CoChat
Sign Up
Cited by 84Parasites and Host InteractionsHelminth infection and controlMollusks and Parasites Studies

Secreted venom allergen-like proteins of helminths: Conserved modulators of host responses in animals and plants

Open access
Wilbers, Ruud H. P., Schneiter, Roger, Holterman, Martijn H. M., Drurey, Claire, Smant, Geert, Asojo, Oluwatoyin A., Maizels, Rick M., Lozano-Torres, Jose L.·2018·PLOS Pathogens
DOI 10.1371/journal.ppat.1007300PMC PMC6193718
Open this paper in CoChat — free accountOpen PDF

Abstract

Despite causing considerable damage to host tissue at the onset of parasitism, invasive helminths establish remarkably persistent infections in both animals and plants. Secretions released by these obligate parasites during host invasion are thought to be crucial for their persistence in infection. Helminth secretions are complex mixtures of molecules, most of which have unknown molecular targets and functions in host cells or tissues. Although the habitats of animal- and plant-parasitic helminths are very distinct, their secretions share the presence of a structurally conserved group of proteins called venom allergen-like proteins (VALs). Helminths abundantly secrete VALs during several stages of parasitism while inflicting extensive damage to host tissue. The tight association between the secretion of VALs and the onset of parasitism has triggered a particular interest in this group of proteins, as improved knowledge on their biological functions may assist in designing novel protection strategies against parasites in humans, livestock, and important food crops.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.ppat.1007300

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The Pfam00188 gene family is dramatically expanded in many parasitic nematodes, especially hookworms and strongylides, and has been implicated in lipid binding, immune modulation, and pathogen resistance.

    “This gene family is dramatically expanded in many parasitic nematodes (especially the hookworms and strongylides) and have been implicated in lipid binding, immune modulation, and pathogen resistance, so they may, like the CCP domain family, represent an adaptable scaffold upon which a range of functions can be developed (Wilbers et al., 2018).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Wilbers et al., 2018

    The paper identifies Pfam00188 as the CAP domain of helminth VALs and describes lipid binding and modulation of host immune responses, including plant defenses against pathogens (Introduction, “Helminth VALs bind lipids” and “Biological functions of VALs from plant parasites”; pages not given). Its phylogenetic analysis reports more than 100 VALs in one hookworm species, but does not establish dramatic expansion across many parasitic nematodes, especially hookworms and strongylides; it says expansion is not linked to a particular lifestyle (Introduction, “Phylogenetic analysis”; page not given). (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • NIF is a member of a multi-gene family (Pfam00188, variously named CAP, SCP, TAPS, or VAL) that is prominent across a wide range of helminths and includes a wide variety of immune response modulators in both animals and plants.

    “Remarkably, NIF is a member of a multi-gene family (Pfam00188, variously named CAP, SCP, TAPS, or VAL) that is prominent across a wide range of helminths, and which includes a wide variety of immune response modulators in both animals and plants (Wilbers et al., 2018).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Wilbers et al., 2018

  • Pfam00188 may, like the CCP domain family, represent an adaptable scaffold upon which a range of functions can be developed.

    “This gene family is dramatically expanded in many parasitic nematodes (especially the hookworms and strongylides) and have been implicated in lipid binding, immune modulation, and pathogen resistance, so they may, like the CCP domain family, represent an adaptable scaffold upon which a range of functions can be developed (Wilbers et al., 2018).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Wilbers et al., 2018

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 89

  1. [1]Goverse A, Smant G. The activation and suppression of plant innate immunity by parasitic nematodes. Annu Rev Phytopathol. 2014; 52: 243– 65. 10.1146/annurev-phyto-102313-050118 24906126 · DOI
  2. [2]Allen J, Wynn T. Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog. 2011; 7(5): e1002003 10.1371/journal.ppat.1002003 21589896 PMC3093361 · DOI
  3. [3]Maizels R, McSorley H. Regulation of the host immune system by helminth parasites. J Allergy Clin Immunol. 2016; 138(3): 666– 75. 10.1016/j.jaci.2016.07.007 27476889 PMC5010150 · DOI
  4. [4]Cuesta-Astroz Y, Oliveira F, Nahum L, Oliveira G. Helminth secretomes reflect different lifestyles and parasitized hosts. Int J Parasitol. 2017; 47(9): 529– 44. 10.1016/j.ijpara.2017.01.007 28336271 · DOI
  5. [5]Cantacessi C, Campbell B, Visser A, Geldhof P, Nolan M, Nisbet A, et al A portrait of the "SCP/TAPS" proteins of eukaryotes—Developing a framework for fundamental research and biotechnological outcomes. Biotechnol Adv. 2009; 27(4): 376– 88. 10.1016/j.biotechadv.2009.02.005 19239923 · DOI
  6. [6]Hewitson J, Harcus Y, Murray J, van Agtmaal M, Filbey K, Grainger J, et al Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins. J Proteomics. 2011; 74(9): 1573– 94. 10.1016/j.jprot.2011.06.002 21722761 PMC4794625 · DOI
  7. [7]Hunt V, Tsai I, Coghlan A, Reid A, Holroyd N, Foth B, et al The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat Genet. 2016; 48(3): 299– 307. 10.1038/ng.3495 26829753 PMC4948059 · DOI
  8. [8]Lozano-Torres J, Wilbers R, Gawronski P, Boshoven J, Finkers-Tomczak A, Cordewener J, et al Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci U S A. 2012; 109(25): 10119– 24. 10.1073/pnas.1202867109 22675118 PMC3382537 · DOI
  9. [9]Sotillo J, Sanchez-Flores A, Cantacessi C, Harcus Y, Pickering D, Bouchery T, et al Secreted proteomes of different developmental stages of the gastrointestinal nematode Nippostrongylus brasiliensis. Mol Cell Proteomics. 2014; 13(10): 2736– 51. 10.1074/mcp.M114.038950 24994561 PMC4188999 · DOI
  10. [10]van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, Bongers T, et al A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology. 2009; 11: 927– S27.
  11. [11]Asojo O. Structure of a two-CAP-domain protein from the human hookworm parasite Necator americanus. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 5): 455– 62. 10.1107/S0907444911008560 21543848 PMC3087624 · DOI
  12. [12]Asojo O, Darwiche R, Gebremedhin S, Smant G, Lozano-Torres J, Drurey C, et al Heligmosomoides polygyrus Venom Allergen-like Protein-4 (HpVAL-4) is a sterol binding protein. Int J Parasitol. PMC5893428 29505764
  13. [13]Asojo O, Goud G, Dhar K, Loukas A, Zhan B, Deumic V, et al X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. J Mol Biol. 2005; 346(3): 801– 14. 10.1016/j.jmb.2004.12.023 15713464 · DOI
  14. [14]Asojo O, Koski R, Bonafe N. Structural studies of human glioma pathogenesis-related protein 1. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 10): 847– 55. 10.1107/S0907444911028198 21931216 PMC3176621 · DOI
  15. [15]Borloo J, Geldhof P, Peelaers I, Van Meulder F, Ameloot P, Callewaert N, et al Structure of Ostertagia ostertagi ASP-1: insights into disulfide-mediated cyclization and dimerization. Acta Crystallogr D Biol Crystallogr. 2013; 69(Pt 4): 493– 503. 10.1107/S0907444912050019 23519657 · DOI
  16. [16]Darwiche R, Lugo F, Drurey C, Varossieau K, Smant G, Wilbers R, et al Crystal structure of Brugia malayi venom allergen-like protein-1 (BmVAL-1), a vaccine candidate for lymphatic filariasis. Int J Parasitol. 2018. PMC5893361 29501266
  17. [17]Ding X, Shields J, Allen R, Hussey R. Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol. 2000; 30(1): 77– 81. 10675748
  18. [18]Fernandez C, Szyperski T, Bruyere T, Ramage P, Mosinger E, Wuthrich K. NMR solution structure of the pathogenesis-related protein P14a. J Mol Biol. 1997; 266(3): 576– 93. 10.1006/jmbi.1996.0772 9067611 · DOI
  19. [19]Gao B, Allen R, Maier T, Davis E, Baum T, Hussey R. Molecular characterisation and expression of two venom allergen-like protein genes in Heterodera glycines. Int J Parasitol. 2001; 31(14): 1617– 25. 11730789
  20. [20]Gibbs G, Roelants K, O’Bryan M. The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins—roles in reproduction, cancer, and immune defense. Endocr Rev. 2008; 29(7): 865– 97. 10.1210/er.2008-0032 18824526 · DOI
  21. [21]Guo M, Teng M, Niu L, Liu Q, Huang Q, Hao Q. Crystal structure of the cysteine-rich secretory protein stecrisp reveals that the cysteine-rich domain has a K+ channel inhibitor-like fold. J Biol Chem. 2005; 280(13): 12405– 12. 10.1074/jbc.M413566200 15596436 · DOI
  22. [22]Hawdon J, Narasimhan S, Hotez P. Ancylostoma secreted protein 2. cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol Biochem Parasit. 1999; 99(2): 149– 65. 10340481
  23. [23]Shikamoto Y, Suto K, Yamazaki Y, Morita T, Mizuno H. Crystal structure of a CRISP family Ca2+-channel blocker derived from snake venom. J Mol Biol. 2005; 350(4): 735– 43. 10.1016/j.jmb.2005.05.020 15953617 · DOI
  24. [24]Wang J, Shen B, Guo M, Lou X, Duan Y, Cheng X, et al Blocking effect and crystal structure of natrin toxin, a cysteine-rich secretory protein from Naja atra venom that targets the BKCa channel. Biochemistry. 2005; 44(30): 10145– 52. 10.1021/bi050614m 16042391 · DOI
  25. [25]Xu X, Francischetti I, Lai R, Ribeiro J, Andersen J. Structure of protein having inhibitory disintegrin and leukotriene scavenging functions contained in single domain. J Biol Chem. 2012; 287(14): 10967– 76. 10.1074/jbc.M112.340471 22311975 PMC3322842 · DOI
  26. [26]Zhan B, Liu Y, Badamchian M, Williamson A, Feng J, Loukas A, et al Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. Int J Parasitol. 2003; 33(9): 897– 907. 12906874
  27. [27]Gibbs G, O’Bryan M. Cysteine rich secretory proteins in reproduction and venom. Soc Reprod Fertil Suppl. 2007; 65: 261– 7. 17644967
  28. [28]Hawdon J, Jones B, Hoffman D, Hotez P. Cloning and characterization of Ancylostoma-secreted protein—A novel protein associated with the transition to parasitism by infective hookworm larvae. J Biol Chem. 1996; 271(12): 6672– 8. 8636085
  29. [29]Tetteh K, Loukas A, Tripp C, Maizels R. Identification of abundantly expressed novel and conserved genes from the infective larval stage of Toxocara canis by an expressed sequence tag strategy. Infect Immun. 1999; 67(9): 4771– 9. 10456930 PMC96808
  30. [30]Kratzschmar J, Haendler B, Eberspaecher U, Roosterman D, Donner P, Schleuning W. The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Eur J Biochem. 1996; 236(3): 827– 36. 8665901
  31. [31]Magdaleno L, Gasset M, Varea J, Schambony A, Urbanke C, Raida M, et al Biochemical and conformational characterisation of HSP-3, a stallion seminal plasma protein of the cysteine-rich secretory protein (CRISP) family. FEBS Lett. 1997; 420(2–3): 179– 85. 9459306
  32. [32]Mason L, Tribolet L, Simon A, von Gnielinski N, Nienaber L, Taylor P, et al Probing the equatorial groove of the hookworm protein and vaccine candidate antigen, Na-ASP-2. Int J Biochem Cell B. 2014; 50: 146– 55. 24631931
  33. [33]Milne T, Abbenante G, Tyndall J, Halliday J, Lewis R. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J Biol Chem. 2003; 278(33): 31105– 10. 10.1074/jbc.M304843200 12759345 · DOI
  34. [34]Udby L, Johnsen A, Borregaard N. Human CRISP-3 binds serum alpha B-1-glycoprotein across species. Bba-Gen Subjects. 2010; 1800(4): 481– 5. 20116414
  35. [35]Udby L, Lundwall A, Johnsen A, Fernlund P, Valtonen-Andre C, Blom A, et al beta-Microseminoprotein binds CRISP-3 in human seminal plasma. Biochem Bioph Res Co. 2005; 333(2): 555– 61. PMC1939934 15950934
  36. [36]Urayama S, Harada Y, Nakagawa Y, Ban S, Akasaka M, Kawasaki N, et al Ascidian sperm glycosylphosphatidylinositol-anchored CRISP-like protein as a binding partner for an allorecognizable sperm receptor on the vitelline coat. J Biol Chem. 2008; 283(31): 21725– 33. 10.1074/jbc.M802631200 18524765 · DOI
  37. [37]Volpert M, Mangum J, Jamsai D, D’Sylva R, O’Bryan M, McIntyre P. Eukaryotic expression, purification and structure/function analysis of native, recombinant CRISP3 from human and mouse. Sci Rep-Uk. 2014; 4. PMC3936225 24573035
  38. [38]Wang Y, Kuo J, Lee S, Liu J, Hsieh Y, Shih Y, et al Cobra CRISP functions as an inflammatory modulator via a novel Zn2+- and heparan sulfate-dependent transcriptional regulation of endothelial cell adhesion molecules. J Biol Chem. 2010; 285(48): 37872– 83. 10.1074/jbc.M110.146290 20889969 PMC2988390 · DOI
  39. [39]Cantacessi C, Gasser R. SCP/TAPS proteins in helminths—where to from now? Mol Cell Probes. 2012; 26(1): 54– 9. 10.1016/j.mcp.2011.10.001 22005034 · DOI
  40. [40]Schneiter R, Di Pietro A. The CAP protein superfamily: function in sterol export and fungal virulence. Biomol Concepts. 2013; 4(5): 519– 25. 10.1515/bmc-2013-0021 25436594 · DOI
  41. [41]Van Galen J, Van Balkom B, Serrano R, Kaloyanova D, Eerland R, Stuven E, et al Binding of GAPR-1 to negatively charged phospholipid membranes: unusual binding characteristics to phosphatidylinositol. Mol Membr Biol. 2010; 27(2–3): 81– 91. 10.3109/09687680903507080 20095951 · DOI
  42. [42]Choudhary V, Schneiter R. Pathogen-Related Yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins. P Natl Acad Sci USA. 2012; 109(42): 16882– 7. PMC3479496 23027975
  43. [43]Darwiche R, Mene-Saffrane L, Gfeller D, Asojo O, Schneiter R. The pathogen-related yeast protein Pry1, a member of the CAP protein superfamily, is a fatty acid-binding protein. J Biol Chem. 2017; 292(20): 8304– 14. 10.1074/jbc.M117.781880 28365570 PMC5437237 · DOI
  44. [44]Kelleher A, Darwiche R, Rezende W, Farias L, Leite L, Schneiter R, et al Schistosoma mansoni venom allergen-like protein 4 (SmVAL4) is a novel lipid-binding SCP/TAPS protein that lacks the prototypical CAP motifs. Acta Crystallogr D Biol Crystallogr. 2014; 70(Pt 8): 2186– 96. 10.1107/S1399004714013315 25084337 PMC4118828 · DOI
  45. [45]Franchini G, Porfido J, Shimabukuro M, Burusco M, Belgamo J, Smith B, et al The unusual lipid binding proteins of parasitic helminths and their potential roles in parasitism and as therapeutic targets. Prostag Leukotr Ess. 2015; 93: 31– 6. 25282399
  46. [46]Jasmer D, Goverse A, Smant G. Parasitic nematode interactions with mammals and plants. Annu Rev Phytopathol. 2003; 41: 245– 70. 10.1146/annurev.phyto.41.052102.104023 14527330 · DOI
  47. [47]Ding X, Shields J, Allen R, Hussey R. Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol. 2000; 30(1): 77– 81. 10675748
  48. [48]Duarte A, Curtis R, Maleita C, Tiago I, Abrantes I. Characterization of the venom allergen-like protein (vap-1) and the fatty acid and retinol binding protein (far-1) genes in Meloidogyne hispanica. Eur J Plant Pathol. 2014; 139(4): 825– 36.
  49. [49]Duarte A, Maleita C, Abrantes I, Curtis R. Tomato root exudates induce transcriptional changes of Meloidogyne hispanica genes. Phytopathol Mediterr. 2015; 54(1): 104– 8.
  50. [50]Kang J, Koh Y, Moon Y, Lee S. Molecular properties of a venom allergen-like protein suggest a parasitic function in the pinewood nematode Bursaphelenchus xylophilus. Int J Parasitol. 2012; 42(1): 63– 70. 10.1016/j.ijpara.2011.10.006 22142561 · DOI
  51. [51]Peng H, Gao BL, Kong L, Yu Q, Huang W, He X, et al Exploring the host parasitism of the migratory plant-parasitic nematode Ditylenchus destuctor by expressed sequence tags analysis. PLoS ONE. 2013; 8(7): e69579 10.1371/journal.pone.0069579 23922743 PMC3726699 · DOI
  52. [52]Petitot A, Dereeper A, Agbessi M, Da Silva C, Guy J, Ardisson M, et al Dual RNA-seq reveals Meloidogyne graminicola transcriptome and candidate effectors during the interaction with rice plants. Mol Plant Pathol. 2016; 17(6): 860– 74. 10.1111/mpp.12334 26610268 PMC6638361 · DOI
  53. [53]Wang X, Li H, Hu Y, Fu P, Xu J. Molecular cloning and analysis of a new venom allergen-like protein gene from the root-knot nematode Meloidogyne incognita. Exp Parasitol. 2007; 117(2): 133– 40. 10.1016/j.exppara.2007.03.017 17481609 · DOI
  54. [54]Yan X, Cheng X, Wang Y, Luo J, Mao Z, Ferris V, et al Comparative transcriptomics of two pathogenic pinewood nematodes yields insights into parasitic adaptation to life on pine hosts. Gene. 2012; 505(1): 81– 90. 10.1016/j.gene.2012.05.041 22705985 · DOI
  55. [55]Rehman S, Butterbach P, Popeijus H, Overmars H, Davis E, Jones J, et al Identification and Characterization of the Most Abundant Cellulases in Stylet Secretions from Globodera rostochiensis. Phytopathology. 2009; 99(2): 194– 202. 10.1094/PHYTO-99-2-0194 19245333 · DOI
  56. [56]Duarte A, Maleita C, Egas C, Abrantes I, Curtis R. Significant effects of RNAi silencing of the venom allergen-like protein (Mhi-vap-1) of the root-knot nematode Meloidogyne hispanica in the early events of infection. Plant Pathol. 2017; 66(8): 1329– 37.
  57. [57]Lozano-Torres J, Wilbers R, Warmerdam S, Finkers-Tomczak A, Diaz-Granados A, van Schaik C, et al Apoplastic Venom Allergen-like Proteins of Cyst Nematodes Modulate the Activation of Basal Plant Innate Immunity by Cell Surface Receptors. PLoS Pathog. 2014; 10(12). PMC4263768 25500833
  58. [58]Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell. 2006; 18(2): 465– 76. 10.1105/tpc.105.036574 16377758 PMC1356552 · DOI
  59. [59]Gomez-Gomez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell. 2000; 5(6): 1003– 11. 10911994
  60. [60]Gonzalez-Hernandez A, Van Coppernolle S, Borloo J, Van Meulder F, Paerewijck O, Peelaers I, et al Host protective ASP-based vaccine against the parasitic nematode Ostertagia ostertagi triggers NK cell activation and mixed IgG1-IgG2 response. Sci Rep-Uk. 2016; 6. PMC4941725 27403891
  61. [61]Hewitson J, Filbey K, Esser-von Bieren J, Camberis M, Schwartz C, Murray J, et al Concerted activity of IgG1 antibodies and IL-4/IL-25-dependent effector cells trap helminth larvae in the tissues following vaccination with defined secreted antigens, providing sterile immunity to challenge infection. PLoS Pathog. 2015; 11(3): e1004676 10.1371/journal.ppat.1004676 25816012 PMC4376884 · DOI
  62. [62]Kalyanasundaram R, Balumuri P. Multivalent vaccine formulation with BmVAL-1 and BmALT-2 confer significant protection against challenge infections with Brugia malayi in mice and jirds. Res Rep Trop Med. 2011; 2011(2): 45– 56. 10.2147/RRTM.S13679 21760754 PMC3134236 · DOI
  63. [63]MacDonald A, Tawe W, Leon O, Cao L, Liu J, Oksov Y, et al Ov-ASP-1, the Onchocerca volvulus homologue of the activation associated secreted protein family is immunostimulatory and can induce protective anti-larval immunity. Parasite Immunol. 2004; 26(1): 53– 62. 10.1111/j.0141-9838.2004.00685.x 15198646 · DOI
  64. [64]Meyvis Y, Geldhof P, Gevaert K, Timmerman E, Vercruysse J, Claerebout E. Vaccination against Ostertagia ostertagi with subfractions of the protective ES-thiol fraction. Vet Parasitol. 2007; 149(3–4): 239– 45. 10.1016/j.vetpar.2007.08.014 17881131 · DOI
  65. [65]Schallig H, vanLeeuwen M, Cornelissen A. Protective immunity induced by vaccination with two Haemonchus contortus excretory secretory proteins in sheep. Parasite Immunol. 1997; 19(10): 447– 53. 9372512
  66. [66]Loukas A, Bethony J, Brooker S, Hotez P. Hookworm vaccines: past, present, and future. Lancet Infect Dis. 2006; 6(11): 733– 41. 10.1016/S1473-3099(06)70630-2 17067922 · DOI
  67. [67]Mendez S, D’Samuel A, Antoine A, Ahn S, Hotez P. Use of the air pouch model to investigate immune responses to a hookworm vaccine containing the Na-ASP-2 protein in rats. Parasite Immunol. 2008; 30(1): 53– 6. 10.1111/j.1365-3024.2007.00994.x 18086017 · DOI
  68. [68]Xiao S, Zhan B, Xue J, Goud G, Loukas A, Liu Y, et al The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Exp Parasitol. 2008; 118(1): 32– 40. 10.1016/j.exppara.2007.05.010 17645877 · DOI
  69. [69]Diemert D, Pinto A, Freire J, Jariwala A, Santiago H, Hamilton R, et al Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J Allergy Clin Immunol. 2012; 130(1): 169– 76 e6. 10.1016/j.jaci.2012.04.027 22633322 · DOI
  70. [70]Heizer E, Zarlenga D, Rosa B, Gao X, Gasser R, De Graef J, et al Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora. BMC Genomics. 2013; 14: 118 10.1186/1471-2164-14-118 23432754 PMC3599158 · DOI
  71. [71]Chalmers I, McArdle A, Coulson R, Wagner M, Schmid R, Hirai H, et al Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC Genomics. 2008; 9: 89 10.1186/1471-2164-9-89 18294395 PMC2270263 · DOI
  72. [72]Hansell E, Braschi S, Medzihradszky K, Sajid M, Debnath M, Ingram J, et al Proteomic analysis of skin invasion by blood fluke larvae. PLoS Negl Trop Dis. 2008; 2(7): e262 10.1371/journal.pntd.0000262 18629379 PMC2467291 · DOI
  73. [73]Murray J, Gregory W, Gomez-Escobar N, Atmadja A, Maizels R. Expression and immune recognition of Brugia malayi VAL-1, a homologue of vespid venom allergens and Ancylostoma secreted proteins. Mol Biochem Parasitol. 2001; 118(1): 89– 96. 11704277
  74. [74]Datu B, Gasser R, Nagaraj S, Ong E, O’Donoghue P, McInnes R, et al Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva. PLoS Negl Trop Dis. 2008; 2(1): e130 10.1371/journal.pntd.0000130 18235850 PMC2217673 · DOI
  75. [75]Stroehlein A, Young N, Hall R, Korhonen P, Hofmann A, Sternberg P, et al CAP protein superfamily members in Toxocara canis. Parasite Vector. 2016; 9. PMC4921028 27342979
  76. [76]Mohandas N, Young N, Jabbar A, Korhonen P, Koehler A, Amani P, et al The barber’s pole worm CAP protein superfamily—A basis for fundamental discovery and biotechnology advances. Biotechnol Adv. 2015; 33(8): 1744– 54. 26239368
  77. [77]Morante T, Shepherd C, Constantinoiu C, Loukas A, Sotillo J. Revisiting the Ancylostoma Caninum Secretome Provides New Information on Hookworm–Host Interactions. PROTEOMICS. 2017; 17(23–24): 1700186. 29052354
  78. [78]Tang Y, Gao X, Rosa B, Abubucker S, Hallsworth-Pepin K, Martin J, et al Genome of the human hookworm Necator americanus. Nat Genet. 2014; 46: 261 10.1038/ng.2875 24441737 PMC3978129 · DOI
  79. [79]McNeilly T, Frew D, Burgess S, Wright H, Bartley D, Bartley Y, et al Niche-specific gene expression in a parasitic nematode; increased expression of immunomodulators in Teladorsagia circumcincta larvae derived from host mucosa. Sci Rep. 2017; 7(1): 7214 10.1038/s41598-017-07092-0 28775251 PMC5543109 · DOI
  80. [80]Bethony J, Loukas A, Smout M, Brooker S, Mendez S, Plieskatt J, et al Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. Faseb J. 2005; 19(9): 1743– +. 16037096
  81. [81]Rofatto H, Parker-Manuel S, Barbosa T, Tararam C, Wilson R, Leite L, et al Tissue expression patterns of Schistosoma mansoni Venom Allergen-Like proteins 6 and 7. Int J Parasitol. 2012; 42(7): 613– 20. 10.1016/j.ijpara.2012.04.008 22575701 · DOI
  82. [82]Tribolet L, Cantacessi C, Pickering D, Navarro S, Doolan D, Trieu A, et al Probing of a Human Proteome Microarray With a Recombinant Pathogen Protein Reveals a Novel Mechanism by Which Hookworms Suppress B-Cell Receptor Signaling. J Infect Dis. 2015; 211(3): 416– 25. 10.1093/infdis/jiu451 25139017 · DOI · Paper page
  83. [83]Bower M, Constant S, Mendez S. Necator americanus: The Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro. Experimental Parasitology. 2008; 118(4): 569– 75. 10.1016/j.exppara.2007.11.014 18199436 PMC2359483 · DOI
  84. [85]Rieu P, Sugimori T, Griffith D, Arnaout M. Solvent-accessible residues on the metal ion-dependent adhesion site face of integrin CR3 mediate its binding to the neutrophil inhibitory factor. J Biol Chem. 1996; 271(27): 15858– 61. 8663417
  85. [86]Schnyder-Candrian S, Maillet I, Le Bert M, Brault L, Jacobs M, Ryffel B, et al Neutrophil Inhibitory Factor Selectively Inhibits the Endothelium-Driven Transmigration of Eosinophils In Vitro and Airway Eosinophilia in OVA-Induced Allergic Lung Inflammation. J Allergy (Cairo). 2012; 2012: 245909. 23304174 PMC3523160
  86. [87]Chadderdon R, Cappello M. The hookworm platelet inhibitor: functional blockade of integrins GPIIb/IIIa (alphaIIbbeta3) and GPIa/IIa (alpha2beta1) inhibits platelet aggregation and adhesion in vitro. J Infect Dis. 1999; 179(5): 1235– 41. 10.1086/314724 10191228 · DOI
  87. [88]Del Valle A, Jones B, Harrison L, Chadderdon R, Cappello M. Isolation and molecular cloning of a secreted hookworm platelet inhibitor from adult Ancylostoma caninum. Mol Biochem Parasit. 2003; 129(2): 167– 77. 12850261
  88. [89]Yoshino T, Brown M, Wu X, Jackson CJ Ocadiz-Ruiz R, Chalmers I, et al Excreted/secreted Schistosoma mansoni venom allergen-like 9 (SmVAL9) modulates host extracellular matrix remodelling gene expression. Int J Parasitol. 2014; 44(8): 551– 63. 24859313 PMC4079936
  89. [90]Osman A, Wang C, Winter A, Loukas A, Tribolet L, Gasser R, et al Hookworm SCP/TAPS protein structure—A key to understanding host-parasite interactions and developing new interventions. Biotechnol Adv. 2012; 30(3): 652– 7. 22120067

Cited by

Sorted by citations

Authors
Wilbers, R. H. P., Schneiter, R., Holterman, M. H. M., Drurey, C., Smant, G., Asojo, O. A., Maizels, R. M., & Lozano-Torres, J. L.
Affiliations
  • Wageningen University & Research (NL)
  • University of Fribourg (CH)
  • Wellcome Centre for Molecular Parasitology (GB)
  • Hampton University (US)
Corresponding author
Wilbers, Ruud H. P.
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2018-10-18
Volume
14
Issue
10
Pages
e1007300
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1007300
PMC
PMC6193718
OpenAlex
W2896988915
Cited by
84
References
1
Citations by year
2026: 4 · 2025: 14 · 2024: 15 · 2023: 16 · 2022: 10 · 2021: 8 · 2020: 12 · 2019: 3 · 2018: 2
FWCI
1.07
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Pathogens (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by-sa)
  • Socio-Environmental Systems Modeling (acceptedVersion, cc-by)
  • RERO DOC (Universität Bern) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
Funders
  • Wellcome Trust (106122/A/14/Z)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (84713008)
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
  • Health Sciences › Veterinary › Small Animals › Helminth infection and control
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Mollusks and Parasites Studies
Keywords
venom allergen-like proteins, helminths, host-parasite interactions, parasite persistence, host tissue damage, host response modulation
MeSH terms
Allergens, Animals, Helminths, Host-Parasite Interactions, Nematode Infections, Venoms, Helminth Proteins, Crops, Agricultural

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review