Major SCP/TAPS protein expansion in Lucilia cuprina is associated with novel tandem array organisation and domain architecture.
CAP superfamily
Fly biology
Host-parasite interactions
Lucilia cuprina
SCP/TAPS protein
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
27 Nov 2020
27 Nov 2020
Historique:
received:
12
08
2020
accepted:
05
11
2020
entrez:
28
11
2020
pubmed:
29
11
2020
medline:
7
8
2021
Statut:
epublish
Résumé
Larvae of the Australian sheep blowfly, Lucilia cuprina, parasitise sheep by feeding on skin excretions, dermal tissue and blood, causing severe damage known as flystrike or myiasis. Recent advances in -omic technologies and bioinformatic data analyses have led to a greater understanding of blowfly biology and should allow the identification of protein families involved in host-parasite interactions and disease. Current literature suggests that proteins of the SCP (Sperm-Coating Protein)/TAPS (Tpx-1/Ag5/PR-1/Sc7) (SCP/TAPS) superfamily play key roles in immune modulation, cross-talk between parasite and host as well as developmental and reproductive processes in parasites. Here, we employed a bioinformatics workflow to curate the SCP/TAPS protein gene family in L. cuprina. Protein sequence, the presence and number of conserved CAP-domains and phylogeny were used to group identified SCP/TAPS proteins; these were compared to those found in Drosophila melanogaster to make functional predictions. In addition, transcription levels of SCP/TAPS protein-encoding genes were explored in different developmental stages. A total of 27 genes were identified as belonging to the SCP/TAPS gene family: encoding 26 single-domain proteins each with a single CAP domain and a solitary double-domain protein containing two conserved cysteine-rich secretory protein/antigen 5/pathogenesis related-1 (CAP) domains. Surprisingly, 16 SCP/TAPS predicted proteins formed an extended tandem array spanning a 53 kb region of one genomic region, which was confirmed by MinION long-read sequencing. RNA-seq data indicated that these 16 genes are highly transcribed in all developmental stages (excluding the embryo). Future work should assess the potential of selected SCP/TAPS proteins as novel targets for the control of L. cuprina and related parasitic flies of major socioeconomic importance.
Sections du résumé
BACKGROUND
BACKGROUND
Larvae of the Australian sheep blowfly, Lucilia cuprina, parasitise sheep by feeding on skin excretions, dermal tissue and blood, causing severe damage known as flystrike or myiasis. Recent advances in -omic technologies and bioinformatic data analyses have led to a greater understanding of blowfly biology and should allow the identification of protein families involved in host-parasite interactions and disease. Current literature suggests that proteins of the SCP (Sperm-Coating Protein)/TAPS (Tpx-1/Ag5/PR-1/Sc7) (SCP/TAPS) superfamily play key roles in immune modulation, cross-talk between parasite and host as well as developmental and reproductive processes in parasites.
METHODS
METHODS
Here, we employed a bioinformatics workflow to curate the SCP/TAPS protein gene family in L. cuprina. Protein sequence, the presence and number of conserved CAP-domains and phylogeny were used to group identified SCP/TAPS proteins; these were compared to those found in Drosophila melanogaster to make functional predictions. In addition, transcription levels of SCP/TAPS protein-encoding genes were explored in different developmental stages.
RESULTS
RESULTS
A total of 27 genes were identified as belonging to the SCP/TAPS gene family: encoding 26 single-domain proteins each with a single CAP domain and a solitary double-domain protein containing two conserved cysteine-rich secretory protein/antigen 5/pathogenesis related-1 (CAP) domains. Surprisingly, 16 SCP/TAPS predicted proteins formed an extended tandem array spanning a 53 kb region of one genomic region, which was confirmed by MinION long-read sequencing. RNA-seq data indicated that these 16 genes are highly transcribed in all developmental stages (excluding the embryo).
CONCLUSIONS
CONCLUSIONS
Future work should assess the potential of selected SCP/TAPS proteins as novel targets for the control of L. cuprina and related parasitic flies of major socioeconomic importance.
Identifiants
pubmed: 33246493
doi: 10.1186/s13071-020-04476-6
pii: 10.1186/s13071-020-04476-6
pmc: PMC7694928
doi:
Substances chimiques
Insect Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
598Références
Anstead CA, Batterham P, Korhonen PK, Young ND, Hall RS, Bowles VM, et al. A blow to the fly—Lucilia cuprina draft genome and transcriptome to support advances in biology and biotechnology. Biotechnol Adv. 2016;34:605–20.
pubmed: 26944522
doi: 10.1016/j.biotechadv.2016.02.009
Bisdorff B, Milnes A, Wall R. Prevalence and regional distribution of scab, lice and blowfly strike in Great Britain. Vet Rec. 2006;158:749–52.
pubmed: 16751308
doi: 10.1136/vr.158.22.749
pmcid: 16751308
Hall M, Wall R. Myiasis of humans and domestic animals. Adv Parasit. 1995;35:257–334.
doi: 10.1016/S0065-308X(08)60073-1
Azeredo-Espin AM, Lessinger AC. Genetic approaches for studying myiasis-causing flies: molecular markers and mitochondrial genomics. Genetica. 2006;126:111–31.
pubmed: 16502089
doi: 10.1007/s10709-005-1439-y
Williams KA, Richards CS, Villet MH. Predicting the geographic distribution of Lucilia sericata and Lucilia cuprina (Diptera: Calliphoridae) in South Africa. Afr Invertebr. 2014;55:157–70.
doi: 10.5733/afin.055.0109
Bisdorff B, Wall R. Sheep blowfly strike risk and management in Great Britain: a survey of current practice. Med Vet Entomol. 2008;22:303–8.
pubmed: 19120956
doi: 10.1111/j.1365-2915.2008.00756.x
Anstead CA, Perry T, Richards S, Korhonen PK, Young ND, Bowles VM, et al. The battle against flystrike—past research and new prospects through genomics. Adv Parasit. 2017;98:227–81.
doi: 10.1016/bs.apar.2017.03.001
Sandeman RM, Levot GW, Heath ACG, James PJ, Greeff JC, Scott MJ, et al. Control of the sheep blowfly in Australia and New Zealand – are we there yet? Int J Parasitol. 2014;44:879–91.
pubmed: 25240442
doi: 10.1016/j.ijpara.2014.08.009
pmcid: 25240442
Levot GW. Cyromazine resistance detected in Australian sheep blowfly. Aust Vet J. 2012;90:433–7.
pubmed: 23106323
doi: 10.1111/j.1751-0813.2012.00984.x
pmcid: 23106323
Levot GW. Resistance and the control of sheep ectoparasites. Int J Parasitol. 1995;25:1355–62.
pubmed: 8635885
doi: 10.1016/0020-7519(95)00070-I
Sneddon J, Rollin B. Mulesing and animal ethics. J Agric Environ Ethics. 2010;23:371–86.
doi: 10.1007/s10806-009-9216-z
Anstead CA, Korhonen PK, Young ND, Hall RS, Jex AR, Murali SC, et al. Lucilia cuprina genome unlocks parasitic fly biology to underpin future interventions. Nat Commun. 2015;6:7344.
pubmed: 26108605
doi: 10.1038/ncomms8344
pmcid: 26108605
Cantacessi C, Campbell BE, Visser A, Geldhof P, Nolan MJ, Nisbet AJ, et al. A portrait of the “SCP/TAPS” proteins of eukaryotes—developing a framework for fundamental research and biotechnological outcomes. Biotechnol Adv. 2009;27:376–88.
pubmed: 19239923
doi: 10.1016/j.biotechadv.2009.02.005
Gibbs GM, Roelants K, O’Bryan MK. The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins—roles in reproduction, cancer, and immune defense. Endocr Rev. 2008;29:865–97.
pubmed: 18824526
doi: 10.1210/er.2008-0032
Chalmers IW, McArdle AJ, Coulson RMR, Wagner MA, 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.
pubmed: 18294395
pmcid: 2270263
doi: 10.1186/1471-2164-9-89
Kovalick GE, Griffin DL. Characterization of the SCP/TAPS gene family in Drosophila melanogaster. Insect Biochem Mol Biol. 2005;35:825–35.
pubmed: 15944079
doi: 10.1016/j.ibmb.2005.03.003
Da Ros VG, Maldera JA, Willis WD, Cohen DJ, Goulding EH, Gelman DM, et al. Impaired sperm fertilizing ability in mice lacking Cysteine-RIch Secretory Protein 1 (CRISP1). Dev Biol. 2008;320:12–8.
pubmed: 18571638
pmcid: 2603034
doi: 10.1016/j.ydbio.2008.03.015
Teixeira PJPL, Thomazella DPT, Vidal RO, Prado PFV, Reis O, Baroni RM, et al. The fungal pathogen Moniliophthora perniciosa has genes similar to plant PR-1 that are highly expressed during its interaction with cacao. PLoS ONE. 2012;7:e45929.
pubmed: 23029323
pmcid: 3447762
doi: 10.1371/journal.pone.0045929
Cantacessi C, Hofmann A, Young ND, Broder U, Hall RS, Loukas A, et al. Insights into SCP/TAPS proteins of liver flukes based on large-scale bioinformatic analyses of sequence datasets. PLoS ONE. 2012;7:e31164.
pubmed: 22384000
pmcid: 3284463
doi: 10.1371/journal.pone.0031164
Osman A, Wang CK, Winter A, Loukas A, Tribolet L, Gasser RB, et al. Hookworm SCP/TAPS protein structure—a key to understanding host-parasite interactions and developing new interventions. Biotechnol Adv. 2012;30:652–7.
pubmed: 22120067
doi: 10.1016/j.biotechadv.2011.11.002
Wilbers RHP, Schneiter R, Holterman MHM, Drurey C, Smant G, Asojo OA, et al. Secreted venom allergen-like proteins of helminths: Conserved modulators of host responses in animals and plants. PLoS Pathog. 2018;14:e1007300.
pubmed: 30335852
pmcid: 6193718
doi: 10.1371/journal.ppat.1007300
Moyle M, Foster DL, McGrath DE, Brown SM, Laroche Y, Meutter J, et al. A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. J Biol Chem. 1994;269:10008–15.
pubmed: 7908286
doi: 10.1016/S0021-9258(17)36982-X
Winkler B, Bolwig C, Seppälä U, Spangfort MD, Ebner C, Wiedermann U. Allergen-specific immunosuppression by mucosal treatment with recombinant Ves v 5, a major allergen of Vespula vulgaris venom, in a murine model of wasp venom allergy. Immunology. 2003;110:376–85.
pubmed: 14632666
pmcid: 1783061
doi: 10.1046/j.1365-2567.2003.01751.x
Bower MA, Constant SL, Mendez S. Necator americanus: The Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro. Exp Parasitol. 2008;118:569–75.
pubmed: 18199436
doi: 10.1016/j.exppara.2007.11.014
Asojo OA, Loukas A, Inan M, Barent R, Huang J, Plantz B, et al. Crystallization and preliminary X-ray analysis of Na-ASP-1, a multi-domain pathogenesis-related-1 protein from the human hookworm parasite Necator americanus. Acta Crystallogr F. 2005;61:391–4.
doi: 10.1107/S1744309105007748
Lu G, Villalba M, Coscia MR, Hoffman DR, King TP. Sequence analysis and antigenic cross-reactivity of a venom allergen, antigen 5, from hornets, wasps, and yellow jackets. J Immunol Res. 1993;150:2823.
King TP, Spangfort MD. Structure and biology of stinging insect venom allergens. Int Arch Allergy Immunol. 2000;123:99–106.
pubmed: 11060481
doi: 10.1159/000024440
Charlab R, Valenzuela JG, Rowton ED, Ribeiro JMC. Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc Natl Acad Sci. 1999;96:15155.
pubmed: 10611354
pmcid: 24789
doi: 10.1073/pnas.96.26.15155
Yamazaki Y, Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon. 2004;44:227–31.
pubmed: 15302528
doi: 10.1016/j.toxicon.2004.05.023
Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105–11.
pubmed: 19289445
pmcid: 2672628
doi: 10.1093/bioinformatics/btp120
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–5.
pubmed: 20436464
pmcid: 3146043
doi: 10.1038/nbt.1621
Tang S, Lomsadze A, Borodovsky M. Identification of protein coding regions in RNA transcripts. Nucleic Acids Res. 2015;43:e78.
pubmed: 25870408
pmcid: 4499116
doi: 10.1093/nar/gkv227
Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30:1236–40.
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Kent WJ. BLAT - the BLAST-like alignment tool. Genome Res. 2002;12.
Borodovsky M, Lomsadze A. Eukaryotic gene prediction using GeneMark.hmm-E and GeneMark-ES. Curr Protoc Bioinformatics. 2011;4:4.6.1-10.
Slater GS, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinform. 2005;6:31.
doi: 10.1186/1471-2105-6-31
Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–6.
pubmed: 21221095
pmcid: 3346182
doi: 10.1038/nbt.1754
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER Suite: protein structure and function prediction. Nat Methods. 2015;12:7–8.
pubmed: 25549265
pmcid: 4428668
doi: 10.1038/nmeth.3213
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat methods. 2012;9:357–9.
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Quinlan AR. BEDTools: the swiss-army tool for genome feature analysis. Curr Protoc Bioinform. 2014;47:11.2.1-34.
doi: 10.1002/0471250953.bi1112s47
Ramírez F, Dündar F, Diehl S, Grüning BA, Manke T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 2014;42:W187–91.
pubmed: 24799436
pmcid: 4086134
doi: 10.1093/nar/gku365
Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytolog Bull. 1987;19:11–5.
Sović I, Šikić M, Wilm A, Fenlon SN, Chen S, Nagarajan N. Fast and sensitive mapping of nanopore sequencing reads with GraphMap. Nat Commun. 2016;7:11307.
pubmed: 27079541
pmcid: 4835549
doi: 10.1038/ncomms11307
Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–100.
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–3.
pubmed: 27899674
doi: 10.1093/nar/gkw1129
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.
pubmed: 9254694
pmcid: 146917
doi: 10.1093/nar/25.17.3389
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.
pubmed: 15034147
pmcid: 15034147
doi: 10.1093/nar/gkh340
Thurmond J, Goodman JL, Strelets VB, Attrill H, Gramates LS, Marygold SJ, et al. FlyBase 2.0: the next generation. Nucleic Acids Res. 2018;47:D759-65.
pmcid: 6323960
doi: 10.1093/nar/gky1003
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:323.
doi: 10.1186/1471-2105-12-323
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.
pubmed: 22357727
pmcid: 3329765
doi: 10.1093/sysbio/sys029
Stroehlein AJ, Young ND, Korhonen PK, Chang BCH, Sternberg PW, La Rosa G, et al. Analyses of compact Trichinella Kinomes reveal a MOS-like protein kinase with a unique N-terminal domain. G3 (Bethesda). 2016;6:2847–56.
doi: 10.1534/g3.116.032961
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. The Pfam protein families database. Nucleic Acids Res. 2012;40:D290-301.
pubmed: 22127870
doi: 10.1093/nar/gkr1065
Scott MJ, Atapattu A, Schiemann AH, Concha C, Henry R, Carey BL, et al. Organisation and expression of a cluster of yolk protein genes in the Australian sheep blowfly, Lucilia cuprina. Genetica. 2011;139:63–70.
pubmed: 20844939
doi: 10.1007/s10709-010-9492-6
Murray J, Gregory WF, Gomez-Escobar N, Atmadja AK, Maizels RM. Expression and immune recognition of Brugia malayi VAL-1, a homologue of vespid venom allergens and Ancylostoma secreted proteins. Mol Biochem Parasitol. 2001;118:89–96.
pubmed: 11704277
doi: 10.1016/S0166-6851(01)00374-7
Hawdon JM, Narasimhan S, Hotez PJ. Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol Biochem Parasitol. 1999;99:149–65.
pubmed: 10340481
doi: 10.1016/S0166-6851(99)00011-0
pmcid: 10340481
Hawdon JM, Jones BF, Hoffman DR, Hotez PJ. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. J Biol Chem. 1996;271:6672–8.
pubmed: 8636085
doi: 10.1074/jbc.271.12.6672
Cantacessi C, Gasser RB. SCP/TAPS proteins in helminths - where to from now? Mol Cell Probes. 2012;26:54–9.
pubmed: 22005034
doi: 10.1016/j.mcp.2011.10.001
Ding X, Shields J, Allen R, Hussey RS. Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol. 2000;30:77–81.
pubmed: 10675748
doi: 10.1016/S0020-7519(99)00165-4
Stroehlein AJ, Young ND, Hall RS, Korhonen PK, Hofmann A, Sternberg PW, et al. CAP protein superfamily members in Toxocara canis. Parasit Vectors. 2016;9:360.
pubmed: 27342979
pmcid: 4921028
doi: 10.1186/s13071-016-1642-y
Reams AB, Neidle EL. Selection for gene clustering by tandem duplication. Annu Rev Microbiol. 2004;58:119–42.
pubmed: 15487932
doi: 10.1146/annurev.micro.58.030603.123806
Harms CT, Armour SL, DiMaio JJ, Middlesteadt LA, Murray D, Negrotto DV, et al. Herbicide resistance due to amplification of a mutant acetohydroxyacid synthase gene. Mol Gen Genet. 1992;233:427–35.
pubmed: 1620098
doi: 10.1007/BF00265440
Lenormand T, Guillemaud T, Bourguet D, Raymond M. Evaluating gene flow using selected markers: a case study. Genetics. 1998;149:1383–92.
pubmed: 9649528
pmcid: 1460252
doi: 10.1093/genetics/149.3.1383
Anderson RP, Roth JR. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505.
pubmed: 334045
doi: 10.1146/annurev.mi.31.100177.002353
Stark GR. Regulation and mechanisms of mammalian gene amplification. Adv Cancer Res. 1993;61:87–113.
pubmed: 8346721
doi: 10.1016/S0065-230X(08)60956-2
Pan D, Zhang L. Tandemly arrayed genes in vertebrate genomes. Comp Funct Genom. 2008;2008:545269.
doi: 10.1155/2008/545269
Maizels RM, Gomez-Escobar N, Gregory WF, Murray J, Zang X. Immune evasion genes from filarial nematodes. Int J Parasitol. 2001;31:889–98.
pubmed: 11406138
doi: 10.1016/S0020-7519(01)00213-2
Kovalick GE, Schreiber MC, Dickason AK, Cunningham RA. Structure and expression of the antigen 5-related gene of Drosophila melanogaster. Insect Biochem Mol Biol. 1998;28:491–500.
pubmed: 9718681
doi: 10.1016/S0965-1748(98)00031-9
Megraw T, Kaufman TC, Kovalick GE. Sequence and expression of Drosophila antigen 5-related 2, a new member of the CAP gene family. Gene. 1998;222:297–304.
pubmed: 9831665
doi: 10.1016/S0378-1119(98)00489-2
Goud GN, Bottazzi ME, Zhan B, Mendez S, Deumic V, Plieskatt J, et al. Expression of the Necator americanus hookworm larval antigen Na-ASP-2 in Pichia pastoris and purification of the recombinant protein for use in human clinical trials. Vaccine. 2005;23:4754–64.
pubmed: 16054275
doi: 10.1016/j.vaccine.2005.04.040
Goud GN, Zhan B, Ghosh K, Loukas A, Hawdon J, Dobardzic A, et al. Cloning, yeast expression, isolation, and vaccine testing of recombinant Ancylostoma-secreted protein (ASP)-1 and ASP-2 from Ancylostoma ceylanicum. J Infect Dis. 2004;189:919–29.
pubmed: 14976610
doi: 10.1086/381901
pmcid: 14976610
Hotez PJ, Diemert D, Bacon KM, Beaumier C, Bethony JM, Bottazzi ME, et al. The human hookworm vaccine. Vaccine. 2013;31:B227–32.
pubmed: 23598487
pmcid: 3988917
doi: 10.1016/j.vaccine.2012.11.034
Asojo O. Structure of a two-CAP-domain protein from the human hookworm parasite Necator americanus. Acta Crystallogr D. 2011;67:455–62.
pubmed: 21543848
pmcid: 3087624
doi: 10.1107/S0907444911008560
Sen L, Ghosh K, Bin Z, Qiang S, Thompson MG, Hawdon JM, et al. Hookworm burden reductions in BALB/c mice vaccinated with recombinant Ancylostoma secreted proteins (ASPs) from Ancylostoma duodenale, Ancylostoma caninum and Necator americanus.. Vaccine. 2000;18:1096–102.
pubmed: 10590331
doi: 10.1016/S0264-410X(99)00371-0
pmcid: 10590331
Ghosh K, Hawdon J, Hotez P. Vaccination with alum-precipitated recombinant Ancylostoma-secreted protein 1 protects mice against challenge infections with infective hookworm (Ancylostoma caninum) larvae. J Infect Dis. 1996;174:1380–3.
pubmed: 8940240
doi: 10.1093/infdis/174.6.1380
Ghosh K, Hotez PJ. Antibody-dependent reductions in mouse hookworm burden after vaccination with Ancylostoma caninum secreted protein 1. J Infect Dis. 1999;180:1674–81.
pubmed: 10515831
doi: 10.1086/315059
pmcid: 10515831
Port F, Chen H-M, Lee T, Bullock SL. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. PNAS. 2014;111:2967–76.
doi: 10.1073/pnas.1405500111
Paulo DF, Williamson ME, Arp AP, Li F, Sagel A, Skoda SR, et al. Specific gene disruption in the major livestock pests Cochliomyia hominivorax and Lucilia cuprina using CRISPR/Cas9. G3 (Bethesda). 2019;9:3045–55.
pubmed: 31340950
pmcid: 6723136
doi: 10.1534/g3.119.400544