against soil-transmitted helminths in an area with high drug pressure. PLoS Negl Trop Dis 15: e0009888. PubMed PMC

Wang H., Paesen G. C., Nuttall P. A. and Barbour A. G., 1998. Male ticks help their mates to feed. Nature 391: 753–754. PubMed

Wang J., Barr M. M. and Wehman A. M., 2024. Extracellular vesicles. Genetics 227. PubMed PMC

Wang T., Ma G., Ang C. S., Korhonen P. K., Koehler A. V. et al., 2019. 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. PubMed

Wang Z., Lu Q. Q., Weng M. M., Li Y. L., Han L. L. et al., 2023. Binding of Trichinella spiralis C-type lectin with syndecan-1 on intestinal epithelial cells mediates larval invasion of intestinal epithelium. Vet Res 54: 86. PubMed PMC

Waterhouse R. M., Seppey M., Simao F. A., Manni M., Ioannidis P. et al., 2018. BUSCO applications from quality assessments to gene prediction and phylogenomics. Molecular biology and evolution 35: 543–548. PubMed PMC

Wei J., Damania A., Gao X., Liu Z., Mejia R. et al., 2016. The hookworm Ancylostoma ceylanicum intestinal transcriptome provides a platform for selecting drug and vaccine candidates. Parasites & vectors 9: 518. PubMed PMC

Wilbers R. H. P., Schneiter R., Holterman M. H. M., Drurey C., Smant G. et al., 2018. Secreted venom allergen-like proteins of helminths: Conserved modulators of host responses in animals and plants. PLoS Pathog 14: e1007300. PubMed PMC

Williamson A. L., Lustigman S., Oksov Y., Deumic V., Plieskatt J. et al., 2006. Ancylostoma caninum MTP-1, an astacin-like metalloprotease secreted by infective hookworm larvae, is involved in tissue migration. Infect Immun 74: 961–967. PubMed PMC

Wisniewski M., Jaros S., Baska P., Cappello M., Dlugosz E. et al., 2016. Hamsters vaccinated with Ace-mep-7 DNA vaccine produced protective immunity against Ancylostoma ceylanicum infection. Exp Parasitol 163: 1–7. PubMed

Wisniewski M., Jaros S., Baska P., Cappello M. and Wedrychowicz H., 2013. Ancylostoma ceylanicum metalloprotease 6 DNA vaccination induces partial protection against hookworm challenge infection. Acta Parasitol 58: 376–383. PubMed

Wootton J. C., 1994. Non-globular domains in protein sequences: automated segmentation using complexity measures. Computers and Chemistry 18: 269–285. PubMed

Wu C. W., Wimberly K., Pietras A., Dodd W., Atlas M. B. et al., 2019. RNA processing errors triggered by cadmium and integrator complex disruption are signals for environmental stress. BMC Biol 17: 56. PubMed PMC

Xiao S., Zhan B., Xue J., Goud G. N., Loukas A. et al., 2008. The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Experimental Parasitology 118: 32–40. PubMed

Xie Y., Hoberg E. P., Yang Z., Urban J. F. Jr. and Yang G., 2017. Ancylostoma ailuropodae n. sp. (Nematoda: Ancylostomatidae), a new hookworm parasite isolated from wild giant pandas in Southwest China. Parasit Vectors 10: 277. PubMed PMC

Yadav S., Sharma P., Sharma A., Ganga L., Saxena J. K. et al., 2021. Immunization with Brugia malayi calreticulin protein generates robust antiparasitic immunity and offers protection during experimental lymphatic filariasis. ACS Infect Dis 7: 790–799. PubMed

Yang X., Khan S., Zhao X., Zhang J., Nisar A. et al., 2020. Suppression of hyaluronidase reduces invasion and establishment of Haemonchus contortus larvae in sheep. Vet Res 51: 106. PubMed PMC

Yang Y., Wen Y., Cai Y. N., Vallee I., Boireau P. et al., 2015. Serine proteases of parasitic helminths. Korean J Parasitol 53: 1–11. PubMed PMC

Yatsuda A. P., Eysker M., Vieira-Bressan M. C. and De Vries E., 2002. A family of activation associated secreted protein (ASP) homologues of Cooperia punctata. Res Vet Sci 73: 297–306. PubMed

Yoshida A., Nagayasu E., Horii Y. and Maruyama H., 2012. A novel C-type lectin identified by EST analysis in tissue migratory larvae of Ascaris suum. Parasitology Research 110: 1583–1586. PubMed

Zawawi A., and Else K. J., 2020. Soil-transmitted helminth vaccines: are we getting closer? Frontiers in immunology 11: 576748. PubMed PMC

Zhan B., Hotez P. J., Wang Y. and Hawdon J. M., 2002. A developmentally regulated metalloprotease secreted by host-stimulated Ancylostoma caninum third-stage infective larvae is a member of the astacin family of proteases. Mol Biochem Parasitol 120: 291–296. PubMed

Zhan B., Liu Y., Badamchian M., Williamson A., Feng J. et al., 2003. Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. International Journal for Parasitology 33: 897–907. PubMed

Zhan B., Perally S., Brophy P. M., Xue J., Goud G. et al., 2010. Molecular cloning, biochemical characterization, and partial protective immunity of the heme-binding glutathione S-transferases from the human hookworm Necator americanus. Infection and Immunity 78: 1552–1563. PubMed PMC

Zhang Q., Pell J., Canino-Koning R., Howe A. C. and Brown C. T., 2014. These are not the k-mers you are looking for: efficient online k-mer counting using a probabilistic data structure. PLoS One 9: e101271. PubMed PMC